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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.

—Charles Darwin. people thought investigating the origin of life was something old scientists did at the end of their career. 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 elegance of the grasses. Peter Bowler analyzes the originality of Darwin’s contribution to the understanding of the diversity and diversification of the living world. his interpretations of Darwin and his contributions to evolutionary thought. Dolph Schluter reviews how research on speciation has shifted in focus from morphological evolution to reproductive isolation. The Voyage of the Beagle. That common ancestor was part. RNA-based life may have evolved the ability to assemble amino acids into proteins. in is that all living things inherited it built his argularge part. the South American tropics were a critical inspiration. Over time. When scientists tried to replicate Miller’s experiments with carbon dioxide in the mix. He did namely. their sparks seemed to make almost no amino acids. into which life organisms use double-stranded DNA to encode was first breathed. for DNA to evolve from RNA. they are inching their way toward making life from scratch. and endeavoured to fix in my mind for ever. The genetic code it is made of today. It’s a reasonable pursuit.” 3 . scientists have wondered how it In 1871. the novelty of the parasitical plants. however. RNA is remarkably versatile. In an iconic experiment in 1953. (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. an issue that would surely have vexed Darwin horribly had the bewildering diversity of microbes been known in his day. In modern cells. present. Darwin’s Legacy The day has passed delightfully. and many processes he prevent it from emerging. who model evolutionary processes in endemic tree-frog species in the Brazilian Atlantic Forest. from geology to domestication. Some now argue that more on evolutionary around him. then at the University of Chicago. genetic information. A most paradoxical mixture of sound and silence pervades the shady parts of the wood. In 2008. that it may be heard even in a vessel anchored several hundred yards from the shore. —Charles Darwin. L examines the extent to which biotic and abiotic factors have shaped species diversity in the fossil record. GEORGE RICHMOND/BRIDGEMAN ART LIBRARY. and. which would not have been the case before living creatures were formed. heat. LONDON (SUPERSTOCK) ike many other scientists raised in temperate latitudes. in large lived more than 3.. emus or bread mold. By the 1990s. In the first of four Review articles reprinted here. because the prospects for success are greater than they have ever been. “Now making an artificial cell doesn’t sound like science fiction any more.) A book review by Lynn Nyhart explores two recent volumes on Ernst Haeckel’s work. At the same time.C.org/origins RNA inside predated both DNA and proteins. but above all the general luxuriance of the vegetation. and how the first cells arose. methane. They copy Darwin believed that life likely emerged their genes into RNA and then translate RNA spontaneously from the chemicals into proteins. Each nucleotide in turn consists of three parts: a base (which functions as a 2 198 9 JANUARY 2009 VOL 323 SCIENCE www. the building blocks of proteins. with predecessor. It can sense the levels of various compounds inside a cell and switch genes on and off to adjust these concentrations. But he teins is identical. the accumulated evidence indicated that the early Earth was dominated by carbon dioxide. AN AMAZON OF WORDS FLOWED FROM Charles Darwin’s pen. Later. and other gases. membrane-bound cells with only what a big if!) we could conceive sciencemag. yet within the recesses of the forest a universal silence appears to reign. is a weak term to express the feeling of a naturalist who. Michael Benton Finally. filled me with admiration. Hydrothermal vents spew out other compounds that could have been incorporated into the first life forms. biochemically. that a protein compound was chemically formed ready to undergo still more complex changes. for example. botanist in a monthly series.org CREDITS (TOP TO BOTTOM): KATHARINE SUTLIFF/SCIENCE. however. Darwin returned to the Brazilian coast on his final homeward leg. with a focus on conservation. His books covered the gamut from barnacles to orchids. THE YEAR OF they use to translate DNA into pronitrogen. etc.. with a pinch of nitrogen—two gases not found in Miller’s flask. 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. Stanley Miller.NEWSFOCUS Darwin’s Inspiration. In doing so. however. Meteorites that fall to Earth contain amino acids and organic carbon molecules such as formaldehyde. The simplest naturalist had The English naturalist had built explanation for this shared biology his argument for evolution. researchers have been honing theories about the sources of the amino acids and RNA’s building blocks. for the first time. but the encounter with the Brazilian Atlantic Forest had an enduring influence on the development of his ideas over the following decades. the beauty of the flowers. The spark created a goo rich in amino acids. Thus. light. and who died 150 years ago in the year of the publication of Darwin’s Origin. for whom. Raw materials were not an issue. based on his results. they concluded. the very biodiversity hotspot that so inspired Darwin on his South American landfall. a picture full of indistinct. a Report by Ana Carnaval et al. It’s a small step. the experiments generated hundreds of times more amino acids than scientists had previously found. Joseph Hooker: “But if (and Oh! roots online at blogs. Just about all from some one primordial form. such a day as this brings with it a deeper pleasure than he can ever hope to experience again. whether they are The English did not publish these musings. when they could sit in an armchair and speculate. Feb 29th [1832] Introduction On the Origin of of Life on Earth in some warm little pond. and phosphorus. Charles Darwin was enthralled by his first glimpse of the tropical rain forest. His Beagle diary entry conveyed those immediate and thrilling first impressions. Christophe Fraser and colleagues discuss the contentious area of microbial species formation.sciencemag. he says: “The real hurdle is how you put together organic compounds into a living system. “When I was in graduate school.This essay is the first might have evolved from a simpler could observe lem in a letter to his friend. electricity. 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. “Now is a good time to be doing this research.” Darwin wrote. A Perspective by Stephen Jackson then considers the legacy of Alexander von Humboldt. he outlined the prob. Deputy Editor CREDIT: KATHARINE SUTLIFF/SCIENCE DARWIN Step 1: Make RNA An RNA molecule is a chain of linked nucleotides. The noise from the insects is so loud.. August 1836 Andrew Sugden. Miller suggested that lightning on the early Earth could have created many compounds that would later be assembled into living things. The Voyage of the Beagle. like Darwin. lightning began to look promising once again. with all sorts of ammonia and phosphoric salts.” says John Sutherland. In my last walk I stopped again and again to gaze on these beauties. DNA-based microbes that lution.” Scientists today who study the origin of life do not share Darwin’s pessimism about our ability to reconstruct those early moments. like a tale heard in childhood. When they added buffering chemicals that could take up these nitrogen compounds. tracing the links between Darwin’s ideas and current thinking. a chemist at the University of Manchester in the United Kingdom. how complex organic molecules such as RNA formed. D. prepared by Science’s news writers. on the the life that’s already here would already fairly complex. For 60 years. an impression which at the time I knew sooner or later must fail … they will leave. with resounding echoes even today in 21st century evolutionary science. We start with four of the essays from our “On the Origin of” series. for example. more than four years after his first landfall there. he filled notebooks with his ruminations and scribbled thousands of letters packed with observations and speculations on nature. has wandered by himself in a Brazilian forest.” The collection reprinted here is a sample of the articles published in 2009 by Science magazine in celebration of the Darwin bicentenary. ignited a spark that zapped through a chamber filled with ammonia. He and others are addressing each of the steps involved in the transition to life: where the raw materials came from. His enthusiasm for the tropical forested landscape was undiminished.5 billion years not think it would be possible to see life originating now because ago. the first cells might have tapped RNA for all the tasks on which life depends. further essays in this series are appearing monthly in Science throughout the year. and that is now reduced to a collection of small fragments scattered along the coast. such as carbon. Delight itself. at the present day such matter would be instantly devoured or absorbed. Cleaves suspects that lightning was only one of several ways in which organic compounds built up on Earth. To a person fond of natural history. on the processes he from a common ancestor— ment for evocould observe around him. The raw materials for life would have had to come from elsewhere. but most beautiful figures. the glossy green of the foliage. they have had to refine their ideas to take into account an ever-clearer understanding of what early Earth was like.” says Henderson James Cleaves of the Carnegie Institution for Science in Washington. It can also join together amino acids.

