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Pernambuco modeled refugia in black. (A) H. enclosed carpel. When Kevin Nixon and their inner structures, allowing the fossil to camps, depending on how the evolutionary refugium albomarginatus, (B) colleagues at CornellH. semilineatus, University compared remain intact while Friis peers inside it trees were26 Evidence for Ecological Speciation and Its Alternative constructed. (C) H. faber. Note the absence of large 1171 www.sciencemag.org many angles (Science, 7 December SCIENCE VOL 323 27 FEBRUARY 2009 its stable regions in the southern portion living from traits with those same traits in 173 In the mid-1980s, Schluter Bahia refugium Dolph Peter Crane, now at plants, Archaefructus cameBahiaas a sister to * out and 2007, p. 1546). “We can get fantastic reso- the University of Chicago in Illinois, pro- 737-741 * Science 6 February 2009 323: of the forest (south of the living angiosperms and closer to the com- lution,” says Friis. “It’s really exciting.” But posed a solution, the anthophyte hypothesis. São Paulo refugia) relative to the mon ancestor northern areas. Asterisks so far, the flowers Friis finds are Using several lines of evidenceSpecies Challenge: Making Sense of Genetic and noting central and than even Amborella. 30 The Bacterial refugium Sã o Paulo Archaefructus’s distinction the that both Bennettitales and denote refugia inferred beyond was short- too diverse to trace back to a and Ecological Diversity current ranges of the months, better dat- particular ancestor. “From lived, however. Withintarget species. Gnetales organize their male 5.4% Christophe Fraser, Eric J. Alm, Symbols sediments in which it for ing of the indicate localities sampled was found these fossils, we cannot and female organs together Martin F. Polz, et al. Science 6 Februarybe con- 741-746 molecular analysis. Scale bar, 400 km. f irst say what is the basic yielded younger dates, putting this in what could 2009 323: (Bottom) The 50% majority-rule conflower squarely with other early fossil form,” she says. strued as a preflower, sensus Bayesian phylogenetic trees, 7% 36 Stability Predicts Genetic Diversity in the Brazilian Atlantic flower parts, about 125 million years old. he 7.8%considered them, rooted with sequences from the othAlso, a 2009 phylogenetic analysis of Before flowers along with angiosperms, Forest Hotspot er two congeneric species studied 67 (root not shown). Thick Peter Endress of the Although they have yet taxa by Doyle and internodes deas Carolina Carnaval, Michael J. Hickerson, Célio F. B. Haddad, et al. Anacomprising a single page 36 5.3 – University ofwith posterior probability placed to find the oldest fossil angiosperm entity called note clades Zurich, Switzerland, Science 6 February 2009 323: 785-789 4% Larger than 5.8%Although merely life. thegreater thanwith water liliesindicate than at flowers, researchers fossil in 90%. Percentages rather anthophytes. For the next 2.2 millimeters in diameter, this 3D the base of corrected distances between decade, most family trees fossil flower shows that grasses date Around the world, governments turn to AAAS as an objective, multidisciplinary scientific authority to Tamura-Neithe angiosperms, although this assume that the ancesclades (20). conclusion is contested. tral angiosperm evolved based on morphology supback to 94 million years ago. Cover image: ©Tui De Roy/Minden Pictures/FLPA 5.6% educate public officials and judicial figures on today’s most pressing issues. Our goal is to promote Inset: George Richmond/Bridgeman Art Library, London (Superstock) informed policy decisions that benefit society. And this is just one of the ways that AAAS is committed to www.sciencemag.org SCIENCE VOL 324 3 APRIL 2009 29 advancing science to support a healthy and prosperous world. Join us. Together we can make a difference. aaas.org/plusyou/policy

CREDITS (TOP TO BOTTOM): COURTESY OF STEPHEN MCCABE, UC SANTA CRUZ; PHOTO BY JENNIFER SVITKO, COURTESY OF WILLIAM L. CREPET, CORNELL UNIVERSITY

19th-century idealistic morphologists such natural-theological assumptions about a per- gram as one not dominated by a typological as Carl F. Kielmeyer and J. F. Meckel that Page 29 God who had created a perfectly and linear-recapitulationist mindset but sonified 0403NewsFocus.qxp 3/30/09 5:23 PM retained their teleology, their typological adapted nature. Bronn’s translation, though it rather as continuing to wrestle with the need emphasis on form, and their linear recapitula- altered key ideas to make Darwin comprehen- to account for variability and unpredictable tionism. This story, emphasizing the long per- sible to a German academic audience, was not change in terms of mechanistic laws of sistence of a German transcendental approach a conservative throwback. It represented the nature—among which Haeckel included, at to nature, has been deeply entrenched in the dynamic engagement of a leading paleontolo- the top of his list, natural selection. Haeckel’s Introduction history of biology. gist who had also long been working on many Darwinism thus shows continuity with earlyGliboff challenges “When we started, from of the questions Darwin claimed as his own— 19th-century concerns, mediated through this history right Stockholm. 2 Darwin’s Inspiration, Darwin’s Legacy the beginning. The ascriptionwas simple linear a critical yet generous equal, who saw himself Bronn. But those concerns were always more the search profile of bigger, Andrew Sugden a magnolia views of she recapitulationism to the[flower],” Romantic as moving science forward through the modi- flexible than has been acknowledged, and recalls. But owes much she embryologists, he notes,30 years ago,to a carica- fications he made to Darwin’s flawed theory. their articulation changed over time. Of and others discovered Baer ture developed by Karl Ernst vontiny in a Bronn’s death in 1862 afforded him little course Haeckel’s Darwinism was not Articles ancient flowers by sieving polemical context, then adopted uncritically by chance to steer the conversation further. Darwin’s own, but it was not an aberration or through sand and clay sedi3 On the true theory, any Earth influential historians such as E. S. a distortion of some Origin of Life onmore ments. With this technique, Russell and they have now collected hunStephen Jay Gould. than any other post-Darwinian additions or Carl Zimmer Science 9 January 2009 323: on. Gliboff’s fresh reading of the origadjustments were. It was science moving198-199 dreds of millimeter-size inal sources flowers, some preserved in interprets Kielmeyer Gliboff ’s overall picture of scientific 5 On the Richards’s emphasis on and Meckelthree far less rigidly Poras dimensions, from advance, in contrast to Origin of Art and Symbolism tugal and other locations typological in their orientation and with charisma andMichael Balter one of scientists passion, is Cretaceous deposits 70 milScience 6 February 2009 323: 709-711 much more lion to 120 to nature’s old. attentive million years building and innovating incrementally, workvariability than has fossil seen ing with what their predecessors have handed This been diversity 8 On the Origin of Photosynthesis before. Bothshows that early-19th- were for these angiosperms them and sculpting it into something new yet Mitch Leslie century naturalists and for theirgroups understandable to those around them. His senthriving, with several well-established, by 100 intellectual heirs, Gliboff argues, milsitive readingScience 6 Marchthe past. 1286-1287 allows Out of 2009 323: us to see post-1859 page 10 lionwas to understand the years ago. In some, Tiny Amborella sits the critical issue German evolutionists as rational actors rather 10 On theat Origin of Flowering Plants flower variety while nature’s manifold parts are whorled like than irrationally stuckthe bottom of early-19thin some the Elizabeth Pennisi tree. angiosperm family those of modern flowers; in seeking out underlying strict natu- concentury moment with unmodern commitothers they are spiraled, Science 3 April 2009 324: 28-31 ral laws to account for it. ments. By challenging the very foundations of sidered by some researchers This provides a newprimitive arrangement. Some the standard narrative of von Humboldt as the more starting from one 14 the nonflowering seed plants and the General Physics of Alexander German morpholpoint for analyzingfossils have prescribed numbers of “We are realizing that this or gymnosperms, the Earth account does at ogy, this careful, whose heyday was 200 flower Darwin’s first of compelling petals, another modern translator, the prominent paleon- feature, whereas in huge diversity is probably million years ago.Richards’s to undermine the least as much Stephen T. Jackson as Modern gymnosperms others the petal count include conifers, ginkgoes, and the cycads, tologist H. G. Bronn—a figure lit-varies. association of Science 1 May 2009 324:Darwin19th-century German 596-597 In 1998, standard with with a dangerously exceptional view of tle attended to in the Chinese geologist Ge Sun of the result of one innovaism their stout trunks and large fronds. Jilin University in Changchun, China, came Before angiosperms came along, these story but the lynchpin seemed to be a much older of Glinature. But the two books offer very different 16 Making German Evolution: Translation and Tragedy across what plants were much more diverse and boff’s. IntriguinglyThe fossil, called Archaefructus, was tion piled on top of reads. Is scientific species, a matter of Lynn progress flower. and plausibly, included cycadlike K. Nyhartsuch as the perGliboff arguesaquatic plant that looked to be 144 mil- another innovation.” that Bronn’s use sonal anguish Science 27 February woody 1170-1171 and triumph, or of intellectual an extinct Bennettitales, and many 2009 323: REPORTS of terms like “vervollkommnet” chugging along? Our concept it should be lion years old. By 2002, Sun and David plants called Gnetales, ofof which population expansion (23) are found presence the Florida —Peter Crane, capacious enough to include both. in 18 Darwin’s including (perfect) as Dilcher of of two lineages that co-occur in the ad- 6.2% divergence). In contrast, sites located a few representatives, Originalitythethe translations for Dar- Museum of Natural unstable survive albomarginatus and tree, jacent refugia. In all species, average net nucle- outside (south of) the refugia are genetically joint firs, area for H.today (see family H. faber, Historyor “favored” (FLMNH) in University of Chicago Peter J. Bowler win’s “improved” differences across Gainesville had otide localities to reflects more similar to each other, although to a lesser as well as incommon refugium area for H. faber described an entire plant, from roots(22)flow31). Also the Bahia 9 January 2009 323: 223-226 References and Notes lack of signature Science were not abouthigh geographic structure within refugia (2.6 to extent in H. faber (0.1 to 1.6%). Signatures of p. and H. semilineatus. in the Jurassic were of dragging Darwin The ers, entombed on a slab of rock unearthed in These fossils often spark debate because seed E. Haeckel, group now long gone; their 1. ferns, a Generelle Morphologie der Organismen backward into a German teleo- China. page specimens tend to be imperfectly preserved most(Georg Reimer, Berlin, 1866). 16 Liaoning in northeastern famous member is Caytonia, which The Red Queen and the logical view of one sense, Archaefructus wasn’t much and leave room for interpretation. To help seems to 22 previously served as astructures. Court Jester: Species Diversity 2. The reviewer precarpel-like press reader for both In 2. Genetic has have Fig.nature (asdiversity in putative C and the Role A B books at the manuscript stage. of Biotic and been claimed by those who versus unstableplant before remedy that, Friis and her colleagues have These g roups’ perceived relevance to Abiotic Factors Through Time have to refugial (stable) a flowering areas look at. “It’s Michael J. relationships to there the flowers,” Dilcher notes. It lacked begun to examine highlands in Java, from paid attention in wereBrazilian all). Arainforest. too. Haeckel’s oil landscape of flowers using synchro- flower evolution and theirBenton to Bronn at Atlantic painter, (Top) Species-specific Science 6 February 2009 323: petals and Bronn’s stability maps; (1905). 10.1126/science.1169621 Instead, Gliboff asserts, sepals, but it did have an tron radiation to generate a 3D image of angiosperms have ping-ponged between 728-732 Wanderbilder

Contents

ORIGINS

CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. KOEHLER, GERA-UNTERMHAUS, 1905)

© 2009 by The American Association for the Advancement of Science. All rights reserved.

NEWSFOCUS

Darwin’s Inspiration, Darwin’s Legacy
The day has passed delightfully. Delight itself, however, is a weak term to express the feeling of a naturalist who, for the first time, has wandered by himself in a Brazilian forest. The elegance of the grasses, the novelty of the parasitical plants, the beauty of the flowers, the glossy green of the foliage, but above all the general luxuriance of the vegetation, filled me with admiration. A most paradoxical mixture of sound and silence pervades the shady parts of the wood. The noise from the insects is so loud, that it may be heard even in a vessel anchored several hundred yards from the shore; yet within the recesses of the forest a universal silence appears to reign. To a person fond of natural history, such a day as this brings with it a deeper pleasure than he can ever hope to experience again. —Charles Darwin, The Voyage of the Beagle, Feb 29th [1832]

Introduction

On the Origin of of

Life on Earth
in some warm little pond, with all sorts of ammonia and phosphoric salts, light, heat, electricity, etc., present, that a protein compound was chemically formed ready to undergo still more complex changes, at the present day such matter would be instantly devoured or absorbed, which would not have been the case before living creatures were formed.” Scientists today who study the origin of life do not share Darwin’s pessimism about our ability to reconstruct those early moments. “Now is a good time to be doing this research, because the prospects for success are greater than they have ever been,” says John Sutherland, a chemist at the University of Manchester in the United Kingdom. He and others are addressing each of the steps involved in the transition to life: where the raw materials came from, how complex organic molecules such as RNA formed, and how the first cells arose. In doing so, they are inching their way toward making life from scratch. “When I was in graduate school, people thought investigating the origin of life was something old scientists did at the end of their career, when they could sit in an armchair and speculate,” says Henderson James Cleaves of the Carnegie Institution for Science in Washington, D.C. “Now making an artificial cell doesn’t sound like science fiction any more. It’s a reasonable pursuit.”

The collection reprinted here is a sample of the articles published in 2009 by Science magazine in celebration of the Darwin bicentenary. We start with four of the essays from our “On the Origin of” series, prepared by Science’s news writers; further essays in this series are appearing monthly in Science throughout the year. A Perspective by Stephen Jackson then considers the legacy of Alexander von Humboldt, for whom, like Darwin, the South American tropics were a critical inspiration, and who died 150 years ago in the year of the publication of Darwin’s Origin. (Humboldt’s Personal Narrative of his tropical explorations was acknowledged by Darwin as ‘far exceed[ing] in merit anything I have read’ on the subject.) A book review by Lynn Nyhart explores two recent volumes on Ernst Haeckel’s work, his interpretations of Darwin and his contributions to evolutionary thought. In the first of four Review articles reprinted here, Peter Bowler analyzes the originality of Darwin’s contribution to the understanding of the diversity and diversification of the living world. Michael Benton

Finally, with a focus on conservation, a Report by Ana Carnaval et al., who model evolutionary processes in endemic tree-frog species in the Brazilian Atlantic Forest, the very biodiversity hotspot that so inspired Darwin on his South American landfall, and that is now reduced to a collection of small fragments scattered along the coast. Darwin returned to the Brazilian coast on his final homeward leg, more than four years after his first landfall there. His enthusiasm for the tropical forested landscape was undiminished. In my last walk I stopped again and again to gaze on these beauties, and endeavoured to fix in my mind for ever, an impression which at the time I knew sooner or later must fail … they will leave, like a tale heard in childhood, a picture full of indistinct, but most beautiful figures. —Charles Darwin, The Voyage of the Beagle, August 1836 Andrew Sugden, Deputy Editor
CREDIT: KATHARINE SUTLIFF/SCIENCE

DARWIN

Step 1: Make RNA An RNA molecule is a chain of linked nucleotides. Each nucleotide in turn consists of three parts: a base (which functions as a

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CREDITS (TOP TO BOTTOM): KATHARINE SUTLIFF/SCIENCE; GEORGE RICHMOND/BRIDGEMAN ART LIBRARY, LONDON (SUPERSTOCK)

ike many other scientists raised in temperate latitudes, Charles Darwin was enthralled by his first glimpse of the tropical rain forest. His Beagle diary entry conveyed those immediate and thrilling first impressions, but the encounter with the Brazilian Atlantic Forest had an enduring influence on the development of his ideas over the following decades, with resounding echoes even today in 21st century evolutionary science.

L

examines the extent to which biotic and abiotic factors have shaped species diversity in the fossil record. Dolph Schluter reviews how research on speciation has shifted in focus from morphological evolution to reproductive isolation, tracing the links between Darwin’s ideas and current thinking. Christophe Fraser and colleagues discuss the contentious area of microbial species formation, an issue that would surely have vexed Darwin horribly had the bewildering diversity of microbes been known in his day.

AN AMAZON OF WORDS FLOWED FROM Charles Darwin’s pen. His books covered the gamut from barnacles to orchids, from geology to domestication. At the same time, he filled notebooks with his ruminations and scribbled thousands of letters packed with observations and speculations on nature. Yet Darwin dedicated only a few words of his great verbal flood to one of the biggest questions in all of biology: how life began. The only words he published in a book appeared near the end of On the Origin of Raw ingredients Species: “Probably all the organic beings which Life—or at least life as we know it—appears to have ever lived on this earth have descended have emerged on Earth only once. Just about all from some one primordial form, into which life organisms use double-stranded DNA to encode was first breathed,” Darwin wrote. genetic information, for example. They copy Darwin believed that life likely emerged their genes into RNA and then translate RNA spontaneously from the chemicals into proteins. The genetic code it is made of today, such as carbon, THE YEAR OF they use to translate DNA into pronitrogen, and phosphorus. But he teins is identical, whether they are The English did not publish these musings. emus or bread mold. The simplest naturalist had The English naturalist had built explanation for this shared biology his argument for evolution, in is that all living things inherited it built his argularge part, on the processes he from a common ancestor— ment for evocould observe around him. He did namely, DNA-based microbes that lution, in large lived more than 3.5 billion years not think it would be possible to see life originating now because ago. That common ancestor was part, on the the life that’s already here would already fairly complex, and many processes he prevent it from emerging. scientists have wondered how it In 1871, he outlined the prob- This essay is the first might have evolved from a simpler could observe lem in a letter to his friend, botanist in a monthly series, with predecessor. Some now argue that more on evolutionary around him.. Joseph Hooker: “But if (and Oh! roots online at blogs. membrane-bound cells with only what a big if!) we could conceive sciencemag.org/origins RNA inside predated both DNA

and proteins. Later, RNA-based life may have evolved the ability to assemble amino acids into proteins. It’s a small step, biochemically, for DNA to evolve from RNA. In modern cells, RNA is remarkably versatile. It can sense the levels of various compounds inside a cell and switch genes on and off to adjust these concentrations, for example. It can also join together amino acids, the building blocks of proteins. Thus, the first cells might have tapped RNA for all the tasks on which life depends. For 60 years, researchers have been honing theories about the sources of the amino acids and RNA’s building blocks. Over time, they have had to refine their ideas to take into account an ever-clearer understanding of what early Earth was like. In an iconic experiment in 1953, Stanley Miller, then at the University of Chicago, ignited a spark that zapped through a chamber filled with ammonia, methane, and other gases. The spark created a goo rich in amino acids, and, based on his results, Miller suggested that lightning on the early Earth could have created many compounds that would later be assembled into living things. By the 1990s, however, the accumulated evidence indicated that the early Earth was dominated by carbon dioxide, with a pinch of nitrogen—two gases not found in Miller’s flask. When scientists tried to replicate Miller’s experiments with carbon dioxide in the mix, their sparks seemed to make almost no amino acids. The raw materials for life would have had to come from elsewhere, they concluded. In 2008, however, lightning began to look promising once again. Cleaves and his colleagues suspected that the failed experiments were flawed because the sparks might have produced nitrogen compounds that destroyed any newly formed amino acids. When they added buffering chemicals that could take up these nitrogen compounds, the experiments generated hundreds of times more amino acids than scientists had previously found. Cleaves suspects that lightning was only one of several ways in which organic compounds built up on Earth. Meteorites that fall to Earth contain amino acids and organic carbon molecules such as formaldehyde. Hydrothermal vents spew out other compounds that could have been incorporated into the first life forms. Raw materials were not an issue, he says: “The real hurdle is how you put together organic compounds into a living system.”

3

EVOLUTIONARY ROOTS
“letter” in a gene’s recipe), a sugar molecule, and a cluster of phosphorus and oxygen atoms, which link one sugar to the next. For years, researchers have tried in vain to synthesize RNA by producing sugars and bases, joining them together, and then adding phosphates. “It just doesn’t work,” says Sutherland. This failure has led scientists to consider two other hypotheses about how RNA came to be. Cleaves and others think RNA-based life may have evolved from organisms that used a different genetic material—one no longer found in nature. Chemists have been able to use other compounds to build backbones for nucleotides (Science, 17 November 2000, p. 1306). They’re now investigating whether these humanmade genetic molecules, called PNA and TNA, could have emerged on their own on the early Earth more easily than RNA. According to this hypothesis, RNA evolved later and replaced the earlier molecule. But it could also be that RNA wasn’t put together the way scientists have thought. “If you want to get from Boston to New York, there is an obvious way to go. But if you can’t get there that way, there are other ways you could go,” says Sutherland. He and his colleagues have been trying to build RNA from simple organic compounds, such as formaldehyde, that existed on Earth before life began. They find they make better progress toward producing RNA if they combine the components of sugars and the components of bases together instead of separately making complete sugars and bases first. Over the past few years, they have documented almost an entire route from prebiotic molecules to RNA and are preparing to publish even more details of their success. Discovering these new reactions makes Sutherland suspect it wouldn’t have been that hard for RNA to emerge directly from an organic soup. “We’ve got the molecules in our RNA, producing the first protocells. “The goal sights,” he says. is to have something that can replicate by itself, Sutherland can’t say for sure where these using just chemistry,” says Szostak. reactions took place on the early Earth, but he After 2 decades, he and his colleagues notes that they work well at the temperatures have come up with RNA molecules that can and pH levels found in ponds. If those ponds build copies of other short RNA molecules. dried up temporarily, They have been able to they would concentrate mix RNA and fatty “Now making an the nucleotides, making acids together in such a conditions for life even artificial cell doesn’t way thatinthe RNA gets more favorable. trapped vesicles. The Were these Darwin’s vesicles are able to add sound like science warm little ponds? “It fatty acids to their might just be that he fiction any more. It’s membranes and grow. wasn’t too far off,” says In July 2008, Szostak Sutherland. a reasonable pursuit.” reported that he had figured out how proto—HENDERSON JAMES CLEAVES, cells could “eat” and Step 2: The cell CARNEGIE INSTITUTION FOR SCIENCE bring in nucleotides to If life did start out with RNA alone, that RNA build the RNA. would need to make copies of itself without All living cells depend on complicated help from proteins. Online in Science this channels to draw nucleotides across their week (www.sciencemag.org/cgi/content/ membranes, raising the question of how a abstract/1167856), Tracey Lincoln and Ger- primitive protocell membrane brought in these ald Joyce of the Scripps Research Institute in molecules. By experimenting with different San Diego, California, have shown how that recipes for membranes, Szostak and his colmight have been possible. They designed a leagues have come up with protocells leaky pair of RNA molecules that join together and enough to let nucleic acids slip inside, where assemble loose nucleotides to match their they could be assembled into RNA, but not so partner. Once the replication is complete, old porous that the large RNA could slip out. and new RNA molecules separate and join Their experiments also show that these with new partners to form new RNA. In 30 vesicles survive over a 100°C range. At high hours, Lincoln and Joyce found, a population temperatures, protocells take in nucleotides of RNA molecules could grow 100 million quickly, and at lower temperatures, Szostak times bigger. found, they build RNA molecules faster. Lincoln and Joyce kept their RNA moleHe speculates that regular temperature cules in beakers. On the early Earth, however, cycles could have helped simple protocells surreplicating RNA might have been packed in the vive on the early Earth. They could draw in first cells. Jack Szostak and his colleagues at nucleotides when they were warm and then use Harvard Medical School in Boston have been them to build RNA when the temperature investigating how fatty acids and other mole- dropped. In Szostak’s protocells, nucleotides cules on the early Earth might have trapped are arranged along a template of RNA. Strands of RNA tend to stick together at low temperatures. When the protocell warmed up again, the heat might cause the two strands to pull apart, allowing the new RNA molecule to function. Now Szostak is running experiments to bring his protocells closer to life. He is developing new forms of RNA that may be able to replicate longer molecules faster. For him, the true test of his experiments will be whether his protocells not only grow and reproduce, but evolve. “To me, the origin of life and the origin of Darwinian evolution are essentially the same thing,” says Szostak. And if Darwin was alive today, he might well be willing to write a lot Protocell. Researchers at more about how life began. Harvard are trying to make
simple life forms, shown here in a computer image.

EVOLUTIONARY ROOTS ORIGINS
“letter” in a gene’s recipe), a sugar molecule, soup. “We’ve got the molecules in our RNA, producing the first protocells. “The goal Venus, phallus, or pebble? and a cluster of phosphorus and oxygen sights,” he says. is to have something thatknow much about Art, but I know what “I don’t can replicate by itself, atoms, which link one sugar to the next. For Sutherland can’t say for sure where these using just chemistry,” says Szostak. humorist and art critic I like,” quipped the years, researchers have tried in vain to synthe- reactions took place on the early Earth, but he After 2 decades, he and his colleagues For archaeoGelett Burgess back in 1906. size RNA by producing sugars and bases, notes that they work well at the temperatures have come up with RNA molecules that can nonart is still logists, distinguishing art from joining them together, and then adding phos- and pH levels found in ponds. If those ponds build copies of quite ashort RNA Take the 6-centimeter-long other challenge. molecules. phates. “It just doesn’t work,” says Sutherland. dried up temporarily, piece They have been able to the Venus of of quartzite known as This failure has led scientists to consider they would concentrate mix RNA and fatty Tan-Tan. Found in Morocco in 1999 next to a “Now making an two other hypotheses about how RNA came to the nucleotides, communicate meaning, whether they be the rich trove of stone in suchestimated to be making acids together tools a be. Cleaves and others think RNA-based life conditions for life even make up our languages, the musi- between 300,000 and 500,000 years old, it way that the RNA gets words that artificial cell doesn’t may have evolved from organisms that used a more favorable. cal sounds that convey emotion, or the dra- resembles a human figure with stubby arms trapped in vesicles. The different genetic material—one no longer Were these Darwin’s vesicles are able to add matic paintings that, 30,000 years after their and legs. Robert Bednarik, an independent sound like science found in nature. Chemists have been able to warm little ponds? “It caused the discoverers of the Chau- archaeologist based in Caulf ield South, fatty acids to their creation, use other compounds to build backbones for might just be vet Cave to break down in tears.more. It’s that he membranes that an ancient human Australia, insistsand grow. fiction any nucleotides (Science, 17 November 2000, wasn’t too far off,” While sites like Chauvet might be vivid deliberately modified the stone to says In July 2008, Szostak p. 1306). They’re now investigating whether Sutherland. a reasonable pursuit.” reported that a had examples of what some researchers still make it look more likehe person. these humanmade genetic molecules, called figured d’art is protoconsider a “creative explosion” that began If so, this objetout how so old PNA and TNA, could have emerged on their Step 2: The cell when modern humans —HENDERSON JAMES CLEAVES, it was created not by our colonized Europe that cells could “eat” and CARNEGIE INSTITUTION FOR own on the early Earth more easily than RNA. If life did start out with about 40,000 years ago, an increasing num-SCIENCE species, which first to own bring in nucleotides According to this hypothesis, RNA evolved RNA alone, that RNAprehistorians are tracing our sym- appears in Africa nearly build the RNA. ber of later and replaced the earlier molecule. would need to make roots much further back in time—and cells depend on complicated All living 200,000 years ago, but bolic copies of itself without But it could also be that RNA wasn’t put help from proteins. Online in Science this channels to draw one of our ances- their in some cases, to species ancestral to Homo by nucleotides across together the way scientists have thought. “If week (www.sciencemag.org/cgi/content/ themselves, raising the question of how a sapiens. Like modern humans membranes, tors, perhaps the you want to get from Boston to New York, abstract/1167856), Tracey Lincolnseems to have its origins large-brained H. in these symbolic behavior and Ger- primitive protocell membrane brought there is an obvious way to go. But if you can’t ald Joyce of thein Africa. Recent Institute in have turnedBy experimenting with different Scripps Research excavations molecules. heidelbergensis, get there that way, there are other ways you San Diego, California, have shown tools,that recipes for membranes, by someand his colup elaborate stone how beads, and ochre thought Szostak could go,” says Sutherland. He and his col- might have been possible. They designed a leaguesago, come up with protocells leaky dating back 100,000 or more years have anthropologists to leagues have been trying to build RNA from pair of RNA molecules that join togetherare still debating nucleic acids slip inside, where although researchers and enough to let be the common simple organic compounds, discovery by Frenchassemble loose nucleotides to f inds really demonstrate assembled into RNA, but not so Since their such as formaldespelunkers which of these match their they could be ancestor of modhyde, that existed on Earth before life began. partner. Once the replication is complete,But there’s wide- large humans and out. in 1994, the magnificent lions, horses, and symbolic expression. old porous that the ern RNA could slip They find they rhinosbetterseem to leap from the walls RNA spread agreement that the building blocks Neandertals. show that these make that progress toward and new of molecules separate and join Their experiments also That producing RNA if they combinein southern France have of symbolism preceded30 vesicles art. would 100°C that At high Chauvet Cave the compo- with new partners to form new RNA. In full-blown survive over a mean range. nents of sugars reigned components of bases cave paint- and Joyce found,about beads andtemperatures, protocells extremely and the as the world’s oldest hours, Lincoln “When we talk a population art, we are art is an take in nucleotides together instead of separately making com- red ochre and actually talking aboutmillion technologies at ancienttemperatures, Szostak ings. Expertly composed in of RNA molecules could grow 100 material quickly, and lower part of the Homo plete sugars andblack charcoal, the vivid drawings demon- for symbolic expression that certainly they build RNA molecules faster. Symmetry in stone. bases first. times bigger. found, post- repertoire. “Ignoring the Over the past few years, they have docu-stretches backanddate the origins RNA mole- thoughtspeculates that regularwe have Some stone tools Lincoln Joyce kept their of symbolic He and few specimens temperature strate that the artistic gift mented almost an entire route from years. These paintings communication, potentially by a verycould have helpedearly paleoart, surmore than 30,000 prebiotic cules in beakers. On the early Earth, however, cycles wide of very simple protocells require a mental molecules to RNA almost sure to be mentionedreplicating RNAmargin,” says archaeologist Dietrich Stoutearly Earth. They could draw in to create. might have been packed in the vive on the are and are preparing to pubin any artiexplaining them away, image lish even more cle or paper about the earliest art. But what of University College London. nucleotides when they were warm and then use details of their success. Dis- first cells. Jack Szostak and his colleagues at or rejecting them out covering these new reactions makes Suther- the originsMedical School in Boston of symbolism wasto build RNA when the temperature do they really tell us about Harvard of The evolution have been them once of hand does not serve this discipline well,” land suspect it wouldn’t have been that hard investigating how fatty acids and other mole- as dropped. In Szostak’s protocells, in a 2003 analysis of the artistic expression? thought to have been as rapid “flicking on Bednarik wrote nucleotides for RNA to emerge directly from an organicwho decorated early Earth might have trapped Clivearranged along a template of RNA. StrandsAnthropology. cules on the a light switch,” as archaeologist are Gamble Venus of Tan-Tan in Current The prehistoric humans of RNA tend Chauvet’s walls by torchlight arrived at the of the Royal Holloway, University of Lon- to stick together archaeologists are skeptical, Yet many at low temperatures. When arguing that the stone’s the cave with their artistic genius already in full don, put it some years ago. But given newthe protocell warmed up again, resemblance to a heat might cause the two strands to pull coincidence. Indeed, flower. And so, most researchers agree that evidence that symbolic behavior appears human figure might be apart, the origins of art cannot simply long before cave allowing the new RNA molecule to Tan-Tan “figurine” is rempaintings, the debate over the function. Now Szostak is running similar controversy over a be pegged to the latest discovery THE YEAR OF Gamble now says that his much- iniscent of aexperiments to Recent bring mod- smaller stone discovered in 1981 of ancient paintings or sculpcited comment needs to behis protocells closer to life. He is devel- at the site of ture. Some of the earliest art ified: “It’s a dimmer oping new forms of RNARam may beIsraeli-occupied Golan switch now, Berekhat that in the able to excavations likely perished over the ages; a stuttering candle.” replicate longer molecules faster. For him, Heights. To some archaeologists, this have turned the true test 250,000-year-old object resembles a woman, much remains to be found; and As they more precisely pin- of his experiments will be whether his but others argue that it was shaped by natural up elaborate archaeologists don’t always point when symbolic behavior protocells not only grow and agree on how to interpret what is began, scientists are reproduce, but evolve. and, in any case, looks more like a hoping they forces, stone tools, “To me, origin of life and the Even of unearthed. As a result, instead of might one day crack the tough-the penguin or a phallus. originafter an exhaustive beads, and Darwinian evolution are essentially the same chasing after art’s first appearest question of all: What was its microscopic study concluded that the thing,” says ance, many researchers seek to evolutionary advantage toSzostak. AndRam object had indeed been etched Berekhat if Darwin was alive ochre dating today, he might well tool to emphasize a lot understand its symbolic roots. humans? Did symbols, as many with abe willing to write what some consider Protocell. Researchers at back 100,000 more about After all, art is an aesthetic This essay continues our are trying to make its “head” and Harvard researchers suspect, serve as ahow life began. “arms,” many researchers have or more simple life forms, shown expression of something more monthly series. See more social glue that helped tribes of rejected it as a–CARLof art. For some, proof of work ZIMMER on humans’ evolutionary computer image. Carl Zimmer is author of Microcosm: E. coli and evidence that the fundamental: the cognitive abil- journey onlineago.here in aearly humans to survive and the symbolic behavior requiresthe years at blogs. New Science of Life. ity to construct symbols that sciencemag.org/origins. reproduce? symbols had a commonly understood mean-

On the Origin of of

Art and Symbolism

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–CARL ZIMMER

Carl Zimmer is the author of Microcosm: E. coli and the New Science of Life.

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tools, which Wynn and many others argue are clear examples of an imposed form based on a mental template. Some have even argued that these skillfully crafted hand axes had symbolic meanings, for example to display prestige or even attract members of the opposite sex. The half-million-year mark also heralded the arrival of H. heidelbergensis, which had a much larger brain than H. erectus. Not long afterward, our African ancestors began to create a wide variety of finely crafted blades and projectile points, which allowed them to exploit their environment in more sophisticated ways, and so presumably enhance their survival and reproduction. Archaeologists refer to these tools as Middle Stone Age technology and agree that they did require mental templates. “The tools tell us that the hominid world was changing,” says Wynn. ing and were shared within groups of people. ity to hold an abstract concept in one’s head— As one moves forward in time, humans For example, the hundreds of bone and stone and, in the case of the tool, to “impose” a pre- appear able to imagine and create even more “Venus figurines” found at sites across Eura- determined form on raw material based on an elaborate tools, sharpening their evolutionsia beginning about 30,000 years ago were abstract mental template. That kind of ability ary edge in the battle for survival. By skillfully carved and follow a common motif. was probably not needed to make the earliest 260,000 years ago, for example, ancient They are widely regarded not only as sym- known tools, say Wynn and other researchers. humans at Twin Rivers in what is now Zambia bolic expression, but full-fledged art. These implements, which date back 2.6 mil- could envision a complex finished tool and Thus many researchers are reluctant to lion years, consist mostly of rocks that have put it together in steps from different compoaccept rare, one-off discoveries like the Tan- been split in two and then sharpened to make nents. They left behind finely made blades Tan or Berekhat Ram objects as signs of simple chopping and scraping implements. and other tools that had been modified— symbolic behavior. “You can imagine [an Then, about 1.7 million years ago, large, usually by blunting or “backing” one edge— ancient human] recognizing a resemblance teardrop-shaped tools called Acheulean hand to be hafted onto handles, presumably made but [the object] still hav[ing] no symbolic axes appeared in Africa. Likely created by of wood. These so-called backed tools have meaning at all,” says Philip Chase, an anthro- H. erectus and probably used to cut plants and been widely regarded as evidence of sympologist at the University of Pennsylvania. butcher animals, these hand-held tools vary bolic behavior when found at much younger Thomas Wynn, an anthropologist at the greatly in shape, and archaeologists have sites. “This flexibility in stone tool manufacUniversity of Colorado, Colorado Springs, debated whether creating the earliest ones ture [indicates] symbolic capabilities,” says agrees: “If it’s a one-off, I don’t think it required an abstract mental template. But by archaeologist Sarah Wurz of the Iziko Musecounts. It’s not sending a message to anyone.” about 500,000 years ago, ancient humans were ums of Cape Town in South Africa. creating more symmetrical Late Acheulean Similar cognitive abilities were possibly Tools of the imagination required to make the famous Given how difficult it is to detect 400,000-year-old wooden spears “If it’s a one-off, I don’t think the earliest symbolic messages in from Schöningen, Germany. One the archaeological record, some recent study concludes that these it counts. It’s not sending a researchers look instead for proxy spears’ creators—probably membehaviors that might have bers of H. heidelbergensis—carmessage to anyone.” required similar cognitive abiliried out at least eight preplanned ties, such as toolmaking. Charles steps spanning several days, —THOMAS WYNN, UNIVERSITY OF COLORADO, Darwin himself saw an evoluincluding chopping tree branches COLORADO SPRINGS tionary parallel between toolwith hand axes and shaping the making and language, probably spears with stone flakes. the most sophisticated form of The idea that sophisticated symbolic behavior. “To chip a toolmaking and symbolic flint into the rudest tool,” Darwin thought require similar cognitive wrote in The Descent of Man, skills also gets some support demands a “perfect hand” as well from a surprising quarter: brainadapted to that task as the “vocal imaging studies. Stout’s team ran organs” are to speaking. positron emission tomography To many researchers, making scans on three archaeologists— sophisticated tools and using Symbolic start. Some scientists argue that this 77,000-year-old engraved ochre all skillful stone knappers—as symbols both require the capac- shows symbolic capacity. they made pre-Acheulean and
A roaring start. Researchers agree that Chauvet Cave’s magnificent paintings, including these lions, are full-blown art.

ORIGINS
Late Acheulean tools. Both methods turned on visual and motor areas of the brain. But only Late Acheulean knapping turned on circuits also linked to language, the team reported last year. Color me red At Twin Rivers, it’s not just the tools that hint at incipient symbolic behavior. Early humans there also left behind at least 300 lumps of ochre and other pigments in a rainbow of colors: yellow, red, pink, brown, purple, and blue-black, some of which were gathered far from the site. Excavator Lawrence Barham of the University of Liverpool in the United Kingdom thinks they used the ochre to paint their bodies, though there’s little hard evidence for this. Most archaeologists agree that body painting, as well as the wearing of personal ornaments such as bead necklaces, was a key way that early humans symbolically communicated social identity such as membership in a particular group, much as people today declare social allegiances and individual personalities by their clothing and jewelry. Yet while the Twin Rivers evidence is suggestive, it’s hard to be sure how the ochre was actually used. There’s little sign that it was ground into powder, as needed for decoration, says Ian Watts, an independent ochre expert in Athens. And even ground ochre could have had utilitarian uses, says archaeologist Lyn Wadley of the University of Witwatersrand in Johannesburg, South Africa. Modern-day experiments have shown that ground ochre can be used to tan animal hides, help stone tools adhere to bone or wooden handles, and Eye of the beholder. Archaeologists debate whether this modified stone was meant to represent a woman. even protect skin against mosquito bites. “We simply don’t know how ancient people used ochre 300,000 years ago,” Wadley consider diagnostic elements of symbolic says. And since at that date the ochre users behavior came together. And in work now were not modern humans but our archaic in press, the Blombos team reports finding ancestors, some experts are leery of assign- engraved ochre in levels dating back to ing them symbolic savvy. 100,000 years ago (Science, Yet many archaeologists are 30 January, p. 569). willing to grant that our species, There are other hints that the H. sapiens, was creating and sciencemag.org modern humans who ventured Hear author using certain kinds of symbols out of Africa around this time Michael Balter by 75,000 years ago and per- discuss the roots of art at might also have engaged in symhaps much earlier. At sites such www.sciencemag.org/ bolic behavior. At the Skhul rock as Blombos Cave on South darwin. shelter in Israel, humans left Africa’s southern Cape, people 100,000-year-old shell beads left sophisticated tools, including elabo- considered by some to be personal ornarately crafted bone points, as well as perfo- ments (Science, 23 June 2006, p. 1731). At rated beads made from snail shells and the 92,000-year-old Qafzeh Cave site pieces of red ochre engraved with what nearby, modern humans apparently strongly appear to be abstract designs. At this single preferred the color red: Excavators have site, a number of what many archaeologists studied 71 pieces of bright red ochre associated with human burials. Some researchers argue that this represents an early case of “color symbolism,” citing the universal importance of red in historical cultures worldwide and the apparently great lengths to which early humans went to gather red ochre. ”There is very strong circumstantial evidence for the very great antiquity of the color red as a symbolic category,” says anthropologist Sally McBrearty of the University of Connecticut, Storrs. These finds of colorful ochre, fancy tools, and beads have convinced many researchers that the building blocks of symbolism had emerged by at least 100,000 years ago and possibly much earlier. But why? What selective advantages did using symbols confer on our ancestors? To some scientists, the question is a no-brainer, especially when it is focused on the most sophisticated form of symbolic communication: language. The ability to communicate detailed, concrete information as well as abstract concepts allowed early humans to cooperate and plan for the future in ways unique to our species, thus enhancing their survival during rough times and boosting their reproductive success in good times. “What aspects of human social organization and adaptation wouldn’t benefit from the evolution of language?” asked Terrence Deacon, a biological anthropologist at the University of California, Berkeley, in his influential book The Symbolic Species: The Coevolution of Language and the Brain. Deacon went on to list just some of the advantages: organizing hunts, sharing food, teaching toolmaking, sharing past experiences, and raising children. Indeed, many researchers have argued that symbolic communication is what held groups of early humans together as they explored new environments and endured climatic shifts. As for art and other nonlinguistic forms of symbolic behavior, they may also have been key to cementing these bonds, by expressing meanings that are difficult or impossible to put into words. In that way, artistic expression, including music, may have helped ensure the survival of the fittest. This may also explain why great art has such emotional force, because the most effective symbols are those that convey their messages the most powerfully— something the artists at Chauvet Cave seem to have understood very well.
–MICHAEL BALTER

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On the Origin of of

Photosynthesis
piece together how and when organisms first began to harness light’s energy. Although most modern photosynthesizers make oxygen from water, the earliest solar-powered bacteria relied on different ingredients, perhaps hydrogen sulfide. Over time, the photosynthetic machinery became more sophisticated, eventually leading to the green, well-oxygenated world that surrounds us today. In the lab, some biochemists are recapitulating the chemical steps that led to this increased complexity. Other researchers are locked in debates over just when this transition happened, 2.4 billion years ago or much earlier. Looking so far into the past is difficult. The geological record for that time is skimpy and tricky to interpret. Eons of evolution have blurred the molecular vestiges of the early events that remain in living organisms. But “it’s a terribly important problem,” says biochemist Carl Bauer of Indiana University, Bloomington, one well worth the travails.