000 years ago. Jack Szostak and his colleagues at or rejecting them out covering these new reactions makes Suther. Robert Bednarik. horses. researchers have tried in vain to synthe. he might well tool to emphasize a lot understand its symbolic roots.for symbolic expression that certainly they build RNA molecules faster. Harvard are trying to make simple life forms. For some.” says ance.” reported that a had examples of what some researchers still make it look more likehe person. it way that the RNA gets words that artificial cell doesn’t may have evolved from organisms that used a more favorable. resemblance to a heat might cause the two strands to pull coincidence. Yet many at low temperatures.000-year-old object resembles a woman. originafter an exhaustive beads. See more social glue that helped tribes of rejected it as a–CARLof art. Cleaves and others think RNA-based life conditions for life even make up our languages. Researchers at back 100. that existed on Earth before life began. Like modern humans membranes. notes that they work well at the temperatures have come up with RNA molecules that can nonart is still logists. researchers have tried in vain to synthesize RNA by producing sugars and bases. scientists are reproduce.first cells. They could draw in to create.” says In July 2008. but bolic copies of itself without But it could also be that RNA wasn’t put help from proteins. insistsand grow. that RNA build the RNA.” he says. University of Lon. would need to make roots much further back in time—and cells depend on complicated All living 200. a reasonable pursuit. On the early Earth.org SCIENCE VOL 323 6 FEBRUARY 2009 199 5 709 . Strands of RNA tend to stick together at low temperatures. fatty acids to their creation. proof of work ZIMMER on humans’ evolutionary computer image. It’s that he membranes that an ancient human Australia.” says Szostak. phates. Szostak ings.reactions took place on the early Earth. soup. “If week (www. Szostak Sutherland. 30. They designed a leaguesago. Szostak times bigger. 1306).” says Sutherland. instead of might one day crack the tough-the penguin or a phallus. or pebble? and a cluster of phosphorus and oxygen sights. THE BOXGROVE PROJECT CREDITS (TOP TO BOTTOM): KATHARINE SUTLIFF/SCIENCE. They could draw in first cells. an independent sound like science found in nature. Lincoln and Joyce kept their RNA moleHe speculates that regular temperature cules in beakers. For him. But it could also be that RNA wasn’t put together the way scientists have thought. or the dra.appears in Africa nearly build the RNA.might have been possible. As a result.dropped.” many researchers have or more simple life forms. In Szostak’s protocells. we are art is an take in nucleotides together instead of separately making com. perhaps the you want to get from Boston to New York. 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.” replicate longer molecules faster. cycles wide of very simple protocells require a mental molecules to RNA almost sure to be mentionedreplicating RNAmargin. Szostak and his colmight have been possible. He is developing new forms of RNA that may be able to replicate longer molecules faster. art is an aesthetic This essay continues our are trying to make its “head” and Harvard researchers suspect. Expertly composed in of RNA molecules could grow 100 material quickly. 1306).000 years ago. coli and evidence that the fundamental: the cognitive abil. a stuttering candle. 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.” says archaeologist Dietrich Stoutearly Earth. In full-blown survive over a mean range.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. to species ancestral to Homo by nucleotides across together the way scientists have thought. To some archaeologists. Now Szostak is running experiments to bring his protocells closer to life. ber of later and replaced the earlier molecule. “To me. Sutherland can’t say for sure where these using just chemistry. GEORGE RICHMOND/BRIDGEMAN ART LIBRARY. Lincoln and Joyce found. By experimenting with different San Diego. “It just doesn’t work.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.red ochre and actually talking aboutmillion technologies at ancienttemperatures. It’s membranes and grow. They have been able to they would concentrate mix RNA and fatty “Now making an the nucleotides. he and his colleagues For archaeoGelett Burgess back in 1906. tors. “Ignoring the Over the past few years. surmore than 30. Indeed. And if Darwin was alive today.” land suspect it wouldn’t have been that hard investigating how fatty acids and other mole. the magnificent lions. They’re now investigating whether Sutherland. p.000 prebiotic cules in beakers. When arguing that the stone’s the cave with their artistic genius already in full don. but evolve.archaeologist based in Caulf ield South. many researchers seek to evolutionary advantage toSzostak. however. and ochre thought Szostak could go.” says Szostak. Carl Zimmer is author of Microcosm: E.more. In Szostak’s protocells. coli and the New Science of Life. in 1994. Online in Science this channels to draw one of our ances. but not so Since their such as formaldespelunkers which of these match their they could be ancestor of modhyde. cules on the a light switch. Heights. partner. the heat might cause the two strands to pull apart.large humans and out. 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. RNA evolved later and replaced the earlier molecule. these humanmade genetic molecules. Szostak p. making acids together in such a conditions for life even artificial cell doesn’t way thatinthe RNA gets more favorable. which first to own bring in nucleotides According to this hypothesis. Cleaves and others think RNA-based life may have evolved from organisms that used a different genetic material—one no longer found in nature. a population temperatures.to stick together archaeologists are skeptical.” says Sutherland.and pH levels found in ponds. this have turned the true test 250. When the protocell warmed up again. a sugar molecule. in these symbolic behavior and Ger. the debate over the function. an increasing num-SCIENCE species.org/cgi/content/ themselves. But if you can’t get there that way. dried up temporarily.repertoire. nucleotides cules on the early Earth might have trapped are arranged along a template of RNA. is to have something thatknow much about Art. protocells take in nucleotides of RNA molecules could grow 100 million quickly. For Sutherland can’t say for sure where these using just chemistry. there is an obvious way to go. heidelbergensis.resembles a human figure with stubby arms trapped in vesicles. Researchers at more about how life began. a reasonable pursuit. joining them together. there are other ways you could go. could have emerged on their own on the early Earth more easily than RNA.” quipped the years. But what of University College London. but I know what “I don’t can replicate by itself. dried up temporarily.000 years after their and legs. wasn’t too far off. called figured d’art is protoconsider a “creative explosion” that began If so. These paintings communication.000 years old. might have been packed in the vive on the are and are preparing to pubin any artiexplaining them away. would 100°C that At high Chauvet Cave the compo. For him. most researchers agree that evidence that symbolic behavior appears human figure might be apart. found.sciencemag. the origin of life and the origin of Darwinian evolution are essentially the same thing. come up with protocells leaky dating back 100. wasn’t too far off. they have docu-stretches backanddate the origins RNA mole. would need to make copies of itself without All living cells depend on complicated help from proteins. New Science of Life. 17 November 2000. but he After 2 decades.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. and then adding phosphates.EVOLUTIONARY ROOTS “letter” in a gene’s recipe).at the site of ture. But given newthe protocell warmed up again. which link one sugar to the next. cycles could have helped simple protocells surreplicating RNA might have been packed in the vive on the early Earth. Symmetry in stone.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.iniscent of aexperiments to Recent bring mod. but evolve. and then adding phos. shown here in a computer image.” While sites like Chauvet might be vivid deliberately modified the stone to says In July 2008. 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. allowing the new RNA molecule to function. Chemists have been able to use other compounds to build backbones for nucleotides (Science. use other compounds to build backbones for might just be vet Cave to break down in tears. where assemble loose nucleotides to match their they could be assembled into RNA. The different genetic material—one no longer Were these Darwin’s vesicles are able to add matic paintings that. discovery by Frenchassemble loose nucleotides to f inds really demonstrate assembled into RNA. and at lower temperatures. called PNA and TNA. ity to construct symbols that sciencemag. 17 November 2000. Some of the earliest art ified: “It’s a dimmer oping new forms of RNARam may beIsraeli-occupied Golan switch now. however. phallus. trapped vesicles.and Joyce found. California. Found in Morocco in 1999 next to a “Now making an two other hypotheses about how RNA came to the nucleotides. and.here in aearly humans to survive and the symbolic behavior requiresthe years at blogs. “The goal Venus. Once the replication is complete.” reported that he had figured out how proto—HENDERSON JAMES CLEAVES. 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. “It just doesn’t work. humorist and art critic I like. “We’ve got the molecules in our RNA. have shown tools.sciencemag. If those ponds build copies of quite ashort RNA Take the 6-centimeter-long other challenge. and new RNA molecules separate and join Their experiments also show that these with new partners to form new RNA. This failure has led scientists to consider two other hypotheses about how RNA came to be. origin of life and the Even of unearthed.” says Szostak. size RNA by producing sugars and bases.000 and 500. where although researchers and enough to let be the common simple organic compounds. reproduce? symbols had a commonly understood mean- On the Origin of of Art and Symbolism CREDITS (LEFT TO RIGHT): KATHERINE SUTLIFF/SCIENCE. could have emerged on their Step 2: The cell when modern humans —HENDERSON JAMES CLEAVES. but not so partner. Discovering these new reactions makes Sutherland suspect it wouldn’t have been that hard for RNA to emerge directly from an organic soup. nucleotides when they were warm and then use details of their success.that recipes for membranes.primitive protocell membrane brought in these ald Joyce of the Scripps Research Institute in molecules. as many with abe willing to write what some consider Protocell. He and his colleagues have been trying to build RNA from simple organic compounds.org/origins. the vivid drawings demon. that existed on Earth before life began. that RNAprehistorians are tracing our sym.org SCIENCE VOL 323 9 JANUARY 2009 199 www. “We’ve got the molecules in our RNA. nents of sugars reigned components of bases cave paint. and lower part of the Homo plete sugars andblack charcoal. 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. On the early Earth. Dis.journey onlineago. shown expression of something more monthly series. He is devel. he might well be willing to write a lot Protocell. LONDON (SUPERSTOCK) DARWIN CREDIT: JANET IWASA –CARL ZIMMER Carl Zimmer is the author of Microcosm: E. much remains to be found. “arms.sciencemag. this objetout how so old PNA and TNA. EVOLUTIONARY ROOTS ORIGINS “letter” in a gene’s recipe). Over the past few years. the origins of art cannot simply long before cave allowing the new RNA molecule to Tan-Tan “figurine” is rempaintings. reactions took place on the early Earth. At high hours.primitive protocell membrane brought there is an obvious way to go. a sugar molecule. producing the first protocells. Tracey Lincolnseems to have its origins large-brained H. But if you can’t ald Joyce of thein Africa. Online in Science this channels to draw nucleotides across their week (www. the musi.org/cgi/content/ membranes.” 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. looks more like a hoping they forces. distinguishing art from joining them together. Chemists have been able to warm little ponds? “It caused the discoverers of the Chau. 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. Berekhat that in the able to excavations likely perished over the ages.sciencemag. post.org SCIENCE VOL 323 9 JANUARY 2009 www. For years. 4 CREDIT: JANET IWASA www. potentially by a verycould have helpedearly paleoart.as dropped. 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. RNA evolved RNA alone. Now Szostak is running similar controversy over a be pegged to the latest discovery THE YEAR OF Gamble now says that his much.between 300. “The goal sights. in any case. protocells extremely and the as the world’s oldest hours. they have documented almost an entire route from prebiotic molecules to RNA and are preparing to publish even more details of their success. California. have shown how that recipes for membranes.” says Sutherland. stone tools. times bigger. AndRam object had indeed been etched Berekhat if Darwin was alive ochre dating today. fiction any nucleotides (Science. StrandsAnthropology. is to have something that can replicate by itself.smaller stone discovered in 1981 of ancient paintings or sculpcited comment needs to behis protocells closer to life. humans? Did symbols. cells could “eat” and Step 2: The cell CARNEGIE INSTITUTION FOR SCIENCE bring in nucleotides to If life did start out with RNA alone. abstract/1167856). In 30 vesicles survive over a 100°C range. Lincoln “When we talk a population art. but he After 2 decades.about beads andtemperatures. Recent Institute in have turnedBy experimenting with different Scripps Research excavations molecules.with new partners to form new RNA. molecules. put it some years ago. “If you want to get from Boston to New York. and a cluster of phosphorus and oxygen atoms. According to this hypothesis.000 more about After all. He and his col. 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. bases first. they build RNA molecules faster. get there that way. They’re now investigating whether these humanmade genetic molecules. and As they more precisely pin. Tracey Lincoln and Ger. by someand his colup elaborate stone how beads. the true test of his experiments will be whether his protocells not only grow and reproduce. producing the first protocells. THE BOXGROVE PROJECT.” he says. And so. 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. Once the replication is complete. serve as ahow life began. flower. and symbolic expression. If life did start out with about 40. 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. raising the question of how a sapiens. whether they be the rich trove of stone in suchestimated to be making acids together tools a be. which link one sugar to the next. atoms. old porous that the large RNA could slip out. raising the question of how a abstract/1167856).” says Sutherland.their in some cases. communicate meaning. there are other ways you San Diego.sciencemag.But there’s wide. such as formaldehyde. cal sounds that convey emotion. “To me. found. If those ponds build copies of other short RNA molecules. image lish even more cle or paper about the earliest art.

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. Darwin himself saw an evoluincluding chopping tree branches COLORADO SPRINGS tionary parallel between toolwith hand axes and shaping the making and language. But by archaeologist Sarah Wurz of the Iziko Musecounts.000 years ago. p. even protect skin against mosquito bites. –MICHAEL BALTER CREDITS (TOP TO BOTTOM): FRENCH MINISTRY OF CULTURE AND COMMUNICATION/DRAC RHONE-ALPES/DEPARTMENT OF ARCHAEOLOGY. The half-million-year mark also heralded the arrival of H. “The tools tell us that the hominid world was changing. the Blombos team reports finding ancestors. “What aspects of human social organization and adaptation wouldn’t benefit from the evolution of language?” asked Terrence Deacon. ing and were shared within groups of people.” says agrees: “If it’s a one-off. especially when it is focused on the most sophisticated form of symbolic communication: language. red. the question is a no-brainer. willing to grant that our species.” says Philip Chase.000 years ago and per. 100.known tools.org/ bolic behavior.shows symbolic capacity. Indeed. UNIVERSITY OF COLORADO. positron emission tomography To many researchers. This may also explain why great art has such emotional force. 1731).considered by some to be personal ornarately crafted bone points. At this single preferred the color red: Excavators have site. Likely created by of wood. says Ian Watts. an anthro. humans at Twin Rivers in what is now Zambia bolic expression. ancient humans were ums of Cape Town in South Africa. But only Late Acheulean knapping turned on circuits also linked to language. It’s not sending a researchers look instead for proxy spears’ creators—probably membehaviors that might have bers of H. by expressing meanings that are difficult or impossible to put into words. These so-called backed tools have meaning at all.sciencemag. some experts are leery of assign. modern humans apparently strongly appear to be abstract designs. artistic expression. and blue-black.” Wadley consider diagnostic elements of symbolic says. ”There is very strong circumstantial evidence for the very great antiquity of the color red as a symbolic category. they made pre-Acheulean and A roaring start. erectus and probably used to cut plants and been widely regarded as evidence of sympologist at the University of Pennsylvania.” Darwin thought require similar cognitive wrote in The Descent of Man. presumably made but [the object] still hav[ing] no symbolic axes appeared in Africa. And since at that date the ochre users behavior came together.000-year-old Qafzeh Cave site pieces of red ochre engraved with what nearby. was a key way that early humans symbolically communicated social identity such as membership in a particular group. But why? What selective advantages did using symbols confer on our ancestors? To some scientists. “This flexibility in stone tool manufacUniversity of Colorado. and beads have convinced many researchers that the building blocks of symbolism had emerged by at least 100. for example to display prestige or even attract members of the opposite sex. they may also have been key to cementing these bonds. in his influential book The Symbolic Species: The Coevolution of Language and the Brain. Both methods turned on visual and motor areas of the brain. Germany. say Wynn and other researchers. the team reported last year. some of which were gathered far from the site. “You can imagine [an Then.” about 500. and Eye of the beholder.been split in two and then sharpened to make nents. It’s not sending a message to anyone. and raising children.” says anthropologist Sally McBrearty of the University of Connecticut. Some researchers argue that this represents an early case of “color symbolism. Deacon went on to list just some of the advantages: organizing hunts. probably spears with stone flakes. Modern-day experiments have shown that ground ochre can be used to tan animal hides. skills also gets some support demands a “perfect hand” as well from a surprising quarter: brainadapted to that task as the “vocal imaging studies. debated whether creating the earliest ones ture [indicates] symbolic capabilities. Yet many archaeologists are 30 January. the most sophisticated form of The idea that sophisticated symbolic behavior.” citing the universal importance of red in historical cultures worldwide and the apparently great lengths to which early humans went to gather red ochre. ORIGINS Late Acheulean tools.appear able to imagine and create even more “Venus figurines” found at sites across Eura. which date back 2. sharing past experiences. “To chip a toolmaking and symbolic flint into the rudest tool. some recent study concludes that these it counts. These implements.engraved ochre in levels dating back to ing them symbolic savvy. Color me red At Twin Rivers. shelter in Israel. and archaeologists have sites. 569). Researchers agree that Chauvet Cave’s magnificent paintings. purple. At rated beads made from snail shells and the 92. though there’s little hard evidence for this. Charles steps spanning several days. an independent ochre expert in Athens. Excavator Lawrence Barham of the University of Liverpool in the United Kingdom thinks they used the ochre to paint their bodies. many researchers have argued that symbolic communication is what held groups of early humans together as they explored new environments and endured climatic shifts. Most archaeologists agree that body painting. Storrs.could envision a complex finished tool and Thus many researchers are reluctant to lion years. but full-fledged art.ORIGINS tools. including these lions. And in work now were not modern humans but our archaic in press. are full-blown art. was probably not needed to make the earliest 260. They left behind finely made blades Tan or Berekhat Ram objects as signs of simple chopping and scraping implements.000 years ago (Science. Some scientists argue that this 77. That kind of ability ary edge in the battle for survival. consist mostly of rocks that have put it together in steps from different compoaccept rare.000 years ago and possibly much earlier. ity to hold an abstract concept in one’s head— As one moves forward in time. it’s hard to be sure how the ochre was actually used. a number of what many archaeologists studied 71 pieces of bright red ochre associated with human burials. fancy tools. One the archaeological record.sciencemag. South Africa. our African ancestors began to create a wide variety of finely crafted blades and projectile points. Berkeley. may have helped ensure the survival of the fittest. which allowed them to exploit their environment in more sophisticated ways. usually by blunting or “backing” one edge— ancient human] recognizing a resemblance teardrop-shaped tools called Acheulean hand to be hafted onto handles. In that way. erectus. sharing food. as needed for decoration. There are other hints that the H. says archaeologist Lyn Wadley of the University of Witwatersrand in Johannesburg. These finds of colorful ochre.000-year-old shell beads left sophisticated tools. pink.000 years ago.6 mil. Yet while the Twin Rivers evidence is suggestive. sapiens. butcher animals. and so presumably enhance their survival and reproduction.000-year-old wooden spears “If it’s a one-off. one-off discoveries like the Tan.H. At the Skhul rock as Blombos Cave on South darwin. humans For example. Not long afterward. Archaeologists refer to these tools as Middle Stone Age technology and agree that they did require mental templates. which had a much larger brain than H. Archaeologists debate whether this modified stone was meant to represent a woman. humans left Africa’s southern Cape. teaching toolmaking. in the case of the tool. to “impose” a pre. including music.7 million years ago. thus enhancing their survival during rough times and boosting their reproductive success in good times. I don’t think it required an abstract mental template.000 years ago. 23 June 2006. making scans on three archaeologists— sophisticated tools and using Symbolic start. sharpening their evolutionsia beginning about 30.ments (Science. including elabo. As for art and other nonlinguistic forms of symbolic behavior. such as toolmaking. much as people today declare social allegiances and individual personalities by their clothing and jewelry. Colorado Springs. —THOMAS WYNN. Early humans there also left behind at least 300 lumps of ochre and other pigments in a rainbow of colors: yellow. 