Try to picture the world without photosynthesis. Obviously, you’d have to strip away the greenery—not just the redwoods and sunflowers, but also the humble algae and the light-capturing bacteria that nourish many of the world’s ecosystems. Gone, too, would be everything that depends on photosynthetic organisms, directly or indirectly, for sustenance—from leaf-munching beetles to meat-eating lions. Even corals, which play host to algal partners, would lose their main food source. Photosynthesis makes Earth congenial for life in other ways, too. Early photosynthesizers pumped up atmospheric oxygen concentrations, making way for complex multicellular life, including us. And water-dwellers were able to colonize the land only because the oxygen helped create the ozone layer that shields against the sun’s ultraviolet radiation. Oxygen-producing, or oxygenic, photosynthesis “was the last of the great inventions of microbial metabolism, and it changed the planetary environment forever,” says geobiologist Paul Falkowski of Rutgers University in New Brunswick, New Jersey. Given its importance in making and keeping Earth lush, photosynthesis ranks high on the top-10 list of evolutionary milestones. By delving into ancient rocks and poring over DNA sequences, researchers are now trying to

To catch a photon Over more than 200 years, researchers have ironed out most of the molecular details of how organisms turn carbon dioxide and water into food. Chlorophyll pigment and about 100 other proteins team up to put light to work. Plants, some protists, and cyanobacteria embed their chlorophyll in two large protein clusters, photosystem I and photosystem II. And they need both systems to use water as an electron source. Light jump-starts an electrical circuit in which The electron thief electrons flow from the photosystems Either way, it took some fancy fiddling to through protein chains that convert the primitive reaction make the energy-rich molecules THE YEAR OF centers to oxygen-generating Given its ATP and NADPH. These molephotosystems. Oxygenic photocules then power the synthesis synthesis was a huge upgrade, importance in of the sugars that organisms leading to a land of plenty, says making and depend on to grow and multiply. biochemist John Allen of Queen keeping earth Photosystem II—the strongest Mary, University of London. naturally occurring oxidant— “Water is everywhere, so the lush, photoregains its lost electrons by organisms never ran out of elecsynthesis ranks swiping them from water, genertrons. They were unstoppable.” ating oxygen as a waste product. But water clings to its elechigh on the However, some bacteria trons. With its oxidizing power, top- 10 list of don’t rely on water as an elec- This essay is the third photosystem II can wrench them monthly series. More tron source, using hydrogen sul- in aevolutionary away, but the reaction centers in on evolution online at fide or other alternatives. These blogs.sciencemag.org/ nonoxygenic photosynthesizers milestones. nonconformists, which today origins. cannot. Biochemists James

live in habitats such as scalding hot springs, don’t generate oxygen. Their photosynthetic proteins huddle in relatively simple “reaction centers” that may have been the predecessors of the two photosystems. Envisioning the steps that led to this complex biochemistry is mind-boggling. Similarities between proteins in photosynthetic and nonphotosynthetic bacteria suggest that early microbes co-opted some photosynthesis genes from other metabolic pathways. But protophotosynthesizers might also have helped each other piece these pathways together by swapping genes. Biochemist Robert Blankenship of Washington University in St. Louis, Missouri, and colleagues say they’ve uncovered traces of these lateral gene transfers by comparing complete bacterial genomes. For example, their 2002 study of more than 60 photosynthetic and nonphotosynthetic bacteria (Science, 22 November 2002, p. 1616) suggested that bugs had passed around several photosynthesis genes, including some involved in synthesizing the bacterial version of chlorophyll. Gene-sharing might also explain the puzzling distribution of the photosystems, Blankenship says. A cell needs both photosystems to carry out oxygenic photosynthesis. Yet modern nonoxygenic bacteria have the presumptive predecessor either of photosystem I or of photosystem II, never both. To explain how the two protein complexes wound up together, Blankenship favors “a large-scale lateral [gene] transfer” or even a fusion of organisms carrying each photosystem. However, other researchers remain skeptical, arguing that one photosystem evolved from the other, possibly through the duplication of genes, creating an ancient cell with both. No one knows for sure.

Allen (no relation to John Allen) and JoAnn Williams of Arizona State University, Tempe, and colleagues are working out how a bacterial reaction center could have evolved photosystem II’s appetite for electrons. Taking a hands-on approach, they have been tinkering with the reaction center of the purple bacterium Rhodobacter sphaeroides to determine if they can make it more like photosystem II. First they targeted bacteriochlorophyll, the bacterial version of chlorophyll that’s at the core of the reaction center, and altered the number of hydrogen bonds. Adding hydrogen bonds hiked the molecule’s greed for electrons, they found. The water-cleaving portion of photosystem II sports four manganese atoms that become oxidized, or lose electrons. So the team equipped the bacterial reaction center with one atom of the metal. In this modif ied version, the added manganese also underwent oxidation, the researchers reported in 2005. James Allen says that their creations aren’t powerful enough to split water. But eventually, they hope to engineer a reaction center that can oxidize less possessive molecules, such as hydrogen peroxide, that would have been present on the early Earth. Even if the researchers never replicate photosystem II, “if we def ine the intermediate stages, we’ve accomplished a lot,” he says.

Catching rays. Long before plants got in on the act, photosynthetic cyanobacteria living in pools like this one in Yellowstone National Park were changing the composition of the atmosphere.

DARWIN

says astrobiologist Roger Buick of the University of Washington, Seattle. These hints could push the origin back 600 million years or more. One line of evidence is oil biomarkers that researchers think are the remains of cyanobacteria. They’ve turned up in rocks that are up to 2.7 billion years old. And in western Australia, thick shale deposits that are 3.2 billion years old hold rich bacterial remains but no traces of sulfur or other possible electron sources, suggesting that the microbes were using water to make energy. Geologist Euan Nisbet of Royal Holloway, University of London, and colleagues found additional support for an early origin when they went searching for traces of RuBisCO, a key photosynthetic enzyme. RuBisCO feeds carbon dioxide into the reactions that yield sugars. The enzyme version found in oxygenic photosynthesizers Oxygenic photosynthesis “was the plays favorites: It prefers carbon dioxide that contains the carbonlast of the great inventions of micro12 isotope over the bulkier carbon-13. In 2007, Nisbet and bial metabolism, and it changed the his colleagues found disproportionately low carbon-13 values planetary environment forever.” indicative of RuBisCO activity —Paul Falkowski, Rutgers University when they analyzed organic matter in rocks from three sites Something in the air about 2.4 billion years ago, geologists see in Zimbabwe and Canada that are between How the photosystems got their start is cru- the first unmistakable signs of significant, 2.7 billion and 2.9 billion years old. Nisbet cial for understanding the origin of photo- sustained levels of atmospheric oxygen. concludes that oxygen-making photosynthesis. But the question that’s drawn the These signs include red beds, or layers synthesis began at least 2.9 billion years ago. most attention—and provoked the most tinged by oxidized iron, i.e., rust. Further The early-origin case isn’t ironclad. For wrangling—is when photosynthesis began. support that the GOE marks an atmospheric example, a 2008 paper that has some Most researchers accept that nonoxygenic revolution comes from a technique that researchers fuming claims that the oil biophotosynthesis arose first, probably shortly detects skewed abundances of sulfur iso- markers are contaminants that seeped in after life originated more than 3.8 billion topes that occur if the air lacks oxygen. from younger rocks. Advocates also have to years ago. “Life needs an energy source, and These imbalances persisted until the GOE, explain why it took hundreds of millions of the sun is the only ubiquitous and reliable when they vanished. years for oxygen to build up in the air. energy source,” says Blankenship. Hard-liners construe these data to mean Although the last word on the origins of The sharpest disputes revolve around that oxygenic photosynthesis could not have oxygen-making photosynthesis isn’t in, when organisms shifted to oxygenic photo- emerged until shortly before the GOE. But researchers say they are making progress. One synthesis. At issue is how to interpret a other scientists disagree. “We are finding thing is for certain, however: Without this watershed in the fossil record known as the more and more hints that oxygenic photo- innovation, Earth would look a lot like Mars. –MITCH LESLIE great oxidation event (GOE). In rocks from synthesis goes deeper into the fossil record,”
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embryo that serves as its food supply. Darwin was perplexed by the diversity of flowering plants; they were too numerous and too varied, and there were too few fossils to sort out which were more primitive. Throughout much of the 20th century, magnolia relatives with relatively large flowers were leading candidates for the most primihow flowers got started—and from which tive living flowers, although a few ancestor. Today, researchers have analytical researchers looked to small herbs instead. tools, fossils, genomic data, and insights that In the late 1990s, molecular systematics Darwin could never have imagined, all of came to the rescue, with several reports prewhich make these mysteries less abom- senting a fairly consistent picture of the inable. Over the past 40 years, techniques lower branches of the angiosperm tree. An for assessing the relationships between obscure shrub found only in New Caledonia organisms have greatly improved, and gene emerged as a crucial window to the past. sequences, as well as morphology, now help Amborella trichopoda, with its 6-millimeter researchers sort out which angiosperms greenish-yellow flowers, lives deep in the arose early and which arose late. New fossil cloud forests there. In multiple gene-based finds and new ways to study them—with assessments, including an analysis in 2007 synchrotron radiation, for example—pro- of 81 genes from chloroplast genomes vide a clearer view of the detailed anatomy belonging to 64 species, Amborella sits of ancient plants. And researchers from var- at the base of the angiosperm family tree, ious fields are figuring out genomic changes the sister group of all the rest of the that might explain the amazing success of angiosperms. this fast-evolving group. Given that placement, Amborella’s tiny These approaches have given researchers flowers may hint at what early blossoms a much better sense of what early flowers were like. It’s one of “the most similar living were like and the relationships among them. flower[s]” to the world’s first flower, says But one of Darwin’s mysteries remains: the James Doyle of the University of Californature and identity of the angiosperm ances- nia, Davis. The petals and sepals of its sintor itself. When flowering plants show up in gle-sex flowers are indistinguishable and the fossil record, they appear with a bang, vary in number; so too do the numbers of with no obvious series of intermediates, as seed-producing carpels on female flowers Darwin noted. Researchers still don’t know and pollen-generating stamens on male which seed- and pollen-bearing flowers. The organs are spirally organs eventually evolved into THE YEAR OF arranged, and carpels, rather the comparable flower parts. than being closed by fused tisFor more on “We’re a bit mystif ied,” says sue as in roses and almost all botanist Michael Donoghue of familiar flowers, are sealed by a flower origins, Yale University. “It doesn’t secretion. listen to a appear that we can locate a close Most genetic analyses showed relative of the flowering plants.” that water lilies were the next podcast by branch up the angiosperm tree, author Elizabeth Seeking the first flower followed by a group represented One of two major living groups by star anise, which also has a Pennisi at of seed plants, angiosperms have primitive look about it, says “covered” seeds that develop This essay is the fourth Doyle, “though each of these www. encased in a protective tissue in a monthly series. has deviations from the ancesFor more on evolutionary sciencemag. called a carpel (picture a bean topics online, see the tral type.” pod). That’s in contrast to the Origins blog at org/ nonflowering gymnosperms, blogs.sciencemag.org/ Fossil records origins. For more on multimedia/ such as conifers, which bear flower origins, listen Although some fossil pollen naked seeds on scales. An to a podcast by author dates back 135 million years, no podcast.at Elizabeth Pennisi angiosperm’s carpel sits at the www.sciencemag.org/ credible earlier fossil evidence center of the flower, typically multimedia/podcast. exists. In Darwin’s day, and for surrounded by pollen-laden stamany decades afterward, palemens. In most flowers, the carpel and stamens obotanists primarily found leaves or pollen are surrounded by petals and an outer row of but almost no fossil flowers. They had the leaflike sepals. Seeds have a double coating wrong search image, says Else Marie Friis of as well as endosperm, tissue surrounding the the Swedish Museum of Natural History in Stockholm. “When we started, the search profile was bigger, a magnolia [flower],” she recalls. But 30 years ago, she and others discovered tiny ancient flowers by sieving through sand and clay sediments. With this technique, they have now collected hundreds of millimeter-size flowers, some preserved in three dimensions, from Portugal and other locations with Cretaceous deposits 70 million to 120 million years old. This fossil diversity shows that angiosperms were thriving, with several groups well-established, by 100 million years ago. In some, the flower parts are whorled like those of modern flowers; in others they are spiraled, considered by some researchers as the more primitive arrangement. Some flower fossils have prescribed numbers of petals, another modern feature, whereas in others the petal count varies. In 1998, Chinese geologist Ge Sun of Jilin University in Changchun, China, came across what seemed to be a much older flower. The fossil, called Archaefructus, was an aquatic plant that looked to be 144 million years old. By 2002, Sun and David Dilcher of the Florida Museum of Natural History (FLMNH) in Gainesville had described an entire plant, from roots to flowers, entombed on a slab of rock unearthed in Liaoning in northeastern China. In one sense, Archaefructus wasn’t much to look at. “It’s a flowering plant before there were flowers,” Dilcher notes. It lacked petals and sepals, but it did have an enclosed carpel. When Kevin Nixon and colleagues at Cornell University compared its traits with those same traits in 173 living plants, Archaefructus came out as a sister to living angiosperms and closer to the common ancestor than even Amborella. Archaefructus’s distinction was shortlived, however. Within months, better dating of the sediments in which it was found yielded younger dates, putting this f irst flower squarely with other early fossil flower parts, about 125 million years old. Also, a 2009 phylogenetic analysis of 67 taxa by Doyle and Peter Endress of the University of Zurich, Switzerland, placed the fossil in with water lilies rather than at the base of the angiosperms, although this conclusion is contested.

On the Origin of of

Flowering Plants

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Out of the past. Tiny Amborella sits at the bottom of the angiosperm family tree.

IN 1879, CHARLES DARWIN PENNED A LETTER

to British botanist Joseph Dalton Hooker, lamenting an “abominable mystery” that threw a wrench into his theory of evolution: How did flowering plants diversify and spread so rapidly across the globe? From rice paddies to orange groves, alpine meadows to formal gardens, prairies to oakhickory forests, the 300,000 species of angiosperms alive today shape most terrestrial landscapes and much of human life and culture. Their blooms color and scent our world; their fruits, roots, and seeds feed us; and their biomass provides clothing, building materials, and fuel. And yet this takeover, which took place about 100 million years ago, apparently happened in a blink of geological time, just a few tens of millions of years. The father of evolution couldn’t quite fathom it. Darwin had an “abhorrence that evolution could be both rapid and potentially even saltational,” writes William Friedman in the January American Journal of Botany, which is devoted to this “abominable mystery.” Throughout his life, Darwin pestered botanists for their thoughts on the matter, but they couldn’t give him much help. Now, 130 years later, evolutionary biologists are still pestering botanists for clues about what has made this plant group so successful, as well as when, where, and

DARWIN

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“We are realizing that this huge diversity is probably the result of one innovation piled on top of another innovation.”

from one of the nonflowering seed plants or gymnosperms, whose heyday was 200 million years ago. Modern gymnosperms include conifers, ginkgoes, and the cycads, with their stout trunks and large fronds. Before angiosperms came along, these plants were much more diverse and included cycadlike species, such as the extinct Bennettitales, and many woody plants called Gnetales, of which —Peter Crane, a few representatives, including the University of Chicago joint firs, survive today (see family tree, p. 31). Also common in the Jurassic were These fossils often spark debate because seed ferns, a group now long gone; their specimens tend to be imperfectly preserved most famous member is Caytonia, which and leave room for interpretation. To help seems to have precarpel-like structures. remedy that, Friis and her colleagues have These g roups’ perceived relevance to begun to examine flowers using synchro- flower evolution and their relationships to tron radiation to generate a 3D image of angiosperms have ping-ponged between their inner structures, allowing the fossil to camps, depending on how the evolutionary remain intact while Friis peers inside it trees were constructed. from many angles (Science, 7 December In the mid-1980s, Peter Crane, now at 2007, p. 1546). “We can get fantastic reso- the University of Chicago in Illinois, prolution,” says Friis. “It’s really exciting.” But posed a solution, the anthophyte hypothesis. so far, the flowers Friis finds are Using several lines of evidence and noting too diverse to trace back to a that both Bennettitales and particular ancestor. “From Gnetales organize their male these fossils, we cannot and female organs together say what is the basic in what could be conform,” she says. strued as a preflower, he considered them, Before flowers along with angiosperms, Although they have yet as comprising a single to find the oldest fossil angiosperm entity called Larger than life. Although merely flowers, researchers anthophytes. For the next 2.2 millimeters in diameter, this 3D assume that the ancesdecade, most family trees fossil flower shows that grasses date tral angiosperm evolved based on morphology supback to 94 million years ago.
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ORIGINS

ORIGINS
such a causal relationship is not settled. Later, animals that ate fruit and SEED PLANT Paleozoic seed ferns dispersed seeds likely helped evolvPHYLOGENY ing species expand quickly into new Asterids » territory. Some think the answer lies Eudicots in genes: duplications that gave the angiosperm genome opportunities to Rosids try out new floral shapes, new chemical attractants, and so forth. This Monocots flexibility enabled angiosperms to exploit new niches and set them up for long-term evolutionary success. Magnolias » “My own view is that in the past, we have looked for one feature,” says Crane. Now, “we are realizing that Water lilies this huge diversity is probably the result of one innovation piled on top ? of another innovation.” Archaefructus » The latest insights into diversification come from gene studies. From Amborella 2001 to 2006, Pamela Soltis of the FLMNH and Claude dePamphilis ? of Pennsylvania State University, Caytonia University Park, participated in the Floral Genome Project, which ? Bennettitales searched for genes in 15 angiosperms. Now as a follow-up, the Ancestral Angiosperm Genome Project looks at gene activity in five early angioCycads sperms and a cycad, a gymnosperm. DePamphilis and his colleagues Ginkgoes » matched all the genes in each species against one another to deter? Gnetales mine the number of duplicates. They then looked at the number of differences in the sequences of each gene Conifers » pair to get a sense of how long ago Extinct taxa the duplication occurred. In most early angiosperms, including water lilies and magnolias, they saw many Shifting branches. As this simplified family tree shows, gene studies have helped clarify the relationships of many simultaneous duplications—but not living angiosperms, but fitting in extinct species is still a challenge, and some nodes are hotly debated. in Amborella, they reported in the January 2009 American Journal of Botany, The Floral Genome Project also looked are not as well-defined as they are in Araconfirming earlier reports. The data suggest to see whether the genetic programs guiding bidopsis. This sloppiness may have made that a key genome duplication happened flower development were consistent development flexible enough to undergo after the lineage leading to Amborella split throughout the angiosperms. “We found that many small changes in expression patterns off but before water lilies evolved. “We’re there are fundamental aspects that are con- and functions that helped yield the great beginning to get the idea that polyploidiza- served in the earliest lineages,” says Soltis. diversity in floral forms. tion may have been a driving force in creat- “But there are differences in how the genes In his letter to Hooker, Darwin wrote ing many new genes that drive floral devel- are deployed.” that he would like “to see this whole probopment,” dePamphilis says. Take the avocado, a species on the lower lem solved.” A decade ago, Crepet thought Others have noted that a duplication branches of the angiosperm tree. In most Darwin would have gotten his wish by now. occurred in the evolution of grasses, and the angiosperms, the flower parts are arranged in That hasn’t happened, but Crepet is optiFloral Genome Project confirms that yet concentric circles, or whorls, around the mistic that he and his colleagues are on the another duplication paved the way for eudi- carpels, with stamens innermost, then petals, right track, as analyses of various kinds of cots, the group that includes apples, roses, and finally sepals. Each tissue has its own data become more sophisticated. “We are beans, tomatoes, and sunflowers. “There are distinct pattern of gene expression, but not less likely to go around in circles in the next some real ‘hot spots’ in angiosperm evolu- in the avocado. Genes that in Arabidopsis 10 years,” he says. “I believe a solution to tionary history,” says dePamphilis, who is are active only in, say, the developing petals the problem is within reach. … The mystery working to fully sequence the genome of spill over in avocado to the sepals. Thus in is solvable.” –ELIZABETH PENNISI Amborella with his colleagues. the more primitive plants, petals and sepals

Angiosperms

Flowers, food, fuel. Darwin marveled at the diversity of angiosperms. Given that they represent nine in 10and sense of beauty. surprise that they serve as fuel. Darwin marveled at the diversity of angiosperms. Given mainstays of both our welfare land plants, it’s no Clockwise from left: aspens, mainstays of both our welfareland plants,of beauty. Clockwisethey serve left: aspens, orchids, grasses, sunflowers, tulips,walnuts. walnuts. that they represent nine in 10 and sense it’s no surprise that from top as orchids, grasses, sunflowers, tulips, apples, apples,

ported this idea. Crane and others carefully dissected and described fossils of these groups, looking for the precursors to carpels, the seed’s double coat, and other distinctive angiosperm traits. But they have run into problems. “We do not really know how to compare them because the structures are very differentlooking; figuring out what’s homologous is quite a difficult thing,” says Crane. He and his colleagues argue, for example, that the seeds in the Bennettitales have two coverings, which may be a link to angiosperms. But in the January American Journal of Botany, Gar Rothwell of Ohio University, Athens, and two colleagues disagree, saying that what Crane calls the outer layer is the only layer, and f ind fault with the hypothesis in general. To make matters worse for anthophyte proponents, genebased evolutionary trees break up this grouping, pulling the Gnetales off any angiosperm branch and placing them among or next to the other gymnosperms. “The molecular work points in one direction; the paleobotanical

work points you in another direction,” Crane says. And if the molecular work is correct, then the field doesn’t know in which direction to turn, because in most analyses the genetic data don’t place any living plant close to angiosperms. The angiosperms group together, the living gymnosperms group together, and there’s nothing in between. “The nonangiosperm ancestor just isn’t there,” says paleobotanist William Crepet of Cornell. “I’m starting to worry that we will never know, that it transformed without intermediates.” Seeds of success The angiosperm’s ancestor may be missing, but what is very clear—and was quite annoying to Darwin—is that the angiosperm prototype so readily proved a winner. Seed ferns and other gymnosperms arose about 370 million years ago and dominated the planet for 250 million years. Then in a few tens of millions of years, angiosperms edged them
Inside and out. Synchrotron radiation helped produce a 3D rendering (gold) of this fossil male flower (right) and insights into its internal structure.

out. Today, almost nine in 10 land plants are angiosperms. The exact timing of the angiosperms’ explosion and expansion is under debate, as is the cause. At least one estimate based on the rate at which gene sequences change—that is, the ticking of the molecular clock— pushes angiosperm evolution back to 215 million years ago. “There appears to be a gap in the fossil record,” says Donoghue, who also notes that molecular dating methods “are still in their infancy” and, thus, could be misleading. He and others think that flowering plants lingered in obscurity for tens of millions of years before radiating toward their current diversity. Whatever the timing, there was something special about the angiosperm radiation. During the 1980s and again in 1997, Cornell’s Karl Niklas compiled a database showing the first and last occurrences of fossil plants. When he and Crepet used that and more recent information to look at species’ appearances and disappearances, they found that new angiosperms appeared in bursts through time, whereas other plants, such as gymnosperms, radiated rapidly only at first. Moreover, angiosperms proved less likely to disappear, somehow resisting extinction, says Crepet. Once the angiosperms arrived, how did they diversify and spread so quickly? Darwin suspected that coevolution with insect pollinators helped drive diversification, though

Living gymnosperms

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TIVES PERSPECTIVES
HISTORY OF SCIENCE HISTORY OF SCIENCE HISTORY OF SCIENCE

E

vonAlexander von Humboldt and Humboldt and the General Physics of l Physics of the Earth the Earth
Stephen T. Jackson Stephen T. Jackson Stephen T. Jackson

In the early 19th century, Alexander von In the early 19th century, Alexander von In the early 19th century, Alexander century, Alexander von In the early 19th von Humboldt laid the foundations for today’s Humboldt for today’s Humboldt laid the foundations for today’s Humboldt laid the foundationslaid the foundations for today’s Earth system sciences. Earth system sciences. Earth system sciences.

Earth system sciences.

RIGINAL COPY IN THE NATURAL HISTORY MUSEUM, PARIS

s scientists are celebrating the 200th s scientists are celebrating the 200th s scientists are celebrating the 200th anniversary of Charles Darwin’s birth anniversary of Charles Darwin’s birth anniversary of Charles Darwin’s birth rating the 200thand the 150th anniversary of the puband the 150th anniversary of the puband the 150th anniversary of the publication of his On the Origin of Species, s Darwin’s birthof his On the Origin of Species, lication lication of his On the Origin of Species, Darwin’s ideas continue to shape and enrich rsary of the pub- ideas continue to shape and enrich Darwin’s Darwin’s ideas continue to shape and enrich the sciences (1). 6 May 2009 marks the 150th the sciences the sciences (1). 6 May 2009 marks the 150th gin of Species, (1). 6 May 2009 marks the 150th anniversary of the death of another 19th-cenanniversary of the death another 19th-cenanniversary of the death of another 19th-cenhape andtury figure—Alexanderofvon Humboldt— enrich tury figure—Alexander von Humboldt— tury figure—Alexander von Humboldt— marks the 150th whose scientific legacy also flourishes in the whose scientific legacy also flourishes in the whose scientific legacy also flourishes in the 21st century. Humboldt helped create the nother 19th-cen21st century. Humboldt helped create the 21st century. Humboldt helped create the intellectual world Darwin inhabited, and his n Humboldt— world Darwin inhabited, and his intellectual intellectual world Darwin inhabited, and his writings inspired Darwin to embark on writings writings inspired Darwin to embark on flourishes in the inspired Darwin to embark on H.M.S. Beagle. More pertinent to our time, H.M.S. Beagle. More pertinent to our time, H.M.S. Beagle. More pertinent to our time, lped create the established the foundation for the Humboldt established the foundation for the Humboldt Humboldt established the foundation for the habited, Earthhis sciences: the integrated system and system sciences: the integrated system Earth system Earth system sciences: the integrated system of knowledge on which human society may to embark on of knowledge on which human society may of knowledge on which human society may depend in the face of global climate change. depend in ent to our time, the face of global climate change. depend in the face of global climate change. Like Darwin, Like Darwin, Humboldt undertook a undationmajor voyage that Humboldt undertook a forLike Darwin, Humboldt undertook a the major voyage that would shape his ideas would shape his ideas major voyage that would shape his ideas tegrated and thinking. Humboldt spent 5 years (1799 system and thinking. Humboldt spent 5 years (1799 and thinking. Humboldt spent 5 years (1799 man society1804) with botanist Aimé Bonpland explorto 1804) with botanist Aimé Bonpland explorto may to 1804) with botanist Aimé Bonpland exploring Venezuela, the northern Andes, and cenlimate change. ing Venezuela, the northern Andes, and cening Venezuela, the northern Andes, and central Mexico, with visits to Tenerife, Cuba, and tral Mexico, dt undertook a with visits to Tenerife, Cuba, and tral Mexico, with visits to Tenerife, Cuba, and the United States. They collected botanical, the United States. They collected botanical, the United States. They collected botanical, hape his ideas geological, and ethnological speczoological, geological, and ethnological speczoological, zoological, geological, and ethnological specnt 5 years (1799 extensive atmospheric and geoimens, made extensive atmospheric and geo- Intellectual riches. The central portion of Humboldt’s Physical Tableau of the Andes and Neighboring imens, made imens, made extensive atmospheric and geo- Intellectual riches. The central portion of Humboldt’s Physical Tableau of the Andes and Neighboring Intellectual riches. The central portion of Humboldt’s Tableau of the Andes and Bonplandphysical measurements, and recorded the Countries, published as part of (2, 3), shows Chimborazo inPhysicalwith vegetation zones, plantNeighboring explorphysical measurements, and recorded the Countries, published as part of (2, 3), shows Chimborazo in profile, with vegetation zones, plant species, and physical measurements, and recorded the Countries, published as part of (2, 3), shows Chimborazo in profile, with vegetation zones, plant species, and profile, species, and geographic location of their thousands of Andes, and cen- location of their thousands of snowline depicted at appropriate elevations. In the original, the profile is flanked on both sides by tables geographic geographic location of their thousands of snowline depicted at appropriate elevations. In the original, the profile is flanked on both sides by tables snowline depicted at appropriate elevations. In the original, the profile is flanked on both sides by tables specimens and tens of thousands of measure- describing elevational patterns in temperature, humidity, light refraction and intensity, agriculture, fauna, and specimens specimens and tens of thousands of measure- describing elevational patterns in temperature, humidity, light refraction and intensity, agriculture, fauna, and erife, Cuba, and and tens of thousands of measure- describing elevational patterns in temperature, humidity, light refraction and intensity, agriculture, fauna, and ments. Humboldt spent the next 22 years and other physical, chemical, and biological features. ments. Humboldt spent the next 22 years and ments. Humboldt spent the next 22 years and other physical, chemical, and biological features. ected botanical,his inherited fortune in Paris, pre- other physical, chemical, and biological features. most of his inherited fortune in Paris, premost of most of his inherited fortune in Paris, prehnological spec- publishing 45 volumes of a never- distribution of incident radiation, the transport serving as both an index of climate and a proxparing and publishing 45 volumes of a never- distribution of incident radiation, the transport serving as both an index of climate and a proxparing and paring and publishing 45 volumes of a never- distribution of incident radiation, the transport serving as both an index of climate and a proxspheric and geo-report on his travels. The central portion ofportion ofmaterials in windsthe Andes andcur-of the Andes and microclimate, animal habitat, finished report on his travels. finished of heat and Humboldt’s Physicalocean Neighboring control of microclimate, heat and Physical Tableau of and Tableau imal control published as part finished report on his travels. of heat and materials in winds and ocean cur- imal control of Neighboring animal habitat, Intellectual riches. Intellectual riches. The centralofHumboldt’smaterials in winds and ocean cur- imal Countries,of microclimate, animal habitat, Of these volumes,shows Chimborazo in work with vegetation zones, plant temperature on plant and cultural practices (6–8). the first was a slim work rents, the influence of temperature on plant and cultural practices (6–8). d recordedOf these volumes, thepublisheda as part of (2,rents, the influence of species, and snowline depicted atcultural practices (6–8). the of (2, 3), appropriate first was slim work Of these volumes, the first was a slim profile, rents, the influence of temperature on plant andzones, plantelevations. and Countries, 3), shows Chimborazo in profile, with vegetation Humboldt’s species, entitled Essay on the Geography of flanked In on the Geography of Plants the profile is Plants form, and the effect of latitude and continenentitled form, and tables describing elevationalcontineneffect of latitude and patterns of latitude dream entitled Essay on the Geography of Plants form, and the effect original, the profile is flankedHumboldt’s dream of systematic observaHumboldt’s dream of systematic observair thousands ofEssay the original, intensity, agriculture, on both sides bytheIn thechemical, andand continen-in temperature, humidity, lightof systematic observasnowline elevations. on both sides by refraction and fauna, and other physical, (2, 3). The modest title depicted at appropriatetality on mountain snowline. biological features.tional arrays across the tablestook hold in the (2, 3). The modest title belies the intellectual tality on mountain snowline. belies tional arrays across the globe took hold in the globe (2, 3). The modest title belies the intellectual tality on mountain snowline. tional arrays across the globe took hold in the nds of measure-within. In the text and the intellectual in temperature, humidity, light refraction and intensity, agriculture, fauna,the century, countless describing elevational patterns and richness within. In the text and accompanying He expanded this vision in the succeeding 19th century. Throughout the century, countless richness accompanying He expanded this vision in the succeeding 19th century. Throughout richness within. In the text and accompanying He expanded this vision in the succeeding 19th century. Throughout the century, countless ext 22 years and (see the figure), Humboldt lays out years, features. international cooperative Humboldt-inspired explorations were launched, other figure), Humboldt lays out years, establishing international cooperative Humboldt-inspired explorations were launched, physical, chemical, and biological color plate (see the figure), Humboldt lays out years, establishing international cooperative Humboldt-inspired explorations were launched, color plate color plate (see the establishing a vision of a comprehensive “general physics networks of meteorological and geomagnetic each involving systematic measurement and e in Paris, pre-of a comprehensive “general physics networks of meteorological and geomagnetic each involving systematic measurement and a vision of a comprehensive “general physics networks and his writings inspired Darwin to each involving geophysical measurements, a vision s scientists are celebrating the 200th inhabited, of meteorological and geomagnetic atmospheric andsystematic measurement and of the Earth” aimed at nothing less than a radiation, the transport umes of a never- distribution of less than a birth embark on H.M.S. Beagle.inventing isothermsindex of climate and a prox- location of their of the Earth” aimed at nothing incident syn- measurement stations, inventing isotherms mapping of physical, biological, and often culsyn- measurement stations, inventing both an mapping of physical, biological, of the Earth” aimed at nothing less than a syn- measurement stations,serving asisotherms and recorded the geographic and often culMore pertinent to our mapping of physical, biological, and often culanniversary of thesis of atmospheric,Charles Darwin’s thesis of atmospheric, oceanic, geological, time,other graphical devices to portray spatial tural features of landscapes and oceans (8–10). oceanic, geological, and other graphical devices to portray of microclimate, animal habitat, oceans (8–10). geological, and other graphical devices to foundation for tural features of landscapes and of thousands and ocean curspatial tural features of landscapes tens thesis of atmospheric, oceanic, of thein winds andHumboldt established the portray spatial thousands of specimens andand oceans (8–10). of heat and materials publiimal control and the 150th anniversary ecological, and cultural phenomena across the patterns, and noting that plant form is often These surveys were relentlessly inductive, typecological, rents, the of Species, Darwin’s patterns, and noting that plant form system ecological, On cultural phenomena across the patterns, and noting that plant form practicesThese surveys were relentlessly inductive, 22 Humboldt spent the cation of and the Origin influence of the the Earth system sciences: thecultural is often These surveys were relentlessly inductive, typwas a slim workhisand cultural phenomena acrosstemperature on plantlocal environment is often of measurements. detailed descriptive nexttypand integrated (6–8). globe. Humboldt’s obsession with geographi- better predicted by local environment than by ically producing detailed descriptive reports globe. Humboldt’s obsession geographi- better predicted which environment than by icallyand most of his inherited fortune in than by ically producing detailed producing reports globe. Humboldt’s obsession withthe to shape and enrich geographi- better predicted by raphy ofideas continueform, and thewithandsciences of knowledge on by localparadox resolved dream of little integration withindescriptivetheParis, Plants effect of latitude and continen- (a human society may de- yearslittle integration within or among the comHumboldt’s by with little integration withinor among the comsystematic observa- among reports cally referenced measurements and collec- taxonomic affinity (a paradox resolved by with cally referenced measurements collec- taxonomic affinity with cally referenced measurements and collec- taxonomic affinity (a climate resolved (1). 6 May 2009 marks the 150th anniversary of pend in the face of globalparadox change. by preparing and publishing 45 or volumes of a comnevtions was central to his vision. He recognized Darwin). Humboldt’s genius lay in his geo- ponent entities. However, for a few intellectus the intellectualof another 19th-centuryHe recognized Darwin). Humboldt’s genius lay in hismajor the globe tookHowever, thea few intellectutional arrays across ponent entities. hold in for tions was tality his vision. figure—Alextions was central to on mountain snowline. the death central to his vision. He recognized Darwin). Humboldt’s genius lay in his geo- er-finished reportHowever, for a few intellectuLike Darwin, Humboldt undertook a geo- ponent entities. on his travels. that spatial arrays of observations could be graphical vision, and in his intuition that ally nimble participants—including Charles that von in his and thinking. d accompanying Humboldt—whose scientific vision ingraphical vision,shape19th century. Throughout the century, countlesswas a slim work He observations could be the succeeding that spatial arrays of observations could be graphical would and in ideasintuition that ally nimble participants—including Charles Of these participants—including Charles anderspatial arrays ofexpanded this legacy voyage thatvision, and his his intuition that ally nimble volumes, the first aggregated to reveal patterns that would in Earth’s land surface, oceans, atmosphere, and Darwin, T. H. Huxley, Matthew Maury, Asa aggregated to reveal patterns that international cooperative aggregated to in the patterns that would in Earth’s land surface, oceans, atmosphere, and Darwin, T. H. Huxley, Matthew Maury, Asa umboldt also reveal underlying21st century. Humboldt Humboldt spent 5 an oceans, atmosphere,with explorationsH. on the Geography Kropotkin— lays flourishes revealestablishingwouldthe Earth’s land form years (1799 to 1804) with entitled EssayMerriam, and Peter of PlantsAsa out years, processes—such as in inhabitants surface, integrated whole, and Gray, C. Hart Huxley, Matthew Maury, (2, Humboldt-inspired Darwin, T. were launched, turn reveal underlying processes—such as the botanist Aimé Bonpland exploring Venezuela, 3). The modest title belies the intellectual richturn inhabitants form an integrated whole, with Gray, C. Hart Merriam, and turn reveal underlying processes—such as the inhabitants form an integrated whole, with Gray, C. Hart Merriam, and Peter Kropotkin— the intellectual world Darwin “general helped createnetworks of meteorological and geomagnetic various components systematic measurementand Peter Kropotkin— physics each involving linkages among the various components (4, these explorations provided data and experilinkages among the (4, these explorations provided data and experilinkages among the various components (4, these explorations provided data and experithe northern Andes, and central Mexico, with ness within. In the text and accompanying color g less than a syn- measurement stations, inventingto Tenerife,generaland the United States. plate that spurred the development of biogeogisotherms mappingof the Earth ence that spurred the development of out a vioften cul5). Humboldt’s general physics of the Earth biological, andthe development of biogeog5). Humboldt’s Cuba, physics of physical, ence (see the figure), Humboldt lays biogeogvisits 5). Humboldt’s general physics of the Earth ence that spurred Botany Department and Program in Ecology, University of Botany Department in Ecology, University of Botany Department and Program in Ecology, University of raphy, ecology, oceanography, and other envinic, geological,Laramie,andother graphical jackson@ to portray spatial astural features of landscapesecology, oceanography, and other of the and Program USA. E-mail: jackson@ envisioned climate as a major control of sion of ecology, oceanography, and other enviand oceans (8–10). physics enviWyoming, Laramie, WY 82071, USA. E-mail: devices They collected botanical, zoological,control of envisioned climate a major control of raphy, envisioned climate as a major geological, raphy, a comprehensive “general Wyoming, WY 82071, Wyoming, Laramie, WY 82071, USA. E-mail: jackson@ uwyo.edu Earth-surface phenomena, with vegetation ronmental sciences (11). uwyo.edu Earth-surface phenomena, made extensive ronmental sciences (11). omena across the patterns, and noting that plant form is often These surveys were relentlessly inductive,less than a synthesis of and ethnological specimens, with vegetation Earth” aimed at nothing typuwyo.edu Earth-surface phenomena, with vegetation ronmental sciences (11).

A

atmospheric, oceanic, geological, ecological, and cultural phenomena across the globe. Humboldt’s obsession with geographically referenced measurements and collections was central to his vision. He recognized that spatial arrays of observations could be aggregated to reveal patterns that would in turn reveal underlying processes—such as the distribution of incident radiation, the transport of heat and materials in winds and ocean currents, the influence of temperature on plant form, and the effect of latitude and continentality on mountain snowline. He expanded this vision in the succeeding years, establishing international cooperative networks of meteorological and geomagnetic measurement stations, inventing isotherms and other graphical devices to portray spatial patterns, and noting that plant form is often better predicted by local environment than by taxonomic affinity (a paradox resolved by Darwin). Humboldt’s genius lay in his geographical vision, and in his intuition that Earth’s land surface, oceans, atmosphere, and inhabitants form an integrated whole, with linkages among the various components (4, 5). Humboldt’s general physics of the Earth envisioned climate as a major control of Earth-surface phenomena, with vegetation serving as both an index of climate and a proximal control of microclimate, animal habitat, and cultural practices (6–8). Humboldt’s dream of systematic observational arrays across the globe took hold in the 19th century. Throughout the century, countless Humboldt-inspired explorations were launched, each involving systematic measurement and mapping of physical, biological, and often cultural features of landscapes and oceans (8–10). These surveys were relentlessly inductive,

typically producing detailed descriptive reports with little integration within or among the component entities. However, for a few intellectually nimble participants—including Charles Darwin, T. H. Huxley, Matthew Maury, Asa Gray, C. Hart Merriam, and Peter Kropotkin— these explorations provided data and experience that spurred the development of biogeography, ecology, oceanography, and other environmental sciences (11). Unfortunately, the conceptual unification among the sciences of the Earth that Humboldt sought never developed in the century following his death. Disciplinary specialization played a large role in eclipsing Humboldt’s integration, as did 20th-century trends toward reductionism, experimentalism, and fine-scale processes in many disciplines. A new incarnation of Humboldt’s general physics of the Earth began to emerge with the plate tectonics revolution in the 1960s. Drawing on Humboldtian spatial arrays of observations, this theory provided a unified explanatory framework for disparate geophysical, geological, paleontological, and biogeographic phenomena. Today, a second, even broader manifestation of Humboldt’s vision aspires to understand the interactions and feedbacks among the components of the Earth system, encompassing the lithosphere, atmosphere, hydrosphere, cryosphere, and biosphere as well as human societies and economies. This effort is often referred to as Earth system science, but it could just as well be designated “general physics of the Earth,” using the early-19th century definition of physics as the study of the material world and its phenomena (which we now call science).