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.discuss the roots of art at might also have engaged in symhaps much earlier.sciencemag. large. help stone tools adhere to bone or wooden handles. a biological anthropologist at the University of California.000-year-old engraved ochre all skillful stone knappers—as symbols both require the capac. I don’t think the earliest symbolic messages in from Schöningen. “We simply don’t know how ancient people used ochre 300. for example. was creating and sciencemag. Stout’s team ran organs” are to speaking. brown. concrete information as well as abstract concepts allowed early humans to cooperate and plan for the future in ways unique to our species.” says Wynn. heidelbergensis—carmessage to anyone.org SCIENCE VOL 323 6 FEBRUARY 2009 711 7 .org modern humans who ventured Hear author using certain kinds of symbols out of Africa around this time Michael Balter by 75. as well as the wearing of personal ornaments such as bead necklaces. By skillfully carved and follow a common motif. heidelbergensis. the hundreds of bone and stone and. an anthropologist at the greatly in shape. The ability to communicate detailed. which Wynn and many others argue are clear examples of an imposed form based on a mental template. people 100. And even ground ochre could have had utilitarian uses. as well as perfo.000 years ago were abstract mental template. CHRIS HENSHILWOOD AND FRANCESCO D’ERRICO Online 710 6 CREDIT: FRANCESCO D’ERRICO AND APRIL NOWELL 6 FEBRUARY 2009 VOL 323 SCIENCE www. ancient They are widely regarded not only as sym.determined form on raw material based on an elaborate tools. Some have even argued that these skillfully crafted hand axes had symbolic meanings. these hand-held tools vary bolic behavior when found at much younger Thomas Wynn. about 1.” required similar cognitive abiliried out at least eight preplanned ties. p. There’s little sign that it was ground into powder. and other tools that had been modified— symbolic behavior. At sites such www.org www. it’s not just the tools that hint at incipient symbolic behavior.

and cyanobacteria embed their chlorophyll in two large protein clusters. and altered the number of hydrogen bonds. At issue is how to interpret a other scientists disagree. A cell needs both photosystems to carry out oxygenic photosynthesis. other researchers remain skeptical. 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. More tron source. Biochemists James live in habitats such as scalding hot springs. rust. which today origins. p. To explain how the two protein complexes wound up together.emerged until shortly before the GOE. possibly through the duplication of genes.” says geobiologist Paul Falkowski of Rutgers University in New Brunswick. But “it’s a terribly important problem.org 9 1287 . RuBisCO feeds carbon dioxide into the reactions that yield sugars. a key photosynthetic enzyme. 22 November 2002. DARWIN says astrobiologist Roger Buick of the University of Washington.2 billion years old hold rich bacterial remains but no traces of sulfur or other possible electron sources. However. years for oxygen to build up in the air. Nisbet cial for understanding the origin of photo. These blogs.” he says. Try to picture the world without photosynthesis. One synthesis. Over time. Their photosynthetic proteins huddle in relatively simple “reaction centers” that may have been the predecessors of the two photosystems. making way for complex multicellular life. Eons of evolution have blurred the molecular vestiges of the early events that remain in living organisms. creating an ancient cell with both.8 billion topes that occur if the air lacks oxygen. Rutgers University when they analyzed organic matter in rocks from three sites Something in the air about 2. energy source. And in western Australia. and colleagues found additional support for an early origin when they went searching for traces of RuBisCO. says making and depend on to grow and multiply. Chlorophyll pigment and about 100 other proteins team up to put light to work. and These imbalances persisted until the GOE. 2. one well worth the travails. Louis.7 billion years old. however: Without this watershed in the fossil record known as the more and more hints that oxygenic photo. too. –MITCH LESLIE great oxidation event (GOE).” says biochemist Carl Bauer of Indiana University. “if we def ine the intermediate stages. They’ve turned up in rocks that are up to 2. probably shortly detects skewed abundances of sulfur iso. top. and it changed the his colleagues found disproportionately low carbon-13 values planetary environment forever. Similarities between proteins in photosynthetic and nonphotosynthetic bacteria suggest that early microbes co-opted some photosynthesis genes from other metabolic pathways. Plants. thick shale deposits that are 3. Other researchers are locked in debates over just when this transition happened. using hydrogen sul. or oxygenic. But the question that’s drawn the These signs include red beds.ORIGINS On the Origin of of Photosynthesis piece together how and when organisms first began to harness light’s energy. But researchers say they are making progress.9 billion years old. Nisbet and bial metabolism. directly or indirectly. researchers have ironed out most of the molecular details of how organisms turn carbon dioxide and water into food. would be everything that depends on photosynthetic organisms. genertrons.” indicative of RuBisCO activity —Paul Falkowski. don’t generate oxygen. they found. but the reaction centers in on evolution online at fide or other alternatives. photosynthesis ranks high on the top-10 list of evolutionary milestones. too. In 2007. naturally occurring oxidant— “Water is everywhere. 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. Oxygen-producing. 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. One line of evidence is oil biomarkers that researchers think are the remains of cyanobacteria. support that the GOE marks an atmospheric example. the bacterial version of chlorophyll that’s at the core of the reaction center. Although most modern photosynthesizers make oxygen from water. when organisms shifted to oxygenic photo. they hope to engineer a reaction center that can oxidize less possessive molecules. The geological record for that time is skimpy and tricky to interpret. photosynthetic cyanobacteria living in pools like this one in Yellowstone National Park were changing the composition of the atmosphere. Tempe. Gone.org SCIENCE VOL 323 6 MARCH 2009 8 1286 CREDIT: NEALE CLARK/GETTY IMAGES CREDIT: K. but also the humble algae and the light-capturing bacteria that nourish many of the world’s ecosystems. Biochemist Robert Blankenship of Washington University in St. which play host to algal partners.the first unmistakable signs of significant. and colleagues are working out how a bacterial reaction center could have evolved photosystem II’s appetite for electrons. Oxygenic photocules then power the synthesis synthesis was a huge upgrade. Envisioning the steps that led to this complex biochemistry is mind-boggling. the added manganese also underwent oxidation. Yet modern nonoxygenic bacteria have the presumptive predecessor either of photosystem I or of photosystem II. i. photosynthesis “was the last of the great inventions of microbial metabolism. 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. perhaps hydrogen sulfide.4 billion years ago. Obviously. arguing that one photosystem evolved from the other. from younger rocks. that would have been present on the early Earth. including some involved in synthesizing the bacterial version of chlorophyll. First they targeted bacteriochlorophyll.” says Blankenship. Blankenship says. For example. University of London. researchers are now trying to To catch a photon Over more than 200 years. Adding hydrogen bonds hiked the molecule’s greed for electrons. These hints could push the origin back 600 million years or more. the researchers reported in 2005. They were unstoppable. Photosynthesis makes Earth congenial for life in other ways.This essay is the third photosystem II can wrench them monthly series. suggesting that the microbes were using water to make energy. Earth would look a lot like Mars. The water-cleaving portion of photosystem II sports four manganese atoms that become oxidized. For wrangling—is when photosynthesis began.e.sustained levels of atmospheric oxygen. In this modif ied version. explain why it took hundreds of millions of the sun is the only ubiquitous and reliable when they vanished. Looking so far into the past is difficult. Missouri. 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. concludes that oxygen-making photosynthesis. or layers synthesis began at least 2.9 billion years ago. or lose electrons. some bacteria trons. “Life needs an energy source. we’ve accomplished a lot. and it changed the planetary environment forever.org/ nonoxygenic photosynthesizers milestones. such as hydrogen peroxide. nonconformists.innovation. would lose their main food source. including us.sciencemag. Even corals. New Jersey. importance in of the sugars that organisms leading to a land of plenty. So the team equipped the bacterial reaction center with one atom of the metal.in aevolutionary away. Seattle. SUTLIFF/SCIENCE 6 MARCH 2009 VOL 323 SCIENCE www.sciencemag. But eventually.10 list of don’t rely on water as an elec. never both.4 billion years ago or much earlier. the earliest solar-powered bacteria relied on different ingredients. and colleagues say they’ve uncovered traces of these lateral gene transfers by comparing complete bacterial genomes.7 billion and 2. Further The early-origin case isn’t ironclad. eventually leading to the green. Taking a hands-on approach. James Allen says that their creations aren’t powerful enough to split water. In rocks from synthesis goes deeper into the fossil record. But protophotosynthesizers might also have helped each other piece these pathways together by swapping genes. some biochemists are recapitulating the chemical steps that led to this increased complexity. most attention—and provoked the most tinged by oxidized iron. Geologist Euan Nisbet of Royal Holloway.sciencemag. the photosynthetic machinery became more sophisticated. No one knows for sure. 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. biochemist John Allen of Queen keeping earth Photosystem II—the strongest Mary. Blankenship favors “a large-scale lateral [gene] transfer” or even a fusion of organisms carrying each photosystem. geologists see in Zimbabwe and Canada that are between How the photosystems got their start is cru. By delving into ancient rocks and poring over DNA sequences. for sustenance—from leaf-munching beetles to meat-eating lions. 2. you’d have to strip away the greenery—not just the redwoods and sunflowers.” www.” ating oxygen as a waste product. University of London. Gene-sharing might also explain the puzzling distribution of the photosystems. In the lab. Given its importance in making and keeping Earth lush. so the lush. Advocates also have to years ago. some protists. These molephotosystems.markers are contaminants that seeped in after life originated more than 3. well-oxygenated world that surrounds us today. “We are finding thing is for certain. Catching rays. photoregains its lost electrons by organisms never ran out of elecsynthesis ranks swiping them from water. Allen (no relation to John Allen) and JoAnn Williams of Arizona State University. 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. photosystem I and photosystem II. Long before plants got in on the act. their 2002 study of more than 60 photosynthetic and nonphotosynthetic bacteria (Science. 1616) suggested that bugs had passed around several photosynthesis genes. Early photosynthesizers pumped up atmospheric oxygen concentrations. cannot. Even if the researchers never replicate photosystem II. But water clings to its elechigh on the However.. With its oxidizing power. Bloomington.

GEORGE RICHMOND/BRIDGEMAN ART LIBRARY.” writes William Friedman in the January American Journal of Botany.000 species of angiosperms alive today shape most terrestrial landscapes and much of human life and culture. with several reports prewhich make these mysteries less abom. researchers anthophytes. IN 1879. Within months. with several groups well-established. prairies to oakhickory forests. Yale University. whereas in others the petal count varies. Before angiosperms came along. with their stout trunks and large fronds. another modern feature.2 millimeters in diameter. vary in number. so too do the numbers of with no obvious series of intermediates. this 3D assume that the ancesdecade. all of came to the rescue. Given that placement. It’s one of “the most similar living were like and the relationships among them. no podcast. the carpel and stamens obotanists primarily found leaves or pollen are surrounded by petals and an outer row of but almost no fossil flowers. see the tral type. and the cycads. In multiple gene-based finds and new ways to study them—with assessments. where. as well as morphology. putting this f irst flower squarely with other early fossil flower parts.and pollen-bearing flowers. With this technique.senting a fairly consistent picture of the inable. ROYAL BOTANIC GARDENS. 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. SCIENCE VOL 324 3 APRIL 2009 3 APRIL 2009 VOL 324 SCIENCE www. he considered them. CORNELL UNIVERSITY “We are realizing that this huge diversity is probably the result of one innovation piled on top of another innovation. of which —Peter Crane. Darwin was perplexed by the diversity of flowering plants. Modern gymnosperms include conifers. listen to a appear that we can locate a close Most genetic analyses showed relative of the flowering plants. with its 6-millimeter researchers sort out which angiosperms greenish-yellow flowers. are sealed by a flower origins. exists. When Kevin Nixon and colleagues at Cornell University compared its traits with those same traits in 173 living plants.” says Friis. 130 years later. “We can get fantastic reso. Davis. which bear flower origins. 7 December In the mid-1980s. says But one of Darwin’s mysteries remains: the James Doyle of the University of Californature and identity of the angiosperm ances. although this conclusion is contested. 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. Sun and David Dilcher of the Florida Museum of Natural History (FLMNH) in Gainesville had described an entire plant.” she recalls. “though each of these www. which also has a Pennisi at of seed plants. rather the comparable flower parts. PHOTO BY JENNIFER SVITKO. prolution. blogs. the flower parts are whorled like those of modern flowers. Researchers still don’t know and pollen-generating stamens on male which seed. entombed on a slab of rock unearthed in Liaoning in northeastern China. angiosperms have primitive look about it. says Else Marie Friis of as well as endosperm. That’s in contrast to the Origins blog at org/ nonflowering gymnosperms. the 300. And researchers from var. “When we started. 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. by 100 million years ago. they appear with a bang. Today. Switzerland. LONDON (SUPERSTOCK) CREDITS (TOP TO BOTTOM): REPRODUCED WITH THE KIND DIRECTOR AND THE BOARD OF TRUSTEES. Archaefructus wasn’t much to look at. alpine meadows to formal gardens. Also common in the Jurassic were These fossils often spark debate because seed ferns.” Dilcher notes. a group now long gone. a few representatives. By 2002. typically multimedia/podcast. from roots to flowers. and their biomass provides clothing. Chinese geologist Ge Sun of Jilin University in Changchun. CHARLES DARWIN PENNED A LETTER to British botanist Joseph Dalton Hooker. For more on multimedia/ such as conifers.org 11 29 . a magnolia [flower]. Although they have yet as comprising a single to find the oldest fossil angiosperm entity called Larger than life. An to a podcast by author dates back 135 million years. Darwin pestered botanists for their thoughts on the matter. she and others discovered tiny ancient flowers by sieving through sand and clay sediments. came across what seemed to be a much older flower. placed the fossil in with water lilies rather than at the base of the angiosperms. It lacked petals and sepals.nia. was an aquatic plant that looked to be 144 million years old. lives deep in the arose early and which arose late. In some.NEWSFOCUS ORIGINS embryo that serves as its food supply. 31). Also. Throughout much of the 20th century. On the Origin of of Flowering Plants CREDIT: REPRODUCED WITH THE KIND PERMISSION OF THEPERMISSION OF THE DIRECTOR AND THE BOARD OF TRUSTEES. allowing the fossil to camps. whose heyday was 200 million years ago. listen Although some fossil pollen naked seeds on scales. encased in a protective tissue in a monthly series. genomic data. In most flowers. but it did have an enclosed carpel.” from one of the nonflowering seed plants or gymnosperms. and carpels. we cannot and female organs together say what is the basic in what could be conform. Some flower fossils have prescribed numbers of petals. They had the leaflike sepals. their fruits. In one sense.” Throughout his life. the anthophyte hypothesis. Archaefructus came out as a sister to living angiosperms and closer to the common ancestor than even Amborella. UC SANTA CRUZ.sciencemag.sciencemag.sciencemag. “It’s a flowering plant before there were flowers. the search profile was bigger.” But posed a solution. and many woody plants called Gnetales. however. and DARWIN 28 10 CREDITS (TOP TO BOTTOM): COURTESY OF STEPHEN MCCABE. The father of evolution couldn’t quite fathom it. Amborella sits of ancient plants. flower[s]” to the world’s first flower. building materials. which is devoted to this “abominable mystery. Archaefructus’s distinction was shortlived.” that water lilies were the next podcast by branch up the angiosperm tree. In 1998.org/ Fossil records origins. roots. COURTESY OF WILLIAM L. Darwin had an “abhorrence that evolution could be both rapid and potentially even saltational. for example—pro. now at 2007. including the University of Chicago joint firs. this fast-evolving group. 1546). “From Gnetales organize their male these fossils. Tiny Amborella sits at the bottom of the angiosperm family tree. “It’s really exciting. considered by some researchers as the more primitive arrangement. KEW. from many angles (Science. apparently happened in a blink of geological time. p. The petals and sepals of its sintor itself. In Darwin’s day. some preserved in three dimensions. a 2009 phylogenetic analysis of 67 taxa by Doyle and Peter Endress of the University of Zurich. KEW Out of the past. their specimens tend to be imperfectly preserved most famous member is Caytonia. called a carpel (picture a bean topics online. The organs are spirally organs eventually evolved into THE YEAR OF arranged. Peter Crane. tissue surrounding the the Swedish Museum of Natural History in Stockholm. which took place about 100 million years ago. An for assessing the relationships between obscure shrub found only in New Caledonia organisms have greatly improved. as seed-producing carpels on female flowers Darwin noted. they have now collected hundreds of millimeter-size flowers. just a few tens of millions of years. But 30 years ago. depending on how the evolutionary remain intact while Friis peers inside it trees were constructed. This fossil diversity shows that angiosperms were thriving. but they couldn’t give him much help. And yet this takeover. as well as when. now help Amborella trichopoda. p.at Elizabeth Pennisi angiosperm’s carpel sits at the www.” she says. author Elizabeth Seeking the first flower followed by a group represented One of two major living groups by star anise. they were too numerous and too varied. and insights that In the late 1990s. and gene emerged as a crucial window to the past. so far. survive today (see family tree. than being closed by fused tisFor more on “We’re a bit mystif ied. Before flowers along with angiosperms. magnolia relatives with relatively large flowers were leading candidates for the most primihow flowers got started—and from which tive living flowers. says “covered” seeds that develop This essay is the fourth Doyle. and fuel. To help seems to have precarpel-like structures. ROYAL BOTANIC GARDENS.the University of Chicago in Illinois. Over the past 40 years. palemens. including an analysis in 2007 synchrotron radiation.” pod). strued as a preflower. “It doesn’t secretion. most family trees fossil flower shows that grasses date tral angiosperm evolved based on morphology supback to 94 million years ago. fossils.org www.org/ credible earlier fossil evidence center of the flower. Their blooms color and scent our world.at the base of the angiosperm family tree. which and leave room for interpretation. and for surrounded by pollen-laden stamany decades afterward. has deviations from the ancesFor more on evolutionary sciencemag. from Portugal and other locations with Cretaceous deposits 70 million to 120 million years old. CREPET. When flowering plants show up in gle-sex flowers are indistinguishable and the fossil record. about 125 million years old. better dating of the sediments in which it was found yielded younger dates. China.of 81 genes from chloroplast genomes vide a clearer view of the detailed anatomy belonging to 64 species. in others they are spiraled. techniques lower branches of the angiosperm tree. and there were too few fossils to sort out which were more primitive. tools. ious fields are figuring out genomic changes the sister group of all the rest of the that might explain the amazing success of angiosperms. such as the extinct Bennettitales. researchers have analytical researchers looked to small herbs instead.flower evolution and their relationships to tron radiation to generate a 3D image of angiosperms have ping-ponged between their inner structures. and seeds feed us. The fossil. although a few ancestor. Seeds have a double coating wrong search image. called Archaefructus. For the next 2.sciencemag. sequences. New fossil cloud forests there. Now. Friis and her colleagues have These g roups’ perceived relevance to begun to examine flowers using synchro. remedy that. ginkgoes. evolutionary biologists are still pestering botanists for clues about what has made this plant group so successful. Although merely flowers. molecular systematics Darwin could never have imagined. these plants were much more diverse and included cycadlike species.” says sue as in roses and almost all botanist Michael Donoghue of familiar flowers.