Global environmental change may be the greatest challenge faced by human societies since the advent of agriculture. Humboldt advocated for science that spoke to human needs and concerns (5). It is fitting that on the 150th anniversary of his death, we recognize his role in fostering the sciences that speak to the most profound human concerns—sustainability of human societies and the ecosystems on which they depend.
1. P. J. Bowler, Science 323, 223 (2009).[Abstract/ Free Full Text] 2. A. de Humboldt, Essai sur la géographie des plantes (Levrault, Schell & Co., Paris, 1807). 3. An English translation of (2) is currently in press at the University of Chicago Press, Chicago. 4. A. de Humboldt, Personal Narrative of Travels to the Equinoctial Regions of the New Continent, During the Years 1799–1804, by Alexander de Humboldt and Aime Bonpland; with Maps, Plans, &c. (Longman, Hurst, Rees, Orme, & Brown, London, 1814 to 1829), vols. 1 to 7. 5. A. von Humboldt, Cosmos: A Sketch of the Physical Description of the Universe (Johns Hopkins Univ. Press, Baltimore, 1997), vol. 1. 6. M. Nicolson, Hist. Sci. 25, 167 (1987). [ISI] 7. M. Nicolson, in Romanticism and the Sciences, A. Cunningham, N. Jardine, Eds. (Cambridge Univ. Press, Cambridge, 1990), p. 169. 8. M. Dettelbach, in Cultures of Natural History, N. Jardine, et al., Eds. (Cambridge Univ. Press, Cambridge, 1996), p. 287. 9. S. F. Cannon, Science in Culture: The Early Victorian Period (Dawson, New York, 1978). 10. W. H. Goetzmann, New Lands, New Men: America and the Second Great Age of Discovery (Viking, New York, 1986). 11. P. J. Bowler, The Norton History of the Environmental Sciences (Norton, New York, 1993).

References and Notes

CREDIT: REPRODUCED FROM AN ORIGINAL COPY IN THE NATURAL HISTORY MUSEUM, PARIS CREDIT: REPRODUCED FROM AN ORIGINAL COPY IN THE NATURAL HISTORY MUSEUM, PARIS CREDIT: REPRODUCED FROM AN ORIGINAL COPY IN THE NATURAL HISTORY MUSEUM, PARIS

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In the early 19th century, Alexander von Humboldt laid the foundations for today’s Earth system sciences.

with geographi14 596 596 ents596 collecand

better predicted by local environment than by ically producing detailed descriptive reports 1 MAY 2009 VOL 324 SCIENCE www.sciencemag.org 1 paradox VOL 324 SCIENCE www.sciencemag.org 1 MAY 2009 VOL 324 SCIENCE www.sciencemag.org taxonomic affinity (a MAY 2009 resolved by with little integration within or among the com-

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BOOKS ET AL.
HISTORY OF SCIENCE

BOOKS ETAL.
mer students who challenged his ideas as they gained intellectual independence, and debated the pro-evolution (but anti-Haeckel) Jesuit priest and entomologist Erich Wasby Robert J. Richards mann—the list could go on University of Chicago and on. These were not isoPress, Chicago, 2008. duced important books. Robert lated episodes but rather 579 pp. $39, £27. J. Richards, the director of the moments in a lifelong camISBN 9780226712147. University of Chicago’s Fishpaign to advance his philosobein Center for the History of phy, which was accompanied H. G. Bronn, Science and Medicine and a by a bitter hostility to orgaErnst Haeckel, and much-published author on Darwin nized religion. the Origins of and German Romantic biology, Richards does not negGerman Darwinism has written a biography of Haeclect Haeckel’s science proA Study in Translation kel. Sander Gliboff, a professor per, treating us to fascinatand Transformation in Indiana University’s Departing and original discussions ment of History and Philosophy of his pathbreaking systemby Sander Gliboff of Science, places Haeckel at the atic and phylogenetic work MIT Press, Cambridge, MA, end of a study that examines the on radiolaria and other marine 2008. 271 pp. $35, £22.95. larger process through which organisms, the importance ISBN 9780262072939. Darwin’s words were translated, of linguistic analysis to his and his ideas modified, in the phylogenetic trees of the context of German biology. Both illuminate races of humans, and his remarkable experithe twists and turns that evolutionary thought mental work with siphonophores. These contook in Germany, but they do so in dramati- stitute important contributions to our undercally different ways. standing of the technical development of Richards’s book, though over twice as long evolutionary biology. as Gliboff’s, is the more entertaining read of The big picture here, however, is an arguthe two. In his characteristically rich and ment about the power of personality—at least rolling prose, Richards weaves a compelling one personality—to shape the course of scistory of a life marked by tragedy and of an ence. In Richards’s presentation, German evointense, larger-than-life figure whose passions lutionism was profoundly shaped by both drove his scientific research and philosophy. In Haeckel’s charisma and his combativeness. Richards’s rendering, the scientific Haeckel Perhaps the late-19th-century opposition of cannot be understood separately from the evolutionary science to Christianity would not man’s personality and private circumstances. have been so fiery, he suggests, had Haeckel His love of nature was surpassed only by his not continually fanned its flames. And love for his first wife, Anna Sethe, who died in although Richards absolves Haeckel of perabdominal agony on his 30th birthday. Over sonal responsibility for fascism and Nazism, the next year, he wrote his way through the in part by situating him firmly in his time and despair that enveloped him, producing his place, he does show how the scientist’s ardent foundational work, Generelle Morphologie temperament led him to the occasional intem(1). Although he remarried, the union was not perate statement that could be taken up by happy, and passionate love would elude him extreme thinkers. One cannot leave this book until his sixties, when he had a secret affair that without a deep appreciation for Haeckel as a ended tragically with the death of his lover. tragic figure and for the force of personality in Science remained his salvation and refuge. shaping the direction science may take. His professional life was also filled with Gliboff’s account is of a completely differdrama, much of which centered on his philos- ent order. His is not a story of personalities or ophy of evolutionary monism—a science- private lives (although he mentions salient centered faith that became one of the most details), but of German academics seeking to successful alternatives to the Judeo-Christian live up to the highest (if changing) ideals of religion among those searching for a secular Wissenschaft and of the ways in which spirituality. Haeckel could not turn down a Darwin’s theory was translated into this envifight: He battled the physician-statesman ronment. He thus situates Haeckel at the end Rudolf Virchow over the role of evolution in of a revised intellectual history of 19ththe schools (Haeckel argued that it should century German evolutionism. Central to his replace religious education), sparred with reli- account is the idea of translation, which he giously conservative scientists and with for- uses both synchronically, especially in treatThe Tragic Sense of Life Ernst Haeckel and the Struggle over Evolutionary Thought VOL 323 SCIENCE www.sciencemag.org

Making German Evolution: Translation and Tragedy
Lynn K. Nyhart

CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. KOEHLER, GERA-UNTERMHAUS, 1905)

n this year of Darwin anniversaries (the 200th year of his birth and the 150th anniversary of On the Origin of Species), The Tragic Sense of Life and H. G. Bronn, Ernst Haeckel, and the Origins of German Darwinism remind us that the history of evolutionary thought in the 19th century extended well beyond Darwin himself. Darwin did not launch his theory onto an unprepared public and scientific community, nor was the evolutionism that developed after 1859 a mere extension of his views—it was not even one thing. How, then, should we think about the history of evolution in the 19th century? What sorts of accounts best help us understand the reception of Darwin’s theory, its relations to earlier ideas about nature, the directions that evolutionary investigation subsequently took, and the relations of all of these to the broader social, cultural, and religious concerns scientists shared with their contemporaries? These questions become especially pointed when one considers German Darwinism, and especially Germany’s best-known follower of Darwin, Ernst Haeckel. Most often remembered by biologists as the author of the biogenetic law (“ontogeny recapitulates phylogeny”), Haeckel has also been accused of promoting European fascism via his monistic philosophy and of presenting a eugenic, biologically determinist vision of humanity that led to Hitler’s “final solution.” Can one scientist be responsible for so much? Most historians would say no, arguing that it takes a community, rather than an individual, to make a movement; that single-cause explanations are insufficient to account for something as broad as fascism; and that an individual cannot be held responsible for the ways in which others (such as Hitler) took up his ideas and molded them to new agendas after his death. But that still leaves open the questions of how to write responsibly about what Haeckel actually believed and how we should situate him in the history of evolutionary thought. The historians under consideration here have chosen two radically different strategies to understanding Haeckel’s place within German evolutionism, and both have proThe reviewer is at the Department of the History of Science, University of Wisconsin, Madison, WI 53706–1393, USA. E-mail: lknyhart@wisc.edu

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ing the translation of Origin of Species into translations involved an attempt to recast existGerman, and (more intriguingly) diachroni- ing German terms in a newer, more up-to-date cally, as scientists reworked older words such mode that encompassed selection yet tamed as “perfection” and “type” to lend them new Darwin’s emphasis on unpredictability to meet meanings. Gliboff’s own clear, crisp prose is the more rigorous requirements of a German key to the success of this analysis, as he deftly academic scientist’s understanding of a “law” leads his reader through dense philosophical of organic nature. Simultaneously, Bronn and terminological thickets with nary a thorn sought to translate Darwin’s ideas about selecscratch. This is some of the best close reading tion into a language without an exact equivaI have seen. It also represents a profound chal- lent for the term, and for an academic audience lenge to our standard picture of 19th-century lacking the gentlemanly traditions of breeding German biology. pigeons and dogs so central to Darwin’s expoThe old story, crudely put, is that Haeckel’s sition. The selection metaphor was further version of evolution was a Darwinism in name fraught with an anthropomorphism foreign to only, best understood as an update on early- Germans, who were not brought up on British 19th-century idealistic morphologists such natural-theological assumptions about a peras Carl F. Kielmeyer and J. F. Meckel that sonified God who had created a perfectly retained their teleology, their typological adapted nature. Bronn’s translation, though it emphasis on form, and their linear recapitula- altered key ideas to make Darwin comprehentionism. This story, emphasizing the long per- sible to a German academic audience, was not sistence of a German transcendental approach a conservative throwback. It represented the to nature, has been deeply entrenched in the dynamic engagement of a leading paleontolohistory of biology. gist who had also long been working on many Gliboff challenges this history right from of the questions Darwin claimed as his own— the beginning. The ascription of simple linear a critical yet generous equal, who saw himself recapitulationism to the views of Romantic as moving science forward through the modiembryologists, he notes, owes much to a carica- fications he made to Darwin’s flawed theory. ture developed by Karl Ernst von Baer in a Bronn’s death in 1862 afforded him little polemical context, then adopted uncritically by chance to steer the conversation further. influential historians such as E. S. Russell and Stephen Jay Gould. Gliboff’s fresh reading of the original sources interprets Kielmeyer and Meckel as far less rigidly typological in their orientation and much more attentive to nature’s variability than has been seen before. Both for these early-19thcentury naturalists and for their intellectual heirs, Gliboff argues, the critical issue was to understand nature’s manifold variety while seeking out underlying strict natural laws to account for it. This provides a new starting point for analyzing Darwin’s first translator, the prominent paleontologist H. G. Bronn—a figure little attended to in the standard story but the lynchpin of Gliboff’s. Intriguingly and plausibly, Gliboff argues that Bronn’s use of terms like “vervollkommnet” (perfect) as translations for Darwin’s “improved” or “favored” were not about dragging Darwin backward into a German teleological view of nature (as has been claimed by those who have paid attention to Bronn at all). A painter, too. Haeckel’s oil landscape of highlands in Java, from Instead, Gliboff asserts, Bronn’s Wanderbilder (1905).
www.sciencemag.org SCIENCE VOL 323

And so, finally, we come to Haeckel. Gliboff ’s key insight here is that Haeckel originally read Bronn’s translation of Darwin, not Darwin in the original. Gliboff shows Haeckel as both echoing and responding to Bronn’s concerns, rather than either reflecting directly on Darwin’s original writing or reaching directly back to the Romantic embryologists. (Although Gliboff acknowledges the centrality of monism to Haeckel’s thought, he focuses on the working evolutionary theorist, not the popular ideologue.) Like Bronn himself, Haeckel made further amendments both terminological and intellectual, and Gliboff rereads Haeckel’s research program as one not dominated by a typological and linear-recapitulationist mindset but rather as continuing to wrestle with the need to account for variability and unpredictable change in terms of mechanistic laws of nature—among which Haeckel included, at the top of his list, natural selection. Haeckel’s Darwinism thus shows continuity with early19th-century concerns, mediated through Bronn. But those concerns were always more flexible than has been acknowledged, and their articulation changed over time. Of course Haeckel’s Darwinism was not Darwin’s own, but it was not an aberration or a distortion of some true theory, any more than any other post-Darwinian additions or adjustments were. It was science moving on. Gliboff ’s overall picture of scientific advance, in contrast to Richards’s emphasis on charisma and passion, is one of scientists building and innovating incrementally, working with what their predecessors have handed them and sculpting it into something new yet understandable to those around them. His sensitive reading allows us to see post-1859 German evolutionists as rational actors rather than irrationally stuck in some early-19thcentury moment with unmodern commitments. By challenging the very foundations of the standard narrative of German morphology, this careful, compelling account does at least as much as Richards’s to undermine the association of 19th-century German Darwinism with a dangerously exceptional view of nature. But the two books offer very different reads. Is scientific progress a matter of personal anguish and triumph, or of intellectual chugging along? Our concept of it should be capacious enough to include both.
References and Notes
1. E. Haeckel, Generelle Morphologie der Organismen (Georg Reimer, Berlin, 1866). 2. The reviewer previously served as a press reader for both books at the manuscript stage. 10.1126/science.1169621

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by by the organisms’ own as genetic mutascience, this case present shaped something (later identified activities (the so- vancing through a predetermined sequence of ulation became divided up, in explainingby in- distributions), but it was not aimed in any one direction opments that would push other naturalists toward tions to oceanic islands. called Lamarckian effect), but this too permitted stages within each family, driven by force derived dependent acts of migrationin terms of past migrations, Here, Darwin followed Lyell in seeing (for Darwin but not and, thus, left adaptive evolution essentially open- from individual development. an evolutionary vision during the years he worked extinctions and that biomultiple vectors of change. Evolution had to be REVIEW opments that would push other naturalists toward geography must become a historical ended. He allowed a limited role for variation in isolation. By the late 1850s, the idea of profor Lyell) evolutionary adaptations. depicted asby branching treeown activities (the soa the organisms’ in which each act of an evolutionary vision during the years he worked science, explaining present distribushaped gressive evolution was widelyto predict an orderly pattern of branchingLamarckian effect), ina athis too permitted was thevariantsofbut more or less was result unhis theory recognized, and the proposals evolution was widely recognized, of the individual variants in a population was the relations among species. Several isolation. By the late 1850s, the idea of proin progressive tions hasPopulations divided Darwin’s move called It in terms of past migrations, been argued that by geographical of of the individual population positive that relations. opments role would push competition was being barriers will develop predictable migration of ruled Evolution had to be essentially undirected ruled out any possibility available in the 1830s deflected attention awayof individualother naturalistsand the opments that would push more naturalists viewpoint was inspired other and (for Darwin but independently extinctionshistorical toward not multiple undirected organisms to a new locavectors of change. out any possibilgressive evolution role widely recognized, toward was of individual competition and the positive essentially to a articulated by Peter J. Bowler that evolution could be shaped by a predeter- from the model of the branching evolutionarythinkers such the argued that Darwin’s move to a an tree (11). vision during as Herbert Spencer as its tion.depictedsamebranching tree intheory undermined At the as a time, Darwin’s which each act of It has been years he worked an evolutionary visionforGermaneach adapts to[e.g.new environduring the years he worked positive role of individual competition was being was being articulated by thinkers such as Herbert by Lyell) evolutionary adaptations. romanticism (12)], but a ity that evolution could be shaped by a prede(Fig. circularBy more historical viewpoint of pro1). But keythe late 1850s,Darwinian vision aspects of the the idea was inspired by German in isolation. thinkers such as Herbert Spencer ment idea geographical the branching that the resultwere more or less unold idea was species of a idealized types, Populations thein its of pro- and the posmined developmental trend. There was no ob- William Sharp Macleay’s quinary or in isolation. By the late 1850s, divided byown way, provided by articulated by 1). But key aspects of the DarwinPeter J. Bowler Spencer (Fig. termined developmental trend. There was no more practical incentive was Charles Darwin’s theory of natural selection was been hailed as one of theof classification supposedwere1).everykey romanticism recognized, and the more practical predictable migration of organisms natural locagressive evolution was widely [e.g.have occurred fixed elements in a clearly defined to a new order. thattruly original and would not (12)], have vious goal toward which it has aimed, and it system most innovative gressive evolution wasbarriers will develop independently be crossed widely sibility that and the can recognized, barriers gained on the (Fig. But truly original and would notbut a aspects ianany other naturalist atof the Darwinian vision obvious goal toward which it theoryaimed, and the each adapts to as biogeographical insightsfor tion. had to be time, Darwin’s was undermined to vision contributions todid not produce an orderly pattern of in 1859, however, contained fiverejected that were truly were individualthe time. havewas being biogeographical modern science. When first proposed relations genus it was widely species positive role of incentive competition occurred occasionally allows Species At the sametreated as populations of varywasnot Here, Wallace provided by the could be arpositive role of individual competition its new environ-the branchwas being Charles Darwin’s theory of natural selection has been hailed as one of the most innovative occurreda original and would at the time. Here, any Beagle voyage way, and the The Galapagos it did not produce an orderly pattern of relations ment in its own (1831–36). posprovides toby other naturalist on the Beagle voyagePeter J. Bowlering the old idea that species were idealized types, by his contemporaries, species. The who accepted articulated good comparison: He too moved toward ing process individuals, with no fixed limit on the range Peter J. Bowler moderneven by those accusation that the general idea of evolution. This article insights the as Herbert gained (1831–36). articulated by thinkers such provided theof evolution that Darwin as Herbert Spencer to any other naturalistgood comparison: Spencer contributions to between science. When first proposedthe 1859, however, it was widely rejected five genera, and so thinkersatsuch time. Here, Wallace in theory ranged in a circle; each family obvious Wallace of branching evolution driven by too between elements in a accusation that the theospecies that barriers can be crossed example sibility conceived inmostlate fixed species. The identifies those depended on aspects of Darwin’s work that led him to develop thisthrough the taxonomic hierarchy.the ideaaprovides a Galapagostoo moved Helocalthe most obvious revolutionary theory, (Fig. 1). good comparison: He Darwiniantoward aspects of the species provided vision the It was of possible variation. clearly defined natural order. Chambers’s (Fig. 1). But key aspects of the Darwinian within a 1830s. can be provides But keyThe by his contemporaries, even “random” who accepted the the con- idea of evolution. This article by those variation indicated general on occasionally allows forvision group branchSpecies had to “random” populations of varyry depended on be treated as variation indicated of how the relations thethe problem of the adaptation, but even he of branching Darwin’s didhow share occurred including his studies of biogeography andthis score. As Darwin one recognitionthe the role played the idea toward the andevolution drivenevolution animal breeding, and his of the mostof Natural History moved of original ideawouldnot the relations within a group can were truly branching Charles Darwin’scerns ofof Darwin’s selection has been hailed as this revolutionary theory, theory of natural work that led him to develop Vestiges of innovative approaching of Creation example of not have by local his opponents on were truly original and wouldbyof evolution that Darwin not have occurred Charles Darwin’s theory of natural selection has beenthe rangeas one of the most innovative hailed identifies those aspects ing process did not the ing individuals,his opponents onon concerns of with no fixed limit this score. driven that the adaptation, explained by of new species through a study insight by the animal breeders throws by the struggle for existence. to any otherbut workexplained by share Darwin’s contributions to himself made clear, variation was certainly caused hisdepicted was of the role played adaptation,localeven ofat the but even he Wallace modern science. When first proposed in 1859, origin supposing that an original be to any other naturalistconceived in the late Wallace was at the time. Here, 1830s. It contributions The Tree science. When modern of Life not Here, including his studies of biogeography and animal breeding, and however, it evolution inrejected parallel lines ad-naturalisthe did time.supposing that an original pop- toAs of possible variation. first proposed in 1859, however, it was widely rejected recognition widely terms of share on a good comparison: He selection. toward Darwin’s insight that the moved of the work Darwin himself made clear, variation was population became divided up,Darwin case light provides the process of natural too by his struggle for existence. (later identified as genetic muta- vancing through a predetermined insight that the work of the animal divided up, in this case by inof biogeography of in this was One innovation those who of Darwin’s general sequence of ulation became breeders throws by something provides a good comparison: He too moved toward the by his contemporaries, even by at the heartaccepted the theory idea of evolution. This article by approaching the problem that by the contemporaries, even by those who accepted the general idea of evolution. This article throws original and process of the disturbing. certainly caused by something is hardidentified (later for us to by independent acts of his model of openmigration to ocetheory was both light ondriven he those tions), of Charlesnotwork that any him directionones in a progressive sequence lead- by lightThebreeders dependent acts of migration to oceanic islands. publication but it was Darwin’s in led one to develop this revolutionary theory, driven animal the process of natural selection. by local On pre-existing The of Darwin’s the idea of branching evolution identifies aspects of Darwin’s aimed led species by local stages within each family, forceon derived the idea of branchingorigin of newdriven through a study evolution to construct identifies those seems so obvious today that it led him to develop this revolutionary theory, aspects Tree of Life work that as genetic mutations), but it of Darwin’s theoryit islands. Here, Darwin was ing up to humans general played It was selection. thehis studies of biogeography and animal breeding, and from But if the the role idea Origin of Species in even he did offollowed selection including publicationthus,Charles1859 evolution essentially open- hisin(5).individual development. of natural not justwas both idea notnatural Darwin’s seeing that bio- studies of biogeography new animal not radicaland his recognition of the role played adaptation, but evenanicdid not share Darwin’s followed Lyell ended, that Darwin appreciate just howthe heart was breeding, in of biogeographydivergent evolution. Wallace One innovation at and and how aimed Here, Darwin share Lyell in and, of left adaptive is widely pre-existing ones recognition of sequence lead- adaptation, but that the original and disturbing. he including his The theory a progressive he publication of Charles Darwin’s On of he The theory one direction and, thus, left adaptive evoin seeing that biogeography must become challenged the beliefof original and disturbing. that animal breeders throws was supposedfor have initiatedDarwin’s On for variation not entirely new, Darwin’s vi- insight that the was thethethe world was designed led to construct his model of model by thethe Origin to existence.in 1859 revolution ingevolution was not entirelythe Darwin’s vision It was not just workbothidea of natural selection struggle ended. He allowedaa is widely developed a throws wasexistence. geography must becomeby historical a the struggle any seems so time. Lamarck hadisproposedusthat limited role evolutionhumans (5). But if new, insight that the work of the animal breederssimilar open- and tested for at the obvious today that it hard for to that up to general idea of of Species natural lutionmight be natural processeshowallowed ita aended, divergent evolution. Wallace historical science, explaining present appreciate just open-ended. adapting speby a on the process both inthe Origin of Species inculture.is widely sion of how process worked certainly was.was. light wise and benevolent God.selection.selection present distribuscience and in Western 1859 Yet there of how the the process worked certainly Al- It was not just that the idea ofThere was a wider during his there essentially how new and He radical light on the process of naturalitselection. explorations in South that the world was designed supposed shaped by the organisms’ own activities (the was not entirely new, Darwin’s vision challenged the beliefof naturalscience, explaining to have initiated a revolution evolution sodeveloped a similarand the Malay migrations, model and the variation shaped the world in designed the organdistributionsand terms of past Archipelago supposedcalled Lamarckian effect), but this pre-existing ones in a was eventually paralleled element of teleology or original and disturbing. to have initiated a limitedofatCharles their environment.pre-existing ones in a progressive sequence leadthough by have beenpublication of Charles Darwin’s was too permitted theory progressive sequence lead- by aThe theory belief thatGod.tions wasterms of past migrations, claims that Darwinism On Although the he frequentin Western culture.revolution of how the theory was eventually paralleledAl- challenged the was bothgoal-directedness almost America disturbing.tested cieswas role forin Darwin’s On proposed that to changes time. Lamarck had byBut Darwin The theory was both original in he publication wise and benevolent There was a wider the process worked certainly was. both in science and Yet there it his explorations in South there might be natural processes if adaptation science and in Western culture. Yet there by up to humans (5). But if the general outline universally and benevolent God. Thereand (for was a isms’Speciesthe 1859to realize thatadapting to humans (5). But if the general idea of It was not just that the duringof natural(for Darwin but not for own activities (thewidely ing up speso-called Lamarckian extinctions and Indonesia). both inthe “in the air”Species in 1859 is waiting ingWallace, Darwin had conceived its basic out- It waswise just that the the time.natural selection Darwin but not somehow Origin of at the time, of change. Evolution had to Darwin had conceived its basic idea of by a not accepted at idea of Most thinkers— merely widely Wallace, be was extinctions multiple vectors idea (modern selection the Origin of perhaps in first is environment. But Darwin have been frequent claims that Darwinism was though the theory was eventually paralleled by element of teleology or goal-directedness almost America and the Malay Archipelago cies to changes in their have been frequentahave readilyDarwinism was evolution 1830s, after his return Darwin’svoyage wider element belief that theorforand Chambers— goal-directedness in the the late for someone to put claims that available points line inlate of 1830s, after his from the vision challenged the of teleology world was designed supposed air” few initiated a revolution Wallace, Darwin had conceived return from the including Jean-Baptiste Lamarck Lyell) evolutionary adaptations. to at the a branching waiting Adrian adaptations. James toto was perhaps the first was the onlyifmechanism the localinitiated a permitted that evolution was that the world was designed supposedeffect), but environmentto realize multiple vectors not entirely new, Darwin’s vision challenged the belief Lyell) evolutionary Desmond andPopulahave this too revolution somehow “in thedepicted astime, merely tree in which each actwas not entirely new, its basic outline universally accepted at the time. Most thinkers— (modern Indonesia). adaptation took it universally accepted Populations wider of H.M.S. somehow “in the in at the time, merely wait- of how theH.M.S. Beagle. He workedwas. in almost forand benevolent God.at the was a life on of change. Evolution hadbe major of how as together in the and way [for culture. (1)].there voyage un-processHe worked on it relative by a wise granted that the development ofdivided right tions divided byhave wider barriers that There time. Most both in science putair” Westerninstance YetofThe in or lessof1830s, afterworked certainlyin on itAl- including Jean-Baptiste Lamarck and Chambers— by geographical Moore geographical of to the local environment there depicted the branching was the result pointsmore the late Beagle. his return from the voyage a God. There was and James both in science andevolution, there wouldwas the only mechanisma process worked certainly was. Al- by a wise and benevolentAdrian Desmondarecently proposed will in Western culture. Yet to be implications for someone to a few readily available earth represents the of a coherent fact been Russel Wallace (Fig. of organisms isolation over the next eventually ing for Alfredright put a[for readily indepen- though isolation over 20 next on paralleled of thinkers—including Jean-Baptiste Lamarck plan branching tree there by each species are clasindependently of slavery havethat in frequent claims migration 1)available of new the theory Hetheyears, untilitthe arrivalby element of teleologyunfoldingbarriers will almost for of whole system would be major though the theory was eventually paralleled by element of teleology develop Darwin’s hatredas each adapts to its or goal-directednessproposed that prompted claims that Darwinism was Moore have recently almost implications the development of develop have been on in relative together someonepredictablefewinstance (1)]. The to aH.M.S. Beagle. was worked20 years, until the took it for granted thator goal-directedness lifeand independentlyfrequent theevolution, in which which act of branching the to way that Darwinism was relative locadently formulatedair”At the same time,selection in arrival paper had conceived its precipitated Chambers—took it for the time. Most thinkers— in athe Wallace (Fig. Darwin’s theory undermined wasforinto whole system by which species geology, result of more or less in are claspoints together Russelat right natural1) indepen- Wallace,over the next paper in 1858 basicflurry of universally predetermined goal. (This assumption somehow “in thetion.theory of waymerelyinstance isolationofDarwinin 1858 precipitatedthe arrival of earth represents the unfolding asthat the develop-its new environ- the air”the thegroups. aDarwin’s mentorWallace, Darwin had conceived its basic outline universally accepted new environment towardown way, and(13). the time, [for waiting Wallace’s Wallace’s 20 years, until the outline aimed at a accepted at granted each adapts to sified atthe time, merely waiting unpredictable Darwin’shisMost thinkers— hatred of in its evolutionism the at the time. moveslavery prompted somehow “in of a coherent plan fact that Alfred activity leading after publication of the voyage is still preserved in the very term “evolution”; way, for someone migrationinto groups. Darwin’s new in the late 1830s, after his return from the voyage including Jean-Baptiste Lamarck and Chambers— (13).crossed oc1858 is taken put few Russel Wallace were in the types, activity his return the the Origin. ment at predetermined goal. the Chambers— evidence forthat species (Fig. the flurry of this position. possibility that barriers slaveholders argued (1)]. The fact that a old idea natural selectionBut Wallace’s 1830s,to theleading tofrompublication includingaJean-Baptiste Lamarck and in its own of for someone toastheAlfredreadily available points idealizedlate paper in 1858 precipitated the flurry of aimedof life on earth represents(Thisunfoldingthe and the pos- to put a few readily availableto a mentorlocation. At Charles Lyell,organisms how his uniformitarian his moveBecause many can be toward evolutionism sified of had shown points in geology, ment assumption dently formulated a theory of in Latin for plan aimed the predeterminedlife on Historians Darwin had created the many slaveholders argued took itevolutio refers to at development a scroll.) 1) independentlyevidence[forainstanceof theory of the leading formulated theory (1)]. But of H.M.S. Beagle. quarried Darwin’s notebooks a coherentgranted the the a unrolling of of barriers the Charles Lyell, had shownbiogeographer to the casionally allows for life on together in the right way outlines of the natural naturalOrigin. have He worked on the relative is still preserved in that very term “evolution”; the cantogether in the rightsame time,instancethe theoryhis uniformitarianBeagle. He worked on it in relative took it for granted thatBecause that the black race was separately theory would allow (1)]. The undermined resibility that goal. be crossed the development of the branching process of H.M.S. way [for Darwin’s how 1858 is taken asfixed elementsthis aposition.defined activity order. to the publication ofit in Origin. for in clearly The that the black coherent separately centered on the 20 that earlier,Species and Wallace (Fig. diffact yearsAlfred Russelthere were significant populations letters to have quarried Darwin’s process by (This evolutio refers unfolding occasionally allows Historians establish the Darwin’s notebooks The assumption still unrolling in the plan selection in created taken to be of 1) for this and of over have quarried complex notebooks earth explanatory framework of a coherent very old theory the species were idealized on antoeveridea would allow the species types, reof evolutionathat Darwin conceived in the constructthat migrations of biogeographer fixed the that Alfred Russel Wallace (Fig. 1) indepen- isolation over the next 20 years, until the arrival of earth represents the unfoldingcreated from plan white, Darwin of race was the Historians Darwin had 1858 is the hadas evidenceindepen- isolationvary- the next 20 years, until the arrival of Latin represents theisto the preserved of a scroll.) for fact branchoutlines treated theory the as created wanted towhite, Darwin from the construct clearly defined could sometimes (This assumption dently formulated a individuals, with no fixed limit Wallace’s paper in 1858 precipitated process of aimed at a predetermined goal. centered of the changing earth. Populations natural order. Speelements in the migrations of species on an everlate goal. It was by approaching the share that Darwin on letters to assumption theory of natural selection 20 years earlier, ing theory of natural selection in and the range establish the complex the flurryby The explanatory framework ing process on evolution dently formulated a changingaearth. Populationsin Wallace’s paper in 1858 precipitated the flurry of aimed at a predetermined1830s.(Thisthat show that all races proband there were significant difwanted to common ancestry, all races share could is still preserved in the very term “evolution”; the 1830s. It was as evidence for treated as populations sometimes 1858 is taken asof possiblefor this position. But activity leading to the publication of the Origin. evidence variation. a show become to be this geographical activity leading of so that lem of the “evolution”; the and he realized conceived in the late 1858 is taken cies haddivided by position. But barriers,varying to the publication of the Origin. is still preserved in theavery term origin of new species through common ancestry, and he realized become divided by geographical barriers, so that Historians have quarried Darwin’s notebooks Latin evolutio refers to the unrolling of a scroll.) problem of the created the outlines no fixed limit on the Historians have quarried Darwin’s notebooks Latin evolutio refers a study of biogeography that be defended Darwin had created the outlines of the theory that this claim could what was once a a single theory could split into range of by approaching the to the unrollingcould scroll.) Darwin was Darwin had individuals, with single species could split into that this claim of a be defended what was once of the species centered on the 20 years earlier,The Tree of Life significant dif- and letters to establish the complex process by The explanatory frameworkorigin of new species through a study and there were multiple branchessignificant dif-separate environled to construct his on the ideaopen-ended, centered model and letters 20 years earlier,possible variation. adapting to separate environ-to establish the complex process by The explanatory frameworkby extending throughout throughout and there were by extending the idea the of multiple branches adapting to the animal As a basis developed a ments (10). Evolution would become a divergent of biogeography that Darwin was One innovation at the heart of Darwin’s theory divergent evolution. Wallacefor a basis for the animal kingdom. kingdom. As ments (10). Evolution would become a divergent his this thesis is thesis process, withLife branches splitting over and led to construct his model of openseems so obvious today that it is hard for us to his thinking, thinking, this it during his to Theprocess, with some branchessplitting over and Tree of some similar model and tested sure to is sureexover innovation at the heart of Darwin’s theory Fig. Tree of of Life, from Darwin’s notebooks again, whereas others came to dead end generate generate much controversy, but if much controversy, but if ended, divergent evolution. Wallace appreciate just how new and how radical it Oneover again, whereas otherscame to a dead end Fig. 2.2. Tree Life, from Darwin’s notebooks (22). (22). plorations in South America and the Malay acceptedaccepted it would emphasize the it (modern Indonesia). through extinction. through extinction.today that it is hard for us to developed a similar model and tested was at the time. Lamarck had proposed that seems so obvious Archipelagowould emphasize the played played by toward a model These rigidly structured models of taxo- taxo- crucial roleby his move his move toward a model These rigidly structured models of crucial roleAdrian Desmond and James Moore have TheThe image thenew and life had appeared in image how tree of how radical it was it during his explorations in South there might be natural processes adapting speThe idea of common descent now seems so appreciate just of of the tree oflife had appearedin evolution Darwin’s notebooks of thelate 1830s (Fig. 2) Darwin’s notebooks ofhad proposed that there nomic relations andand wonder what sense of branching evolutionevolution based on geographical the late 1830s (Fig. 2) nomic relations might made good alternative of branching based on geographical America and the Malay Archipelago cies to changes in their environment. But Darwin at the time.proposed independently by Wallace in toobvious embedded in evolution made good sense recently proposed that Darwin’s hatred of slavanyone that we vision of nature as a and was Lamarck diversity. and was proposedprocesses independently by species to models could have been proposed to nature diversity. prompted in to anyone embeddedain a vision (modern Indonesia). was perhaps the first to realize that if adaptation mightpaper published in 1855. adapting Wallace it predictable, orderly system governed byof divine as a This model was so his move towardlate radical that many evolutionism a account for ery a be natural Both realized that This model predictable, orderly system governed by a divine a paper published in 1855. Both realized that it plan. Such a world view species.difficult toproposals (13). evolutionistswas so radical thatargued that Adrian Desmond and James to the local environment was the only mechanism changes in their environment. But Darwin was the relations among made it Several ac- 19th-century Because many unable to accept many late were slaveholders explained why naturalists were able to arrange plan. Such world life made it difficult it in 19th-century argued that the theory of explained whygroups within groups, using descent Moore have recently proposed that of evolution, there would be major implications species into naturalists that able to arrange available inathe 1830s deflected might be away the black race was separately unable to accept perhaps the first to realizewere if adaptation to cept that the history ofview on earth attention to ac- full. Ernst Mayr evolutionists werecreated from the cept the the history of life on tree might be it descent Ernst Mayr argued that the species into groups within theexplainmechanism from that model of unpredictable, dependant common in full. was one of Darwin’s greatest all races Darwin’s hatred of slavery prompted for the whole system by which species are clasfrom environment was to only the underthe local a common ancestorgroups, using descent essentially irregular andthe branchingearth (11). Wil- white, Darwin wanted to show that theory of essentially of migration, isolation, and dependant common descent to one selection from a common ancestor to explain the under- liam hazardsMacleay’s quinary or circular system share common wasnaturalof Darwin’s greatest his move toward evolutionism (13). sified into groups. Darwin’s mentor in geology, lying similarities. Closely related species have diof evolution, there would be major implications on the Sharpirregular and unpredictable, local achievements,ain addition ancestry, and he realized that lying similarities. Closely related ancestor, whereas adaptation. Darwin was led toward his alterna- local (14). So it was, but additionMayr natural selection verged recently from a common species have di- on the hazards of migration, isolation, and itself achievements, in I think to overBecause many slaveholders argued Charles Lyell, had shown how his uniformitarian for the whole system by which species are clas- of classification supposed that every genus con- this claim could be defended by extending the the ancestry from a distantly ancestor, whereas adaptation. part because led toward inter- estimated the rapidity with which other think verged recently of more commonrelated forms must tive model in Darwin was he was more his alterna- itself (14). So it was, but I natural-Mayr overthat the black race was separately theory would allow the biogeographer to resified into groups. Darwin’s mentor in geology, ested in adaptation thanthat could be arranged in a were converted to thethe animal kingdom. As a baidea throughout theory. Many of tained five species cosmic teleology, Fig. 1. Charles constructAlfred Russel Wallace, and on an everDarwin, the migrations of species Herbert Spencer. be traced further distantly the family tree to other more ists the ancestry of moreback downrelated forms must tive model in part because he was thanks inter- estimated the rapidity with which the naturalcreated from the white, Darwin Charles the common shown how his uniformitar- tocircle; each family five genera, and so on through sis for his thinking, this thesis is sure to generthe in adaptation than Paley’s natural the- non-Darwinian theories of evolution proposed find Lyell, had point of origin. family tree to estedinfluence of William cosmic teleology, thanks ists were converted to the theory. Many of the be traced further back down the wanted to show that changing created the Wallace,could Herbert Spencer. earth. Populations sometimes Fig. 1. Charles Darwin, Alfred Russeloutlines ofandand letters to establish the complex process by term “evolution”; the Latin evolutio refers to the all races share to the taxonomic hierarchy. Chambers’s Vestiges of ate much of Darwinism” in if accepted position. But Darwin had ian theory idea of commonthe biogeographer so ology. Natural selection replaced divine benev- during the “eclipsecontroversy, butthe late 19th it would The would allow descent ferences between the ways in by geographical barriers, so that to the influence of William Paley’s natural the- non-Darwinian theories of evolution proposed find the common point of origin. now seems a common ancestry, become divided which he and which he developed his theory (6–9). Darwin theory of natural selection challenged this vision and he realized century were introduced with the aim played by obvious the we might wonder what alternative the theory 20 years earlier, and there were sig- which highly creative his theory (6–9). Darwin unrolling of aan orderly pattern of relations. he developed thinker who synthesized a of nature as scroll.) The explanatory framework reconstruct that migrations of species on an ever- olence as an explanation of adaptation. Unlikeevolu- emphasize the crucial role of subvert- his move the Natural History of Creation depicted Wallace formulated their ideas. aIn this essay, I could split into of Darwinism” in the ology. The idea of common descent now seems so Macleay Natural selection replaced divine benev- the during the “eclipseprinciple of common late 19th that this claim could be defended what was once which he and which he developed his theory (6–9). Darwin theory of natural selection challenged this vision single species was a ferences differences between the ways in which was a highly creative thinker who synthesized centered on the theory of natural selection chalthe ways in implications of the models earth. have been proposed to account for could Populations could sometimes tion and Chambers, Darwin did not expect ing nificant between was truly original in his think-andnumber of key insights, some derived from Darwin’s world view was profoundly the argue that Darwin Fig. 1. Charles multiple Alfred Russel Wallace,Iseparate a highly creative thinker who synthesizedhis of nature as an orderly patternby relations. differ-idea Fig. 1. Charles changingthat weRussel Wallace, whatHerbert Spencer. in terms of parallel lines advancing through toward a model of branching evolution based on Darwin, branches adapting to Herbert Spencer. obvious Alfred might wonder and alternative olence as an explanation of adaptation. Unlike century were introduced with the aim of subvertextending throughout Darwin, a Wallace formulated their ideas. ideas. Inessay, In this this es- was environ-key insights, some derived from his lenged this vision of nature as of orderly pattern he and Wallace formulated their addressing the a number of and others from currents circulat- ent because he argued that the an becomecould have been proposed tobarriers, for a predetermined sequence of stages within each geographical diversity. the principle of common adaptation of popscientific work ing, and I support this(10). Evolution models divided by geographical account so Macleay and Chambers, Darwin did not expect ing the implications of ments claim by become a divergent Darwin’s profoundly differkey argue that Darwin was truly original in would his number ofwork insights, some derived from his of relations. world view was the animal kingdom. As a basis for his thinksay, I argue that defining was trulywhich heinand which his cultural environment. Few would now theory ofto their local environment was the sole that what was once a single species could split family, VOL 323 force ing in he related issue of Darwinways why thebranches splitting over and and others from currents circu- ent because he argued that the his thinking,visionthesis is sure to 224the ways in which he and which he developed his theory (6–9). derived www.sciencemag.org This model was so radical that many late just in original was scientific developed his theory (6–9). Darwin ulations natural selection challenged this poptheory 9 JANUARY 2009 driven by SCIENCE from individual ferences support the with some process, Darwin theory of natural selection challenged this vision ferences between of this ing, and Ibetween this claim by addressing the scientific work and others from currents circulatDarwin’s world separate en- development. thinking, and tosupport this claim by addressing was a highly creative thinker whoby natural se- of nature as an orderly patternadaptation found it into multiple branches 19th-century evolutionists accept the claim thatenvironment. so disturbing I overtheir ideas. In others came lating in his his again, whereas relations. controversy, butformulated their ideas. In this adapting to was a highly creative thinker who synthesized a of nature as an orderly pattern of relations. were unable to accept synthesized a cause of their localview wasofpeoplemuchdifWallace formulated contemporaries. this essay, I to a in his end cultural 2.evolutionLife,Few would ulations totransmutation. Many profoundly sole Wallace if essay, I environment adaptation was related issue of defining just why whytheory was ing dead cultural environment. Few would Darwin’sferent because he argued thatgenerate the of the the theory now accept the claim that evolution from now Fig. Tree of notebooks (22). by natural the These VOL structured models taxonomic it in full. the Darwinissuethrough extinction. in his think- number was in insights, Darwin related was of definingoriginal 224 vironments (10). Evolution would become a 9 JANUARY 2009 rigidly323 SCIENCE ofwww.sciencemag.org Ernst Mayr argued that the theory of of either lection of key the air. some derived from his hard of transmutation. Manythe agentfound it the Darwin’s world view was accepted it would argue that Darwincertainly not the first to sug- accept the claim that evolution approached se- causeto see natural selection asprofoundly differ- emphasize the was truly just Darwin’s world view was profoundly differargue that Darwin was truly original in his think- number of key insights, some derived from his people by natural so disturbing to histo his contemporaries. contemporaries. air. Darwin approached the populations to their local rationally his move was and I support this claim of the tree of the scientific work and These significantly circulat- ent because he argued that a played by structured common divergent process, with some branches splitting relations divine taxo- crucial role in gest the idea of The image an alternative to selection was ing, so disturbingevolution asby addressing life hadsubject wasininin theothers from currents different hardof see natural selectionthe adaptationwas the toward a and I support this claim by addressing the scientific work and othersand evolution made good sense to any-he argued thatdescent was one of Darwin’s greatest appeared a way that was rigidly structured models to benevolence or of environmentof either the adaptation of popfrom currents circulat- ent because ing, model as the agent of popthe air. Darwin approached the Darwin was certainly not the first to sug- lection certainly not the Lamarck’s subject in a the that relationsFew would now cosmic teleology. first the Many species sole over and over again, whereas others came to a one embedded as a predictfrom theDarwin of species just whyJ. B. of to was ing (Fig. ofwaynomic efforts being made to ex- sole cause of transmutation.adaptedpeoplebased creation environment. and evolution made good to their local environment was found related issuewasdefiningby notebooks theory sug- 1830sin any culturalotherwas significantly different divine benevolence branching evolution the to anon geographical of defining just why the theory was ing in his cultural environment.in a vision of nature ulations to their achievements, in addition tosole Darwin’s God.thealternative late subjecthis a way that was significantly different ulationssense ofSelection rationally structured 2) local environment was the natural selection itFew would now related issue or of a in gest the idea of evolution as an to gest thepublished evolution hadan alternativedis- accept theofclaimother on earth. He made to ex- it hard to see environment, and itas the by able, orderly system natural sedivine plan. self (14). So it was, but think it ever-changing natural selection did so agent of plain the life evolution by in theory, idea and was as been widely to from any the of anyone embeddednatural se- cause in 1809, so creation of ofhis contemporaries.independently from any history other efforts being had a unique cosmicof transmutation. adapted specieskilling accept the claim that evolution by governed by a cause of transmutation. Many peopleI foundMayr overestimatso disturbing to dead end through extinction. his contemporaries. teleology. Selection to it of to exthe disturbing tospecies byproposedB. Lamarck’s by Wallace inthe tothat efforts being made a vision of nature as a diversity.Many people foundan God. J. The image the first to sug- lection was the Darwin was acertainly God.theB. Lamarck’s realized that itin the life on earth. He had a unique harduseless natural selectionruthless “struggle for that many late was certainly not of the tree of life had appeared in the air. world view made it the hard to see natural selection as the agent of either naturalists were creation of species by not J. (2–4).to Both plain the history of air. Darwin approached the either divine benevolenceas of a so radical Such a Darwin approached difficult to accept ed the rapidity with which other combination scientific orderly that alerted off a see variations in a orit did so rationally cussed, although generally rejected in 1855. sug- lection was of predictable,interests system governed by todivine environment, and the agent ofkilling either first Robert plain the history of life on earth. He had a unique ever-changing This model was by paper published Darwin theory, published in 1809, had been widely distheory, publishedevolutionhad been widelywere subject in a of scientific interests view alerted divine to cosmic teleology. the kind ofadapted that made in Darwin’s notebooks of the late 1830s (Fig. 2) that the history of life on earth might be essen- converted to the theory. Many of the non-Darexistence.” Chambers’s of in of theas naturalists dis- combination Natural History of him to topics that was other naturalists. He structured This did not seem Selection process gest the ideaVestiges1809, whyan (2–4). Robert combination ofignored by interests that alerted off uselessac- 19th-century evolutionists were gest accept variations in a ruthless “struggle for scientific a world cussed, although explained rejected alternative to able to arrangewayplan. Suchsignificantly differentit difficult benevolence or of a rationally structured unable to the idea of evolution as an alternative to subject in a way that was significantly different divine benevolence or of a rationally structured generally cussed, although sparked debate within Rob- from descenttheon ideas widely discussed at He cosmic teleology. SelectionErnstbenevolent to that the creation and was proposed independently by Wallace in tially irregular and unpredictable, dependant on winian theories of evolution proposed during the certainly of Creation of other by other naturalists. on that would be it in full. a kind argued it the creation 1844generallyarejectedover thegroups, him to topics ignored by the history of to ex- existence.”an ever-changingadapted speciesandan species the groups (2–4). pos- him any drew cept that other naturalists. the species to This instituted byenvironment, God, Chambers’s of species by God. J. B. History of usingto topics ignored efforts being madelife He earth might be did not seem the Mayrof process the theory of of species by God. J. B. Lamarck’s from any of the other efforts being made to ex- cosmic teleology. Selection adapted species to an Vestiges of into Natural Lamarck’s especially time, undersibility that new in 1809, had Natural History plain but drew essentiallyearth. He and at the ever-changing off useless it did so by ruthspecies the ancestor dis- certainly was of ideas widely discussed ert Chambers’s Vestigescommonproduced to explain thethe drew forced by hisirregular had aunpredictable, so by killingcommonby variations in killing a paper published in widely Both realizedthe historythelife on earth. He had a unique and local ad- environment, and it did so by killing 19th century and benevolent of Darwin’s greatest life on scientific interests to did wouldbecause its essentially was oneGod, theory, published sparked ofwerebeen widelyfrom certainly historyon ideas widely discussedunique thatdependant environment,descent“selfish”anature of hazards of migration, isolation, ever-changing “eclipse of Darwinism” in the late theory, published in 1809, had been 1855. dis- plain that it be instituted a on at the Creation of 1844from a a debate over the posmeant local achievements, use but diof Creation new generally were debate over the time, have wasforced by hazards of migration, isolation, useless a parasitic essentiallyinwas anot seem of 1844 similarities. Closely related combination forcedinspiration in a that alerted off andthat variations way of This addition to “struggle for scientific scientific interests to cussed, althoughlying sparked a producedRobert speciesthosewas of on theby his scientific interests especially because existence.” life“selfish” naturenatural selection rejected (2–4). from time, but sources of his interests highly orig- less “struggle for its in a ruthless did perfectly scientific interests that toward off useless variations in a ruthless “struggle for cussed, althoughexplained why naturalists were able to arrange of aptation. Darwin was led alerted his alternative were introduced with the aim of subverting the generally rejected (2–4). Robert combination sibility that species response inal whereas adaptation. Darwin in a highly existence.” This itself (14). some circumstances. to to topics ignored inspiration was led towardnatural adaptive did not seemlife bewas, perfectly possibility that new Anthropological Studies, common the kind of process wayin So was species the Natural History of him to topics model by other naturalists. more interested This did not seem the kind of process process Chambers’s Vestiges ofrecently from aHistory ofancestor, way. sources of inspiration innaturalists. He meantalterna-parasiticthat would itkindaofbut I by his that a Chambers’s School of Philosophy verged thewere produced from useuse those sources ofby other a highly origand species Natural The Queen's himthose of the instituted think Mayr over- Vestiges ofinto groups within groups, using descent ignored in part because he wasHe existence.”in implications of the principle of common descent original drew tive Darwin discussed the natural inter- God, especiallya rapidity withGod, a benevolent response byidea circumstances. from a common ancestor pos- certainly drew adaptation than cosmic teleology, that would pre-existing 1844 sparked progressive sequence inal To must on ideas widely may have at he (15). The American neo-Lamarckians Edward thatMore seriously for the some of cosmic telewould be estimated benevolent which Creation of Creationof Belfast, thein a Road of more distantly related forms some extent,model in part becausebeenwas more adaptiveinstituted inthe because its essen- other natural- 1844 sparked a debate over theto explain the under- on ideas widely discussed at the thanks to thebe instituted by a benevolent God, University of ones ancestrydebate over the posUniversity a Belfast, Belfast, Northern certainlyway. way. School of BT7 1NN, UK. species But if Studies, The Queen's “ahead ested time,” may interests to Ireland, that humans (5). were produced because were idea sibility Philosophy andE-mail: p.bowler@qub.ac.uk from family but was extent, by his scientific have devel- especiallyseriously its essentially of parasitic tele- Many of that new species were produced from species have forced by his scientific interests to especially because its essentially “selfish” nature proposed that To some of his Darwin may have been ology, Darwin’s supposition thatathe production leading up tonew Anthropological the general idea time, tree to extent, in adaptation than cosmic teleology,“selfish” nature meant that “selfish” nature lying similarities. Closely related time, but was influence of William Paley’s natural theology. Drinker Cope and Alpheus Hyatt theory. sibility the be traced further back down the merelysome forced Darwinanticipating been tially thanks istsfor theconverted to the way More cosmic To University of Belfast, University Road Belfast, Belfast, Northern use those sources his time,” anticipating devel- ology, Darwin’s non-Darwinian was production merely “ahead of his time,” anticipating devel- meant that a perfectly naturallife the a response diverged recently from a common ancestor, Natural selection a highly orig- benevolence parasitic way of life each a perfectly to the influence of highly orig- of life was a find the common point use those sources of inspiration in replaced divine meant that a the evolution of was group should be seen as a supposition adaptive perfectly Ireland, BT7 1NN, UK. E-mail: p.bowler@qub.ac.ukof origin. merely “ahead of of inspiration in a William Paley’s natural the-parasitic way of that theories of evolution proposed opments in some circumstances. whereas the ancestry of more distantlyway. The idea of Studies, The Queen's now seemsthat would push other naturalists to- divine benev- response in“eclipse of Darwinism” in the late 19th common descent inal way. so ology. Natural selection replaced natural adaptive during the some circumstances. natural adaptive response in some circumstances. inal related as an explanation of adaptation. Unlike Macleay series of parallel lines moved through the same School of Philosophy and Anthropological School of Philosophy and Anthropological Studies, The Queen's www.sciencemag.org SCIENCE VOL 323 9 been 2009 More seriously for were introduced with the To some olence as an may have JANUARYMore seriously for the idea of cosmic tele- 223of subvertward an evolutionary Darwin explanation of adaptation. Unlike centurythe idea of cosmic tele- aimUniversity of Belfast, forms must Belfast, Belfast,further back down the extent, Darwin may have been be traced Northern obvious that we might wonder More seriously for the idea of cosmic stages, an updated To some and Chambers, Darwin did not expect his theory hierarchy of developmentalteleUniversity of Belfast, University Road Belfast, Belfast, Northern what alternative extent, vision during the years he University Road merely “ahead of his time,”late 323 Ireland, BT7 1NN, UK. E-mail: p.bowler@qub.ac.uk proposed to account for SCIENCEtheVOL 1850s, theJANUARYnot expect www.sciencemag.orgisolation. By andanticipating9Darwin did 2009 Macleay Chambers, devel- ology, Darwin’s ing the implications of the principle of common UK. E-mail:tree to find the common point of origin. models could have been idea ology, Darwin’s supposition that the production 223Ireland, BT7 1NN, family p.bowler@qub.ac.uk supposition that the production to his time,” anticipating devel- ology, worked in supposition that the suggested merely “ahead of predict an orderly pattern of relations. Darwin’sversion of the idea production in Chambers’s