Cornell’s Karl Niklas compiled a database showing the first and last occurrences of fossil plants. “We are beans. “We’re there are fundamental aspects that are con. walnuts. animals that ate fruit and SEED PLANT Paleozoic seed ferns dispersed seeds likely helped evolvPHYLOGENY ing species expand quickly into new Asterids » territory.served in the earliest lineages. participated in the Floral Genome Project. Darwin marveled at the diversity of angiosperms. Later. new chemical attractants. Darwin marveled at the diversity of angiosperms. But in the January American Journal of Botany. as is the cause. … The mystery working to fully sequence the genome of spill over in avocado to the sepals. The exact timing of the angiosperms’ explosion and expansion is under debate. Now as a follow-up. they reported in the January 2009 American Journal of Botany. and other distinctive angiosperm traits. Magnolias » “My own view is that in the past. He and his colleagues argue.COM. but fitting in extinct species is still a challenge. though Living gymnosperms 12 30 CREDITS (TOP TO BOTTOM): PHOTOS.” Archaefructus » The latest insights into diversification come from gene studies. tulips. or whorls. saying that what Crane calls the outer layer is the only layer.walnuts. This Monocots flexibility enabled angiosperms to exploit new niches and set them up for long-term evolutionary success. “I believe a solution to tionary history. it’s no Clockwise from left: aspens. The angiosperms group together. as analyses of various kinds of cots. and finally sepals. Crepet thought Others have noted that a duplication branches of the angiosperm tree.ORIGINS ORIGINS such a causal relationship is not settled. almost nine in 10 land plants are angiosperms. grasses. At least one estimate based on the rate at which gene sequences change—that is. occurred in the evolution of grasses. say. Each tissue has its own data become more sophisticated. fuel. who is are active only in.” that he would like “to see this whole probopment. but Crepet is optiFloral Genome Project confirms that yet concentric circles. Moreover. the ticking of the molecular clock— pushes angiosperm evolution back to 215 million years ago.” says Crane. “We do not really know how to compare them because the structures are very differentlooking. there was something special about the angiosperm radiation. ELSE MARIE FRIIS CREDITS (TOP TO BOTTOM): PHOTOS. thus. in Amborella.” –ELIZABETH PENNISI Amborella with his colleagues. and there’s nothing in between.” says Crane. and the angiosperms. grasses. Some think the answer lies Eudicots in genes: duplications that gave the angiosperm genome opportunities to Rosids try out new floral shapes. gene studies have helped clarify the relationships of many simultaneous duplications—but not living angiosperms. He and others think that flowering plants lingered in obscurity for tens of millions of years before radiating toward their current diversity. And if the molecular work is correct. “The nonangiosperm ancestor just isn’t there. surprise that they serve as fuel. To make matters worse for anthophyte proponents. “There are distinct pattern of gene expression. Whatever the timing. the paleobotanical work points you in another direction. “We found that many small changes in expression patterns off but before water lilies evolved.” A decade ago.org SCIENCE VOL 324 3 APRIL 2009 13 31 .and functions that helped yield the great beginning to get the idea that polyploidiza. the seed’s double coat. tion may have been a driving force in creat. ported this idea. Given that they represent nine in 10and sense of beauty.“But there are differences in how the genes In his letter to Hooker. a species on the lower lem solved. for example. (ALL OTHER IMAGES) PHOTOS. ELSE MARIE FRIIS CREDITS: (ARCHAEFRUCTUS IMAGE) DAVID DILCHER. diversity in floral forms. how did they diversify and spread so quickly? Darwin suspected that coevolution with insect pollinators helped drive diversification.carpels.” he says. angiosperms edged them Inside and out. which may be a link to angiosperms. that the seeds in the Bennettitales have two coverings. they found that new angiosperms appeared in bursts through time. “we are realizing that Water lilies this huge diversity is probably the result of one innovation piled on top ? of another innovation. Caytonia University Park. roses.” says Soltis. Gar Rothwell of Ohio University. angiosperms proved less likely to disappear. that it transformed without intermediates. could be misleading. the flower parts are arranged in That hasn’t happened. Darwin wrote ing many new genes that drive floral devel. the more primitive plants.org www. Synchrotron radiation helped produce a 3D rendering (gold) of this fossil male flower (right) and insights into its internal structure. tomatoes. somehow resisting extinction. figuring out what’s homologous is quite a difficult thing.” says paleobotanist William Crepet of Cornell. Genes that in Arabidopsis 10 years. In most Darwin would have gotten his wish by now. because in most analyses the genetic data don’t place any living plant close to angiosperms. a gymnosperm. but what is very clear—and was quite annoying to Darwin—is that the angiosperm prototype so readily proved a winner. Pamela Soltis of the FLMNH and Claude dePamphilis ? of Pennsylvania State University. Once the angiosperms arrived.in the avocado. including water lilies and magnolias.of beauty. and so forth. Given mainstays of both our welfare land plants. around the mistic that he and his colleagues are on the another duplication paved the way for eudi.COM. we have looked for one feature. says Crepet. and sunflowers. whereas other plants.” Seeds of success The angiosperm’s ancestor may be missing. apples. radiated rapidly only at first. such as gymnosperms. sunflowers. Now. 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. and f ind fault with the hypothesis in general.” says Donoghue. who also notes that molecular dating methods “are still in their infancy” and. mainstays of both our welfareland plants. and some nodes are hotly debated.” dePamphilis says. Seed ferns and other gymnosperms arose about 370 million years ago and dominated the planet for 250 million years. “I’m starting to worry that we will never know. that they represent nine in 10 and sense it’s no surprise that from top as orchids. Crane and others carefully dissected and described fossils of these groups. Thus in is solvable.sciencemag. sunflowers. 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. The Floral Genome Project also looked are not as well-defined as they are in Araconfirming earlier reports. From Amborella 2001 to 2006. with stamens innermost. In most early angiosperms. the living gymnosperms group together. genebased evolutionary trees break up this grouping.COM 3 APRIL 2009 VOL 324 SCIENCE www. they saw many Shifting branches. looking for the precursors to carpels. When he and Crepet used that and more recent information to look at species’ appearances and disappearances. food. DePamphilis and his colleagues Ginkgoes » matched all the genes in each species against one another to deter? Gnetales mine the number of duplicates. the Ancestral Angiosperm Genome Project looks at gene activity in five early angioCycads sperms and a cycad. then petals. Clockwisethey serve left: aspens. tulips. petals and sepals Angiosperms Flowers. Then in a few tens of millions of years. the developing petals the problem is within reach. As this simplified family tree shows. out. The data suggest to see whether the genetic programs guiding bidopsis. Athens.” says dePamphilis. then the field doesn’t know in which direction to turn. which ? Bennettitales searched for genes in 15 angiosperms.sciencemag. right track.” Crane says.are deployed. pulling the Gnetales off any angiosperm branch and placing them among or next to the other gymnosperms. apples. Today. “The molecular work points in one direction. But they have run into problems. and two colleagues disagree. “There appears to be a gap in the fossil record. Take the avocado. but not less likely to go around in circles in the next some real ‘hot spots’ in angiosperm evolu. During the 1980s and again in 1997. orchids. the group that includes apples.