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Vestiges. The similarities linking the species in directed variation among individual organisms. tion thinking, and although he may have exa genus were due not to a recent common ances- Although convinced that the degree of variabil- aggerated the extent to which Darwin himself try, but to parallel trends independently reaching ity was artificially enhanced under domestica- made the conceptual transition, the subsequent the same stage of development. Like Chambers, tion, Darwin, nevertheless, accepted that there development of the selection theory brought this they endorsed the recapitulation theory (ontog- must be some equivalent variability in every implication out more clearly. In the debates that followed the publication eny recapitulates phylogeny, in the terminology wild population. The analogy with artificial seintroduced by Ernst Haeckel) and saw evolution lection then allowed him to depict natural selec- of On the Origin of Species, the analogy with as the addition of preordained stages to ontog- tion as a parallel process in which a few variant artificial selection continued to play a key role REVIEW eny. Adaptation was not crucial once the basic individuals, in this case with characters useful to by forcing even Darwin’s critics to think about descent (15). The American neo-Lamarckians scale and that could be investigated directly. interbreeding individuals. Traditionally, species character of the group was established, and the species rather than the human breeder, sur- the problems of heredity and variation in a new Edward Drinker Cope and Alpheus Hyatt pro- There was a well-developed network of breeders were treated as idealized types with a fixed esthe linear, orthogenetic evolution of the of each group should be by this Thoseand although their ideas about (18). Opponents such as Fleeming Jenkin, vive and reproduce. time, with harmful charac- way sence, any variation from the norm being trivial posed that the evolution group might eventually generate a series of parallel lines moved through heredity and variation were existence, who saw impermanent. The breeders knew that they ters are eliminated by the struggle for distinctly pregenet- and selection working on large variations seen as bizarre nonadaptive could of nature,” were, in structure by acthe to extinction—the thejust an up- ical (like Darwin’s own), any animal or characters as a prelude same hierarchy of developmental stages,as the breeder will not permit they had a very clear “sports produce huge changesnevertheless, still in cumulating the framework defined by of dated version could make no Chambers’s appreciation of how the produced he ory of “racial senility.” Darwin of the idea suggested into reproduce if it does not have they characterchangesworking within normal variations over a numberthis Vestiges. The similarities linking the species in a their artificially small populations. The insight generations. When Darwin linked this informasense of the theory proposed by Cope to a recent common ancestry, that they workedwho selection Darwin been tionFor supporters such species couldGalton, and Hyatt, wants. It was the breeders by taught may have analogy. with his conviction that as Francis change genus were due not because he could not imagine an evolutionary that variation important (this is toward some preor- among indefinitely over time, he was driven toward a artificial selection helped to clarify the nature but to parallel trends independently reaching the is not directed the point of contention dained goal, experts studying Darwin’s notebooks), process driven by predetermineddevelopment. Like Chambers, they allowing him to build on his exist- but of both heredity and selection,in which the popthe new form of species concept paving the way same stage of trends. But the endorsed the recapitulation theory (ontogeny breeders certainly taught him one thing. He ulation becomes paramount. of natural range of fact that such theories flourished in the late 19th ing conviction that adaptive evolution must be for the revolutionary impact TheMendelian gecentury demonstratesrecapitulatesradical the in the terminology intro- realized that in process. just how phylogeny, theory an open-ended, branching a domesticated population there variability becomes part of thehereditycharacter, netics. The notion of “hard” species’ was induced by Ernst Haeckel) and saw evolution as is always a fund of apparently purposeless and not the result of accidental deviations from a At the undirected the breeders’ attitude organisms. fixed norm. This is what the called form of of open-ended, divergent evolution was to the to ontogeny. same time, variation among individual to- troduced in opposition to Mayr “soft”the transithe addition of preordained stages ward char- Although convinced that the the view inheritance implied by thinking to population thinknaturalists of the time. Adaptation was not crucial once the basic variation pushed Darwin toward degree of variabil- tion from typological the Lamarckian process. that linear, ity is just a population of inter- The ing, and although of variation was clarified acter of the group was established, and the the specieswas artificially enhanced under domestication, undirected naturehe may have exaggerated the be extent to which Darwin himself made the conmight even- Darwin, nevertheless, accepted species Artificial Selection orthogenetic evolution of the group breeding individuals. Traditionally, that there mustboth through the study of large populations by tually generate bizarre nonadaptive characters some equivalent variability a every esThese non-Darwinian models were ultimately were treated as idealized types with in fixed wild popu- ceptual through the subsequent developmentthe Galton and transition, the breeding studies of of as a prelude to extinction—the theory of “racial lation. The analogy with artificial selection then the selection theory brought this implication out synthesis of the selection sence, the allowed from depict natural selection as geneticists. Although it took some time for the marginalized by thesenility.” Darwin could make no sense ofany variation him tothe norm being trivial a par- more clearly. theory and genetics theory proposed20th century. and impermanent. The breeders a few variantthey geneticists the accept the situation, their studies in the early by Cope and Hyatt, because he allel process in which knew that individuals, In to debates that followed the publication Genetic mutations seemed toimagine an evolutionary process driven inhuge changes in structure by ac- speciesmutation the Origin of Species, the analogyclaim could produce this case with characters useful to the of of On ultimately endorsed Darwin’s with could not be essentially plure- artificial selection environment could affect by predetermined trends. But the cumulating rather variations over a number of ralistic and undirected, providing just the source fact that such normal than the human breeder, survive and that the only way the continued to play a key role theories flourished in the late 19th generations. When Those with harmful characters are the by forcing even Darwin’s critics to think about of “random” variation that Darwin’s mechanism century dem- produce. Darwin linked this infor- elim- population was by selection. Modern evoluonstrates just how radical the theory of open- inated by the struggle for existence, just as the the problems of heredity and variation in a new required as its raw ended, divergent evolution was to the naturalists breeder will not permit any animal to reproduce if way (18). Opponents such ashas reopened the material. This later devel- mation with his conviction that species could tionary developmental biology Fleeming Jenkin, change indefinitelynot have time, he was wants. It wasquestion of whether variation and large variations opment highlights thethe time. it does over the character he driven the who saw selection working on evolution can of importance of another form of species Darwin in which not or as open-ended as Darwin and his folinsight gained by Darwin in the late 1830s, his toward a newbreeders who taughtconceptthat variation is be quite “sports of nature,” were, nevertheless, still Artificial Selection directed toward some preordained goal, allowing working within the framework defined vision decision to investigate the work of the animal the population becomes paramount. The natural lowers believed. But the non-Darwinianby this analogy. For supporters such as Francis Galton, These non-Darwinian models breeders (Fig. 3) and his recognition that theirwere ultimately him to build on hispart of the species’ adapt-evolution unfolding to an orderly, predictable range of variability becomes existing conviction that of marginalized by the synthesis of the selection ive evolution must be an open-ended, branching artificial selection helped to clarify the nature the result of accidental deviations plan has both heredity and selection, paving the way method of artificial theory and genetics in the early 20th century.notprocess. selection offered a useful character, been essentially marginalized by accepof how the equivalent natural from a fixed tance for the revolutionary which of Mendelian way of understandingGenetic mutations seemed to be essentially plu- norm. Thissame time, the called theattitude of the key insights onimpact Darwin based At the is what Mayr breeders’ process operated. The exact role played by Dar- just the sourcefrom typological thinking Darwin toward his theory of natural selection. toward variation pushed to populathe genetics. The notion of “hard” heredity was ralistic and undirected, providing transition of in the formulation of Darwin’s mecha- view that the species is just a population of introduced in opposition to the “soft” form of win’s study of breeding “random” variation thathis nism required as its raw material. theory is much debated by historians (16–17), This later development highof how important but there can be little doubt importance of another lights the artificial and natural selecthe analogy between insight gained by Darwin in the tion became in his later1830s, his decision tocase, late thinking. In this investigate the work of Wallace Darwin was truly unique, because eventhe animal breeders (Fig. 3) and himself did not take this step and dissociated his recognition that their method of artififrom the link with artificial selection expressed cial selection offered a useful way in Darwin’s later writings. of understanding how the equivDarwin turned to alentbreedersprocess operated. the natural in search of a The exact role played by Darwin’s clue as to how a population could be changed— study of breeding in the formulahere at least was a situation where modifications tion of his theory is much debated were actually being produced on(16–17), buttime by historians a human there scale and that could be investigated how imporcan be little doubt of directly. There was a well-developed network of breedtant the analogy between artificial ers by this time, andand natural selection became in his although their ideas about later thinking. In this case, Darwin heredity and variation were distinctly pregenetiwas truly unique, because even cal (like Darwin’s own), they hadtakeverystep and Wallace did not a this clear they produced from the in appreciation of how dissociated himself changes link their artificially small populations. The expressed with artificial selection insight Darwin’s may have that they worked byinselectionlater writings. been Darwin turned to the breeders important (this is the point of contention among in search of a clue as to how a experts studying Darwin’s notebooks),changed— population could be but the breeders certainly taught at least was a situation realhere him one thing. He where ized that in a domesticated population there bemodifications were actually is ing produced on a human time Fig. 3. Pigeons (23). always a fund of apparently purposeless and un-

could be investigated directly. interbreeding descent (15). The American for Existence The Struggle neo-Lamarckians scale and that for that transition in the late 19th century. It individuals. Traditionally, species the Men Who Discovered It (Doubleday, New Edward DrinkerOne of and most disturbing aspects There was a well-developed network of breeders were treated as idealized types with a fixed esCope the Alpheus Hyatt pro- of Darwin’s did, however, highlight the harsher aspects of York, 1958). posed that the evolutionwaseachappeal should be by for exis- and although their of struggle. The potential 2. P. Corsi, The Agebeing trivial Evolutionary theory of its group to the struggle this time, the consequences ideas about sence, any variation from the norm of Lamarck: Theories in knew 1790–1830 heredity the implications were drawn out even and clearly seen as a series tence as thelines moved throughequates with and variation were distinctly pregenet- moreimpermanent. The breedersFrance, that they (Univ. of of parallel natural process that changes Press, Berkeley, 1988). ical (like Darwin’s own), they had a very would could produce the same hierarchy of developmental stages, an up-agent. This very when Galton argued that itclear be necessary huge Californiain structure by acbreeder’s activity as a selecting 3. A. Desmond, The Politics of Evolution: Morover a and Reform how they produced changes in human race dated version of harsh vision of nature certainly threatened the of to apply artificial selection to the cumulating normal variationsMedicinenumber of in Radical the idea suggested in Chambers’s appreciation phology, their artificially small populations. The insight generations. Vestiges. The similarities linking the species in a Creator. The in order to prevent “unfit” individuals from When Darwin linked of Chicago Press, Chicago, London (Univ. this informatraditional belief in a benevolent genus were due not to“strugglecommon ancestry, that Thomas reproducing and undermining the biologicalconviction that species could change a recent for existence” occurs in they worked by selection may have been tion with his 1989). term 4. P. he was Evolution: The History of an but to parallel trends independently reaching the important (this is the point of contention among indefinitely over time, J. Bowler,driven toward a Robert Malthus’s An Essay on the Principle health of the population. This was the eugenics concept in which the Press, same stage of development. Like Chambers, they experts studying Darwin’s notebooks), but the new form of speciesIdea (Univ. of Californiapop- Berkeley, ed. of Population, although used in the context of program, and in its most extreme manifestation 3, 2003). endorsed the recapitulation theory (ontogeny breeders certainly taught him one thing. He ulation becomes paramount. The natural range of tribal groups competing for limited resources. at the hands of the Nazis, it led not just to the 5. J. A. Secord, Victorian Sensation: The Exrecapitulates phylogeny, in the terminology intro- realized that in a domesticated population there variability becomes part of the species’ character, traordinary Publication, Reception, and Secret Darwin saw that population pressure would lead sterilization but also to the actual elimination of duced by Ernst Haeckel) and saw evolution as is always a fund of apparently purposeless and not the result of accidental deviations from aNatural History Authorship of Vestiges of the to competition between individuals and was per- those unfortunates deemed unfit by the state. Did the addition of preordained stages to ontogeny. undirected variation among individual organisms. fixed norm. This is what Mayr called of Chicago Press, Chicago, of Creation (Univ. the transithinking Adaptation was hapscrucial once realize that it might represent Darwin’s the degree on variabil- tion from typological 2000). to population thinknot the first to the basic char- Although convinced that emphasis of the natural elimination a means by which the population ity was artificially maladaptive domestication, ing, and a 6. may have exaggerated the acter of the group was established, and the linear, could change ofenhanced under variants help to createalthough heD. Kohn, Ed., The Darwinian Heritage: A worked by climate of opinion in which through the (19, might evenCentennial Retrospect (Princeton extent to which Darwin himself made the con- Univ. Press, orthogenetic evolution oftime group20). The processDarwin, nevertheless, accepted that there must be such atrocities subsequent development of variability in every tually generate eliminating the least fit variants within theequivalentbecame possible? wild popu- ceptual transition, thePrinceton, NJ, 1985). bizarre nonadaptive characters some popu7. J. Browne, Charles Darwin: Voyaging (Jonahas artificial selection by lation and allowing the better adapted to survive the death itas a prelude to extinction—the theory of “racial lation. The analogyItwith to be admitted that,thenmakingselection theory brought this implication out than Cape, London, 1985). and breed. This was what the philosopher him self a natural selection as a par- more clearly. senility.” Darwin could make no sense of the allowedHer- to depictcreative force in nature, Darwin introduced 8. J. Browne, Charles Darwin: The Power of bert Cope and Hyatt, because he as the “survival in which and profoundly disturbing insight into the In the debates that followed the Cape, London, 2002). theory proposed by Spencer would later refer to allel process a new a few variant individuals, Place (Jonathan publication of the fittest.” Strictly speaking, in selection characters useful to the species of On the Origin Species, the G. Radick, Eds., could not imagine an evolutionary process drivennaturalthis case withworld, an insight that seems to have resonated 9. ofM. J. S. Hodge,analogy with The Cambridge Companion key role requires But differential such rather than the with the thinking of many re- artificial selection continued to play ato Darwin (Cambridge by predetermined trends.only the fact that reproduction among human breeder, survive andwho did not underUniv. variants, late 19th century dem- produce. Those stand or accept the details elim- by Darwincritics to think about theories flourished in the but Darwin thought that the pressure of with harmful characters areof his theory.forcing even Darwin’s Press, Cambridge, 2003). 10. M. J. S. Hodge, Stud. Hist. Biol. 6, 1 (1982). competition was necessary to make it effective. ism was not “responsible” for social Darwinism heredity and variation in a new onstrates just how radical the theory of open- inated by the struggle for existence, just as the the problems of 11. P. F. Rehbock, The Philosophical Naturalists: Malthus, he or eugenics in any reproduce if way (18). Opponents such as Early Nineteenth-Century British It seems that without naturalists ended, divergent evolution was to thethe input frombreeder will not permit any animal tosimple way. After all, some Themes in Fleeming Jenkin, would not have come up with the theory. not have the character he wants. It was the who analogy early geneticists endorsed eugenics by saw selection working (Univ. of Wisconsin Press, Madison, it does of the time. Biology on large variations 1983). The idea of struggle was pervasive in thewho taught Darwin that variation is not ordismissing nature,” were, nevertheless, still breeders lit- with animal breeding even while “sports of Artificial Selection exploited in natural selection goal, allowing working within the framework defined by this erature of the period, but could be directed toward some preordainedas the mechanism of evolution. 12. R. J. Richards, The Meaning of Evolution: The Morphological Construction many models were In the 1850s, Spencer had And the Nazis wanted to purify fixed racial These non-Darwiniandifferent ways. ultimately him to build on his existing conviction that adapt- a analogy. For supporters such as Francis Galton,and Ideological Reconstruction of Darwin’s Theory (Univ. of marginalized by the synthesis of competition could be turned must bewhich they certainly did not want to admit already seen how the selection ive evolution type, an open-ended, branching artificial selection helped toPress, Chicago, 1992). Chicago clarify the nature of both But 13. selection, paving the way theory and genetics ain the different, and in some respects less had evolved gradually from an ape ancestry.heredity andA. Desmond, J. R. Moore, Darwin’s Sacred into very early 20th century. process. At For by proposing that evolution worked the revolutionary impact of Mendelian Quest for HuGenetic mutations seemed to be essentially pluCause: Race, Slavery and the disturbing, mechanism of progress (21).the same time, the breeders’ attitude for primarily man “hard” heredity London, 2009). ralistic and undirected, providing just the source toward variation pushed Darwin toward the variants, Dar- notion ofOrigins (Allen Lane,was Spencer, the interaction between individuals through the elimination of useless genetics. The 14. E. Mayr, the Long form of that the win created an a population of introduced of “random” variation that Darwin’s mecha- toview chang- species is just image that could all too easily bein opposition to One “soft”Argument: Charles Darstimulated their efforts to adapt the win and the Genesis of Evolutionary Thought nism required asing raw material. its social and physical environment. He then exploited by those who wanted the human race (Harvard Univ. Press, Cambridge, MA, 1991). This later development high- concept of the “inheritance to conform to their own pre-existing ideals. In 15. P. J. Bowler, The Eclipse of Darwinism: Antiinvoked Lamarck’s lights the importance of another of acquired characteristics” to explain how these the same way, his popularization of the struggle Darwinian Evolution Theories in the Decades insight gained by Darwin in the accumulated over many gen- metaphor focused attention onto the individualAround 1900 (Johns Hopkins Univ. Press, self-improvements Baltimore, MD, 1983). late 1830s, his decision to inves- to biological evolution and so- istic aspects of Spencer’s philosophy. erations, leading 16. R. J. Richards, Stud. Hist. Philos. Sci. 28, 75 tigate the work ofprogress. Spencer’s self-improvement modthe animal Modern science recognizes the importance cial (1997). breeders (Fig. 3) and his recogel of progress became immensely popular in the of Darwin’s key insights when used as a way 17. M. Ruse, J. Hist. Ideas 36, 339 (1975). nition that their later 19th century, and because it too seemed to of explaining countless otherwise mysterious 18. J. Gayon, Darwinism’s Struggle for Survival: method of artificial selection offered on struggle as the motor of change, it was aspects of the natural world. But some of those Heredity and the Hypothesis of Natural Serely a useful way of understanding howconfused with the Darwinian mechanism. insights came from sources with profoundly dislection (Cambridge Univ. Press, New York, often the equiv1998). alent natural process operated. In fact, Spencer thought that all humans will turbing implications, and many historians now 19. P. J. Bowler, J. Hist. Ideas 37, 631 (1976). The exact role played by Darwin’s eventually acquire the faculties needed to inter- recognize that the theory, in turn, played into 20. A. Desmond, J. R. Moore, Darwin (Michael study of breeding in the formulaact harmoniously with one another. But his occa- the way those implications were developed by Joseph, London, 1991). tion of his theory is much debated sional use of highly individualistic language al- later generations. This is not a simple matter of 21. M. Francis, Herbert Spencer and the Invention by historians (16–17), but there of Modern Life (Acumen, Stocksfield, UK, lowed him to be perceived as the apostle of free science being “misused” by social commentacan be little doubt of how impor2007). tant the analogy enterprise. Much of what later became known tors, because Darwin’s theorizing would almost 22. C. Darwin, Transmutation Notebook B, from between artificial as “social Darwinism” was, in fact, Spencerian certainly have been different had he not drawn Natural Selection portfolio p. 36 (Cambridge and natural selection became in his Univ. Library, Cambridge, 1838); P. H. Barlater thinking. In social Lamarckism expressed in the terminology inspiration from social, as well as scientific, inthis case, Darwin rett, P. J. Gautrey, S. Herbert, D. Kohn, S. of struggle popularized by Darwin. fluences. We may well feel uncomfortable with was truly unique, because even Smith, transcribers and Eds., Charles DarThis step and important in the context of those aspects of his theory today, especially in point is Wallace did not take this win’s Notebooks p. 180 (British Museum of the from the link by modern opponents of light of their subsequent applications to human charge raised dissociated himself Natural History, Cornell Univ. Press, Ithaca, Darwinism that the with artificial selection expressed theory is responsible for the affairs. But if we accept science’s power to upNY, 1987); available at the Darwin Digital Library, http://darwinlibrary.amnh.org/. in Darwin’s laterappearance of a whole range of unpleasant social set the traditional foundations of how we think writings. policies breeders Darwin turned to the based on struggle. Darwin exploited the about the world, we should also accept its po- 23. G. Neumeister, Das Ganze der Taubenzucht (B. F. Voigt, Weimar, 1876). idea of the struggle in search of a clue as to how a for existence in a way that tential to interact with moral values. was unique until paralleled by Wallace nearly population could be changed— here at least was 20 years later. Their theory certainly fed into a situation where the actually bemodifications were movements that led toward various kinds of References and Notes 1. L. Eiseley, Darwin’s Century: Evolution and social Darwinism, Fig. 3. not the (23). ing produced on a human time but it was Pigeonsonly vehicle www.sciencemag.org SCIENCE VOL 323 9 JANUARY 2009

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Speciation
REVIEW

Red Queen and the Court Jester: ies Diversity and the Role of Biotic Abiotic Factors Through Time

disentangle key aspects of clade histories. Clades are monophyletic, including all descendants of an ancestor, whereas taxa may be monophyletic or vestigations, excludingan outline of how of the paraphyletic, provide some descendants these and other Comparative macroecological studies ancestor. studies correspond to the predictions disentangle key aspects of clade and multilevel of the Red Queen, Court Jester,histories. Clades add monophyletic, including all descendants of an REVIEW are rigor to analyses showing that sister clades outline some phymixed models (Table 1), and timing of increases may vary whereas taxa may be monophyletic or ancestor, in rate of evolution, logenetic studies of themorphospace occupation, macroevolution of spein species richness and some descendants of the paraphyletic, excluding cies distributions of evolutionary novelties across and diversity. ancestor. Comparative macroecological studies lineages and subclades. Here, I that sister clades add rigor to analyses showing will explore the The Global global, taxicDiversificationprovide Pattern of investigations, largest-scale rate of evolution, timing of increases may vary in Michael J. Benton Through Time these morphospace occupation, an species of how and and other studies correin outline richness A keytoquestion of evolutionary novelties across spond the predictions of theoriginQueen, Court and distributions about the Red of modern Evolution may be dominated by biotic factors, as in the Red Queen model, or abiotic factors, biodiversity is how mixed models (Tablespecies Jester, and multilevel today’s 10 will exploreand lineages and subclades. Here, I million 1), the as in the Court Jester model, or a mixture of both. The two models appear to operate arose from a single ultimatestudies of the provide outline some global, taxic investigations, macrolargest-scale phylogenetic species of microbial predominantly over different geographic and temporal scales: Competition, predation, and other Michael J. Benton life outlinemillion years ago (Ma) (Fig. 1).correevolution of speciesthese and other studies Two an 3500 of how diversity. biotic factors shape ecosystems locally and over short time spans, but extrinsic factors such as modelsto the predictions of the Red Queen, Court spond for global diversification are termed the key aspects of clade and climate and oceanographic and tectonic events as in the Reddisentanglemodel, regionally histories. Clades saturation/equilibrium model (5–7) and the exof Diversification Evolution may be dominated by biotic factors, shape larger-scale patternsincluding all descendants of an The Global Pattern mixed models (Table 1), and Queen are monophyletic, or abiotic factors, Jester, and multilevel globally, and through thousands and millions of years. Paleobiological studies suggestmonophyletic or pansion model (8–11). The equilibrium model as in the Court Jester model, or a mixture of both. The two ancestor, whereas taxa may be that species Through Time models appear to operate outline some phylogenetic studies of the macrodiversity is driven largely by abiotic factors such as climate, paraphyletic, excluding some descendants of the has prevailed, among the origin of modern biolandscape, or food supply, and A key question about marine paleobiologists at predominantly over different geographic and temporal scales: Competition, predation, and other evolution of species diversity. ancestor. dynamics. macroecological studies diversity is how today’s 10 million species arose Comparative comparative phylogenetic approaches offer new insights into clade but extrinsic factors such as biotic factors shape ecosystems locally and over short time spans, least, for a long time, and represents a classic add rigor to analyses showing that sister clades from Queen viewpoint because climate and oceanographic and tectonic events shape larger-scale patterns evolution, timing of increases Red Global Pattern of species ofitmicrobial priThe a single ultimate Diversification implies life may vary in rate of regionally and not it export organism-level operates to Through Time here are two ways of of viewing evolu- years. Paleobiological studies suggest processes in marily biotic years ago (density dependence) on viewing evolution, portant and to is likely that evolution that species 3500 million controls (Ma) (Fig. 1). Two modglobally, andare two ways here through thousands and millions of scales, in species richness and morphospace occupation, through the spectacles of eitherof either regional or global scales,evolutionary novelties that els key question about the origin of termed the diversity is driven largely by abiotic factorsRed as pluralistic way (3). or food supply,likely across global diversity. diversification are modern biolandscape, tion, through the spectacles the such a climate, and distributions of and it is and A for global lineages in a explore Queen or Queen or the Court Jester. The evolution are two broadpluralistic I will for the diversity is how today’s 10 million and the excomparative phylogeneticJester. The Red Queen insights into clade and subclades. Here,way (3). stud- saturation/equilibrium modelof the species arose There operatesdynamics. investigations, provide methodologies There are two versions (5–7) equilibrium the Red the Court approaches offer new largest-scale global, taxic model (1) stems from Darwin, whoDarwin, evo- ies There areoutline of howthrough time, studies corre- model, model (8–11). The equilibriumthe global enton of species diversity methodologies for studies pansion single ultimate specieswhen model has Red Queen model (1) stems from viewed who from a differing in the time of microbial life an two broad these and other taxic and diversity organism-level processes to lution asevolution asways of of a balance of bi- phylogenetic (4).thethrough time, taxicQueen,phy- marine ecosystemmarine paleobiologists at modprimarily a primarily biotic evolution, portant not to exportpredictions approach involves 3500 million years ago (Ma) (Fig. 1). Two least, viewedhere are two balance viewing pressures, of species spond to The taxic of the Red and Court prevailed, among became saturated. Sepkoski’s y be dominated by biotic factors, as in the Red Queen model, or abiotic factors, Jester, and mostpressures, mostspectacles of was character- treating species, genera, mixed models (Tableinde- coupled globaland represents a classictermed the notably competition, and it scales, and it is as that Red otic a through the notablymodelseither theoperate logenetic or globaltaxic approach involves treat- for a for time, diversification identified Queen competition, and it regional (4). The multilevel or familieslikely1), and els long logistic model (5) are Red three urt Jester model, or mixture of both. The two appear to phylogenetic studies of the macroized characterizedQueen’s Jester. The to Alice in pendent outline some or pluralisticas independent equilibria,because it implies primarilyand of consaturation/equilibrium model (5–7) biotic exoperates Queen or by the Red Competition, Queen evolution evolution ofin a families was by the Red the Court statement Redpredation, ing species, genera, counting their occurrences viewpoint in the Cambrian, most the the y over different geographic and temporal scales:Queen’s statement and other entities andspecies diversity. way (3). Through inand over shortDarwin, who takes allevo- entities and counting their occurrences against Paleozoic, and(8–11). Theaon global diversity. in theThrough time spans, “it viewed factors against are two broad methodologies for studies trols (density dependence) equilibrium model has Looking-Glass that but extrinsic “it shape ecosystems locally stems fromthe Looking-Glass that the such as time and other factors. The phylogenetic pansion model perhaps third, beginning There model (1) to Alice oceanographic and tectonic eventsdo, to larger-scale patterns regionally and speciesThe Global Pattern oftime, taxic and phyother running you can shape you canthe samekeep in time and uses cladograms orDiversification ap- the There areand continuing of the present (Fig. diversity through phylogenetic lution all primarily as the running keep of do, to place.” of takes and millions of a balance in biotic pressures, approach Throughfactors. The molecular trees to prevailed, among marine paleobiologists at least, Pliocene two versions to the equilibrium through thousands Court Jester years. Paleobiological studies suggest that species uses cladograms or molecular trees to The notably competition,(2) isit that evolution, proach (4). TheTime approach involves treat- model, differing in the time classic the global model and was character- logenetic for a long time, and represents when Red Queen taxic most disentangle key aspects of clade histories. Clades 2A). These three equilibriumalevels correspond riven largely the samefactors such as climate, landscape, or food supply, and by abiotic place.” The Court Jester model (2) is A of modern biospeciation,offer newQueen’sinto clade dynamics. in ing species,key question about the origin independent viewpoint because it implies primarily biotic conand genera, ortoday’s all descendants of families as ized evolution, extinction rarely extinction rarely are monophyletic, including 10 million species arose to three sets of phyla, the Cambrian, Paleozoic, by the Red insights and happen except in statement to Alice phylogenetic that approaches speciation, diversity is how response to unpredictable changes“it the physical entities and countingultimate occurrences against trols (density dependence) on global diversity. Through the Looking-Glass that in takes all the Fig. 1. Operation taxa may be monophyletic from a single Red species happen except in response to unpredictable an ancestor, whereasof their Queenof microbial life and Modern, that interacted and successively environment, recalling keep to the same place.” time and other factors. The phylogenetic apTwo re two ways of viewingyou can do,portant not in export organism-level processes to 3500 million years ago (Ma) (Fig. 1).A mod- replaced eachtwo versions of the equilibrium There are other through the Cambrianrunning evolution, to the capricious behavior (biotic causation) and Court Jester changes in the physical environment, recalling or paraphyletic, excluding some descendants h the spectacles theeither the Red model (2) global scales, and it is likely that uses for global diversification are termed Genus model, differing in the time when the global of of Court Jester regional or is that evolution, proach els cladograms or molecular trees the licensed fool of to Thecapricious behaviorMedieval times. Neither (abiotic ancestor. Comparative macroecological Ordovician and Permo-Triassic intervals, differof operates in a pluralistic way of the The Red Queen evolution the licensed fool of (3). the causation) models atmodel (5–7) and the life span saturation/equilibrium exor the Court Jester. model wasand extinction rarely happenand both as speciation, proposed Thereexclusive, except in ent geographic to temporal scales Medieval times. Neither are was proposed as studies pansionand analyses showing that sister My) equilibrium model(3-6 has ms from Darwin, who viewed evobroad Darwin andunpredictablemodeltwo infor methodologies for studies add rigormodel (8–11). Thepaleobiologists at least, reaching higher equilibrium levels after each Van Valen (1) allowed theextrinsic and phy- prevailed, among response toand both of species diversity through time, taxic clades may vary in rate marine at timing of long-term replacement Court The second model changes Van Valen (1) (A). The Red Queen mayof evolution, physical marily a balance of biotic pressures, prevail event. exclusive, Darwin and Fig. 1. for a long time, and represents a classic Red Queen Red Queen Jester competition, influences on evolution in their The taxic approach involves treat- Operation oflevel on short and it was character- logenetic (4). primarily biotic, environment, and species Species allowed to Alicerecalling species, genera,evolution in independent causation) because it implies primarily A con- (6, 7) identifies a single equilibrium level from for views. ing the capricious families as organismicviewpoint and Court Jester extrinsic influences on or behavior increases in species richness and morphospace (biotic biotic life Red Queen’s Red Queen statement in of the licensedbiotic, Red Queen views. Neither time scales, whereas the Court Jesterevolutionary span fool Medieval times. Genus their primarily the of a and Queen their occurrences(abiotic causation)distributions on global diversity. My) early Paleozoic, perhaps 400 Ma, to the occupation, and models at differLooking-Glass that “it takesdiversityentities Red counting world deagainst trols (density dependence) of (1-2 the Species all life his The model same place.” time asa exclusive, andworld novelties own on lineagesversions of the equilibrium span was diversityinin and Red factors. Theboth holdsap- across larger scales. subclades. Here, present (Fig. 2B). In both models, the equilibria proposed There are two and can do, to keep in the other Queen phylogenetic geographic and temporal scales Species ent (3-6 pends primarily on intrinsic factors, such as body stippled green shape showsthe time when the global My) Red Darwin primarily on intrinsic factors, such as I trees to model, differing in an area ester model (2) is that and Van Valen (1)uses cladogramsextrinsic evolution, proach allowed for or molecular (A). The Red Queen may prevail at Court Milankovitch to biodiversityApparent saturation in which depends will explore the largest-scale global, taxic in- correspondQueen? size, breadth of in where Red Queen effects might be d extinction rarely happen except physiological tolerance, or adaptJester Queen Red influences on evolution in their primarily biotic, organismic and species level on short Scale (100 ky) Species body to hard times. of physiological tolerance, from scale effect ability size, breadth In a Court Jester world, spe- identified erroneously, but these are npredictable changes in the physical Red Queen views. life span 1. Operation of Red Queen (biotic causation) Fig. or adaptability to Fig. 1. Operation of Red Queen time the result of spatial Court Jester recalling the capricious behavior hard times. In a Court Jester ciesSpecies diversity(biotic fluctuations in climate, likely scales, whereas theaveraging of diversity dependsin a causation) and worldJester A on Red Queen Court deLocality Average Biotic Entire (1-2 My) his ed fool of Medieval times. Neither and Court Jester (abiotic causation) models at difworld, species diversity depends onmodels course, regional responses to climate change fluctuations holdsGenus own on larger scales. The species region/ continent landscape, and food (abiotic causation) of at differsupply. In reality, life green proposed as pends primarily on intrinsic factors, such as body exclusive, and both Red range climate stippledspan shape shows an area ferent geographic and temporal scales (A). The Red in climate, landscape, and food supply. In real- and other complex physical perturent geographic and temporal scales Apparent (3-6 My) Milankovitch zone Van Valen (1)both aspects might prevail in different ways and at allowed for extrinsic Queen? size, breadth of physiological tolerance, or adapt- where Court be Queen Red Queen The might prevail Scale (100 ky) may prevail at organismic and species level ity, of course, both aspects perhaps be called dif- bations Red Queen effects might dithat may be in opposite what(A). a Court Queen may prevail at could Red Jester levelin short the Jester evolution in different times,times.organismic and speciesworld, spetheir primarily biotic, fromthe scale Jester holds ability to hard In on Species on short time scales, whereas scale effect identified erroneously, but these are Geographical Court iews. ferent ways and model. Traditionally, Court Jester different times, multilevel mixed at time scales, whereas thebiologists rections,span so cancel each other, cies diversity depends on fluctuationswhat could likely life and of spatial in climate, his own on larger scales. The stippled green shape the Locality Average Biotic Entire (1-2 result iversity in a Red Queenbe called the multilevel mixedscales. The suggesting no controlling averaging of effect of the perhaps world think in a his own on larger course, have tended to de- holds RedIn reality, of model. regional My) species region/ continent shows an area where Red Queen effects might be supply. Queen, Darwinian, responses toRed climate change ly on intrinsiclandscape, and food stippled green shape shows an area factors, such as body physical environment on evolution. range these are likely the reclimate Apparent B Traditionally, biologists have tended to think a Milankovitch intrinsic, biotic factors way, and geologists in at and other complexQueen? identified erroneously, but zone of physiological tolerance, or adapt- prevail Reddifferent ways andin both aspects might where in Queen effects might be physical perturRed Queen Scale (100 ky) a Red Queen, Darwinian, erroneously, but these are bations that may be in disruptions Court Jester, extrinsic,could intrinsic, biotic the Physical-environmental opposite scale effect from did times. In a Court Jester world, spe- identifiedperhaps beway. facdifferent times, what physical factors called Genus sult of spatial averaging of regional responses to along Biotic Geographical scale depends on fluctuations inandthe divergencea between averaging of may elicit and soresponsesAverage the result of torsMuch of geologists Traditionally, biologists rections, biotic cancel each other, way, climate, likely in Court Jester,Red exclimate change and other complex physical perturLocality Entire life span multilevel mixed model.theresponsesspatial the change red line separating Red Queen and species region/ continent (3-6 My) d food supply. In reality, ofCourtfactors world views may depend course,Jester way. regional to climate bations that may be in opposite directions, and so Queen and trinsic, physical range the have tended and at in other Queen, Darwinian, suggesting outcomes (B). The ofclimate might prevail in different ways to thinkand a Redcomplex physical pertur- Court Jester no controlling effect usage zone cancel each other, suggesting no controlling effect Court scale of (Fig. bations that interactions in a physical evolution. s, what couldon Much bioticthe divergence and geologistsdrive perhaps be called factors way, may be in the Red intrinsic, (2) the 1): Biotic between opposite di- here is the environment on Red Queen,scale B Species microevolutionary Geographical of the physical environment on evolution. PhysicalJester much ofand local-scale successso cancel each may Physical-environmental disruptions or views QueenJester, Court rections, world failure other, xed model. Traditionally,the extrinsic,Jester and factors way.of inbiologists Court physical life span as opposed to the macroevolutionary Genusenvironmental disruptions may elicit biotic reo think in a Red Queen,onpopulations, and species (Redeffect of the dividuals, of the(2) suggesting nobetween the Red may elicit biotic responses along the (1-2span depend Darwinian, divergenceBiotic interactions (Fig. 1): controlling Queen), life My) Much scale Queen that posits exphysical sponses along the red line separating Red Queen ic factors way, and geologists in a processes environment on evolution. Red line separating Redconstant and B (3-6 My) Queen but perhapsCourt Jester local-scale may depend red are overwhelmed or drive much of the world views success by tinction risk, a view that has been largely Queen and these Physical-environmental disruptions and Court Jester outcomes (B). The usage here is extrinsic, physical factors way. Red Milankovitch Court Genus outcomes (B). The usage Jester substantialindividuals, climaticinteractions drive rejected span Illustration based on (2). failure of the Red 1): Biotic processes along the on scale tectonic may elicit biotic responses at time life (31). the divergence between (2) (Fig. and populations, and species the microevolutionaryCourtQueen, as opposed to Red Queen Scale (100 ky) 5 (3-6 My) Red Queen and Species scales of the local-scaleline separating failure is im- here is the microevolutionary Red Queen, above 10 but red (Court these processes years successJester). It of inJester ourt Jester world views may depend (Red Queen), perhaps or much the Court Jester outcomes (B). The usage life span macroevolutionary Red Queen that posits conas opposed to the macroevolutionary Court (Fig. 1): Biotic interactions drive by substantial tectonic and are overwhelmed stant extinction risk, a view that has More largely been Less dividuals, populations, and species (Red Queen), Species (1-2 My) Jester local-scale success or failure of in- here is the microevolutionary Red Queen, Red Queen that posits constant exlife span Departmentprocesses as opposed to the of Bristol, Bristol rejected (31). Illustration based on (2). at time scales above by climatic of theseSciences, University macroevolutionary but perhaps Earth processes are overwhelmed105 pulations, and species (Red Queen), Environmental scale (1-2 My) tinction risk, a view that has been largely BS8 1RJ, UK. E-mail: mike.benton@bristol.ac.uk at time Red Milankovitch years (Court Jester).Red climatic processes largely It Queen that posits constant exhese processessubstantial tectonic andis important not to export are overwhelmed by tinction risk, a view that has been rejected (31). Illustration based on (2). Queen Scale (100 ky) Red 5 Milankovitch ctonic and climatic processes at time years (Court Jester).or global organism-level processes (31). Illustration based on (2). scales above 10 rejected to regional It is imQueen Scale (100 ky) 5

The Red Queen and the Court Jester: Species Diversity and the Role of Biotic The Red Queen and the Court Jester: and Abiotic Factors Through Time Species Diversity and the Role of Biotic and Abiotic Factors Through Time

Speciation

SPECIALSECTION
new taxa could become established only by on diversity, or vertebrates, because regimes SPECIALSECTION plants, insects, and other correction marine ecosystem became saturated. these groups seem to as to produce Sepkoski’s coupled Key model (5) driving others to extinction.logistic evidence may be so complexhave radiated data in explosively, without diversity plateaus, because origination equilibria, in the which geologic andorbiologic signals are is that ecosystem threeand extinction rates plants, insects, vertebrates, marinebothidentifiedbecame saturated. Camparticularly in separated. million brian, most of the not obviouslythe past 100 to have radiated appear to have been density-dependent (5– these groups seem Sepkoski’s coupled logistic Paleozoic, and permodel (5) years (My) (10). haps a third, beginning in the Pliocene Life on land today may be as much as 7), limitingand continuing to the present rises in diversity and promoting explosively, without diversity identified three equilibria, in the Cam- (Fig. Resolution between the equilibri- plateaus, particularly in the past 100 brian, recoverythe Paleozoic, and per- levels of These three equilibrium 25 times asand between life inand sea, so it rapid most 2A).after extinction events. um models, diverse as these the million years models, haps a third,correspond toinfor globalphyla, the beginning the Pliocene expansionist(My) (10).might seem Alternative models three sets of diversimay be wrong to generalize from marine straightforward, but thebetween the Perhaps Cambrian, Paleozoic, and Modern, that Resolution solution life. and continuing to the present (Fig.global paleontological studies to all de- equilibrification are expansionist, allowing pends um sea showand between on models, similar patterns of ex2A). Theseinteracted rise,successively replaced three equilibrium levels species diversity to and with damping, but land andadequate assessment of the these and quality of the fossil record. The longeach other through the Cambrianexpansionist models, might seem correspond predictable limit (8–11). Dento three sets without a Ordovician andof phyla, the interponential increase for global diverterm saturation model in species numbers (8, Permo-Triassic Cm O S D C P Tr J K Pg Ng straightforward, but arises Cambrian, Paleozoic,origination and extincand Modern, that levels sity dependence of higher equilibrium 9, 11), or perhaps they differ solution key sification (Fig. 2, blue curve)the in their devals, reaching 500 400 300 200 100 0 pends on adequate assessment giant interacted and successively replacement event. from (13, 14), with the sea acting after not preclude expansionist tion rates doeseach long-term replaced rulesextensive attempts to correct data as aof the Time (Ma) quality of dish, where species longeach other The second may Cambrian- by through model (6, 7) identifies sets for sampling the (6, 7), wheremodels because they the be dampened a Gaussian petri errorfossil record. Thediveras theterm saturation modelexpanOrdovician singlePermo-Triassic from of food Fig. 2. Cm O of marine animal genusTr and such as shortage the limiting factors equilibrium level inter- early ismultiple-equilibria and for global diverequilibrial Patterns S D diversification through Ng past sity models originallyand density-dependent, C P J K Pg the sion sification (Fig.used raw data, Paleozoic, perhaps 400 Ma, Fig. 2. animal 2, blue curve) arises vals, reachingactive predation, as well to the 530 My,Patterns of marine two linesgenus diversification through and the land witnessing continuing (dampthe Phanerozoic. The 300 compare current estimates from or space, or higher equilibrium levels asthe 400 0 without correction (5, 8–11), although present (Fig. 2B). In both models, by the past500 My, the Phanerozoic. The200 lines 100 530 two compare current after each long-term replacement event. climate andequilibria correspond to biodiversity the empirical (uncorrected) Sepkoski database (red Sepkoski sampling- ened)from extensive attempts to correct ever other physical factors. Further, estimates from the empirical (uncorrected) line) and database more recent analyses rise inadiversity as data exponential return someTime (Ma) The secondsaturation(6, 7) identifies amodel standardized (corrected) analysis of the Paleobiology Database (blue line). new dampenedsampling errorare conquered model in which new taxa sectors but congruent (6, it seems that the coupled logistic could The empirical curve (red line) suggests that global marine diversity reached what sets for of ecospace signal 7), where(red line) and sampling-standardized (corrected) analysis of the the model for global diversificasinglebe partly anestablished the earlydriving equilibrium level from of taxonomic when as Anymultiple-equilibria and expancorrections are imposed. Corbecome artifact only by may Paleobiology Databaseanimal genus(450 to 250 Ma) and has line) a possible plateau through (blue line). The empirical curve (redrisen, (9, 14). marine the Paleozoic Paleozoic, 2, red to extinction. Key evidenceFig. 2. Patterns of global marine since. Thediversification through the past must encompass the independentdata, perhaps 400 Ma, to the is apparentlythat sampling-standardized curve rection suggests exponentially, ever diversity reached a possible plateau tion for sampling is clearly esscale (Fig. others curve); it was worked out My, the Phanerozoic. The two lines compare current estimates from sion models originally used raw evi530 sential (6, 7), and future investigation that both both extinction present (Fig. 2B). In origination and the not (blue line) suggests that (450 tomarineMa) and has risen, apparently dencewithout correction (5, 8–11),of organthrough (uncorrected) Sepkoski database reached for increasing complexity at ordinal and familial to models, does the empirical the Paleozoic global 250 diversity(red line)near-modern must determine appropriate indepen- although rates appear levels but density- levels some 400 Ma and there has been only modest increaseand samplinghave been since then. a equilibria correspond to biodiversity exponentially, ever analysis of sampling-standardized curve (blue isms, more recent analyses return of somesince. The the Paleobiology Database (blue line). work convincingly (5–7), limiting rises in standardized (corrected) increases in the occupation novel dependent at generic or specific Cm, Cambrian; C, Carboniferous; D, Devonian; J, Jurassic; K, Cretaceous; dent proxies for preservation and hudiwhat dampened but congruent signal saturation in which new taxa could The empirical curve (red line) suggests that global marine near-modern line) suggests that global marine diversity reached diversity reached error; some current proxies (such man levels (10, versity there are problems with Ng, Neogene; O, Ordovician; P, Permian; Pg, Paleogene; S, Silurian; Tr, ecospace, explosive evolution within par11), and promoting rapid recovery imposed. Corbecome established onlyevents. by driving a possible plateau on (6). the Paleozoic been only modest increase as when fossiliferous localities) levels Based through after assumptions (11, 12), and Triassic.some 400 Ma and there has (450 to 250 Ma) and has risen, number ofcorrections are of novel clades key numerical extinction ticular clades, and addition others to extinction. Keymodels for global apparently then. Cm, Cambrian; since. The sampling-standardized curve themselves dependent on diversity,clearly esare rection for sampling is Alternative evidenceaisglobal since exponentially, ever C, Carboniferous; D, Devonian; J, Ju- without the loss of precursors (9, 11, 15), dithe background assumption of that both origination and expansionist, allowingline) suggests that global marineO, Ordovician; P,red near-modern sential (6, mayandso complex and Pg, be future investigation versification are extinction global partly an artifact of taxonomic scale (Fig. (blue rassic; K, Cretaceous; Ng, Neogene; diversity 2, Permian; other correction regimes 7),happened many times in carrying capacitydiversity to (8, 10, 11). Paleogene; S, Silurian; Tr, Triassic. Based on (6). reached all of which have species is doubtful rates appear to have been rise, with damping, but with- curve); it was workedbeen only modest increase as to produce data in which geologic and biologic independensity- levels some 400 Ma and there has out at ordinal and familial since then. must determine appropriate loFurther, it out a predictable to export not dent proxies dependent has proved hardrises in di-theDensity depen- C, Carboniferous;work convincingly Jurassic; K, Cretaceous; obviously separated. preservation and hu(5–7), limiting limit (8–11). Cm, Cambrian; levels but does not D, Devonian; J, at generic signals are the past 500 My. for today may dence of much more speciose rates does curve) arises from extensive attempts with and extinction gistic model to the originationrecovery terrestri- not or specific levels (10, 11), there are problems to cor- Life on land man error; be as much as proxies (such some current 25 versity and promoting rapid Ng, they as preclude expansionist models because Neogene; O, Ordovician; P, Permian; Pg, Paleogene; S, Silurian; Tr, Large-Scale number of so it may be Species Diversity 7), backal realm, whether one considers plants, insects, may key numerical assumptions (11, 12), and thewhereastimes as diverse as life in the sea, fossiliferous rect data after extinction events. by limiting factors such as shortage on (6).sets for sampling error (6, capacity is wrong to generalizeControls on paleontolog- localities) from marine be dampened these groups Triassic. Based multiple-equilibria and expansion models because Taxic paleobiological studies have on diversity, or vertebrates, models for global di- seem to the ground assumption of a global carrying are themselves land and sea Alternative or space, or active predation, as well as by doubtful (8, 10, 11). Further, it has proved hard to ical studies to all life. Perhaps dependent provided a of food have radiatedare expansionist, allowing global it export artifactraw taxonomic the much moreredshow similar patternsevidence about controls,complex originally used of model to scale (Fig. 2, and other of of exponential may be so versification explosively, without diversityFurther, partly an the logistic data, without correction (5, great dealcorrection regimes increase in mainly climate and other physical factors. plateaus, diversity to rise, coupled logistic model may curve); although moreout at ordinal considers 8–11), it was worked recent analyses familial abiotic, on species 11), or perhaps they biologic seems that the past 100 million withas numbers (8, 9, diversity. Biotic and speciesparticularly in the with damping, but years be speciose terrestrial realm, whether oneandreturn aspecies to produce data in which geologicfactors, such (My) predictable Macroevolutionary phenomena and levels but for either work congruent signal when as Jester (physical, extrinsic)separated. somewhat dampened Red Queen (biotic, intrinsic) or signals are not obviously models. Many out a (10). Table 1.limit (8–11). Density depen- their support does not thebut convincingly at generic Court body size, diet, colonizing ability or ecologiResolution between extinction and somodels, or specific mixed.” corrections are imposed. Correction for with specialization, appear to be as much as on could fit either worldview, rates are not dence of origination andthe equilibrium does noted as “multilevellevels (10, 11), there are problemssam- cal Life on land today may have little effect 25 and between these and expansionist models, pling is clearly essential (6, 7), and future back- times as diverse modern organisms, may be preclude expansionist models because they may key numerical assumptions (11, 12), and theinves- the diversity of as life in the sea, so italthough Red Queen Court Jester Multilevel mixed might seem straightforward, such as solution tigation must determine appropriate indepen- wrong to and r-selected life-history characbe dampened by limiting factorsbut the shortage ground assumption of a global carrying capacity is abundancegeneralize from marine paleontologInterspecific competition of the Waxing and waning of clades in association with and humanVicariance and dispersal in major phylogenetic splits (17) litter size, error; ical studies to all life. Perhaps land depends on adequate assessment quality doubtful (8, 10, 11). dent proxies for preservation of food or space, or active predation, as well as by and oceanographic eventsFurther, it has proved hard to teristics (short gestation period, large and sea tectonic (2, 17) fos- show gradient (22–24) of the and record. The long-term Further, extinctions andcurrent extinction events to the muchLatitudinal diversity similar patterns of exponential increase in climatefossil other displacement physical factors. saturation export smaller proxies (such as number ofmore and short interbirth intervals) sometimes correit some the logistic model Character Mass blue siliferous localities) eruptions, model for the coupled logistic model 2, triggered speciose causes such asare whether one considers species high species 9, 11), or perhaps they seems that global diversification (Fig. may be by extrinsicterrestrial realm, themselves dependent late withnumbers (8, richness (16).
3000 600 400

Number of 3000 genera 2000 (empirical; red)

Number of genera 400 600 (corrected; blue)

2000

Number of genera (empirical; red)

1000

tion

T T T

Temporal scale Temporal scale

Table 1. Macroevolutionary phenomena Coordinated support for either the Red Queen (biotic, intrinsic) or Court Jester (25) and their turnovers, originations, and extinctions (physical, extrinsic) models. Many Evolutionary arms races (1) Occupation of new ecospace could fit either worldview, and so are noted response to physical perturbations– termed as “multilevel mixed.” in
Red Queen InterspecificConstancy of ecological competition guilds through time (25) tectonic and oceanographic events (2, 17) Incumbency advantage Lack of evidence for a global carrying capacity and Character displacement Mass extinctions and smaller extinction events (3, 24) equilibrium levels (8, 10) triggered by extrinsic causesgreat “evolutionary Lack of cohesiveness of the such as eruptions, climate change, anoxia, impact (10, 11) faunas” (12) Species richness–energy relationship (18, 19) Evolutionary arms races (1) Coordinated turnovers, originations, and extinctions
“coordinated stasis” or “turnover pulse” hypothesis (2, 29, 30) Court Jester Nonconstant probability of extinction (3, 11)with Waxing and waning of clades in association

climate change, anoxia, impact (10, 11)

0

0

Number of genera (corrected; blue)

1000

200 0

200

0

Multilevel mixed
Subdivision of niches/specialization major phylogenetic splits (17) Vicariance and dispersal in (10, 25) Declining global extinction rates through time (1, 5)

Temporal scale

Latitudinal diversity gradient (22–24)

Onshore-offshore patterns and disturbance (3) Resource use: stenotopes are more speciose than Occupation of new ecospace (25) eurytopes (29, 30)

Temporal scale Temporal scale

Constancy of ecological guilds through time (25) Incumbency advantage (3, 24)

in response to physical perturbations– termed Inverse relationship between global temperature and “coordinated stasis” or “turnover pulse” hypothesis biodiversity (21) (2, 29, 30)clear correlation of species richness with Lack of Nonconstant probability of extinction (3, 11) body size or other biotic factors (16) Lack of evidence for a global carrying capacity and www.sciencemag.org SCIENCE VOL 323 equilibrium levels (8, 10) Lack of cohesiveness of the great “evolutionary faunas” (12) Species richness–energy relationship (18, 19) Inverse relationship between global temperature and biodiversity (21) Lack of clear correlation of species richness with body size or other biotic factors (16)

Subdivision of niches/specialization (10, 25) Declining global extinction rates through time (1, 5) 729 Onshore-offshore patterns and disturbance (3) Resource use: stenotopes are more speciose than eurytopes (29, 30)

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Department of Bristol Earth Sciences, University of Bristol, Earth Sciences, University of Bristol, BS8 1RJ, UK. mail: mike.benton@bristol.ac.uk E-mail: mike.benton@bristol.ac.uk

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their continuing diversification in the Late Jurassic and Cretaceous was mainly indistinguishable from a random walk. In particular, dinosaurs did not participate in the Cretaceous Terrestrial Revolution, some 130 to 100 Ma, when flowering plants, leaf-eating insects, social insects, squamates, and many other modern groups radiated substantially.

shifts should mainly occur low in a clade’s history: Clade shapes vary from bottom-heavy to topheavy, and diversification shifts may be concentrated low (dinosaurs and bats) or high (insects and ants) in a clade (26). In the future, the identification of diversification shifts across numerous taxa may provide evidence

A

245.9

237

232.5 228

203.6 199.6

Anisian

Lad

Crn

Norian
PTEROSAURIA

Rh. EJ

Court Jester worldviews. If the majority of diversification shifts are coordinated, and associated with particular climatic, tectonic, and geographic drivers, then the Court Jester model of macroevolution would prevail. This would link most increases in species diversity to particular largescale radiation events, such as the Cretaceous Terrestrial Revolution (26), or recoveries after mass extinctions. If, on the other hand, the majority of diversification shifts are unique to particular clades, and not coordinated temporally with others, then the Red Queen worldview might be considered. Comparing Sister Taxa A powerful element of the comparative phylogenetic 3. Phylogenetic through time Fig.approach to species diversity relationships and moris the opportunity to compare sister taxa. Sisters phospace occupation so their traarose from a single ancestor, and for Triassic archosaurs. jectories occupy the same phylogeny for (A) Framework amount of time, and Triassic cruthey started with the same genotype and pherotarsans scaledtheir subsequent evonotype. Any similarities in to the Triassic time scale. lution probably Numbers reflect top refer to indeat this phylogenetic signal of millions of years a common origin, but differences reflect pendent aspects of present; gray before the their separate histories. bars represent the Comparisons of sister taxa have allowed tests observed durations of major lineages; verof the resource-use hypothesis (29), that generalists are less speciose and have longer species tical dashed lines denotethetwo extinction durations than specialists. Specialists divide physical environment Carnian-Norian events, at theinto small patches, each and Triassicoccupied by a species, and each probably more Jurassic boundaries; their genersubject to environmental crises than arrowheads indicate alist relatives. that survived the latter event. Lad, of the lineages Classic examples in supportof Neresource-use hypothesis come from studies Ladinian; Crn,For example, two antelope ogene mammals (29). Carnian; Rh, Rhaetian; EJ, Early subgroups, the Jurassic. tribes Alcelaphini and Aepycerotini, diverged 6 to (B) Empirical now highly 8 Ma. The former is morphospace for Late speciose, with some 7 living and based on Triassic archosaurs, 25 extinct spe- the first two cies, and the latter is represented by two species, principalimpala Aepyceros, surviving. The circles, dinoonly one, the coordinates. Large slowly evolving Aepycerotini consists of few saurs; any time, and each of those issquares, poposauovals, pterosaurs; long species at lived, whereas the speciose Alcelaphini consists roids; hexagons, phytosaurs; stars, aetosaurs; of many short-lived species. The ecological crosses, clades differ: The impala has a smaller black habits of both crocodylomorphs; broad, generalist diet, whereas the speciose dots, “rauisuchids”;specialization. al- dots, nondilarger black celaphines show more dietary In nosaurianmany clades of Neogene African Scleromochlus. wider studies of dinosauromorphs, and South American mammals (30), the resourceBased onwas supported, and some subsidiary use hypothesis (28). predictions confirmed: Specialists are more common than generalists, carnivores include more generalists than herbivores, and there are more specialists in habitats that underwent recent environmental change (tropical rain forests and deserts). The resource-use model then stresses the role of climate and tectonic movements in determining species diversity rather than biological controls such as competition and predation.

“Dinosauromorphs”
ORNITHISCHIA

Dinosauria

SAUROPODOMORPHA THEROPODA PHYTOSAURIA

Crurotarsi

AETOSAURIA CROCODYLOMORPHA

“Rauisuchids”
POPOSAUROIDEA ORNITHOSUCHIDAE

B
0.12 0.06
Principal coordinate 2
0

-0.06 -0.12 -0.18 -0.24 -0.3 Crurotarsan morphospace -0.36 -0.24 -0.16 -0.08 0 0.08

Dinosaur morphospace

Pterosaur morphospace

0.16

0.24

0.32

and upland habitats of the later Paleozoic when land animals first burrowed, climbed, and flew, through the introduction of herbivory, giant size, endothermy, and intelligence among vertebrates, and the great blossoming of flowering plants (with associated vast expansions in diversity of plant-eating and social insects and modern vertebrates) during the Cretaceous Terrestrial Revolution 100 Ma (26). The other mode of species increase globally or regionally is by niche subdivision, or increasing specialization. This is hard to document because of the number of other factors that vary between ecosystems through time. However, mean species number in communities (alpha diversity) has increased through time in both marine (15, 25) and terrestrial (10) systems, even though niche subdivision may be less important than occupation of new ecospace in increasing biodiversity. Further, morphological complexity may be quantified, and a comparative study of crustaceans shows, for example, that complexity has increased many times in parallel in separate lineages (27).

Principal coordinate 1

Geographic and tectonic history has generated patterns of species diversity through time. The slow dance of the continents as Pangaea broke up during the www.sciencemag.org has affected323 past 200 My SCIENCE VOL modern distribution patterns. Unique terrestrial faunas and floras, notably those of Australia and South America, arose because those continents were islands for much of the past 100 My. Further, major geologic events such as the formation of the Isthmus of Panama have permitted the dispersal of terrestrial organisms and have split the distributions of marine organisms. A classic example of vicariance is the fundamental division of placental mammals into three clades, Edentata in South America, Afrotheria in Africa, and Boreoeutheria in the northern hemisphere, presumably triggered by the split of those continents 100 Ma (17). Other splits in species trees may relate to dispersal events, or there may be no geographic component at all. Species richness through time may correlate with energy. The species richness–energy relationship (18) posits correlations with evapotranspiration, temperature, or productivity, and studies of terrestrial and marine ecosystems have shown that these factors may explain as much as 90% of current diversity, although relationships between species diversity and productivity change with spatial scale (19). Over long time spans, there are strong correlations between plankton morphology and diversity and water temperature: Cooling sea temperatures through the past 70 My, and consequent increasing ocean stratification, drove a major radiation of Foraminifera, associated with increasing body size (20). More widely, there is close tracking be-

Fig. 3. Phylogenetic relationships and morphospace occupation for Triassic archosaurs. (A) Framework phylogeny for Triassic crurotarsans scaled to the Triassic time scale. Numbers at top refer to millions of years before the present; gray bars represent the observed durations of major lineages; vertical dashed lines denote two extinction events, at the Carnian-Norian and Triassic-Jurassic boundaries; arrowheads indicate lineages that survived the latter event. Lad, Ladinian; Crn, Carnian; Rh, Rhaetian; EJ, Early Jurassic. (B) Empirical morphospace for Late Triassic archosaurs, based on the first two principal coordinates. Large circles, dinosaurs; ovals, pterosaurs; squares, poposauroids; hexagons, phytosaurs; stars, aetosaurs; crosses, crocodylomorphs; smaller black dots, “rauisuchids”; larger black dots, nondinosaurian dinosauromorphs, Scleromochlus. Based on (28).

tween temperature and biodiversity on the globOutlook al scale for bothand evolutionary ecologists have marine and terrestrial organisms Paleontologists debated generic largely independently. (21), wherespecies diversity and familial richness were relatively2009 during warm “greenhouse” phaslow 6 FEBRUARY 731 es of Earth history, coinciding with relatively high origination and extinction rates. A much-studied manifestation of energy and temperature gradients is the latitudinal diversity gradient (LDG), namely the greater diversity of life in the tropics than in temperate or polar regions, both on land and in the sea. There are two explanations (22): (i) the time and area hypothesis, that the tropical belt is older and larger than temperate and polar zones, and so tropical clades have had longer to speciate, or (ii) the diversification rate hypothesis, that there are higher rates of speciation and lower rates of extinction in the tropics than elsewhere. There is geological and paleontological evidence for a mixture of both hypotheses (23, 24). Species diversity may increase by the occupation of new ecospace. The number of occupied guilds, that is, broad ecological groupings of organisms with shared habits, has increased in several steps through time, from 20 in the early Paleozoic to 62 in post-Paleozoic marine faunas (25). Further, marine animals have shown several step increases in tiering, the ability to occupy and exploit different levels in the habitat: At times, burrowers have burrowed deeper, and reef-builders have built taller and more complex reefs. Analogous, if even more dramatic, expansions of ecospace have occurred on land, with numerous stepwise additions of new habitats, from the water-margin plants and arthropods of the early Paleozoic to the forests

Phylogenetic Studies of Clade Histories Species are not randomly distributed; they have an evolutionary history, and so occur as twigs on a great phylogenetic tree. Studying species as members of clades is a fruitful approach to understanding the drivers and controls on speciation. Key questions include (i) Do species diversify early in a clade’s history? (ii) How do diversity and disparity (variance in characters or morphology) covary? (iii) Do major lineages within a clade follow similar, or different, patterns, and if different, why? (iv) Do evolutionary radiations follow the acquisition of new characters or emptying of ecospace? (v) How do major clades of apparent competitors interact over long spans of geologic time? and (vi) How do sister clades vary in species diversity and why? For such analyses, the ideal is a complete species tree, a phylogenetic tree that contains all species living and extinct, plotted accurately against geologic time (4). Simple to say; hard to achieve. More commonly, incomplete trees have been used, with the risk of error in calculations of evolutionary rates or comparisons of subclades. In paleontology, it has proven much easier to work with higher taxa such as genera or families because species fossil records are less complete than those of higher taxa, and yet it is not clear how higher-level patterns relate to those at species level. Many key questions can be tackled by comparing a real tree to a hypothetical tree that follows an equal-rate Markov (ERM) model, equivalent to tree growth after a random walk, where equal chances of speciation and of extinction are shared by all species (4). Major biotic replacements, where one clade replaces another, have been a focus of debate about the roles of competition and progress in

macroevolution, and dinosaurs provide a classic example. The standard view was that dinosaurs originated in the Late Triassic, some 230 Ma, by a process of competition in which they prevailed over their precursors, the crocodile-like crurotarsans and others, because of superior adaptations. A comparative phylogenetic study (28) shows, however (Fig. 3), that the Dinosauria expanded in two steps, one after an extinction event 225 Ma that removed dominant herbivores, and the second following the end-Triassic extinction 200 Ma that removed most of the crurotarsans. Dinosauria remained at moderate diversity and low disparity, and at lower disparity than the crurotarsans they supposedly out competed, during the 25 My between the events, suggesting that there was no insistent competition driving other groups to extinction but rather that the dinosaurs occupied new ecospace opportunistically, after it had been vacated. A further study on Dinosauria explored the subsequent evolution of the clade (26). Classic views that the dinosaurs arose with a flourish, and then finally gave way in the Cretaceous to the superior mammals, or that they dwindled to extinction because of “racial senility,” had long been abandoned. The dinosaurs seemed to be radiating actively in the Cretaceous, with many new clades appearing through their last 55 My, and especially in their final 15 My. The new study (26) shows that most diversification shifts (departures from ERM assumptions) fall in the first one-third of the history of the clade and that their continuing diversification in the Late Jurassic and Cretaceous was mainly indistinguishable from a random walk. In particular, dinosaurs did not participate in the Cretaceous Terrestrial Revolution, some 130 to 100 Ma, when flowering plants, leaf-eating insects, social insects, squamates, and many other modern groups radiated substantially. There is no geometric reason that diversification shifts should mainly occur low in a clade’s history: Clade shapes vary from bottom-heavy to top-heavy, and diversification shifts may be concentrated low (dinosaurs and bats) or high (insects and ants) in a clade (26). In the future, the identification of diversification shifts across numerous taxa may provide evidence for the relative importance of the Red Queen and Court Jester worldviews. If the majority of diversification shifts are coordinated, and associated with particular climatic, tectonic, and geographic drivers, then the Court Jester model of macroevolution would prevail. This would link most increases in species diversity to particular large-scale radiation events, such as the Cretaceous Terrestrial Revolution (26), or recoveries after mass extinctions. If, on the other hand, the majority of diversification shifts are unique to particular clades, and not coordinated temporally with others, then the Red Queen worldview might be considered.

Comparing Sister Taxa A powerful element of the comparative phylogenetic approach to species diversity through time is the opportunity to compare sister taxa. Sisters arose from a single ancestor, and so their trajectories occupy the same amount of time, and they started with the same genotype and phenotype. Any similarities in their subsequent evolution probably reflect this phylogenetic signal of a common origin, but differences reflect independent aspects of their separate histories. Comparisons of sister taxa have allowed tests of the resource-use hypothesis (29), that generalists are less speciose and have longer species durations than specialists. Specialists divide the physical environment into small patches, each occupied by a species, and each probably more subject to environmental crises than their generalist relatives. Classic examples in support of the resource-use hypothesis come from studies of Neogene mammals (29). For example, two antelope subgroups, the tribes Alcelaphini and Aepycerotini, diverged 6 to 8 Ma. The former is now highly speciose, with some 7 living and 25 extinct species, and the latter is represented by two species, only one, the impala Aepyceros, surviving. The slowly evolving Aepycerotini consists of few species at any time, and each of those is long lived, whereas the speciose Alcelaphini consists of many short-lived species. The ecological habits of both clades differ: The impala has a broad, generalist diet, whereas the speciose alcelaphines show more dietary specialization. In wider studies of many clades of Neogene African and South American mammals (30), the resource-use hypothesis was supported, and some subsidiary predictions confirmed: Specialists are more common than generalists, carnivores include more generalists than herbivores, and there are more specialists in habitats that underwent recent environmental change (tropical rain forests and deserts). The resourceuse model then stresses the role of climate and tectonic movements in determining species diversity rather than biological controls such as competition and predation. Outlook Paleontologists and evolutionary ecologists have debated species diversity largely independently. The realization that the Red Queen and Court Jester models may be scale-dependent, and that evolution may be pluralistic (3), opens opportunities for dialog. Taxic studies in paleontology continue to have great value in highlighting correlations between species richness and other factors, but comparative phylogenetic methods will illuminate questions about clade dynamics, species richness, and the origin of novelties. Further, methods are shared by paleontologists and neontologists, and this allows direct communication on the patterns and processes of

macroevolution. Viewed close up, evolution is all about biotic interactions in ecosystems (Red Queen model), but from further away, the large patterns of biodiversity are driven by the physical environment (Court Jester model). References and Notes
1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27. 28. 29. 30. 31. 32.