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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. Huxley. 1. Alexander von In the early 19th century. Humboldt’s obsession with geographi. and often culsyn. J. and other of the and Program USA. and central Mexico.M. Cuba. light refraction and intensity.ponent entities. agriculture. F. and geographic location of their thousands of Andes. countless ext 22 years and (see the figure). geological. figure—Alextions was central to on mountain snowline. atmosphere. this theory provided a unified explanatory framework for disparate geophysical. 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Earth system sciences. 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. and recorded the Countries. 3). p. Hist. von Humboldt. and biological features. and noting that plant form is often These surveys were relentlessly inductive. and Darwin. Hart Merriam. typically producing detailed descriptive reports with little integration within or among the component entities. Alexander von In the early 19th century. animal habitat. Jackson Stephen T. typwas a slim workhisand cultural phenomena acrosstemperature on plantlocal environment is often of measurements.distribution of incident radiation. He expanded this vision in the succeeding years.serving asisotherms and recorded the geographic and often culMore pertinent to our mapping of physical. and ethnological specnt 5 years (1799 extensive atmospheric and geoimens. He recognized Darwin). and recorded the Countries.ideas continue to shape and enrich Darwin’s Darwin’s ideas continue to shape and enrich the sciences (1). Nicolson. inventing both an mapping of physical. Earth system sciences.er-finished reportHowever. and recorded the Countries. plantNeighboring explorphysical measurements. and in his intuition that ally nimble participants—including Charles that von in his and thinking. 1996). References and Notes CREDIT: REPRODUCED FROM AN ORIGINAL COPY IN THE NATURAL HISTORY MUSEUM.distribution of incident radiation. Dettelbach. geological. and cultural phenomena across the patterns. and profile. Plants effect of latitude and continen. de Humboldt. Humboldt’s general physics of the Earth envisioned climate as a major control of Earth-surface phenomena. light refraction and intensity. A atmospheric. d recordedOf these volumes. Goetzmann. and tral Mexico. The Norton History of the Environmental Sciences (Norton. the profile is flankedHumboldt’s dream of systematic observaHumboldt’s dream of systematic observair thousands ofEssay the original. vol. published as part of (2. and biosphere as well as human societies and economies.org taxonomic affinity (a MAY 2009 resolved by with little integration within or among the com- 15 . 223 (2009). countless richness accompanying He expanded this vision in the succeeding 19th century. for a few intellectually nimble participants—including Charles Darwin.less than a synthesis of and ethnological specimens. 10. In the original. In the text and the intellectual in temperature. geological. Chicago. H.measurement stations. depend in the face of global climate change.S. on both sides bytheIn thechemical. C. shows Chimborazo inPhysicalwith vegetation zones. for a few intellectuLike Darwin.other graphical devices to portray spatial tural features of landscapes and oceans (8–10). animal habitat. rents. H. and other graphical devices to portray of microclimate. The central portion ofportion ofmaterials in windsthe Andes andcur-of the Andes and microclimate.Charles Darwin’s thesis of atmospheric.” using the early-19th century definition of physics as the study of the material world and its phenomena (which we now call science). The modest title belies the intellectual richturn inhabitants form an integrated whole.edu Earth-surface phenomena. the influence of temperature on plant and cultural practices (6–8).M. They collected botanical. and inhabitants form an integrated whole. the face of global climate change. Cannon. and noting that plant form is often better predicted by local environment than by taxonomic affinity (a paradox resolved by Darwin).edu Earth-surface phenomena.better predicted which environment than by icallyand most of his inherited fortune in than by ically producing detailed producing reports globe. W. humidity. Throughout richness within. in Cultures of Natural History. Hart Merriam. 6 May 2009 marks the 150th the sciences the sciences (1). the influence of species. Today. a second. with Maps.Intellectual riches. the of Species. A new incarnation of Humboldt’s general physics of the Earth began to emerge with the plate tectonics revolution in the 1960s. time.Laramie. The central portion of Humboldt’s Physical Tableau of the Andes and Neighboring Intellectual riches. the United States.M. New Men: America and the Second Great Age of Discovery (Viking. and his intellectual intellectual world Darwin inhabited.yearslittle integration within or among the comHumboldt’s by with little integration withinor among the comsystematic observa. New Lands. animal habitat. Like Darwin. This effort is often referred to as Earth system science. Paris. Cuba. the northern Andes. Jardine. ecology. They collected botanical. and erife. Throughout the century. and cultural practices (6–8). these explorations provided data and experilinkages among the various components (4. that spatial arrays of observations could be graphical vision. Eds. Throughout the century. On cultural phenomena across the patterns. features. processes—such as in inhabitants surface. London. and cultural phenomena across the globe. thea few intellectutional arrays across ponent entities.S. More pertinent to our time.imal control of Neighboring animal habitat.distribution of less than a birth embark on H.Intellectual riches. T. Beagle.measurement stations. The central portion of Humboldt’s Physical Tableau of the Andes and Neighboring imens. Humboldt lays out years. S. C. (Longman. geological. and the United States. most of his inherited fortune in Paris. inventing isotherms mapping of physical.measurement stations. oceanography. Humboldt spent 5 years (1799 system and thinking. Huxley. geological. biological.taxonomic affinity (a climate resolved (1). ected botanical. New York. with linkages among the various components (4. the transport serving as both an index of climate and a proxparing and paring and publishing 45 volumes of a never. E-mail: jackson@ envisioned climate as a major control of sion of ecology. intensity. with vegetation zones. and other environmental sciences (11). the transport umes of a never. 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. More pertinent to our time.describing elevational patterns in temperature. and central Mexico. appropriate first was slim work Of these volumes. made imens. Jackson Stephen T. A. in Romanticism and the Sciences. Jackson In the early 19th century. the influence of temperature on plant form. H. oceanography. Beagle. 3). the influence of temperature on plant andzones. They collected botanical. A. and other physical. fauna. USA. 1814 to 1829). P. a vision s scientists are celebrating the 200th inhabited. geological. humidity. Humboldt’s Cuba. Jardine. establishing international cooperative Humboldt-inspired explorations were launched. humidity. C. humidity. Humboldt’s genius lay in his geo. Alexander von Humboldt laid the foundations for today’s Earth system sciences. et al. 11. geological. hydrosphere. cryosphere. Orme. with vegetation serving as both an index of climate and a proximal control of microclimate. (2. 4. Humboldt-inspired Darwin. and often cultural features of landscapes and oceans (8–10). Humboldt helped create the intellectual world Darwin inhabited. for a few intellectus the intellectualof another 19th-centuryHe recognized Darwin).better predicted by raphy ofideas continueform. and noting that plant form system ecological.org 1 MAY 2009 VOL 324 SCIENCE www. the of (2. and other enviand oceans (8–10). tional arrays across the globe took hold in the nds of measure-within.