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theories of the process (8, 11). I leave out discussion of sympatric and allopatric speciation but SPECIALSECTION Under this Darwinian of ecological and instead identify the likelihoodperspective, linking R. C. Albertson,with Streelman, T. D. there isJ. Hered. speciation J. T. adaptation Kocheer, gene mutation-order speciation when was relatively 61. 52. O. Seehausen et al., Nature 455, 620 (2008). 41. D. Jablonski, Evolution 62, 715 (2008). straightforward, requiring only test of type of flow.94, ignore reinforcement, aaspecial whether I 291 (2003). 53. R. Lande, Genetics 128, 443 (1991). 42. R. J. Whittaker, K. A. Triantis, R. J. Ladle, J. Biogeogr. 35, 62. K. selection thought to Philos. Trans. R. pre54. D. A. Joyce et al., Nature 435, 90 (2005). 977 (2008). phenotypic differences between stronger were natural Schwenk, N. Brede, B. Streit,favor species Soc. London Ser. B 363, 55. G. Fryer, Environ. Biol. Fishes 45, 109 (1996). 43. R. 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Crespi, Evolution 60, 2311 (2006). major symposium of speciation before York, Natural selection commonly drives 2166 origin of species,Annu. Rev. Ecol. Syst. 33, 475 (2002). as Darwin initially claimed. Mechanisms of 1909), p. 383. 47. J. A. Coyne, T. D. Price, Evolution 54, the (2000). logical species concept (7)], an extensive comspeciation by D. Schluter, Nature 408,two broad categories: ecologicalC.and mutation-order. Under36, 519 Speciation and Adaptation from L. Harmon, 66. We thank A. Birand, R. Glor, A. Harrison, 58. J. J. Wiens, H. Graham, Annu. Rev. Ecol. Syst. 48. J. B. Losos, selection fall into 847 (2000). parative and biogeographic study showcased inD Jablonski, L. Mahler, C. Marshall, and the anonymous 49. D. Lack, Darwin’s Finches (Cambridge Univ. Press, ecological speciation, divergence is driven by divergent(2005). selection between environments, natural Darwin in which derived morphologicalthe NSF stances to Dobzhansky reviewers for useful comments. Supported by and life 59. S. Skulason, T. Cambridge, 1947). whereas under mutation-order speciation, divergence occurs when B. Smith, Trends Ecol. Evol. 10, 366 different mutations arise and (grant DEB-0519777) and the NIH (grant GM56693). (1995). 50. U. Dieckman, M. Doebeli, J. A. J. Metz, D. Tautz, Adaptive Appreciation of the connection between adaptaare fixed in separate populations adapting to similar60. H. D. Bradshaw, D. W.Tests of parallel evolution history forms of fishes had arisen over and over selection pressures. Schemske, Nature 426, 176 Speciation (Cambridge Univ. Press, Cambridge, 2004). tion and speciation began with Darwin whenreagain from the same ancestral type (12). The a of reproductive isolation,Pääbo, Nature 368, 629 (1994). mating, and reproductive isolation by active 10.1126/science.1157966 (2003). 51. U. K. Schliewen, D. Tautz, S. trait-based assortative morphological concept of species largely preselection have demonstrated that ecological speciation is a common means by which new species peated, parallel origin of nonparasitic lamprey vailed. In On the Origin of Species, Darwin wrote in streams from the same migratory, parasitic arise. Evidence for mutation-order speciation by natural selection is more limited and has been that “I look at thethat “Again and again the paraancestor showed term species, as one arbitrarily best documented by instances of reproductive isolation resulting from intragenomic conflict. given forof the processconvenience to aout distheories the sake of (8, 11). I leave set of However, we still have not identified all aspects of selection, and identifying the underlying genes sitic lampreys have evolved into nonparasitic REVIEW individuals sympatric and life in small streams, forms...correlated resembling eachspeciationand cussion of closely with allopatric other...” but for reproductive isolation remains challenging. “The amount of difference is one very important where a identify the likelihood of ecological and instead suitable food supply in the way of large criterion in settling whether two When correlated fish is scarce or seasonal” (12). forms should be mutation-order speciation when there is gene tttook evolutionary biologists nearly 150 years, ries: ecological speciation and mutation-order rankedI as species or factors, such repetition of flow. ignore reinforcement, special type is took evolutionary biologists nearly 150 would nevertheless be advantageous in both of with environmental varieties”a (1). Under this but at last we last we can agree with that the speciation. Ecological speciation importancethe view, speciation is thought as the accumulation of natural to result from chance; environmental years, but at can agree with Darwin Darwin their environments. The relative refers to of unlikelyselection defined to favor stronger preoriginthe species,of species, “that mystery of evolution of reproductivemechanism for thepop- sufficiently many differences betweenthe cause of origin “that mystery of mysteries” these two categories of isolation between ori- selection pressures must therefore be populamating reproductive isolation once postzygotic that (1), really does occur by means of natural selection ulations or subsets of a single population by ad- tions to warrant their Iclassificationspeciation by as separate isolation has “As a result of our recent studies mysteries” (1), really does occur by means of gin of species in nature is unknown. of speciation.evolved. also ignore Dolph Schluter (2–5). Not all species appear to evolve by aptation to different environments or ecological taxonomic species. Darwin understoodbe crucial polyploidy, even though selection might the imIn this review, I summarize progress in un- on fishes...weight is constantly being added to natural selection (2–5). Not all species appear to selection, but the evidence suggests that most of niches (2, 8, 9). Natural selection is divergent, portance of reproductive barriers between species in theory stages. evolve by selection, but the evidence suggests derstanding the general features of speciation thethe early that speciation is...under the rigid Natural The effort leading up to this conclusion acting in contrasting directions between environthem do.selection commonly drives the origin of species, as Darwin initially claimed. Mechanisms of (1), but the study of speciation after the pubthat most of them do. The effort leading up to by selection. Iand mutation-order. Under do not differentiate speciation control of the environment” (12). However, this speciation by experimental and conceptual ad- ments, which involved manyselection fall into two broad categories: ecological drives the fixation of different lication of this work focused mainly on the evoSpeciation referring to the from this conclusion involved many is by sexual selection here because natural selec- case is onlyand Adaptation origin of morphoecological speciation, divergence experimental alleles, each selection between environments, vances, including a revision of the driven by divergent naturaladvantageous in one environment lution of species differences, particularly of notion of Darwin to Dobzhansky and conceptual 80 years after publication of On but occurs when different mutations Mani and morphological traits but also of behavioral and whereas itself, advances, including a revision tion drives the divergence of mate preferences, logical species. speciationunder mutation-order speciation, divergence not in the other. Following G. S. arise and Appreciation of the connection between studies The point speciation adaptaof Originin separate populations 80 years after by C. Clarke (10), I define mutation-order speciaare fixed of of speciation itself, adapting to similar either ecological Tests of parallel evolution the the notionthe Species, to a definition based on B. selection pressures.or mutation-order mecha- other andturning traits. forwith Darwin when a tion phenotypic modern concept of speciation speciation began publication isolation Origin of morphological tion as themost theories of the process (8, 11). I of reproductive isolation, trait-based assortative nisms, in reproductive isolation by active reproductive of On the instead of the Species, to mating, andevolution of reproductive isolation by came withthis Darwinian perspective, linking Under the a definition based on reproductive isolation speciation is a discussion of sympatric and different “Species with adaptationof species stage of preleave out common means fixation new species morphological concept was as a largely the selection (6, 7). differenceshave demonstrated that ecological in- the chance occurrence andby which ofallopatric speciation separation is definedrelatively straightvailed. of Darwin wrote speciation but is more limited and to been stead ofmain question today is howspeciation by natural selection populations adapting has similar forward,In On the Originat Species,physiological arise. Evidence for mutation-order (6, 7). selec- alleles betweeninstead identify the likelihood of evolutionary process a testwhich The morphological differences does requiring term species, of whether arbitrarily that “I look at theonly become as one phenotypdeveloped” by bestlead to speciation? What are howmechanisms selection pressures. Reproductive isolation evolves isolating mechanisms documented by today is the does selec- ecological and from intragenomic conflict. tionThe main questioninstances of reproductive isolation resulting mutation-order speciation when ic differences between species were to a set(6) caused of given tion lead we speciation? What are the mecha- there is populations fix distinct mutationsgenes (here, for the sake of convenience to mean However, to still have not identified all aspects selection, and identifying the underlying that of natural selection, what genes are affected, and ofbecause gene flow. I ignore reinforcement, a spe- natural “physiological” is interpretedAmerican selection. For example, each other...” and at the individuals closely resembling nisms of natural isolation remains challenging. cial type of natural selection thought both of evolved reproductive isolation between populafor do changes these genes yield the are afhowreproductive atselection, what genes habitat, would nevertheless be advantageous in to favor Association forof difference is one very important “The amount the Advancement of Science 1939 barriers to fected, and how do changes at these genes yield stronger premating The relative isolation once tions, as distinct from geographical symposium behavioral, mechanical, chemical, physiological, their environments. reproductive importance of speciationin settling whether two forms should be criterion symposium [the last major the other incompatibilities that are the chemical, postzygotic isolation has evolved. I also origin interbreeding). Subsequently, species were deand thabitat, behavioral, mechanical, reproduc- these two categories of mechanism for the ignore on speciation before or varieties” (1). Under this the biological species concept took evolutionary biologists nearly 150 years, ries: ecological speciation and mutation-order ranked as species physiological, and other species? As a start, the speciation by polyploidy, even though selection fined as “groups of interbreeding biogeographic natural poputive but at last we can agree with Darwin thatthat of species inEcological speciation refers to the (7)], an extensiveis defined as the accumulation of barriers between new incompatibilities the speciation. nature is unknown. view, speciation comparative and are the reproductive new species might arise by new spelations that are reproductively isolated from In be review, I the early stages. many ways by which barriers betweenmysteries” mightthis crucial insummarize progress in under- study showcased instances in which derived morevolution of reproductive isolation between pop- sufficiently many differences between populaorigin of species, “that mystery of other such groups” (7). From this point on, the cies? As a start, the many ways broad categoselection can be grouped into twoby which new standing thesubsets of a single population by se- phologicalwarrant their classification as separate (1), really does occur by means of natural selection ulations or general features of speciation by ad- tions to and life history forms of fishes had and Adaptation from by sexual study of speciation was from the of thethe imspecies Not all species appearcan be grouped lection. I do different environments orDarwin might arise by selection to evolve by Speciation not differentiate speciation ecological arisen over and over again the studysame ancestral aptation to (2–5). taxonomic species. Darwin understood evoluinto two broad categories: ecological Department, selection here because natural selection drives the type of reproductive isolation (3). origin of up to speciation to Dobzhansky Natural selection is divergent, tion (12).of reproductive barriers between species niches (2, 8, 9). selection, Research Centre and Zoology portance The repeated, parallel Progress nonBiodiversity but the evidence suggests that most of and mutation-order leading up to this conclusion Appreciation mate directions between environ- then but lamprey in streams from the same migraUniversity of British Columbia, Vancouver, BC V6T spe- divergence of of the preferences, between adap- parasiticunderstanding the link between morphoacting in contrasting connection by either ecothem do. The effort speciation. Ecological 1Z4, (1), in the study of speciation after the pubCanada. E-mail: schluter@zoology.ubc.ca conceptual ad- logical and mutation-order mechanisms, in when tory, parasitic ancestor showed that was the evothe evolution of with Darwin most ciation refers toexperimental and reproductive tation or speciation beganfixation of different logical speciation and adaptation “Again and ments, which drives the involved many lication of this work focused mainly on largely isolation including a revision of the notion of a morphological concept in one environment forgotten, its contributions uncertain under the between populations or subsets of a alleles, each advantageous of species largely lution of species differences, particularly of vances, single population by adaptation to different en- prevailed. In On the FollowingSpecies, Darwin new concept. traits but also of behavioral and speciation itself, 80 years after publication of On but not in the other. Origin of G. S. Mani and morphological www.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009 737 The biological species concept must surely vironmentsof the Species, to a definition9). Natu- wrote Clarke (10), I at the mutation-order as one other phenotypic traits. the Origin or ecological niches (2, 8, based on B. C. that “I look define term species, speciaral selection is divergent, acting in contrasting arbitrarily evolution of reproductive isolation by have made thismore difficultperspective, linking reproductive isolation instead of morphological tion as the given for the sake of convenience Under it Darwinian to investigate any directions between environments, which drives to a chance individuals closely resembling each link between speciation and natural selection. T. the set of occurrence and fixation of different speciation with adaptation was relatively straightdifferences (6, 7). the The main question today is how does selec- other...” and “The amount of difference similar Dobzhansky (13) only a test of whethergenes unfixation of different alleles, each advanta- alleles between populations adapting to is one forward, requiring suggested that the phenotypgeous in to speciation? What are thein the other. very important criterion in settling whether two derlying differences between populations in ortion lead one environment but not mechanisms selection pressures. Reproductive isolation evolves ic differences between species were caused by Followingselection, what genes are affected, and forms should be ranked as species or varieties” dinary phenotypic traits were unlikely American of natural G. S. Mani and B. C. Clarke (10), I because populations fix distinct mutations that natural selection. For example, at the to be the define mutation-order speciation as the habitat, (1). Under this view,be advantageous in boththe basis of reproductive isolation. He later changed how do changes at these genes yield the evolu- would nevertheless speciation is defined as of Association for the Advancement of Science 1939 tion of reproductive isolation by the chance accumulation of sufficiently many differences his mind, but at the time this viewpoint, and the behavioral, mechanical, chemical, physiological, their environments. The relative importance of speciation symposium [the last major symposium occurrence and fixation of that are the reproduc- between populations of mechanism forclassifica- generally greater difficulty of studying concept and other incompatibilities different alleles be- these two categories to warrant their the origin on speciation before the biological species reprotive barriers between new species? As a start, the of species in nature is unknown. (7)], an isolation comparative and biogeographic tween populations adapting to similar selec- tion as separate taxonomic species. Darwin un- ductive extensive than morphology, must have In this review, I summarize progress barriers study showcased instances in which the connecmany ways by Reproductive isolation arise by tion pressures. which new species might evolves derstood the importance of reproductivein under- discouraged many from pursuing derived morselection can be grouped into two broad catego- standing the general but the of speciation by se- phological and life history forms of fishes had because populations fix distinct mutations that between species (1), features study of speciation tion. Virtually no research effort followed that lection. do not differentiate speciation by sexual arisen over and over again from the same ancestral after theIpublication of this work focused mainly tested the role of adaptation in speciation. selection here because natural selection drives the on the evolution of species differences, particu- type (12). The repeated, parallel origin of nonBiodiversity Research Centre and Zoology Department, divergence of mate preferences, by of behav- parasitic of Speciation by from the same migraUniversity of British Columbia, Vancouver, BC V6T 1Z4, larly of morphological traits but alsoeither eco- Models lamprey in streams Selection logical or mutation-order traits. tory, parasitic ancestor showed in “Again and Canada. E-mail: schluter@zoology.ubc.ca ioral and other phenotypic mechanisms, in most The topic of natural selection thatspeciation is
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Evidence for Ecological Speciation and Its Alternative

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Evidence for Ecological Speciation and Its Alternative

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way becau Both models of have evolved into nononce again receiving attention. The two most again the parasitic lampreysspeciation, ecologi- A Gambusia ulations d general hypotheses involving selection are parasitic forms...correlated with theoretically cal and mutation-order, are life in small mutations ecological and mutation-order speciation. Eco- streams, where a suitable food supply determine plausible, and only data can in the way order. Div of large fish is scarce or seasonal” (12). When corlogical speciation is defined as the evolution related with environmental factors, such repetition their relative importance in nature. The chastic bu of reproductive isolation between populations is unlikely to figure fromby which mechanism key is to result out chance; environmental from gene reproductive isolation first evolved (3). by divergent natural selection arising from dif- selection pressures must therefore be the cause of both smal infinite) p Once the result of our recent studies on ferences between ecological environments (2, speciation. “As aearliest genetic differences can be ec 8, 9, 14). It predicts that reproductive isolation fishes...weight is constantly being added to the have accumulated between populations mutationshould evolve between populations adapting to theory that speciation is...under the rigid control of by either process, subsequent mutations ecology d the environment” (12). However, this case is only contrasting environments but not between pop- referring to the origin of morphological species. might be favored in one population gence as s and not the other because of epistatic ulations adapting to similar environments. The The turning point for speciation studies came evolution basic idea has been around for a while (7), al- with the modern conceptgenetic background interactions with of speciation “Species ductive iso tion of eco though it was tested only recently. The agents of separationHence, epistasis, including that (10). is defined as a stage of the evolupostzygot producing at which physiological isolatdivergent selection are extrinsic and can include tionary process Dobzhansky-Muller incom- B Mimulus Specia ing patibilities in hybrids between species mechanisms become developed” (6) (here, abiotic and biotic factors such as food resources, tragenomi “physiological” is interpreted to mean evolved climate, habitat, and interspecies interactions reproductive result from eitherpopulations, as (3), can isolation between ecological or otic drive such as disease, competition, and behavioral in- distinct from geographical barriers to interbreedmutation-order speciation. sterility (F Speciation species were defined as terference. Ecological speciation can lead to the ing). Subsequently,can be rapid under both mutationcause, by c evolution of any type of reproductive isolation, “groups of interbreeding natural populations that speciation models, because alleles are tions cau reproductively isolated from other such including premating isolation, hybrid sterility, are driven to fixation by natural selection countering groups” (7).cases. However,on, the study of From this point under the muand intrinsic hybrid inviability as well as extrin- in both the same i speciation was the study of the evolution of sic, ecologically based pre- and postzygotic iso- reproductive isolation (3). Progress up toalleles, tation-order process, the same then in Speciation if present, would be favored in every lation. Speciation by sexual selection is ecologi- understanding the link between morphological mutation-o population, at least was largely stages of cal speciation if ecologically based divergent se- speciation and adaptation in the early forgotten, vergence lection drives divergence of mating preferences, its contributions uncertain under the new concept. Fig. 1. (A) Example of ecological speciation. Repeatedly and gamete re divergence. For this reason, mutationThe biological species concept when surely Fig. 1. (A) Example of ecological speciation. Repeatedly and fixation o for example by sensory drive (15). order speciation is difficult must there independently, the mosquito fish, Gambusia hubbsi, inhabiting In accordance with (10), mutation-order spe- have made itflow, because gene flow increas- independently, the mosquitoevolved a larger caudal region and geous mu is gene more difficult to investigate any link blue holes in the Bahamas has fish, Gambusia hubbsi, inhabitbetween speciation and natural selection. T. smaller holes the presence of predators (top) than caudal ulations, ciation is defined as the evolution of reproduc- Dobzhansky (13) suggested that the genes under- ing bluehead in in the Bahamas has evolved a largerin their (16). Div es the possibility that favorable mutaregion and smaller head in the presence of predators (top) tive isolation by the fixation of different advan- lying differences between one population will than in their absence In laboratory trials, laboratory trials, two other learn tions occurring in populations in ordinary absence (bottom) (29). (bottom) (29). In the probability of the individuals mating was higher when they were from different tageous mutations in separate populations ex- phenotypic traits werepopulations, preventing probability having the same predation environment (and similar havior und spread to other unlikely to be the basis of populations of two individuals mating was higher when they divergence (17, He later changed his mind, body from than when they were from the same predaperiencing similar selection pressures. Whereas reproductive isolation. 18). Any process result- were shape) different populations having opposite predation tion, not m at the low levels of gene flow, generally environments. [Photo credit: Brian Langerhans than when they different alleles are favored between populations but ing in time this viewpoint, and theincluding tion environment (and similar body shape)(29)]. (B) Example efficient s under ecological speciation, the same alleles greater difficulty of studying reproductivediver- were from opposite predation environments. mutation-order is the cul selection, facilitates subsequent isola- of reproductive isolation evolving under the [Photo credit: tion than morphology, must have discouraged Brian Langerhans (29)]. (left)Example of reproductiveflowers of mutation-o mechanism. Male-fertile (B) and male-sterile (right) isolation would be favored in different populations under gence by the mutation-order process evolving under thean Oregon population of monkey flowers (M. al scenario many from pursuing the connection. Virtually no F2 hybrids between mutation-order mechanism. Male-fertile mutation-order speciation. Divergence occurs research effort followed ecological the role of (left) and male-sterile (right)male sterility F2 hybrids between (19). In contrast, that tested speciation guttatus) having a cytoplasmic flowers of element and nuclear Both anyway because, by chance, the populations do adaptation in speciation. or without gene flow, an Oregon population of monkey flowers (M. guttatus) hav- ecologica can proceed with restorer and a closely related species (M. nasutus) having neither (46, cytoplasmic male sterility element and cytoplasm. The not acquire the same mutations or fix them in the although it is easiest when gene flow ing a47). Both flowers shown have M. guttatusnuclear restorer are theore flower on the related species (M. nasutus) whereas the one on and a closelyleft also has the nuclear restorer,having neither (46, only data same order. Divergence is therefore stochastic Models of Speciation by Selection is absent. the Both flowers shown anthers, lacks the restorer. [Photo The topic of natural selection in speciation is once 47). right, with undevelopedhave M. guttatus cytoplasm. The ative imp Experiments with laboratory popu- credit: on the left also but the process is distinct from genetic drift. It again receiving attention. The two most general flowerAndrea Case (47)] has the nuclear restorer, whereas the key is to can occur in both small and large (though not lations of Drosophila and yeast dem- one on the right, with undeveloped anthers, lacks the restormechanism hypotheses involving selection are ecological and infinite) populations. Selection can be ecologi- mutation-orderthe plausibility of ecological er. [Photoincluding premating isolation, hybrid first evolved (3). Once the onstrate speciation. Ecological speciation isolation, credit: Andrea Case (47)] cally based under mutation-order speciation, but is defined as the evolution ofinstances when sterility, and intrinsic hybrid inviability as well as ences have accumulated b speciation. In those reproductive isoecology does not favor divergence as such. It lation between populations by postmating re- extrinsic, ecologically based pre- and postzygotic either process, subsequen measurable pre- and divergent natural can lead to the evolution of any type of repro- selection arising isolation evolved, it was greater be- (Odsh, JYAlpha), and selection is favored in one populatio productive from differences between eco- isolation. Speciation by sexual sexual isolation (ds2) beductive isolation, with the exception of ecologi- logical environments (2, 8, 9, to different environments tween Drosophila species. Most of because of epistatic inte tween lines subjected 14). It predicts that ecological speciation if ecologically based diver- these genes reproductive isolation should evolve between gent selection drives divergence of mating background (10). Hence, e than between lines raised under homogeneous show molecular signatures of positive selection, cally based pre- and postzygotic isolation. producing Dobzhansky-M populations adapting to contrasting environments preferences, for example by sensory drive (15). Speciation resulting from intragenomic con- but conditions (20, 21). adapting to similar proving natural mutation-order spe- in hybrids between specie In not between populations Laboratory experimentsaccordance with (10), selection’s role (3), provided that flict such as meiotic drive or cytoplasmic male environments. The basic idea has been around for homo- is defined as the evolution of reproductive reproductive or mutati on various microbes maintained under ciation fixation occurred before complete either ecological sterility (Fig. 1B) is likely to be mutation-order a while (7), although it was tested onlygenerationsisolation by the fixation of than afterward. The top-down can be rapid geneous conditions for many recently. have isolation rather different advantaSpeciation agents of genetic selection are consistent geous phenotypic speciation because, by chance, the initial muta- Thedetected divergent divergence extrinsic and with the mutations in separate populations expe-themodels, because alleles ar approach involves identifying (i) include abiotic and biotic factors such effects riencing traits selection pressures. Whereas those traits tions causing drive and those countering it are can mutation-order process (22), butas food on re- similar under divergent selection, (ii) natural selection in both resources, climate, habitat, and interspecies inter- different alleles are favored between populations the mutation-order proces unlikely to be the same in separate populations. productive isolation have not been explored. associated with reproductive isolation, and (iii) actions such as disease, competition, and behav- under ecological speciation, the same alleles present, would be favored Two approaches investigate can lead would Speciation by sexual selection is mutation-order ioral interference. Ecological speciation the mechanisms be favored in different populations under least in the early stages o the genes underlying traits and reproductive isospeciation if divergence of mate preferences or to the speciationof any type selection in nature. The lation. Step (iii) has been challenging undermutation-order spe of evolution by natural of reproductive mutation-order speciation. Divergence occurs any- reason, both gamete recognition occurs by the fixation of bottom-up approach involves (i) genetic map- approaches but is needed to understand how sealternative advantageous mutations in different ping of reproductive isolation between closely lection has led to reproductive isolation. 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org 738 populations, as by sexual conflict (16). Diver- related species, (ii) testing whether discovered gence in song and other learned components genes exhibit a genomic signature of positive Ecological Speciation of behavior under purely social selection, not selection, and (iii) identifying the phenotype Evidence for ecological speciation has accumumolded by selection for efficient signal trans- and source of fitness effects of alternative alleles lated from top-down studies of adaptation and mission (5), is the cultural equivalent of the at selected loci. The approach has been hugely reproductive isolation [reviewed in (2, 8, 9)]. mutation-order process. Additional scenarios successful in identifying major genes implicated We now know of many real species that have, in hybrid inviability (Hmr, Lhr, Nup96), sterility at least in part, evolved by divergent natural seare elaborated in (5).

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y to mate if they are of nents of reproductive isolation lacking identifiable less of relatedness as causes (Fig. 2). The unidentified component of speciation, if built by selection and not genetic affinity. is also prematComponents – divergent selection plants (28), Littorina marine snail ecotypes n which rentially inhabiting different zones of the intertidal 15 basis of (24), and mosquito fish inhabiting blue e under 10 holes with and without fish predators in the nt selecBahamas (29) (Fig. 1A). In these studies, it ortative 5 was shown that males and females are more insects, likely to mate if they are of the same ecoin fish, 0 or preftype, regardless of relatedness as indicated notypic by phylogenetic affinity. Components – unknown cause flowerEcological speciation is also supported 15 be under by examples of premating reproductive environ10 isolation in which individuals choose or 30, 31)]. preferentially encounter mates on the basis vergent 5 directly of phenotypic traits that are under ecologiuced fitcally based divergent selection. Examples 0 he enviinclude assortative mating by host choice -0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8 1 migrant in insects, body size and coloration in fish, 31, 32)] Cumulative reproductive isolation beak size in birds, pollinator preferences for ybrids in Fig. 2. Estimates of of the magnitude of reproductive Fig. 2. Estimates the magnitude of reproductive isolation specific phenotypic floral traits, and varia[extrinresulting from divergent selection components (top), compared isolation resulting from divergent selection components 3)]. For with other componentswith other components (bottom). tion in flowering time—traits inferred to be lacking identifiable causes lacking (top), compared l perenDivergent selection components include those attributable to under divergent selection between environidentifiable Divergent selection s of the active selection causes (bottom). inviability and extrinsic components on traits (immigrant include those attributable to active ments [see examples in (8, 30, 31)]. uttatus) postzygotic isolation) and to trait-based assortative mating (habitat selection on and extrinsic Ecologically based divergent selection North preference, floraltraits (immigrant inviabilityThe unattributed isolation, and to trait-based assortative postzygotic isolation) and breeding time). s when components include intrinsic hybrid inviability, sexual selection has also been directly measured, as shown mating (habitat preference, floral of the against hybrids, pollen competition, andisolation, and breeding by reduced fitness of each ecotype in the enreduced time). The unattributed components hybrid fecundity. mple of Data were taken from (32, 31) (table S1). include intrinsic vironment of the other [immigrant inviabilA negative value hybrid inviability, sexual selection against hybrids, pollen ypic dif- indicates that hybrids had higher fitness than the parental species competition, and reduced hybrid fecundity. Data were ity; reviewed in (31, 32)] and by reduced fitutes di- for at least one component of postzygotic isolation. One data value taken from (32, 31) (table S1). A negative value indicates ness of hybrids in the parental environments because of –2.66 was left out of the bottom panel. that hybrids had higher fitness than the parental species [extrinsic postzygotic isolation (33)]. For for at least one component of postzygotic isolation. One example, each of the coastal perennial and 739 VOL 323 dataFEBRUARY 2009 left out of the bottom panel. 6 value of –2.66 was
Number of studies

lection between environments. The connections between selection on ordinary phenotypic traits and reproductive isolation are often strong and straightforward. It follows that much of the genetic basis of reproductive isolation should involve ordinary genes that underlie differences in phenotypic traits. But we still know little about the genetics of ecological speciation. One line of evidence comes from tests of parallel speciation, whereby greater reproductive isolation repeatedly evolves between independent populations adapting to contrasting environments than between independent populations adapting to similar environments (20, 23). A major challenge in applying the test to natural populations is to eliminate the possibility that each ecotype has originated just once and has spread to multiple locales. This is difficult because gene flow of neutral markers between closely related but nearby populations can result in the false appearance of multiple independent origins of these populations when evaluated by phylogenies (3, 24). However, multiple origins are supported in several examples of parallel speciation, including the sympatric benthiclimnetic species pairs of threespine stickleback in young lakes of British Columbia (25, 26), the repeated origin of divergent marine and stream populations of threespine stickleback around the Northern Hemisphere (27), ecotypes of Timema walking stick insects living on different host

inland annual races of the monkey flower (Mimulus guttatus) along the west coast of North America has low fitness when transplanted to the habitat of the other (31). This is an example of active selection on phenotypic differences, and it also constitutes direct reproductive isolation because it is an evolved barrier to gene flow between parental populations. Multiple traits are probably involved, including flowering time and tolerance of salt and drought. This type of reproductive isolation is context-dependent and is weakened in intermediate environments. On the other hand, active selection favors the evolution of ever-greater differences between populations, which may strengthen the barrier to gene flow (20). It is unclear how much reproductive isolation typically evolves by ecologically based divergent selection in nature. We can approximate an answer from estimates of the combined contribution of active selection on traits and trait-based assortative mating, as compared with other forms of reproductive isolation (Fig. 2 and table S1). These estimates are incomplete because individual studies may lack data on components of reproductive isolation, separate components may not be independent, and the strength of barriers between species may not be symmetric (34). Nevertheless, compilation of the data shows that the amount of reproductive isolation attributable to active selection and traitbased assortative mating is at least as strong, on average, as the amount from components

of reproductive isolation lacking identifiable causes (Fig. 2). The unidentified component of speciation, if built by selection and not genetic drift, could be the result of either ecological or mutation-order mechanisms. These examples indicate a growing knowledge of the mechanisms of selection and its consequences for reproductive isolation. At this point, the most glaring deficiency is our knowledge of the impact of selection on genes. Optimistically, progress is being made with genetic mapping to identify quantitative trait loci (QTLs) and genes or regulatory control regions that affect individual phenotypic traits on which components of reproductive isolation depend. Examples include the yup QTL, which affects flower color differences between the monkey flowers, Mimulus cardinalis and M. lewisii (35). Swapping alleles of this QTL between the species with repeated backcrossing resulted in shifts in pollinator preference and, hence, indirectly affected premating isolation. Survival and salt tolerance of second-generation hybrids between the sunflowers Helianthus annuus and H. petiolaris transplanted to the salt marsh habitat of their hybrid descendent species (H. paradoxus) mapped strongly to a QTL identified as the salt tolerance gene CDPK3 (36). Another form of investigation involves the analysis of genome scans of ecologically different populations and species. These scans compare allelic variation within and between populations at many marker loci spaced throughout the genome (37). Markers that show excessive differentiation between populations (outliers) may indicate selection on nearby genes. The method is particularly informative when applied to populations with ongoing hybridization, because outlier markers may identify points in the genome that resist the homogenizing influence of gene flow, perhaps indicating genomic regions under divergent selection. However, sets of genes that diverged under a mutation-order process can produce the same pattern (17, 18), which makes analysis of such studies more difficult. Clues to whether ecologically based divergent selection is involved are gained if outliers at the same genomic locations turn up repeatedly in scans between populations that inhabit contrasting environments (38) and by identifying phenotypic traits under divergent selection that map to those locations in the genome (36, 39, 40). As genomic resources increase for more species, it will be possible to measure natural selection directly on genomic regions of interest by transplanting otherwise relatively homogenous experimental populations containing alternative alleles into the environments of the parent species (35).

of mutation-order divergence. It may be that the mutation-order process is more difficult to detect, or perhaps we have not looked hard enough at species with only small ecological differences (5). We still do not know much about the selective factors causing mutation-order speciation. Evidence for mutation-order speciation comes from instances in which reproductive isolation apparently evolved as a by-product of conflict resolution between genetic elements within individuals (intragenomic conflict), such as cytoplasmic male sterility in hermaphroditic plants (Fig. 1B), and genetic elements conferring meiotic drive. Under both mechanisms, a mutation arises that can distort representation in gametes and spreads in a selfish manner, even though such an element reduces overall fitness of the organism that bears it. This, in turn, places selection on mutations in other genes that counter the selfish element’s effects and restore more equal genetic representation in gametes. Distorter and restorer mutations are unlikely to be the same in different populations regardless of environment; thus the process leads to divergence. The mismatch between the distorter in one population and the restorer in the other can result in hybrid sterility or inviability and, thus, reproductive isolation (3, 41). Numerous examples of selfish elements, such as those observed in cytoplasmic male sterility of plants, support these hypotheses (42, 43). In addition, partial reproductive isolation generated by meiotic drive has been identified in Drosophila [reviewed in (3, 41)]. Sexual conflict is also expected to lead to mutation-order speciation, but there are few compelling examples (3). The contribution by these mechanisms to speciation is still uncertain, however. The alleles responsible for meiotic drive and cytoplasmic male sterility may be prevented from spreading to fixation because selection on such elements is frequencydependent (43) and because restorer alleles arise and weaken selection on the distorter elements (44). Second, if divergent populations come into secondary contact, the alleles within each population causing cytoplasmic male sterility or meiotic drive (and the corresponding restorer alleles) will spread between the populations by gene flow, eliminating that component of reproductive isolation (43). Hence, for these mechanisms to contribute to speciation, the fitness of hybrids must be reduced to very low levels, or other incompatibilities must arise that interact with these genes to prevent their spread after secondary contact.

between genes could generate reproductive isolation (45). Mostly, I expect that he would be chuffed by mounting evidence for the role of natural selection on phenotypic traits in the origin of species. This is really what On the Origin of Species was all about. Between 1859 and the present, the general acceptance of the biological species concept altered the focus of speciation studies. Yet, the discovery that reproductive isolation can be brought about by ecological adaptation in ordinary phenotypic traits bridges Darwin’s science of speciation and our own. The most obvious shortcoming of our current understanding of speciation is that the threads connecting genes and selection are still few. We have many cases of ecological selection generating reproductive isolation with little knowledge of the genetic changes that allow it. We have strong signatures of positive selection at genes for reproductive isolation without enough knowledge of the mechanisms of selection behind them. But we hardly have time to complain. So many new model systems for speciation are being developed that the filling of major gaps is imminent. By the time we reach the bicentennial of the greatest book ever written, I expect that we will have that much more to celebrate. References and Notes
1. 2. 3. 4.

5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19.

Mutation-Order Speciation Mounting evidence for divergent selection in speciation does not diminish the potential role

Conclusions Our understanding of the role of natural selection in speciation has come a long way since Darwin’s time. If he were here to witness, he would most likely be staggered by the discoveries of genes and molecular evolution and astonished at the prospect that evolutionary conflict

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Supporting Online Material

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values that place two bacterial isolates into the same or different species. The overall genetic relatedness of isSPECIALSECTION pneumoniae isolates mayhuman pathogen, the a major be measured by S. extent is a commensal bacteria with them, and of DNA hybridization between a history mitis S. that A. Schluter, S. Via, M. Whitlock, J. hybrid40. S. Via, J. West, Mol. Ecol. 17, 4334 (2008). 32. P. Nosil, T. H. Vines, D. J. Funk, Evolution 59, 705 (2005). those Rogers,show 70% or (11), and S. Willis, and of taxonomic uncertainty more DNA work a reviewer for assistance and comments. This pseudo41. H. A. Orr, J. P. Masly, N. Phadnis, J. Hered. 98, 103 33. H. D. Rundle, M. C. Whitlock, Evolution 55, 198 (2001). ization are defined as thedescribed organism of pneumoniae is aby grants from the Natural Sciences10). was supported recently same species (2, and (2007). 34. N. H. Martin, J. H. Willis, Evolution 61, 68 (2007). Such cutoffs imply nonetheless corresponds to Engineering Research Council of Canada that Canada 42. D. A. Levin, Syst. Bot. 28, 5 (2003). 35. H. D. Bradshaw, D. W. Schemske, Nature 426, 176 (2003). uncertain status that that sequences and thecluster Foundation 43. L. H. Rieseberg, J. H. Willis, Science 317, 910 (2007). 36. C. Lexer, Z. Lai, L. H. Rieseberg, New Phytol. 161, 225 together withforaInnovation. amount of There are a distinct cluster certain data (12). similarity in these 44. D. C. Presgraves, Trends Genet. 24, 336 (2008). (2004). must be differences in the amount of moreover Supporting Online same species, and sequence striking from the Material 45. D. C. Presgraves, Curr. Biol. 17, R125 (2007). 37. M. A. Beaumont, Trends Ecol. Evol. 20, 435 (2005). that this cutoff value is applicable to all groups www.sciencemag.org/cgi/content/full/323/5915/737/DC1 diversity observed within homologous house46. L. Fishman, J. H. Willis, Evolution 60, 1372 (2006). 38. P. Nosil, D. J. Funk, D. Ortiz-Barrientos, Mol. Ecol. 18, Tables S1 to S3 of bacteria or archaea. named species, ranging Christophe Fraser,1* Eric J. Alm,2,3,4 Martin F. Polz,2A. L. Case, J. Spratt,1Evolution 62,P. Hanage1 47. Brian G. H. Willis, William 1026 (2008). 375 (2009). keeping genes in these Recent MLSA studies, References which1.2% the concatenated sequences offor S. use for S. pneumoniae to 3.0% mul48. We thank M. Arnegard, R. Barrett, A. Case, H. Hoekstra, 39. S. M. Rogers, L. Bernatchez, Mol. Biol. Evol. 24, 1423 from 10.1126/science.1160006 M. Noor, P. Nosil, S. Otto, of Price, L. Rieseberg, T. life, and techniques (2007). tiple housekeeping genes to discern clustering The Bacteria and Archaea are the most genetically diverse superkingdoms pseudopneumoniae and up to 5.0% for S. mitis. patterns among populations of closely related for exploring that diversity are only just becoming widespread. Taxonomists classify these The distance between two randomly selected organisms into species in much the same way as they classify eukaryotes, but differences in their taxa, suggest that species defined by taxonoS. mitis genotypes is similar to the average disvalues many cases correspond to well-resolved mists inthat place two bacterial isolates into the biology—including horizontal gene transfer between distantly related taxa and variable rates of REVIEW S. pseudotance or same between S. pneumoniae andstudies also clusters. However, these homologous recombination—mean that we still do not understand what a bacterial species is. This sequence different species. The overall genetic pneumoniae genotypesmay be measuredimplies (2). This by the relatedness of isolates (5.1%) cutoff or descripshow that there is no universal is not merely a semantic question; evolutionary theory should be able to explain why species that the use of a fixed level of a species. Furextent of DNA hybridization between them, and tor of clusters that characterizessequence diverexist at all levels of the tree of life, and we need to be able to define species for practical gence that show 70% the clusters does not those for differentiating more DNA hybridthermore, inspection ofor species would tend applications in industry, agriculture, and medicine. Recent studies have emphasized the need to to either rejoin S. pneumoniae and S.hierarchy ization are defined which level in the (2, 10). always clearly revealas the same species pseudocombine genetic diversity and distinct ecology in an attempt to define species in a coherent and pneumoniae, or break up any other that cluster Such cutoffs imply that S. mitis so that nearly is more fundamental than sequences (Fig. 1) (7). convincing fashion. The resulting data may help to discriminate among the many theories of every isolate was certain1A shows own.relationtogether with a aFig. amount of similarity As an example, species of its the This is prokaryotic species that have been produced to date. clearly unsatisfactory. species, three closely must among the same ships be frommultiple isolates of and moreover that this cutoff value applicable to all groups he species debate in microbiology is not reflect only a tiny subset of those characters that related streptococcalis species. Streptococcus he species debate in Alm,2,3,4 Martin F. traordinary variety of microbial P. Hanage of bacteria is archaea. Recent MLSA studies, Christophe about a 1* Eric desire to catalog bac- Polz,2 Brian G. Spratt,1 Williamresources in1 the pneumoniae or a major human pathogen, S. mitis only Fraser, human J.microbiology is not allow bacteria to use different life, much of it Habitats and Ecological Differentiation only about a human desire to catalog uncultured (1). Beyond this, a small similar to A clearuse the criterion with sequences of taxowhich natural bacteria to a history of multerial diversity in a consistent manner, but environment, and only capturetaxa too fraction of is a commensal concatenated identify clusters of The Bacteria and Archaea are the most what it be true diversity in this of life, and techniques evolutionary importance, S. pseudopneumoniae diverse superkingdoms superkingdom of life. tiple housekeeping genes to discern clustering is also abacterial diversity in abecause ofgeneticallythedistinguished and circumscribed by rRNA se- nomic uncertainty (11), andwhich we might want fundamental argument consistent manpatterns among to find ecological features that ner,exploring that diversity of how evolutionary quences have Taxonomists classify [particularly to recently described organism closely related for but is also a ignorance are only just becoming widespread. revealed further diversity reveals about ourfundamental argument because More recently, molecular methodsthese through is acall species, is populations of uncertain status of what it into species inour ignorance of way multilocus hybridization and ribosomal and taxa, suggest corresponds defined by taxonoorganisms reveals and much the same ge- DNA-DNA eukaryotes, but differences inRNA distinguish them species to relatives. Among forces form, shape,aboutextinguish bacterialhowas they classifysequence analysis (MLSA) (2)their that nonethelessthatfrom close a distinct cluster in mists in many ability to cause well-resolved biology—including horizontal gene extinguish metagenomic studies and variable diversity pathogens, the There are striking a distinctive evolutionary forces form, shape, and transfer between distantly related taxa helped to define species, these data (12).cases correspond to differences in netic lineages, of the mechanisms of differen- (rRNA) sequencing] have(1), and this rates of homologous recombination—mean that we still not understand what a serious Thus, practi- sequence clusters. However, these studies also bacterial genetic lineages, of the mechanisms of needs to methods havebacterial limitations and disease has sequence diversity observed define tiation between subpopulations sharing common dobut these be explained by theory.species is. This the amount ofhistorically been used to within show that there is no universal cutoff or named is not merely semantic question; evolutionary cal difficulties, able a explain why species differentiationa the process of adaptation to new cannot reliably lack to large collection of similar species, but housekeeping genes only a minute descent, and of between subpopulations sharing theory should beassignof theory, and observations homologous pathogens constitutein thesedescriptor of of overall bacterial for S. pneumoniae to exist at all changing the tree process and we need to be ablespeciesof asspecies for practicalare too species,clusters that characterizes a species. Furlevels of environments. Animal spe- strains to to define yet unclassified microbial fraction ranging from 1.2% diversity. Mapping of of life, of adapta- of vast amounts (e.g., rRNA sequences common descent, and of the niches and thermore, pseudopneumoniae and up 5.0% for applications in by their agriculture, and medicine. Recent to resolve emphasized the need se- bacterial diversity onto environmental resources cies arenew niches and changing environments. conservedhave allhavesimilar controversy of how 3.0% for S. inspection of the clusterstodoes not tion to defined industry, morphological and be- diversity studies fueled the species). rRNA to always that reveal related two the bacteria combine genetic by their ability or inability to quence surveysdefine however,in(3–8). havioral traits anddiversity and distinct morpho- in an attempt to bacterial speciesrevealed the extra- S. mitis.clearly closelywhich level in randomly seindicatesThe distance betweengroups ofhierarchy Animal species are defined by their ecology one defines a have, species a coherent and is more mitis genotypes is similar to the 1) (7). convincing fashion. categories cannot easily help ordinary variety of microbial theories of resulting data may be interbreed, but such Thetraits and by their abil- to discriminate among the manylife, much of it lected S. fundamental than any For example, finecan be ecologically divergent. other (Fig.average logical and behavioral As an example, pneumoniae and pseudoprokaryotic species that Archaea produced to Genetic Clustering applied to the Bacteria orhave been(orcategories date. ity or inability to interbreed, but such indeed to uncultured (1). Beyond this, taxa too similar to be distance between S. Fig. 1A has beenS.observed scale resource partitioning shows the relationships among multiple populations coexisting many eukaryotic microbes). Instead, taxonomists distinguished and circumscribed by rRNA se- pneumoniae genotypes isolates (2). three implies cannot easily be applied to the Bacteria or Ar- Darwin commented that “all true classification among coastal Vibrio (5.1%) of This closely he forced debate microbiology is not reflect only a revealed 404]. diversity through related streptococcal (13). Partitioning was have been indeed to rely oneukaryotic microbes). quences have tiny subset of those charactershave thatthe use of a column species. Streptococcus chaea (or speciesto manyinbiochemical tests and is genealogical” [(9), p.furtherTaxonomists that in the water fixed level of sequence divergence limitedonly about a human desire forcedthis pur- multilocus sequence relatedness resources cutoff for differentiating species would collected either morphological characteristics for to rely allow bacteria to use different to define in the pneumoniae is a major human pathogen, mitis Instead, taxonomists have been to catalog bac- thus used sequence analysis (MLSA) (2) and discovered because strains were tend toS. from terial diversity and limited morphological values that place two capture a small fraction of distinct, ecologically informative samples, and pose. Naturally, biochemical characters have been metagenomic and only bacterial isolates into the rejoin S. pneumoniae and with a history of taxoon biochemical tests in a consistent manner, but environment, studies (1), and this diversity needs is a commensal bacteria S. pseudopneumoniae, is also a for the for this purpose. Naturally, bio- the true different species. Thus, practical dif- nomic uncertainty so that nearly every isolate was selected fundamental argument because of what it to be or diversity in theory. The overall genetic or break up S. mitis(11), and S.of the ecologically characteristics convenience of taxonomists; they same explained by this superkingdom of life. the phylogenetic structure pseudopneumoniae reveals about our ignorance of how evolutionary More recently, molecular methods [particularly is a recently described organism of uncertain status chemical characters have been selected for the ficulties, lack of theory,may be measured of vast a species of its own. This is clearly superimposed relatedness of isolates and observations by the differentiated populations was unsatisfactory. 1 forces form, shape, and extinguish bacterial ge- DNA-DNA hybridization and ribosomal RNA that nonetheless corresponds to a distinct cluster in Department of Infectious Disease they reflect only a extent of DNA hybridization microbial diversity convenience of taxonomists;Epidemiology, Imperial amounts of as yet unclassified between them, and on their habitats. Habitats were defined using (rRNA) fueled have helped of how species, these data (12). There are striking differences in netic London, London W2mechanisms of differen- have all sequencing]controversy to defineone de- Habitats and Ecological Differentiation of the 1PG, UK. 2 Collegelineages, those characters Department ofbacthat allow Civil those that showthe or more DNA hybridiza- an empirical modeling approach. This analysis tiny subset of 70% and Environmental subpopulations sharing Institute of the amount of sequence diversity observed within but a bacterial species serious tiation between Engineering, Massachusetts common finesthese methods have(3–8). limitations and A clear natural criterion to identify clusters of teria to use different resources in 3the environ- tion are defined as the same species (2, 10). Such revealed high levels of specialization for some Technology, Cambridge,process of adaptation to new homologous importance, which in might want descent, and of the MA 02139, USA. Department of cannot reliably assign a large collection of similar evolutionary housekeeping genes we these named ment, and only capture a small fraction of the cutoffs imply that sequences that cluster together populations (e.g., V. ordalii is only found as Biological Engineering, Massachusetts Institute of Technolspecies, ranging from 1.2% for S. pneumoniae to strains to species (e.g., rRNA sequences are too to call species, is to find ecological features that niches and changing environments. Animal spe- Genetic Clustering ogy, Cambridge, in this superkingdom Institute More MA 02139, USA. 4Broad of life. of MIT true diversity with a certain amount of similarity must be from single free-swimming cells), whereas others are conserved to resolve similar true classification 3.0% for S. them from close and up to Among cies are defined by Cambridge, MA 02139, and Darwin commented that “allspecies). rRNA se- distinguish pseudopneumoniae relatives. 5.0% for and Harvard University, their morphological USA. berecently, molecular methods [particularly DNA- the same species, and moreover that this cutoff more generalist (Fig. 1B) and can colonize a wide quence surveys [(9), p. 404]. revealed the have S. mitis. The distance to cause a distinctive sehavioral correspondence is genealogical”have, however,Taxonomistsextra- pathogens, the ability between two randomlydis*To whom traits and by their ability or inability to DNA hybridization andshould be addressed. E-mail: value is applicable to all groups of bacteria or variety of surfaces, including organic particles lected S. mitis genotypes used to to the average interbreed, but such ribosomal RNA (rRNA) ordinary sequence microbial to define cutoff ease has historically beenis similardefine species, c.fraser@imperial.ac.uk categories cannot easily be thus used variety of relatedness life, much of it sequencing] have helped to define (or indeed to archaea. Recent MLSA studies,too similar tothe and zooplankton in the water column (13). Most applied to the Bacteria or Archaea species, but uncultured (1). Beyond this, taxa which use be distance between S. pneumoniae and S. pseudothese methods have serious Instead, taxonomists concatenated sequences of multiple housekeep- of the predicted Vibrio (5.1%) (2). This implies many eukaryotic microbes). limitations and can- distinguished and circumscribed by rRNA se- pneumoniae genotypes populations are deeply not reliably assign a large biochemical tests and ing genes to SCIENCE VOL patterns6among divergent fromfixed level of sequence divergence 741 of similar quences have revealed further diversity FEBRUARY 2009 have been forced to rely on collection www.sciencemag.org discern clustering 323 through that the use of a each other, and in many cases rRNA sequences are too multilocus of closely related (MLSA) (2) and for differentiating named species; however, V. strains to species (e.g.,characteristics for this pur- populationssequence analysis taxa, suggest that are congruent withspecies would tend to either limited morphological conserved to resolve similarcharacters have been species defined by taxonomists in many needs splendidus is a notable exception and splits into pose. Naturally, biochemical species). rRNA se- metagenomic studies (1), and this diversity cases rejoin S. pneumoniae and S. pseudopneumoniae, quence surveysconvenience of taxonomists; they correspond to well-resolvedThus, practical dif- numerous closely so that nearly every isolate was selected for the have, however, revealed the ex- to be explained by theory. sequence clusters. or break up S. mitis related groups with distinct However, these theory, and observationsthere is ecological preferences, is clearly unsatisfactory. ficulties, lack of studies also show that of vast a species of its own. This presumably indicating no universal cutoff or descriptor of clusters that recent ecological radiation from a sympatric 1 amounts of as yet unclassified microbial diversity Department of Infectious Disease Epidemiology, Imperial characterizes a species. Furthermore, inspection ancestral population (13). Differentiation College London, London W2 1PG, UK. 2Department of Civil have all fueled the controversy of how one de- Habitats and Ecological Thus, genetic clusters and Environmental Engineering, Massachusetts Institute of of the bacterial does not always clearly reveal that correlate with ecology can be discerned. of A clear natural criterion to identify clusters fines a clusters species (3–8). Technology, Cambridge, MA 02139, USA. 3Department of What do importance, which we might want which level in the hierarchy is more fundamen- evolutionarythe genetic data tell us about mechBiological Engineering, Massachusetts Institute of TechnolGenetic Clustering anismsspecies, is to find ecological features that tal than any other (Fig. 1) (7). to call of population differentiation and the ogy, Cambridge, MA 02139, USA. 4Broad Institute of MIT As an example, that “all true the relation- distinguish them from the relatives. Among Darwin commentedFig. 1A shows classification evolutionary history of close microbes in quesand Harvard University, Cambridge, MA 02139, USA. is genealogical” [(9), p. 404]. Taxonomists have pathogens, bacteria are cause a distinctive disships among multiple isolates of three closely tion? That the ability to organized into genetic *To whom correspondence should be addressed. E-mail: c.fraser@imperial.ac.uk thus used sequence relatedness define cutoff ease has historically been used to define species, related streptococcal species. toStreptococcus clusters is not, per se, a very interesting obserREVIEW

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Fig. 1. Multilocus sequence analysis of closely related species. (A) Radial minimum evolution tree constructed using MEGA4, showing clusters among 97 isolates of four Streptococcus species identified as indicated. The tree was built using concatenates of six housekeeping loci, resulting in a total of 2751 positions in the final data set (2). Distances were calculated as the percentage of variant nucleotide sites. The mean distance within the clusters, calculated by MEGA4, is shown. To the right, the pneumococcal cluster is shown at larger scale, and putative subclusters are indicated in dark gray, purple, and green. (B) Ecological

associations of Vibrionaceae sequence clusters (13). Habitats (colored dots) were estimated as differential distributions of groups of closely related strains among samples (size fractions enriched in different environmental resources). Clusters associated with named species are evident, and in most cases species show a clear predilection for one of the habitats. The exception is V. splendidus, which breaks up into many closely related ecological populations. Asterisk denotes that trees based on additional loci indicate that the placement of V. panecida within V. splendidus may be an artifact of horizontal gene transfer at the Hsp60 locus.

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but pathogens constitutemodelsminutepopulation diversity. The first proposed mechanism was makes reference to the neutral diversity. The vation; many or most only a of a fraction of not, per se, a very interesting observation; many or strict the accumulation of unifying biological overall bacterial diversity. Mapping of mutation basedmodels of a population reproducing with a principles of mechanism was based on artificial reproducing with a small amount of bacterial most on artificial selection experiments with first proposed selection and niche partitioning, diversity onto environmental resources indicates small amount of mutation will eventually produce the ecotype has rightly become popular as a will eventually produce populations consisting bacteria grown for extended periods under selection experiments with bacteria grown for that closely of related organisms, irrespective of stable conditions in chemostats, of related orga- framework within which to conditions in cheof clusters related groups of bacteria can be eco- populations consisting of clusters which showed extended periods under stable discuss bacterial logically divergent. For example, fine-scale re- repeated selective of the details of the the whole evolution, speciation, and ecology. the details of the evolutionary forces or ecologi- nisms, irrespective sweeps in which evolution- mostats, which showed repeated selective sweeps which the whole (4, 16, was thought to source partitioningA more substantial observa- genome was ecologicaltodifferentiation. A more in The ecotype modelgenome 24) predicts that cal differentiation. has been observed among ary forces or thought hitchhike to fixation coastal that there is very little neutral the water substantial observation is thatmutation very little common ancestry will be preserved among baction is Vibrio populations coexisting in diversity along with an advantageous there is (periodic hitchhike to fixation along with an advantageous column (13). Partitioning was discovered because neutral diversity inSelective sweeps of microbes, terial populationsselection) (22). Selective sweeps in many populations of microbes, from which selection) (22). many populations can purge mutation (periodic within niches (which should strains were collected from distinct, ecologically almost all genetic diversity in the population be monophyletic), and thus predictsinthat popwe may infer some features of the selective from which we may infer some features of the can purge almost all genetic diversity the ecoinformative Neutral diversityphylogenetic struc- selective constitute a candidate mechanism the types are coherent self-contained genemechalandscape. samples, and the is the amount of and thus landscape. Neutral diversity is for ulation and thus constitute a candidate pools. nism for reducing been suggested (23). ture of the ecologicallyevident in noncoding re- amount of polymorphism that is evident in non- As a result, it has neutral variation that ecotypes polymorphism that is differentiated populations reducing neutral variation (23). was superimposedin synonymous substitutions. coding regions or results in synonymous sub- should be considered as putative or actual spegions or results on their habitats. Habitats were Niches and Ecotypes defined using measure of neutral diversity is the Niches and Ecotypes One common an empirical modeling approach. stitutions. One common measure of neutral cies, depending on the level of genetic differThis analysis revealedsize N , defined as the size To extend this model, one can consider multiple entiation from model, one can population. This high levels of specialization diversity is the effective population size Ne, de- To extend this the ancestral consider multiple effective population e for a population evolving V. ordalii is only of se- fined as the size of a populationby the selective model therefore has the advantage of providing of some populations (e.g., in the absence found ecological niches characterized evolving in the ecological niches characterized by the selective as single free-swimming cells), whereas others are absence of selection that would generate as much a mechanistic understanding of the evolutionlection that would generate as much neutral di- advantages they confer to specific genes. This advantages they confer to specific genes. This is more generalist (Fig. 1B) and can colonize a wide neutral diversity as is actually observed. Esti- the ecotype model, where genes adapted to versity as is actually observed. Estimates of Ne is the ecotype model, where genes adapted to ary processes, as well as an organizing principle variety of surfaces, including organic particles and mates of Ne for bacteria range from 105 to 109 specific niches cause selective sweeps within for bacteria range from 105 to 109 (14–18). To specific niches cause selective sweeps within for classifying species, that is based on experizooplankton in the water column (13). Most of the (14–18). To put this into context, the numbers of those niches but not in other niches. In this way put this into context, the numbers of Vibrio cells those niches but not in other niches. In this mental observations of bacterial populations. predicted Vibrio populations are deeply divergent Vibrio cells per cubic meter of seawater in tem- the population will undergo adaptation and difHowever, these observations of repeated per cubic meter of seawater in temperate coastal way the population will undergo adaptation from each other, and in 8 many cases are congruent perate coastal regions range from 108 to 109 (19), ferentiation while maintaining relatively low levels regions range from 10 to 109 (19), which sug- and differentiation while maintaining relatively selective sweeps were made in chemostats, with named species; however, V. splendidus is a which suggests vast census population sizes of neutral diversity, as selective sweeps confined gests vast census population sizes (>1020). This (>10 levels of neutral diversity, as of many to each natural regularly purge the population notable exception and splits into numerous closely low 20). This observation—a mismatch selective whereasecotype environments are markedly unobservation—a mismatch of many orders of orders of magnitude between ecotype regularly of any diversity that might have accumulated related groups with distinct ecological preferences, sweeps confined to each effective population stable and diverse. How would one detect the magnitude between recent ecological radiation size and population of any size (true of most (Fig. 2A). Crucially, what neutral natural we do presumably indicating effective population size purge the census population diversity that might presence of selective sweeps in diversity bacteand a sympatric ancestral population most bac- bacteria studied to (Fig. 2A). Crucially, what observe is predicted to be associated with adaptfromcensus population size (true of (13). Thus, have accumulated date)—was originally used to rial populations? The most conclusive examples teria studied to date)—was originally used to counter diversity we do and instead predicted ive traits. from bacteria but selective sweeps to genetic clusters that correlate with ecology can be neutral claims of neutralityobserve is argue that come not The ability of such from RNA viruses, counter claims of neutrality and instead argue to be associated with adaptive traits. 21). which mutate at much highersize has been recdiscerned. all genetic variation was adaptive (20, The limit the effective population rates than DNAthatWhat do thevariation wastell us about mech- ability of there are several sweeps to limit the based life forms. time (17, 23), and this model all genetic genetic data adaptive (20, 21). However, such selective different mechanisms ognized for some It has been established from However, population differentiation mecha- that can explain this size has been recognized sequences collected over many by Cohan and has been substantially developed years that the anisms of there are several different and the effective populationmismatch (Fig. 2). some time (17, 23), and this the differ- colleagues structure Because it links patterns of nisms that can explain this mismatch question? for Whatever mechanisms are drivingmodel has population(4, 16, 24).of the human influenza vievolutionary history of the microbes in(Fig. 2). Whatever mechanisms genetic clusters is entiation of bacteria into clusters, Cohan re- genetic differentiation driven by repeated selecThat bacteria are organized intoare driving the been substantially developed bythey mustand rus is predominantly with adaptation, and makes differentiation of bacteria into clusters, they colleagues (4, 16, 24). Because it links patterns tive sweeps (25) and that the resulting effective must restrict the accumulation of neutral of genetic differentiation with adaptation, and population size Ne (<100) is very much smaller 742 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org

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(27). This structure well describes the situation does not predict an association between neutral than observed for bacteria. The use of longitu- Bottlenecks, Metapopulations, and Local for parasites, which can colonize a host but are diversity and adaptive traits. dinal ecological and genetic data to distinguish Extinctions then forced to move on because the host develops The relevance of the metapopulation model to between competing models of evolution has a The essential element of the ecotype model immunity or dies (17). It also describes any the species question is that, although highly idelong pedigree in eukaryotic a limited (26). On with respect to limitingmay capture some is not situation where bacteria use biology resource alized and simplified, it neutral diversity of the the basis of these analogies, any inference of a niche adaptation per se, but rather the effecintensively for short bursts, followed by dispersal effects of complexity and instability of actual population structure driven by selective sweeps tive bottleneck population structure. Selective to new resource patches (e.g., colonization of ecosystems on caused by the replacement of would require good longitudinal data from natu- the whole populationtoby descendants simple, organic particles in seawater by Vibrio popula- sweeps are predicted be inevitable in from a ral bacterial metapopulation well as is fundamen- single environments but not in complex metations). This populations, as model observations stable individual and the resulting extinction of episodic crashes the diversitymodel because it of all other [a point partly 2A). Otherin (28)]. tally different from in ecotype causally associ- populations lineages (Fig. addressed mechaated with genetic changes and not associated nisms that induce or involve regular population with changes in ecological covariates. bottlenecks will also restrict neutral diversity. 743 ww.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 2009

del with ot niche bottlewhole le indill other induce ks will pulation ded into etween e popupatches acterial eria are ig. 2B)

Fig. 2. Different models of microbial evolution that lead to low values of Ne. (A) The ecotype model of bacterial population differentiation. The tree shows a single bacterial lineage that differentiates into two sublineages (E1 and E2) that differ in some aspect of their ecology. Periodic selection (a selective sweep) occurs at the points marked by asterisks and eliminates almost all of the diversity that has arisen since the last episode of periodic selection, which is shown by the dashed branches (diversity purged by periodic selection) or solid branches (existing diversity) on the tree. As the two populations are ecologically distinct (i.e., ecotypes), periodic selection in one sublineage does not influence diversity in the other sublineage and vice versa. Each ecotype can therefore diverge to become separate species. Reproduced from (24) with permission. (B) A metapopulation. Patches of varying size (gray circles) are vacant (empty) or may be colonized by a single genotype randomly acquired from another patch. Strains may diversify within a patch (as shown by different colors representing distinct genotypes), which may colonize empty patches as described above. A characteristic of this sort of metapopulation is patch turnover, in which patches occasionally become unable to support colonization and their inhabitants are removed (solid gray circles). (C) A neutral model with small population size. Different genotypes (different colors) arise by mutation or recombination and increase or decrease in the population by random drift. For some purposes, this simple model is an adequate effective description of the more complex processes represented in (A), (B), and (D), and of other more complex evolutionary models not described in this review. (D) Predator-prey dynamics and population bottlenecks. Regular population bottlenecks can drastically shrink the effective population size. In this case, bacteria-phage predator-prey dynamics are simulated with a classical Lotka-Volterra model, which can generate oscillations in population size of any amplitude. Population sizes and time axes are in arbitrary units for illustrative purposes only.

Choosing Between Models It has proven difficult to discriminate between models of population differentiation that focus on ecotypes or metapopulations. For example, the ecotypic structure of a soil Bacillus has been modeled to predict a priori which sequence clusters were ecotypes, and hence which ones should be associated with specific ecological properties (16). Some clusters are associated with certain phenotypic traits, such as a propensity to grow on shady north-facing slopes or sunny south-facing slopes. However, this model fitted no better (and in fact slightly worse) than a version of the model with several subpopulations and diversity generated only by neutral drift. This version of the model was dismissed because of its association with a very low estimate of population size (14). However, estimates of effective population size Ne are often grossly disconnected from census population sizes. It has proven very challenging to find models that successfully explain low estimated values of Ne while providing better predictions than models based on simple neutral drift. The analysis of Bacillus partly did this by predicting more ecotypes in the model than were observed

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Metapopulation structure, in which the population is divided into patches and where individuals disperse between patches, can generate very low effective population sizes if patches turn over (i.e., if patches are only intermittently able to support bacterial growth, and if a small number of bacteria are dispersed to colonize empty patches) (Fig. 2B) (27). This structure well describes the situation for parasites, which can colonize a host but are then forced to move on because the host develops immunity or dies (17). It also describes any situation where bacteria use a limited resource intensively for short bursts, followed by dispersal to new resource patches (e.g., colonization of organic particles in seawater by Vibrio populations). This metapopulation model is fundamentally different from the ecotype model because it does not predict an association between neutral diversity and adaptive traits. The relevance of the metapopulation model to the species question is that, although highly idealized and simplified, it may capture some of the effects of complexity and instability of actual ecosystems on population structure. Selective sweeps are predicted to be inevitable in simple, stable environments but not in complex metapopulations [a point partly addressed in (28)]. A metapopulation may evolve, differentiate, and adapt without global selective sweeps. Diversity lost by a local selective sweep in one patch may be rescued and reintroduced from other patches. The ecotype model, with its predicted monophyletic relationship between niche and genotype, may therefore not be an appropriate model of speciation in complex ecosystems.

and diversity generated only by neutral drift. This ples shown in Fig. 3 differ only in the rate of to recombination will depend more on the accuand diversity model was dismissed because This ples shown recombination only in the rate of to recombination will depend more loci than at version of thegenerated only by neutral drift.of its homologous in Fig. 3 differbetween the clusters, mulation of differences at neutral on the accuversion of the model was dismissed because of its homologous recombination between the clusters, mulation of The models also assumed homoassociation with a very low estimate of popula- all other parameters being held constant. As re- adaptive loci.differences at neutral lociathan at association with a very low estimate of popula- all other parameters being see constant. As re- adaptive distribution of also assumed a across tion size (14). However, estimates of effective combination increases, we held a distinction be- geneous loci. The modelspolymorphisms homotion size (14). However, estimates of effective population size Ne are often grossly disconnected combination increases, we see a distinction be- geneous distribution of polymorphisms across population size N are often grossly proven very Recombination rate relative to mutation using census population sizes.criteria, a hypothfrom establishede ecological It hasdisconnected Recombination rate relative to mutation from census to find esis that can be tested.models It has successfully challenging population sizes. that proven very 0.10 clonal 3 challenging estimated power that successfully 0.10 clonal This low to of low values of Ne while pro3 explain problem find models to detect selection 0.53 threshold explain low predictions than neutrality) pro(or, more accurately, to rejectof Ne while ison viding better estimated values models based a 0.53 threshold viding neutral drift. The analysis of Bacillus 2.00 sexual simple better predictions than models based on very general problem in population genetics that 2 2.00 sexual simple did this by predicting more ecotypes in neutral drift. The analysis of Bacillus 2 partly does not negate the importance of adaptation in partly did than ratherobservedmore ecotypes in this by predicting using more work the model evolution, but were suggests that established the model criteria, observed using established 1 ecological than were a model-based can be is needed if we wanthypothesis thatmethods 1 ecological criteria, a hypothesis that can be tested. to discriminate among different biologically tested. problem of low power to detect selection This plausible explanations of genetic data. In 0 (or, This problem of low scheme for performing more accurately, a power to detect selection Table 1 we proposeto reject neutrality) is a very 0 (or, more accurately, to reject neutrality)that does is a very general that could be used to test, analysesproblem in population genetics develop, general problem in population genetics that evonot validate different competing models does and negate the importance of adaptation inmore -1 not negate rather suggests adaptation in evolution, but the importance ofthat more work is -1 systematically. lution, but rather suggests that methods to dismore work is "Speciation point" for needed if we want model-based "Speciation point" for sexual species needed if we want model-based methods to discriminate among different biologically plausible -2 sexual species Homologous Recombination criminate among different biologically1plausible -2 explanations challenge to models that invoke One specific of genetic data. In Table 1 we proexplanations of genetic data. analyses we propose a scheme for involves a In Table bacterial ecotypic structure performingfeature ofthat could pose a scheme for performing -3 be used to test, develop, andanalyses that could evolution—homologous and validate different -3 be used to test, develop, recombination—that validate competing models more systematically. different 0% 10% 20% 30% we have not yet discussed. Bacterial reproduccompeting models more systematically. 0% 10% 20% 30% Mean genetic distance between clusters tion does not involve the obligate reassortment Homologous Recombination Mean genetic distance between clusters of genetic material observed in most higher or- Fig. 3. The dynamics of cluster divergence. The figure summarizes some key results from (15) in a Homologous Recombination One specific challenge to models that invoke Fig. 3. The ganisms. However, recombination does occur in phase-spacedynamicsthe cluster divergence. of two populations, with recombination from (15) in a plot of of genetic dynamics The figure summarizes some key results occurring beOne specific challenge to models of invoke ecotypic structure involves a feature thatbacterial phase-space plot of the genetic dynamics of two populations, with recombination occurring bebacteria and archaea (29) and feature of involves tween them at a rate that is varied for the three different simulations. The y axis shows the rate of ecotypic structure involves a typically bacterial evolution—homologous recombination—that tween them at a rate that between the clusters different simulations. The y axis shows the rate of the replacement of a shortrecombination—that change of genetic distanceis varied for the three as a function of the genetic distance itself (x axis). evolution—homologous piece of DNA with we have not yet discussed. Bacterial reproduction When the rate of change isbetween the clusters as a function of the genetic distancenegative,axis). change of genetic distance positive, the populations will diverge genetically; when itself (x they the have not yet discussed. Bacterial reproduction we homologous the obligate another strain. does not involvesegment from reassortment of When the rate of change is positive, the populations will diverge genetically; when negative, they Recombination becomes in most higher orga- converge. The direction of change for each scenario is shown by arrows color-coded to each does not involve the obligate probable with genetic material observed less reassortment of converge. The direction of change for each scenario is shown by arrows color-coded to each increasing sequence divergence does occur in scenario. For low recombination rates, the populations are effectively clonal and always diverge genetic material recombination higher the scenario. For low recombination rates, clonal and always diverge nisms. However,observed in mostbetweenorga- (green line). As the recombination rate the populations are effectively of recombination slow the nisms. and archaea (29) and typically reduces donor and the recipient (30, 31), which occur in (green line). As the recombination rate increases, the cohesive effects of recombination slow the increases, the cohesive effects bacteriaHowever, recombination does involves rate of divergence, until a threshold is passed (red line) and the populations become effectively bacteria not eliminate recombination involves but doesand archaeaa(29) and typically between rate of divergence, until a threshold is passed (red line) and the populations become effectively the replacement of short piece of DNA with sexual in the sense that the populations no longer diverge. For recombination rates above this the homologous segment piece of DNA with closely related species. Because another strain. level, the fate of the that populations will depend on how genetically distinct they are at the outset. the replacement of a shortfrom of such inter- sexual in the sense two the populations no longer diverge. For recombination rates above this the homologous segment given isolate strain. species recombination, any from another within If theythe fate of the two populations will then recombination will cause themtheymerge. the outset. Recombination becomes less probable with in- level, are within the “speciation point,” depend on how genetically distinct to are at If they are Recombination becomes less probable at least a species is almost certain to contain with in- farther are within the “speciation point,” then recombination will cause them to each other. These creasing sequence divergence between the donor If they away than this “speciation point,” they will continue to diverge from merge. If they are creasing sequence divergence reduces but does some genetic material that isbetween the donor curves are derived using the model point,” they will continue to diverge from each other. These and the recipient (30, 31), whichcharacteristic of farther away than this “speciation described in (15). and the recipient (30, 31), which reduces but does other closely related species. Hence, whereas it curves are derived using the model described in (15). was once thought that bacteria do not form spe6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org 744 cies in the eukaryotic sense because they do not 6 FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org 744 recombine at all (32), one current view is that process that reduces the rate of recombination Illegitimate Recombination and Gene they do not form species because they recom- between them—for example, a period of allopa- Content Variation bine too much (5). try or ecological differentiation. The speciation Illegitimate recombination or gene acquisition In asexual clonal organisms, even in the point is the amount of divergence between clus- is another unusual feature of bacteria. In this absence of any selective pressure, clusters will ters that needs to accumulate to prevent them case, genes or clusters of genes are acquired spontaneously split into multiple lineages or from returning to a single cluster if the barriers that typically have no homolog(s) in the recipi“daughter” clusters (15). However, under cer- to recombination are removed. A recent study ent strain. The importance of this phenomenon tain circumstances recombination can prevent hypothesized that two related Campylobacter is evident in the clear and ubiquitous signature this, and we can hence divide the bacteria into species are currently undergoing this process of such events in the growing body of genomic “sexual” and “nonsexual” species. This effect, of merging into a single species as a result of data. These are identified by differences in the described at greater length elsewhere (15), is changes in their environment (33). characteristics of the acquired DNA and that of The above insights were reached using mod- the host strain, for example, in base composition summarized in Fig. 3, which shows the rate at which two clusters diverge over time—that els based on the assumption that genetic varia- or codon usage; in most cases, the donor of the is, the increase in the mean genetic distance tion is neutral. Although this is obviously not DNA in question is unknown. Gene acquisition between them. If this becomes negative, then always an appropriate assumption, it is plau- leads to genomes being punctuated by stretches the two clusters will stop diverging and instead sible that the number of loci explicitly involved of foreign DNA. The largest of these (which converge. The three examples shown in Fig. 3 in adaptive ecological differentiation will be may be many kilobases in length) were initially differ only in the rate of homologous recom- small, and thus that in an unstable landscape, termed “pathogenicity islands,” because the new bination between the clusters, all other param- genomic barriers to recombination will depend functions encoded by the imports were often eters being held constant. As recombination in- more on the accumulation of differences at neu- involved in virulence, but a better term is “gecreases, we see a distinction between a “clonal” tral loci than at adaptive loci. The models also nomic islands” as the phenomenon is far from organism in which clusters are predicted to di- assumed a homogeneous distribution of poly- limited to pathogens (36, 37). Although it is verge (the green line) and a “sexual” organism morphisms across the genome, and violation hard to quantify the selective impact of import(the blue line) in which they are predicted to be of this may alter the tempo and mode of these ing any given gene(s) into a new background, held together by recombination. For “sexual” processes (34, 35). the occasional ability to gain a new adaptation species, the divergence of clusters requires a in this fashion—such as a new metabolic capa-

33

the clear and ubiquitous signature of such events tionary fate of such genes may hence be only acteristics, including the extent of variation in The importance of this phenomenon is evident in between them by mobile elements. The evolu- different genera on the basis of their specific charin the growing body of genomic data. These are loosely coupled with that of any particular gene content and recombination. In any case, no the clear and ubiquitous signature of such events tionary fate of such genes may hence be only acteristics, including the extent of variation in which they any particular biologist would deny the importance of ecology identifiedthe growing bodyin the characteristics of are species or strain in with that of are found, and gene content and recombination. In any case, no by differences of genomic data. These loosely coupled in the acquired DNA and that of in the characteristics of they are maintained through selection by and biologist would deny the importancenot ecology to species or strain in which they are found, the to what we observe, but it may of be easy identified by differences the host strain, for incorporate it in not be easy to example, in base composition orof the host strain, for they are maintained through selection by the to what we observe, but it may a fashion that is cothe acquired DNA andof transbility or a new mode that ticular species taxonomists. convenient in or strain in which don usage; in mostbase composition of cocases, the donor or incorporate it forand fashion that Nonea they are mainis example, for a pathogen—may mission in they are theless, found,taxonomists. Nonethe DNA usage; in most cases, the donor of is unknown. convenientpopulation geneticists may for donofin questionimportance in be enormous tained through selection by the have population but to tackle Gene the DNA inleads to genomes acquisition question is unknown. theless, little choice geneticists may the terms of speciation. habitat to which each host strain is question choice but to tackle the being Gene acquisition leads to genomes punctuated by stretches of have little of defining bacterial species Perhaps even more striking adapted. In the case of very mobile question of defining least, populations. punctuated by stretches or, at the very bacterial species foreignbeing amount largest of these of DNA. The of variation in elements—for example, plasmids is the or, at the we are estimating effective populations. theseEcological Whether very least, to antibiotics (whichforeign be many kilobasesofin may DNA. The largest encoding resistance gene content revealed by mulEcological factor b Whether we sizeestimating effective are from neutral diversity many populationmetals—the ecological length)(which initially from thekilobases in factor b were may be termed “pathotiple genomes same or heavy population size fromappropriate set of length) were initially the “pathoor choosing an neutral diversity genicity islands,” becausetermednew species, which because the specificity an appropriate these or choosing determined by set of at genicity islands,” implies that new strains to test for positive selection functions encoded by the occurs at a imports were gene acquisition by the imports were accessory loci positive selection at strains to of interest, species no link test for may have definitions functions encoded a locussequence we observe using often involved in virulence, but a betfrequency. It surprisingly highvirulence, but a betto the of interest, species definitions a locus often involved in are implicit ingenes of the analytical ter term now commonplace to speak is is “genomic islands” as the housekeeping much the 4). are implicit in much of(Fig.analytical ter term is “genomic islands” as the toolkit of population genetics. phenomenon “core”isgenome, which to limited to of the is far from from limited toolkit of population genetics. phenomenon far Distinguishing among mechapathogens (36, 37). Although it is hardhard encodes fundamental funcIdentifying MechanismsmechaDistinguishing among and pathogens (36, 37). Although it is nisms population differentiation to quantify the selective all members imtions shared selective impact of Delineating Species nisms ofof population differentiation to quantify the by impact of imin bacteria ultimately comes down portingporting any given gene(s) a new new any given (and, it should go of a species gene(s) into into a inWhat do ultimately comesbacterial to bacteria we want from down to Ecological factor aa Ecological factor species? Do we different models without saying, other related testing the ability of different models background, the occasional ability to to testing the ability ofneed theoretical background, the occasional ability 4. 4. Differences between core and auxiliary genes. schematic toexplain highly variable expense the patterns species), adaptation fashion— explain even gain a new a newonto whichin this fashion—Fig.Fig. Differences between core and auxiliary genes. This schematic toconsistency highlyatvariable patterns gain adaptation in this is bolted illustrates relationships between three species in “ecotype space,” within and between genetic-ecological of taxonomic practicality, incorpothe new metabolic capability or “accessory” such as a “auxiliary” metabolic capabilityillustrates thethe relationships betweenthree species in “ecotype space,” within and between genetic-ecological such as a new shown here in two dimensions, and mobile gene common to all three. clusters (Fig. 1). It is “sexual” genome, composed of genes rating (Fig. 1). It is still unclear or mode of transmission for or a new a new mode of transmissionafor ashown here in two dimensions, and a amobile gene common to all three. clusters both “clonal” and still unclear The The areas occupied by the species areshown as solid lines in red, blue, whether theseintopatterns are mainareas occupied by the species are shown as solid blue, whether these a single mainpopulations patterns are theoand operons of may or may pathogen—may be of enormous pathogen—may bethatenormous im- im- and green. The part of the ecological space where the shared in red, gene and green. The part of the ecological space where the shared mobile gene tained by gene flow One selection, mobile retical by gene flow unifying not be present speciation. portance in of in of isolates. It tained framework? or or selection, portance in terms terms all speciation. is selected in each species is shown by a dashed purple line and overlaps theoretical concept of of population seemseven more more striking is the selected in each species is shown by a dashed purple line and overlaps and what the effect is to consider likely that such auxiliaPerhaps even striking is the is and what the effect population Perhaps all three species ranges. Examples of (circular) genomes from each species amount of variation in gene content three and without the purple mobile (circular)are also illustrated. Note that structure is.is. The joint distribution of species as the joint within which ry genes help in gene content all with species ranges. Examples of element genomes from each species structure The arenadistribution of amount of variationto determine the with and without the are also illustrated. Note that individuals are similar can be revealed ecological properties from for each species, purple mobile element for all isolates, specific by multiple genomes genetic and ecological data can revealed by multiple genomes from for each species, thethe locus is not selectedfor all isolates, and its evolu- genetic and ecological dataenough, be locus is not selected and its evolu- or interbreed enough, thatVibrio the same species, which implies of species, which implies that tionary is uncoupled from that of each host species, because used, described above for indithe samethe organism. For example, thattionary fatefate uncoupled from that of each host species, because if one used, asas described above for Vibrio is if define populations gene acquisition occurs at a sur- undergoes a selective sweep or goes extinct, the mobile gene may one species (13), to genes compete dividual a group of related Leptospirilbe (13), gene acquisition occurs at a sur- undergoes a selective sweep or goes extinct, the mobile gene may be speciesvariant to define populations prisinglyrecently been hypoth- now reintroduced from one of the other species. Examples of such distributed without for reproductive success. rectly making a strong theoretlum has high frequency. It is without making either of theoretprisingly high frequency. It of the “core”reintroduced from one of the other species. Examples of such distributed ical commitment to a strong these is now commonplace to speakdifferent loci include drug resistance determinants in pathogens (e.g., b-lactamase Practical advances building on esized to adapt to ical commitment to result from commonplace to speak of thefundamentalloci genes) and heavy metal determinants environmental (e.g., b-lactamase alternatives. One clear either of these include drug resistance resistance in in pathogens organisms. These genome, an acidencodes “core” which mine drainage this or other theoretical concepts areas of alternatives. One clear result from genome, which shared by fundamental of agenes) and heavy metal resistance in environmental organisms. These all of the studies discussed here is functions encodes allof chrogenes may be transferred among strains and species by conjugative plaswill only come when these are system by shuffling members all of the studies discussed here functions shared by all should go of a genes may be transferred among (including transducing phage). species (and, it members without mids or other mobile elements strains and species by conjugative plas- that the underlying theoretical ques- is developed into explicit models mosome segments enriched in that the underlying theoretical quesspecies (and, other related 39). We ontomids or other mobile elements (including transducing phage). tions concerning species will not be saying, it should gospecies), and model-based algorithms that noncore genes (38, without tions concerning detailed will not saying, otherisrelated the be aware or “accessory” habitat to which each host strain is adapted. In answered in the absence of more species genetic- be which however, “auxiliary” bolted species), onto are tested and refined on a wide should, answered in the absence of it may be sensible which genome, composed of genes orand also leadthat habitatcasewhich each hostecologicaladapted. In environmental Alternatively,more detailed geneticis changes in core genes “accessory” that bolted the “auxiliary” may operons to the of different levels of elements—for exam- range of data. mapping. Moreover, some guidetic to of very mobile strain is specificity, may or maydifferentiation,in alloperons It seems ranging from highly resistance core functions to suggest types of application of principles case of very mobile elements—for exam- environmental mapping. Moreover, that guidegenome, composed of present andphenomenon well theple, plasmids encodingconserved to antibiotics or lines for thean ad hocecological studiessomewill ecological not be genes a isolates. that likely not such experimental studies seems may or may that be in auxiliaryall isolates. toof bacteria ple, plasmids encodinggrowth in all environments be different genera on the basis of studies that will present in genes help It determine heavy metals—the ecological specificity deter- to most informative of ecological their specific documented that are essential for resistance to antibiotics or lines for the types are emerging. Most importhe suchin structured environments (40). likely thatspecific ecological propertiesto determine heavyloci by these accessory loci specificityno to a tant, the ecological data collected must be imporgrowing auxiliary genes help of the organism. mined that are involved with adaptation link characteristics, including the extent ofMost relto metals—the ecological may have deter- be most informative are emerging. variation to the sequence clusters loci mayniche-specific in gene content and recombination. In any case, ForEstimates vary, dependingtheLeptospirillum mined by these accessorywe observehave no link evant the ecological data collected must be relexample, a group of related organism. the specific ecological properties of on the genomes specific habitat. Some narrow using house- tant, to the niche boundaries of the populations keeping genes (Fig. 4). has recently been hypothesized to adapt to evant to the if genetic the importancemap exFor example, available,of related Leptospirillumdif- to the sequence clusters we observespecies, being studied. Andwould denygroups do not populations that are a group but as little as 40% of genes genes may be distributed across using house- no biologist niche boundaries of the of ecolferent mine drainage system by studied. onto observe, groups do not easy (Fig. 4). has recently areas of an acid sequenced genomes of a keeping genesbetween themand mobile elements. clusively And sampling categories (as is likely exmay bebeen hypothesized to adapt to difpresent in all transferred Mechanisms by ogy to what weif geneticbut it may not bemap to be the case), more complex statistical models shuffling of chromosome segments enriched in Identifying clusively onto in a fashion that is convenient ferent namedofspecies (41). We may consider by areas an acid mine drainage system genes The evolutionary fate of such genes may hence to incorporate it sampling categories (as is likely will be needed to identify and describe the undernoncore genes (38, 39). We should, however, be Delineating Species and a for be the case), more complexpopulation gebe only Mechanisms within chromosome segments enriched in to taxonomists. Nonetheless, statistical that shuffling of thatnamed species as being characteris- Identifyingloosely coupled with that of any par- lying niche structure. Longitudinal studies models aware changes in core genes may also lead to What do we want from bacterial species? Do we neticistsneeded to identify and describe the the will be may have little choice but to tackle undernoncore genes (38, 39). We should, however, be Delineating Species ecological differentiation, a phenomenon well need theoretical consistency even at the expense measure the dynamics of ecological associations aware documented proposed strategy for developing What do we wantpracticality, incorporating both overH. Ochman, structure. Longitudinal or, athowthat that changesin experimental studies of bacteria and validating models of bacterial evolution that question of defining bacterial to determine the in core genes may also lead to from bacterial species? Do we lying niche A. C. Wilson, in Escherichia coli and 18. time will also be helpful species studies of taxonomic Table 1. A least, populations. of and thus how likely ecological differentiation, used to classify genetic diversity dataand “sexual” populations into expense transient natural habitatsWhether we areassociations a phenomenon well need theoretical consistencyfirm foundationsingle verySalmonella typhimurium: Cellular and Molecular Biology, even at the a for a measure the dynamics are,ecological estimatmight eventually be growing in structured environments (40). “clonal” and provide a F. C. Neidhart, over time are Ed. (ASM helpful to determine how also be Finally, neutral 1987), documented in species concept. taxonomic practicality, unifying theoretical ing effective populationPress, Washington, DC, diverbacterial experimental studies ofthe genomes of theoretical framework? Oneincorporating both bottlenecks will to result.size fromwhole-genome Estimates vary, depending on bacteria sity pp. choosing an appropriate set thusenvironor 1649–1654. entire populations of strains likely growing inare available, but as little as 40% of genes “clonal” and to considerpopulations into a within sequences natural habitats Environ. Microbiol. how to that structured environments (40). concept is “sexual” species as the arena single transient from et al., Appl. are, and of 70, 4103 19. J. R. Thompson 1. vary, depending on to genomes (2004). bottlenecks are to result. Finally, of interest, Estimates Collect samples accordingthe systematic ecological stratification. Focus on longitudinal studies, theoretical framework? One unifying theoretical test for positive selection at a locuswhole-genome geographical studies, and measurement physical 20. M. definitions are implicit in much sequences Trends Biochem. Sci. 1, N152 (1976).environthat are available, but as little as 40% of genes ofconcept and chemical gradients affecting arena within speciesKimura,from entire populations of of the is to consider species as the bacterial 21. 2009 growth. Consider biotic factors www.sciencemag.org competing bacteria or323 6 phage. analytical toolkit of Biochem. Sci. 1, N152 (1976). such as the presence of other SCIENCE VOL parasitic FEBRUARY R. Milkman, Trends population genetics. 745

Speciation

22. K. C. Atwood, L. K. Schneider, F. J. Ryan, Proc. Natl. 2. For each isolate, sequence as much as possible and affordable (16S rRNA, MLSA, auxiliary Distinguishing37, 146 (1951). among mechanisms of popAcad. Sci. U.S.A. genes, full genomes, etc.). ulation Levin, Genetics 99, in bacteria ultimately www.sciencemag.org SCIENCE VOL 323 6 FEBRUARYB. R. differentiation 1 (1981). 23. 2009 3. Use empirical classification algorithms that use genetic and ecological data to jointly map isolates. 24. F. Cohan, E. Perry, Curr. Biol. 17, R373 differcomesM.down to B.testing the ability of(2007). 25. A. Rambaut al., Nature 453, 615 (2008). 4. To guide model formulation, use population genetic tests on observed clusters, focusing on ent models toetexplain highly variable patterns 26. R. A. Fisher, E. B. Ford, Heredity 1, 143 (1947). tests for selection, population structure, and gene flow. within Slatkin, Theor. Popul. Biol. 12, 253 (1977). 27. M. and between genetic-ecological clusters 5. Generate evolutionary models and simulate populations. (Fig.J.1). It is still unclearGenetics 152, 1459patterns 28. Majewski, F. M. Cohan, whether these (1999). 6. Test, then reject or adapt, evolutionary models according to agreement between simulations 29. E. J. Feil, B. G. by Annu. flow or selection, and are maintainedSpratt,gene Rev. Microbiol. 55, 561 (2001). 30. J. Majewski, F. and real populations; if necessary, return to step 1. what the effect M. Cohan, Genetics structure (1999). of population 153, 1525 is. The 31. J. Majewski, P. Zawadzki, P. Pickerill, F. M. Cohan, 7. For successful models, develop model-based methods for interpreting pure genetic data jointC. G. Dowson, J. Bacteriol. 182, 1016 (2000). data distribution of genetic and ecological (without ecological covariates) and test on new data. can beT.used, as described above for Vibrio spe32. S. Cowan, in Microbial Classification, 12th Symposium 8. If one or more validated models emerge, use these to classify genetic data and to develop cies of the Society for General Microbiology, G. C. Ainsworth, (13), to define populations without making bacterial species concepts. P. H. A. Sneath, Eds. (Cambridge Univ. Press, Cambridge, a strong theoretical commitment to either of 1962), pp. 433–455.

these alternatives. One clear result from all of the studies discussed here is that the underlying theoretical questions concerning species will not be answered in the absence of more detailed genetic-environmental mapping. Moreover, some guidelines for the types of ecological studies that will be most informative are emerging. Most important, the ecological data collected must be relevant to the niche boundaries of the populations studied. And if genetic groups do not map exclusively onto sampling categories (as is likely to be the case), more complex statistical models will be needed to identify and describe the underlying niche structure. Longitudinal studies that measure the dynamics of ecological associations over time will also be helpful to determine how transient natural habitats are, and thus how likely bottlenecks are to result. Finally, whole-genome sequences from entire populations of environmental bacteria will be useful in dissecting the roles of the auxiliary and core genome in ecological differentiation. If after this process it emerges that some model or models are consistently validated for different study systems, these would inevitably form a good basis for identifying fundamental levels of clustering, or species. In the foregoing we have emphasized ecotype and metapopulation models, but there are others that deserve consideration—notably the epidemic clonal model (42) and the impact of phage epidemics causing classic Lotka-Volterra boom-bust dynamics (43) illustrated in Fig. 2D—and it is possible, even likely, that more than one of these mechanisms may be relevant to any given problem in speciation and cluster formation. Distinguishing among these mechanisms is the bacterial species challenge (Table 1), described in 1991 by John Maynard Smith as follows: “Ecotypic structure, hitch-hiking, and localized recombination can explain the observed patterns of variation. The difficulty, of course, is that the model is sufficiently flexible to explain almost anything. To test the hypothesis of ecotypic structure, we need to know the distribution of electrophoretic types [i.e., genotypes] in different habitats” (17). Much research on bacterial species to date has come from studies on pathogens, where the correct identification of species is crucial for accurate clinical diagnoses. However, for pathogens the identification of the multiple ecological

niches within (for example) the nasopharynx or gut is difficult, and studies of the relationships between bacterial populations and ecology may be more fruitful for some environmental species where the categorization of niches is a more tractable enterprise. Hopefully, we will soon obtain richer data sets that map bacterial diversity onto ecology and provide a way to distinguish among various models of population differentiation and speciation, including those based on ecotypes or metapopulations.

References and Notes
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15. 16. 17. 18.

19. 20.

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21. R. Milkman, Trends Biochem. Sci. 1, N152 (1976). 22. K. C. Atwood, L. K. Schneider, F. J. Ryan, Proc. Natl. Acad. Sci. U.S.A. 37, 146 (1951). 23. B. R. Levin, Genetics 99, 1 (1981). 24. F. M. Cohan, E. B. Perry, Curr. Biol. 17, R373 (2007). 25. A. Rambaut et al., Nature 453, 615 (2008). 26. R. A. Fisher, E. B. Ford, Heredity 1, 143 (1947). 27. M. Slatkin, Theor. Popul. Biol. 12, 253 (1977). 28. J. Majewski, F. M. Cohan, Genetics 152, 1459 (1999). 29. E. J. Feil, B. G. Spratt, Annu. Rev. Microbiol. 55, 561 (2001). 30. J. Majewski, F. M. Cohan, Genetics 153, 1525 (1999). 31. J. Majewski, P. Zawadzki, P. Pickerill, F. M. Cohan, C. G. Dowson, J. Bacteriol. 182, 1016 (2000). 32. S. T. Cowan, in Microbial Classification, 12th Symposium of the Society for General Microbiology, G. C. Ainsworth, P. H. A. Sneath, Eds. (Cambridge Univ. Press, Cambridge, 1962), pp. 433–455. 33. S. K. Sheppard, N. D. McCarthy, D. Falush, M. C. J. Maiden, Science 320, 237 (2008). 34. A. C. Retchless, J. G. Lawrence, Science 317, 1093 (2007). 35. K. Vetsigian, N. Goldenfeld, Proc. Natl. Acad. Sci. U.S.A. 102, 7332 (2005). 36. A. Tuanyok et al., BMC Genomics 9, 566 (2008). 37. U. Dobrindt, B. Hochhut, U. Hentschel, J. Hacker, Nat. Rev. Microbiol. 2, 414 (2004). 38. P. Wilmes, S. L. Simmons, V. J. Denef, J. F. Banfield, FEMS Microbiol. Rev. 33, 109 (2009). 39. V. J. Denef et al., Environ. Microbiol. 11, 313 (2008). 40. E. Bantinaki et al., Genetics 176, 441 (2007). 41. R. A. Welch et al., Proc. Natl. Acad. Sci. U.S.A. 99, 17020 (2002). 42. J. Maynard Smith, N. H. Smith, M. O’Rourke, B. G. Spratt, Proc. Natl. Acad. Sci. U.S.A. 90, 4384 (1993). 43. K. H. Hoffmann et al., FEMS Microbiol. Lett. 273, 224 (2007). 44. We thank T. Connor and S. Deeny for useful discussions. Supported by University Research Fellowships from the Royal Society (C.F. and W.P.H.), a program grant from the Wellcome Trust (B.G.S.), grants from the U.S. Department of Energy Genomes to Life program (M.F.P. and E.J.A.), and the NSF/ National Institute of Environmental Health Sciences Woods Hole Centre for Oceans and Human Health, the NSF Biological Oceanography Program, and the Moore Foundation (M.F.P.).

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34 mental bacteria will be useful in dissecting the
roles of the auxiliary and core genome in

References and Notes
1. J. Handelsman, Microbiol. Mol. Biol. Rev. 68, 669 (2004).

33. S. K. Sheppard, N. D. McCarthy, D. Falush, M. C. J. Maiden, Science 320, 237 (2008). 34. A. C. Retchless, J. G. Lawrence, Science 317, 1093 (2007).

35

is admitted and accepted as a member of a host society, it mimics adult ant acoustics (particularly queens) to advance its seniority toward the

’s hiermimicry lack the and of. species li (12): studied nsals or with ants e acouslthough s attracts s to siga basal t expect nea. ecies of icularly Diptera, ays the nt’s hicue has ate and

Berlin,

nu. Rev.

9. J. A. Thomas, G. W. Elmes, J. C. Wardlaw, Proc. R. Soc. in persistence have usefully employed post hoc tropical biomesand hence diversity, they lead to London Ser. B 265, 1895 (1998). 10. G. W. Elmes, J. C. Wardlaw, K. Schönrogge, J. A. Thomas, phylogeographic predictions for and individual palaeoclimate models of species both habitats to Entomol. Exp. Appl. 110, 53 (2004). species and assemblages (codistributed taxa; provide insights about processes shaping genetic 11. Materials and methods are available as supporting Fig. 1). Field sampling is driven by them, we and species diversity (5, 7). Building onthe model material on Science Online. first map the cover both predictedof endemic predictions to palaeodistribution refugia and 12. P. J. DeVries, R. B. Cocroft, J. A. Thomas, Biol. J. Linn. Soc. 49, 229 (1993). species to identify colonized) areas, particularly unstable (recently temporally stable (refugial) Ana F. Roces, J. Tautz, J. Acoust.*Soc. Am. 109, 3080 (2001). 2 Célio F. B. Haddad,3 Carolina Carnaval,1 Michael J. Hickerson, 13. and unstable previously colonized) regions for emphasizing (recently undersampled areas. If Miguel T. Rodrigues,4 Craig Moritz1 108, 1920 14. R. Hickling, R. L. Brown, J. Acoust. Soc. Am. species occurrence, which are then validated with the approach correctly predicts current patterns (2000). multispecies molecular data. Going beyond the of biodiversity at the regional scale, species 15. H. Markl, B. Hölldobler, Behav. Ecol. Sociobiol. 4, 183 Biodiversity hotspots, representing regions with high species endemism and conservation threat, (1978). traditional species-by-species approach, the mohaveH. Markl,mapped globally. Yet, biodiversity distribution data from within hotspots are too sparse should consistently show (i) higher genetic di16. been Z. Vgl. Physiol. 60, 103 (1968). lecular analyses contrast the fit of assemblageversity within and among populations in refugia 17. H. Markl, conservation (1965). for effectiveScience 149, 1392in the face of rapid environmental change. Using frogs as indicators, level data to the spatially because demographic relative to unstable areas, explicit of long-term 18. D. A. Grasso, A. Mori, F. under paleoclimates, and simultaneous Bayesian analyses of multispecies ecological niche modelsLe Moli, M. Giovannotti, scenarios suggested by the climate-based models. A. Fanfani, Ital. J. Zool. 65, 167 (1998). persistence and population structure; (ii) genetic molecular data, we J.compare alternative hypotheses of assemblage-scale response to late 19. T. C. Scott-Phillips, Evol. Biol. 21, 387 (2008). We apply population expansion the world’s signature of this approach to one of in unstable Quaternary climate change. This reveals a Apollo within the Brazilian Atlantic forest hotspot. 20. K. G. Schurian, K. Fiedler, Nachr. Entomol. Vereins hotspot most species-rich,multispecies colonization from yet notoriously endangered and We show that the southern Atlantic forest was climatically unstable relative to the central region, areas, reflecting 14, 339 (1994). understudied ecosystems: after the LastAtlantic adjacent refugial regions the Brazilian Glacial 21. C. served as a Entomol.climatic 283 (1993). for neotropical species in the late Pleistocene. This sets J. Hill, J. Aust. large Soc. 32, refugium which 22. Maximum (LGM, 21 kybp); (iii) absence of new D. R. Nash, T.forAls, R. Maile, G. R. in BrazilBoomsma, priorities D. conservation Jones, J. J. and establishes a validated approach to biodiversity 1 Science 319, 88 (2008). Museum of Vertebrate Zoology, University of California, genetic patterns of isolation-by-distance in unprediction in otherMus. Nov. 3025, 1 (1991). understudied, species-rich regions. 23. P. J. DeVries, Am. Berkeley, CA 94720–3160, USA. 2Biology Department, stable areas, given that colonization has been 24. K. Fiedler, B. Hölldobler, P. Seufert, Experientia 52, 14 Queens College, City University of New York, Flushing, NY 3 too recent to permit restoration of equilibrium (1996). ateTravassos, N. E. climate fluctuations helped refugia models have been dismissed because of 11367, USA. Departamento de Zoologia, Instituto de Quaternary Pierce, Anim. Behav. 60, 13 25. M. A. ate Quaternary climate fluctuations being described (8, 9). Our ultimate goal is to Biociências, migration and genetic drift (15); and between UNESP, Rio Claro, SP 3526-4100, Brazil. to shape present-day diversity in temper- conflicting evidence (2, 3) or circularity in iden- 4Departamento de Zoologia, Instituto de Biociências, (2000). helped to shape present-day diversity in pinpoint regions for inventory work and habitat (iv) strong phylogeographic structure between 26. N. ate andetboreal systems (1), 47, 733 (2002). E. Pierce al., Annu. Rev. Entomol. providing a tifying putative refugia (4), but historical pro- Universidade de São Paulo, SP 055008-090, Brazil. and boreal systems 14, protection before we lose a substantial fraction refugia, reflecting assemblage-wide, long-term 27. J. C.temperate C. Allyn, Bull. Mus. Entomol.(1), progeneral Downey, A.for understanding current pat- cesses must be invoked to explain regions of *To whom correspondence should be addressed. E-mail: context 1 (1973). viding a general context for understanding cur- of described and undocumented diversity. The population persistence in isolated areas. ternsWe thank N. ElfferichIn the J.tropics,for introducing high endemism (5, 6). Recent studies from sub- carnaval@berkeley.edu 28. of endemism. and P. DeVries Pleistocene Distribution models developed under current rent patterns of endemism. In the tropics, Pleis- approach differs from previous methods by dius to ant-butterfly acoustics; G. W. Elmes, J. C. Wardlaw, toceneLa Morgia, M. B. Bonsall, and referees for refugia models have been dismissed be- rectly modeling historical processes, as opposed climatic conditions accurately predict distribuV. circularity to observed SCIENCE VOL (10), 6 FEBRUARY 2009 tions of each of the target species along the At- 785 cause of conflicting evidence (2, 3)for designing comments and advice; and M. Charles or www.sciencemag.org biodiversity patterns323 with the the acoustical equipment. in identifying putative refugia (4), but historical aim of informing conservation. lantic rainforest domain [area-under-the-curve

Hypothesis Formulation

Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot

Diversity Distribution Modeling Diversity Model Validation

REPORTS

7. K. Schönrogge et al., J. Chem. Ecol. 30, 91 (2004). 8. T. Akino, J. J. Knapp, J. A. Thomas, G. W. Elmes, Proc. R. Soc. London Ser. B 266, 1419 (1999).

Audio S1 to S4 22 July 2008; accepted 28 November 2008 10.1126/science.1163583

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processes must be invoked to explain regions Supporting Online Material www.sciencemag.org/cgi/content/full/323/5915/782/DC1 of high endemism (5, 6). Recent studies from Materials and subtropicalMethods have usefully employed post biomes SOM Text hoc S1 and S2 Figs. palaeoclimate models of species and habiTable S1 tats to provide insights about processes shaping References genetic and species diversity (5, 7). Building Audio S1 to S4 on them, we first map the palaeodistribution of 22 July 2008; accepted 28 November temporally stable endemic species to identify 2008 10.1126/science.1163583 (refugial) and unstable (recently colonized) regions for species occurrence, which are then validated with have usefully employed post hoc tropical biomesmultispecies molecular data. Going beyond the traditional species-by-species palaeoclimate models of species and habitats to approach, the molecular analyses contrast the provide insights about processes shaping genetic fit of assemblage-level data to the on them, we and species diversity (5, 7). Building spatially explicit map the palaeodistribution of endemic first demographic scenarios suggested by the climate-based models. species to identify temporally stable (refugial) andWe apply this approach to one of regions for unstable (recently colonized) the world’s most species-rich, which are then validated with species occurrence, yet notoriously endangered and understudied ecosystems: the Brazilian multispecies molecular data. Going beyond the Atlantic rainforest. Originally extending motraditional species-by-species approach, the for 1,300,000 km2 along the Brazilian coast and lecular analyses contrast the fit of assemblagereaching into Paraguay and Argentina, this biome level data to the spatially explicit demographic has been reduced to by the climate-based models. scenarios suggested less than 8% of its range (8). Today’s fragments harbor one onethe largest perWe apply this approach to of of the world’s centages of endemic notoriously the world, with most species-rich, yet species in endangered and understudied and even genera Brazilian Atlantic many species ecosystems: the of vertebrates still
1 Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720–3160, USA. 2Biology Department, Queens College, City University of New York, Flushing, NY 11367, USA. 3Departamento de Zoologia, Instituto de Biociências, UNESP, Rio Claro, SP 3526-4100, Brazil. 4 Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, SP 055008-090, Brazil.

ause of n idenal proions of m sub-

*To whom correspondence should be addressed. E-mail: carnaval@berkeley.edu

We use molecular genetic data from multiple, largely codistributed species to test whether spatial modeling of species-specific Late Quaternary refugia sheds light on historical processes and hence improves prediction of genetic endemism and diversity in tropical Brazil (11). We focus on three common species of tree frogs that are widely distributed along the Brazilian Atlantic forest: Hypsiboas albomarginatus, H. semilineatus, and H. faber. Given their life history traits, amphibians are useful indicators of environmental changes through time (12). Whereas H. albomarginatus and H. semilineatus occur in low and mid altitudes and are mostly restricted to the evergreen or semideciduous components of the Atlantic Forest in eastern Brazil, H. faber has a broader altitudinal range and also inhabits mixed and deciduous areas, occupying interior and coastal sites in the Atlantic Forest south to Paraguay and Argentina (figs. S1 and S2) (13). The comparative phylogeographic approach is a powerful test of assemblage-scale responses to former environmental change and thereby provides a means for critical assessment of the scenarios produced by modeling of species’ distributions under palaeoclimates (7). The palaeomodeling method intersects predicted species’ distributions under current conditions and climatic extremes of the Late Quaternary (6000 years before present, or 6 kybp, and 21 kybp) to predict areas of stability (regions in which species are predicted to occupy irrespective of time period) and unstable areas (7, 14). Because the stability maps raise specific hypotheses about regional differences

(AUC) values (16) 0.968, 0.989, and 0.994; maximum Kappa (17) 0.81, 0.925, and 0.94 in H. albomarginatus, H. faber, and H. semilineatus, respectively (fig. S2)]. Stability maps, depicting the intersection of distribution models for each taxon under current, 6 kybp, and 21 kybp climates, predict for all species a large central refugium throughout the Late Quaternary (“Bahia refugium”) (Fig. 2). A second, much smaller refugium is predicted in the northeasternmost portion of the forest (“Pernambuco refugium”). In H. faber, a third, southeastern refugium of intermediate size is also predicted (“São Paulo refugium”). This is not surprising, given that this species occupies a broader environmental niche. In contrast to the central and northern regions, populations south of the Bahia or São Paulo refugia appear much less stable, despite the more extensive (preclearing) range of the forest in southern and southeastern Brazil. We hypothesize that these areas received a significant influx of migrants from adjacent, large refugial populations after the LGM. These palaeomodel results are congruent with the fossil pollen record, which documents a replacement of forests by grasslands in the southern Atlantic forest during the LGM (14, 18) and suggests the occurrence of small forest refugia in the southernmost range of the putative Bahia refugium (19). The results also agree generally with forest models published previously (14), although the central refugium extends farther south in the frog-based models. Such differences are expected because the forest and its associated species may differ slightly in their climatic tolerances and realized

is higher than the central (Bahia) because critical assessment of the scenarios produced by test of forest refugia in thereplacement of forests by magnitude larger in the other species refugium of the phylogeographic approach is a powerful small which documents a southernmost range of modeling of species’ distributions under palaeo-environ- grasslands in the southern Atlantic forest during relative to the less stable (southern) portion of the assemblage-scale responses to former climates (7). mental change and thereby provides a means for the LGM (14, 18) and suggests the occurrence of forest. Diversity of H. faber in this southern area the southernmost range of ofis higher than the other species because of the critical assessment of intersects produced by small forest refugia inSpecies The palaeomodeling methodthe scenarios preMap predicted Current & occurrence stable areas historical climate dicted species’modeling of species’ distributions under palaeodistributions under current condiclimates (7). data niches. Inclimatic extremes of the Late Quaternary (putative refugia) data tions and H. albomarginatus and H. faber, the method intersects Species Map of predicted Current & extension of the The palaeomodeling and 21 kybp) pre(6000 years beforepredicted distributions under current condipresent, orSão Paulo refugium 6 kybp, occurrence stable areas historical climate dicted species’ westward intotions and climatic extremes of in biome the stability (regions the Late Quaternary data (putative refugia) data to predict areas ofneighboring Cerrado which reflects model (6000 years before present, or 6 kybp, and 21 kybp) overprediction (fig. S2) (14). species are predicted to occupy irrespective of Spatially explicit hypotheses Re: Models of to unstable areas stability (regions habitat stability (7, 14). Because time period) and predict areas ofthrough fluctuat-in which species are predicted to occupy irrespective of ing stability maps raisepredict patterns of phyloSpatially explicit hypotheses Re: the climates correctly specific hypotheses about geography in time period) and unstable areas (7, 14). Because the in persistence and rainforest Atlantic hence diregional differencesBrazilian raise specific hypotheses about the stability maps spatial-temporal patterns (Fig. 2 and figs. S3 phylogeographic predictions distribution of congruence versity, they lead to to S5). In allpersistence highhence diregional differences in species, and of colonization genetic diversity across taxa spatial-temporal patterns levels of individual species and phylogeographic predictions for both divergence and population structure(coassemblages are distribution of congruence versity, they lead to and/or vicariance of colonization genetic diversity across taxa for both individual species corrected distributed taxa; refugia (Tamura-Neiand driven observed across Fig. 1). Field sampling isassemblages (coand/or vicariance distributed taxa; cover both predictedis driven Fig. 1). Field and Persampling by the model predictions to distances (20): 4 to 7% between Bahia by Sampling across predicted stable and unstable areas refugia and unstable (recently the nearby Bahiapredicted nambuco refugia,the model predictions to coverareas, 1% between colonized) both Sampling across predicted stable and unstable areas refugia and unstable (recently colonized) areas, particularly emphasizingH. faber). previously undersamrefugia in previously undersamand São Paulo particularly emphasizingSimilarly, in pled areas. If the approachdivergent clades withall taxa there are multiple, the approachpredicts cur- curpled areas. If correctly correctly predicts rent patterns region, agreeing withregional scale, scale, of biodiversity biodiversity at the regional in the Bahia rent patterns of at the model-based Genetic tests Assemblage-scale Genetictests of of Assemblage-scale species should consistently consistentlythis area. In Descriptive Descriptive predictions of species should show (i) higher genetic genetic a large refugium in show (i) higher stability/expansion, hypothesis testingtesting stability/expansion, hypothesis phylogeography diversity within and among populations in phylogeography diversity within and among populations in refugia refugia divergence times (HABC) H. faber, divergent clades are also represented divergence times (HABC) relative to unstable areas, long-termlong-term perbecause of perrelative to unstable areas, because ofpredictions of in the São Paulo region, matching structure; (ii) genetic sigsistence and population sistence and populationpopulation expansion in show a mid-sized refugium instructure; (ii) genetic sig- areas, Fig. 1. Proposed method of biodiversity prediction. Three stages are involved: biodiversity disnature of this area. All taxa unstable nature of population expansionthe unstable from Fig. tribution modeling (top), biodiversity prediction. Three (middle), involved: biodiversity disreflecting across in southernmost low genetic diversity multispecies colonizationareas, adjacent 1. Proposed method of model-based hypothesis formulationstages arehypothesis testing and reflecting the forest, ancolonization from Glacial Maximum model validation (bottom). multispeciesregions after the Last adjacent tribution modeling (top), model-based hypothesis formulation (middle), hypothesis testing and refugial area predicted to be less range of refugial regions after the Last Glacial Maximum stable by the palaeomodels. Furthermore, mito- model validation (bottom). DNA chondrial786 (mtDNA) lineages found in this FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org 6 (one in scale, long-term persistence of populations in and E). Using Bayes factor (25), we also detect region are shared with adjacent refugia FEBRUARY 2009 VOL 323 SCIENCE www.sciencemag.org 786 6 H. albomarginatus and H. semilineatus, two in isolated refugial areas, as opposed to post-LGM evidence for stability in both areas under the noH. faber). migration model [B(Z2 = 0, Z2 > 0) = 4.89], as colonization of refugial regions. Metrics of genetic diversity confirm the To test for assemblage-wide colonization well as under a postisolation migration model above patterns (Table 1). In H. albomarginatus of predicted unstable areas, we group mtDNA [B(Z2 = 0, Z2 > 0) = 4.84]. Relative to nuclear loci, mtDNA data are and H. semilineatus, genetic diversity (21) is an sequences from the southernmost refugial sites order of magnitude larger in the central (Bahia) [population 1 (Fig. 3A)] and from localities in more variable and readily collected and often refugium relative to the less stable (southern) unstable areas south of the refugium [population provide key insights into biological response portion of the forest. Diversity of H. faber in 2 (Fig. 3A)] to contrast two alternative historical to environmental modification (1). Although this southern area is higher than the other spe- models across the three codistributed species, single-locus inference can be imprecise in the cies because of the presence of two lineages that while allowing the taxon-specific demographic face of coalescent variance and the possibility of co-occur in the adjacent refugia. In all species, parameters to vary. In H1, the long-term persis- selection (26), our method benefits from a mulaverage net nucleotide differences across locali- tence model, two contemporary populations split titaxon approach, while explicitly accounting ties (22) reflects high geographic structure with- from an ancestral population prior to the LGM for the stochasticity of a single-locus coalescent in refugia (2.6 to 6.2% divergence). In contrast, (120,000 to 1.2 million years before present, or across taxa. Combining data sets from several sites located outside (south of) the refugia are Mybp, Fig. 3A). In H2, the recent colonization codistributed groups into a single hierarchical genetically more similar to each other, although model, population 2 is modeled as being colo- Bayesian analysis allowed us to estimate conto a lesser extent in H. faber (0.1 to 1.6%). Sig- nized from refugial population 1 subsequent to gruence across species, while borrowing strength natures of population expansion (23) are found the LGM (0 to 20 kybp; Fig. 3A). The results from the full comparative phylogeographic samin the unstable area for H. albomarginatus and indicate that all three species colonized the ple (24). This can translate into higher analytical H. faber, as well as in the Bahia refugium area southern (unstable) areas after the LGM (Z2 = 3, power and be more informative than qualitative for H. faber and H. semilineatus. The lack of the number of species evolved under H2), even comparisons of species-specific analyses. By signature of population expansion in the south- when allowing for postisolation migration (Fig. capturing the historical signal that emerges from ernmost localities of H. semilineatus may reflect 3, B and C). When Bayes factor is used (25), larger, combined multispecies molecular data low statistical power because of the exception- there is strong support for recent colonization in sets, HABC will offer the possibility of looking ally low levels of diversity observed in this spe- all three species (Z2 = 3) under the no-migration at patterns of historical community assembly in cies. As predicted, isolation by distance is not model [B(Z2 = 3, Z2 < 3) = 35.16], and moderate codistributed nonmodel organisms for which observed in unstable regions, but is detected support under a postisolation migration model barcode-type DNA sequence information (e.g., within refugial areas for H. albomarginatus and [B(Z2 = 3, Z2 < 3) = 5.70]. mtDNA data) can be feasibly collected. Using the same framework to test for longCollectively, the results identify the central H. faber. The hierarchical approximate Bayesian com- term persistence of refugial populations, we region as a hotspot within the Atlantic rainforest putation (HABC) method (24) allows us to use compare mtDNA sequences between the pre- hotspot and a refuge for biodiversity during data from all three species at once to test for dicted Pernambuco refugium [population 1 (Fig. climatic extremes of the Late Pleistocene. assemblage-wide responses to Late Quaternary 3A)] and adjacent (northern) populations from This is not to say that southern areas entirely climate change. These analyses support both the Bahia refugium [population 2 (Fig. 3A)] to lacked forested habitats in the late Pleistocene: model-driven hypotheses of (i) simultaneous, contrast alternative historical models H1 and H2. The existence of species and genera endemic multispecies colonization of unstable areas from In this case, the HABC results infer long-term to the southern forests (27), as well as some adjacent refugial populations since the LGM, persistence of populations in isolated refugia for palaeoecological and genetic evidence (28), as opposed to long-term persistence of popu- all three species (Z2 = 0, i.e., Z1 = 3), even when offer evidence to the contrary. Rather, the lations in unstable areas, and (ii) assemblage- allowing for postisolation migration (Fig. 3, D phylogeographically validated palaeomodels
Model Validation Hypothesis Formulation Distribution Modeling

6 FEBRUARY 2009

36

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refugial (stable)In all species, average net nucle- outside (south of) the refugia are genetically unstable area for H. for H. albomarginatus and H. faber, jacent refugia. refugia. In all species, average net nucle- outside (south of) the refugia are genetically unstable area albomarginatus and H. faber, jacent versus unstable areas in thedifferences Atlantic across localities (22) reflects more similar to each other, although to to lesser as well well the in the refugium area for H. faber H. faber as as in as Bahia Bahia refugium area for otide Brazilian across localities (22) reflects more similar to each other, although a a lesser otide differences rainforest. (Top)geographic structure withinwithin refugia (2.6 to extent inin H.faber (0.1 to 1.6%). Signatures of ofand andsemilineatus. The lack of lack of signature of H. H. semilineatus. The signature of extent H. faber (0.1 to 1.6%). Signatures high geographic structure refugia (2.6 to high Species-specific stability maps; Pernambuco modeled refugia in black. (A) H. refugium albomarginatus, (B) H. semilineatus, Fig. 2. in putative C C Fig. faber. NoteGenetic diversity large B (C) H.2. Genetic diversity in putative areas A A the absence of B refugial (stable) versus unstable Bahia refugium refugial (stable) versus unstable areas stable regions in Brazilian Atlantic rainforest. in the the southern portion * in the forest (south of the Bahia andmaps; * of the Brazilian Atlantic rainforest. (Top) Species-specific stability (Top)Paulo refugia) relative black. (A) H. Pernambuco modeled refugia in maps; São Species-specific stability to the refugium Pernambuco modeled albomarginatus, (B) H. (A) H. refugia in black. semilineatus, central and northern areas. Asterisks Sã o Paulo refugium refugium (C) H. (B) H. beyond the albomarginatus, inferred the absence of denote refugiafaber. Notesemilineatus, large Bahia refugium stable (C) H. faber. Note the absence of large current ranges regions(south of the Bahia and of the in the southern portion target species. 5.4% * * of the forest southern portion Bahia refugium stable regions in localities sampled for Symbols indicate the refugia) relative to the São Paulo * * of the forest (southScale bar, areas.and of the Bahia km. molecularcentral and northern 400 Asterisks analysis. Sã o Paulo refugium São Paulo refugia) relative to con- the (Bottom) The 50% majority-rulebeyond denote refugia inferred the central Bayesianrangesareas. Asterisks and northern of the target species. sensus current phylogenetic trees, 5.4% 7% Sã o Paulo refugium 7.8% Symbols indicate beyond the denote with sequences from thesampled for rooted refugia inferredlocalities othmolecular the target species. current ranges of analysis. Scale bar, 400 km. er two congeneric species studied 5.4% (Bottom) The 50% majority-rule Symbols indicate localities sampledde- con(root not shown). Thick internodes fortrees, 5.3 – sensus Bayesian phylogenetic 7% molecular analysis. Scale bar, 400 km. note clades withwith sequences from the oth7.8% 4% 5.8% rooted posterior probability (Bottom) The 50% majority-rule congreater than 90%. Percentages indicate er two congeneric species studied sensus Bayesian phylogenetic trees, deTamura-Nei corrected distances between (root not shown). Thick internodes 7% 5.3 – 7.8% rooted(20). sequences from the probability note 4% clades with clades with posterior oth5.8% 5.6% greater than species studied er two congeneric 90%. Percentages indicate Tamura-Nei corrected distances between (root not shown). Thick internodes de5.3 – clades (20). note clades with posterior probability 4% 5.8% 5.6% greater than 90%. Percentages indicate Tamura-Nei corrected distances between clades (20).
5.6%

presence of two lineages that co-occur in the adA

6.2% divergence). In contrast, sites located B

population expansion (23) are found in the C

Mybp, Fig. 3A). In H2, the recent colonization model, population 2 is modeled as being colonized from refugial population 1 subsequent to

coalescent variance and the possibility of selection (26), our method benefits from a multitaxon approach, while explicitly accounting for the

southern regions. This reassures us that the processes uncovered by the amphibian data may be generalized to and help to explain patterns of

Fig. 3. HABC analyses. (A) Simulated models H1 (long-term persistence) and H2 (recent colonization). In both cases, each species was modeled as two contemporary populations with mutation-drift parameters q1 and q2 that split from an ancestral population at a time t in the past. Ancestral population sizes are represented by (qt)1 and (qt)2; ybp, years before present. (B to E) Hyperposterior (bars) and hyperprior (dashed) densities of Z2 (number of species evolved under H2) given data from three codistributed frog species. (B) and (C) Models of refugial sites (population 1) and unstable, southern areas (population 2). (D) and (E) Models of Pernambuco refugium (population 1) and Bahia refugium (population 2). (B) and (D) Postisolation migration not included in model; (C) and (E) postisolation migration included in model.

788 model-based demographic hypotheses and 6 FEBRUARY 2009 (American Museum of Natural History, 32. We thank U. Caramaschi and H. Zaher for 2008 VOL 323 SCIENCE www.sciencemag.org
Table 1. Population genetic summary metrics used in model validation. n, Table 1. Population genetic summary metrics used in model validation. n, Sample size; S, number number of segregating sites.diversity parameter q q andmean Sample size; S, of segregating sites. The The diversity parameter and mean Da across Da across localities areper base pair (bp).(bp). testtest (23) is usedto detect localities are given given per base pair Hs Hs (23) is used to detect population expansion. BA, Bahia;Bahia;São Paulo refugia. Because predicted population expansion. BA, SP, SP, São Paulo refugia. Because predicted refugia were often larger than predicted unstable (recently colonized) areas, n, S, refugia were often larger than predicted unstable (recently colonized) areas, n, S,
SS Table 1. Population genetic summary metrics usednin n model validation. n, Species Species Area Area (min.; max.) q(min.; max.) Sample size; S, number of segregating sites. The diversitymax.) and max.) (min.; parameter (min.; mean
a q, and average Da values of the former were obtained not only from the total number samples, but also from all possible combinations of spatially number ofof samples, but also from all possible combinations of spatially contiguous localities distributed within the geographic extension of the contiguous localities distributed within the geographic extension of the unstable unstable area. Parentheses encompass minimum and maximum values from subsamples. area. Parentheses encompass minimum and maximum values from subsamples. P values bold highlight statistical significance at 0.05 probability level. P values inin bold highlight statistical significance at 0.05 probability level.

At a broader level, the congruence between

An Online Reference, version 5.2, 15 July

(2000).

q, and average D values of the former were obtained not only from the total

qq Mean Dthe former Hs obtained notcorr. coef.corr. coef. of a were Hs Mantel’sMantel’s the total only from q, and average Da values Mean Da (min.; of samples, but max.) from(Pall possible combinations value) (min.; alsomax.) value) value) (P value) (P of spatially number max.) (min.; max.) (min.; (P 0.076 0.062 0.499 contiguous localities distributed within–20.546 the geographic extension of the unstable 0.076 0.062 –20.546 (0.001) 0.499 (0.034; 0.072) (0.020; 0.082) (0.141) area. Parentheses encompass minimum and maximum values from subsamples. (0.034; bold highlight statistical significance at 0.05–0.140 (0.001) (0.020; 0.082)–11.498 (0.141) 0.003 0.001 P values in0.072) probability level.

Unstable(south of BA) 27 22 0.003 0.001 –11.498 (0.580) –0.140 (0.004) H. semilineatus Stable (BA) 71 0.031 0.036 0.054 (0.580) coef. (south of BA) (0.004) n 28 S q Mean Da –17.778 Hs Mantel’s corr. Species Area (718 (14; 58) (0.009; 0.034) H. semilineatus bp) Stable (BA) 28 71 0.031 0.036 –17.778 (min.; (6; 13) max.) (min.; max.) (min.; max.) (0.007; 0.041) (min.; max.) (0.029) value) (0.460) (P0.054 (P value) Unstable 15 0.003 0.004 0.436 (0.460) (718 bp) (6; 13) (14; 9 58) (0.009; 0.034) (0.007; 0.041) 0.114(0.029) H. albomarginatus Stable (BA) of BA) 36 207 0.076 0.062 –20.546 (0.248) 0.499 (south (0.357) Unstable 15 9 0.003 0.004 0.114 0.436 H. Stable (BA) 28 0.018 0.026 0.803 (0.001) (970 bp) faber (13; 23) (81; 94 155) (0.034; 0.072) (0.020; 0.082)–38.111 (0.141) (south of BA) (0.357) (0.0003) (0.248) (771 bp) (13; 23) (42; 80) (0.012; 0.022) (0.001; 0.044) (0.003) Unstable 27 22 0.003 0.001 –11.498 –0.140 H. faber Stable Stable (SP) (BA) 28 15 94 0.018 0.026 –38.111 0.803 48 0.023 0.028 –5.981 0.305 (0.580) (south of BA) (0.004) (771 bp) (13; 23) (42; 80) (0.012; 0.022) (0.001; 0.044) (0.115) (0.003) (0.221) (0.0003) H. semilineatus Stable (BA) 28 71 0.031 0.036 –17.778 0.054 40 0.015 0.016 –13.255 0.0001 0.305 Stable Unstable (SP) 15 18 48 0.023 0.028 –5.981 (718 bp) (6; 13) (14; 58) (0.009; 0.034) (0.007; 0.041)(0.014) (0.029) (0.456) (0.460) (south of SP) (0.115) (0.221) Unstable 15 9 0.003 0.004 0.114 0.436 Unstable 18 40 0.015 0.016 –13.255 0.0001 (south of BA) (0.357) (0.248) (south of SP) (0.014) (0.456) H. faber Stable (BA) 28 94 0.018 –38.111 0.803 www.sciencemag.org SCIENCE VOL 323 6 FEBRUARY 0.026 2009 787 (771 bp) (13; 23) (42; 80) (0.012; 0.022) (0.001; 0.044) (0.003) (0.0003) Stable central region 15 48 0.028 –5.981 0.305 much more SCIENCE VOL0.023 6 FEBRUARY 2009 presented here show that the (SP) www.sciencemag.org distantly related groups of Atlantic estation in this region relative to the more ex- 787 323 (0.115) (0.221) had much higher stability relative to the south. forest endemics. tensive forests in São Paulo and southern Brazil Unstable 40 0.015 0.016 –13.255 0.0001 Forest lizards (14, 29) and birds (30) also show 18 Because collection efforts, molecular studies, (9, 31). Not only could much unique diversity (south of the (0.014) (0.456) high diversity in the central portionof SP) biome and conservation priorities have been heavily be lost, but ongoing habitat destruction could relative to southern areas, and provide evidence biased toward southern and southeastern Brazil quickly erase the signature of the historical for population expansion in southern regions. (8, 9, 31), we predict that genetic diversity and processes that led to it, preventing a full underwww.sciencemag.org SCIENCE VOL 323 FEBRUARY 2009 This reassures us that the processes uncovered narrow endemism in the central corridor6of the standing of the mechanisms underlying local en- 787 by the amphibian data may be generalized to biome have been substantially underestimated. demism and, therefore, impeding more effective and help to explain patterns of diversity in other, This is serious, given the higher rate of defor- conservation measures.

Da across H. albomarginatus per Stable pair (bp). Hs test 36 is used to 207 localities are given base (BA) (23) detect H. albomarginatus Stable (BA) 36 207 (970 bp) (13; Because predicted (81; 155) population expansion. BA, Bahia; SP, São Paulo refugia.23) (970 bp) (13; 23) (81; 22 155) Unstable refugia were often larger than predicted unstable (recently27 colonized) areas, n, S,

joint, multispecies analyses of mtDNA diversity shows that palaeoclimatic niche models and assemblage-scale molecular genetic analyses can be used to forecast spatial patterns of diversity in poorly explored, highly threatened ecosystems. In a world of ever-accelerating environmental changes, this approach can help to guide research and conservation in other global hotspots or similarly complex tropical ecosystems. References and Notes
1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. G. Hewitt, Nature 405, 907 (2000). [CrossRef] F. E. Mayle, D. J. Beerling, W. D. Gosling, M. B. Bush, Philos. Trans. R. Soc. London B Biol. Sci. 359, 499 (2004). E. P. Lessa, J. A. Cook, J. L. Patton, Proc. Natl. Acad. Sci. U.S.A. 100, 10331 (2003). B. W. Nelson, C. A. C. Ferreira, M. F. da Silva, M. L. Kawasaki, Nature 345, 714 (1990). C. H. Graham, C. Moritz, S. E. Williams, Proc. Natl. Acad. Sci. U.S.A. 103, 632 (2006). W. Jetz, C. Rahbek, R. K. Colwell, Ecol. Lett. 7, 1180 (2004). A. Hugall, C. Moritz, A. Moussalli, J. Stanisic, Proc. Natl. Acad. Sci. U.S.A. 99, 6112 (2002). L. P. C. Morellato, C. F. B. Haddad, Biotropica 32, 786 (2000). M. T. Rodrigues, Conserv. Biol. 19, 659 (2005). C. Kremen et al., Science 320, 222 (2008). Materials and methods are available as supporting material on Science Online. M. B. Araújo et al., Ecography 31, 8 (2008). D. R. Frost, Amphibian Species of the World:

14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 24. 25. 26. 27.

28. 29. 30. 31.

New York, 2008); electronic database accessible at http://research.amnh.org/ herpetology/amphibia/index.php. A. C. Carnaval, C. Moritz, J. Biogeogr. 35, 1187 (2008). M. Slatkin, Evolution 47, 264 (1993). J. A. Hanley, B. J. McNeil, Radiology 143, 29 (1982). J. Cohen, Ed. Psych. Meas. 20, 37 (1960). H. Behling, R. R. B. Negrelle, Quat. Res. 56, 383 (2001). H. Behling, H. W. Arz, J. Pätzold, G. Wefer, Palaeogeogr. Palaeoclimatol. Palaeoecol. 179, 227 (2002). K. Tamura, M. Nei, Mol. Biol. Evol. 9, 678 (1993). F. Tajima, Genetics 143, 1457 (1996). M. Nei, Molecular Evolutionary Genetics (Columbia Univ. Press, New York, 1987). J. C. Fay, C. I. Wu, Genetics 155, 1405 (2000). M. J. Hickerson, C. P. Meyer, BMC Evol. Biol. 8, 322 (2008). R. E. Kass, A. E. Raftery, J. Am. Stat. Assoc. 90, 773 (1995). J. W. O. Ballard, M. Kreitman, Genetics 138, 757 (1994). C. F. B. Haddad, L. F. Toledo, C. P. A. Prado, Anfibios da Mata Atlântica (Atlantic Forest Amphibians) (Editora Neotropica, São Paulo, Brazil, 2008). M.-P. Ledru et al., Divers. Distrib. 13, 761 (2007). K. C. M. Pellegrino et al., Biol. J. Linn. Soc. London 85, 13 (2005). G. S. Cabanne, F. M. d’Horta, E. H. R. Sari, F. R. Santos, C. Y. Miyaki, Mol. Phylogenet. Evol. 49, 760 (2008). J. M. C. da Silva, M. Tabarelli, Nature 404, 72

providing access to collections MNRJ and MZUSP; O. Peixoto, M. Gomes, A. Muri, R. Kautskyi, S. Lima, E. Santos, J. S. Filho, J. V. Filho, G. Barros, J. Queiroz, R. Araújo, L. Japp, H. Japp, J. Giovanelli, J. Alexandrino, L. Toledo, O. Araújo, G. Egito, J. Zina, D. Loebmann, D. Pavan, R. Amaro, V. Verdade, F. Curcio, M. Dixo, and J. Cassimiro for field work assistance; W. Monahan and R. Hijmans for discussions about the modeling work; L. Smith and D. Turong for DNA-sequencing assistance; R. Pereira, R. Damasceno, S. Rovito, J. Kolbe, S. Singhal, R. Puschendorf, and A. Pounds for discussions about earlier versions of the manuscript. Funding was provided by the NSF (awards DBI 0512013 to A.C.C., DEB 0743648 to M.J.H., DEB 416250 and DEB 0817035 to C.M.), Fundação de Amparo à Pesquisa do Estado de São Paulo and Conselho Nacional de Desenvolvimento Científico e Tecnológico (grants to C.F.B.H. and M.T.R.). Sequences are deposited in GenBank (FJ502639-FJ502822). A.C.C. and C.M. designed the study; A.C.C., C.F.B.H., and M.T.R. collected the data; A.C.C., C.M. and M.J.H. analyzed the data; A.C.C. wrote the paper. All authors discussed the results and commented on earlier versions of the manuscript.

Supporting Online Material

www.sciencemag.org/cgi/content/ full/323/5915/785/DC1 Materials and Methods Figs. S1 to S6 Tables S1 and S2 References 8 October 2008; accepted 9 December 2008 10.1126/science.1166955

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