or of intellectual chugging along? Our concept of it should be capacious enough to include both. any more than any other post-Darwinian additions or adjustments were. 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. the prominent paleontologist H. who were not brought up on British 19th-century idealistic morphologists such natural-theological assumptions about a peras Carl F. crisp prose is the more rigorous requirements of a German key to the success of this analysis. is one of scientists building and innovating incrementally. as he deftly academic scientist’s understanding of a “law” leads his reader through dense philosophical of organic nature. influential historians such as E. and the relations of all of these to the broader social. Meckel that sonified God who had created a perfectly retained their teleology. is an arguthe two. Russell and Stephen Jay Gould. 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). and religious concerns scientists shared with their contemporaries? These questions become especially pointed when one considers German Darwinism. The Tragic Sense of Life and H. Richards weaves a compelling one personality—to shape the course of scistory of a life marked by tragedy and of an ence.lent for the term. 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. best understood as an update on early. finally. Cambridge. 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. 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. crudely put. the critical issue was to understand nature’s manifold variety while seeking out underlying strict natural laws to account for it. the importance ISBN 9780262072939. Haeckel’s Darwinism thus shows continuity with early19th-century concerns. though it emphasis on form. which he giously conservative scientists and with for. have been so fiery. In Haeckel’s charisma and his combativeness. But those concerns were always more flexible than has been acknowledged. Richards does not negGerman Darwinism has written a biography of Haeclect Haeckel’s science proA Study in Translation kel. he suggests.ing German terms in a newer. This story. Intriguingly and plausibly. These were not isoPress. 2. and debated the pro-evolution (but anti-Haeckel) Jesuit priest and entomologist Erich Wasby Robert J. Gliboff asserts. Over sonal responsibility for fascism and Nazism. One cannot leave this book until his sixties. mediated through Bronn. Gliboff ’s key insight here is that Haeckel originally read Bronn’s translation of Darwin. he notes.altered key ideas to make Darwin comprehentionism. and both have proThe reviewer is at the Department of the History of Science. is that Haeckel’s sition. Is scientific progress a matter of personal anguish and triumph. larger-than-life figure whose passions lutionism was profoundly shaped by both drove his scientific research and philosophy. is the more entertaining read of The big picture here. Most often remembered by biologists as the author of the biogenetic law (“ontogeny recapitulates phylogeny”).) Like Bronn himself. especially in treatThe Tragic Sense of Life Ernst Haeckel and the Struggle over Evolutionary Thought VOL 323 SCIENCE www. 1905) n this year of Darwin anniversaries (the 200th year of his birth and the 150th anniversary of On the Origin of Species). £22. then. Both for these early-19thcentury naturalists and for their intellectual heirs. which was accompanied H. How. places Haeckel at the atic and phylogenetic work MIT Press. By challenging the very foundations of the standard narrative of German morphology. Sander Gliboff. Haeckel has also been accused of promoting European fascism via his monistic philosophy and of presenting a eugenic. The ascription of simple linear a critical yet generous equal. Robert lated episodes but rather 579 pp. G. rather than an individual. Darwin did not launch his theory onto an unprepared public and scientific community. as Gliboff’s. not the popular ideologue. and for an academic audience lenge to our standard picture of 19th-century lacking the gentlemanly traditions of breeding German biology. Darwin’s words were translated.” Can one scientist be responsible for so much? Most historians would say no.uses both synchronically. we come to Haeckel. in the phylogenetic trees of the context of German biology. S. Generelle Morphologie der Organismen (Georg Reimer. the Origins of and German Romantic biology. Nyhart CREDIT: ERNST HAECKEL/FROM WANDERBILDER (W. Richards.org Making German Evolution: Translation and Tragedy Lynn K. Generelle Morphologie temperament led him to the occasional intem(1). who saw himself recapitulationism to the views of Romantic as moving science forward through the modiembryologists. 1866). E.Germans. Gliboff ’s overall picture of scientific advance. 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. standing of the technical development of Richards’s book. end of a study that examines the on radiolaria and other marine 2008.fications he made to Darwin’s flawed theory. Science and Medicine and a by a bitter hostility to orgaErnst Haeckel. 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. and especially Germany’s best-known follower of Darwin. Haeckel could not turn down a Darwin’s theory was translated into this envifight: He battled the physician-statesman ronment. HISTORY OF SCIENCE BOOKS ETAL. emphasizing the long per. And love for his first wife. and passionate love would elude him extreme thinkers. and (more intriguingly) diachroni. Ernst Haeckel.edu I ing the translation of Origin of Species into translations involved an attempt to recast existGerman. Gliboff argues. J.private lives (although he mentions salient centered faith that became one of the most details). Gliboff shows Haeckel as both echoing and responding to Bronn’s concerns. GERA-UNTERMHAUS. of linguistic analysis to his and his ideas modified. 2008. but they do so in dramati. Richards’s rendering. much of which centered on his philos. rather than either reflecting directly on Darwin’s original writing or reaching directly back to the Romantic embryologists.org SCIENCE VOL 323 And so. In Richards’s presentation. 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. This provides a new starting point for analyzing Darwin’s first translator. and their articulation changed over time. F. that single-cause explanations are insufficient to account for something as broad as fascism. USA. Ernst Haeckel. mer students who challenged his ideas as they gained intellectual independence. the director of the moments in a lifelong camISBN 9780226712147. he does show how the scientist’s ardent foundational work. It represented the to nature.stitute important contributions to our undercally different ways. ture developed by Karl Ernst von Baer in a Bronn’s death in 1862 afforded him little polemical context. University of Wisconsin. he focuses on the working evolutionary theorist. not Darwin in the original. References and Notes 1. from Instead. sparred with reli. $39. Bronn. too. Central to his replace religious education).sciencemag. Bronn—a figure little attended to in the standard story but the lynchpin of Gliboff’s. Haeckel. cultural. Kielmeyer and J. Both illuminate races of humans. tragic figure and for the force of personality in Science remained his salvation and refuge. These contook in Germany. Simultaneously. Haeckel’s oil landscape of highlands in Java. the union was not perate statement that could be taken up by happy. His is not a story of personalities or ophy of evolutionary monism—a science. 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. Anna Sethe. University of Chicago’s Fishpaign to advance his philosobein Center for the History of phy. but it was not an aberration or a distortion of some true theory. duced important books. Bronn’s Wanderbilder (1905). 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. however. then adopted uncritically by chance to steer the conversation further. His professional life was also filled with Gliboff’s account is of a completely differdrama. owes much to a carica. WI 53706–1393. It also represents a profound chal. 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. www. £27. the next year. The reviewer previously served as a press reader for both books at the manuscript stage. when he had a secret affair that without a deep appreciation for Haeckel as a ended tragically with the death of his lover. a professor per. working with what their predecessors have handed them and sculpting it into something new yet understandable to those around them. Bronn.sible to a German academic audience. its relations to earlier ideas about nature. 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. nor was the evolutionism that developed after 1859 a mere extension of his views—it was not even one thing.ent order. Bronn’s translation. was not sistence of a German transcendental approach a conservative throwback. has been deeply entrenched in the dynamic engagement of a leading paleontolohistory of biology. their typological adapted nature. Haeckel made further amendments both terminological and intellectual. had Haeckel His love of nature was surpassed only by his not continually fanned its flames. this careful. 10. natural selection. the directions that evolutionary investigation subsequently took.1126/science. arguing that it takes a community. and their linear recapitula. though over twice as long evolutionary biology. 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. and much-published author on Darwin nized religion. who died in although Richards absolves Haeckel of perabdominal agony on his 30th birthday. to make a movement. producing his place. E-mail: lknyhart@wisc. 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. Madison. biologically determinist vision of humanity that led to Hitler’s “final solution. It was science moving on. $35. This is some of the best close reading tion into a language without an exact equivaI have seen. and the Origins of German Darwinism remind us that the history of evolutionary thought in the 19th century extended well beyond Darwin himself. shaping the direction science may take.account is the idea of translation. Although he remarried. The selection metaphor was further version of evolution was a Darwinism in name fraught with an anthropomorphism foreign to only. Of course Haeckel’s Darwinism was not Darwin’s own.sciencemag. more up-to-date cally. The historians under consideration here have chosen two radically different strategies to understanding Haeckel’s place within German evolutionism. in contrast to Richards’s emphasis on charisma and passion. Berlin. In his characteristically rich and ment about the power of personality—at least rolling prose. he wrote his way through the in part by situating him firmly in his time and despair that enveloped him. (Although Gliboff acknowledges the centrality of monism to Haeckel’s thought. G. Gliboff’s own clear. KOEHLER. MA. at the top of his list.BOOKS ET AL. G. Richards mann—the list could go on University of Chicago and on. German evointense. 271 pp. But the two books offer very different reads. and his remarkable experithe twists and turns that evolutionary thought mental work with siphonophores.95.1169621 1170 16 27 FEBRUARY 2009 27 FEBRUARY 2009 1171 17 . A painter. Bronn and terminological thickets with nary a thorn sought to translate Darwin’s ideas about selecscratch. Chicago. pigeons and dogs so central to Darwin’s expoThe old story. larger process through which organisms.

1). and the The Galapagos it did not produce an orderly pattern of relations ment in its own (1831–36). 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. left adaptive evolution essentially open. but think it ever-changing natural selection did so agent of plain the life evolution by in theory. species. by his contemporaries. withLife branches splitting over and led to construct his model of openseems so obvious today that it is hard for us to his thinking.on the hazards of migration. Most thinkers— in athe Wallace (Fig. now seems a common ancestry. 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. but that the original and disturbing.causeto see natural selection asprofoundly differ. Unlikeevolu.independently from any history other efforts being had a unique cosmicof transmutation. result of more or less in are claspoints together Russelat right natural1) indepen. 1. teleology.difficult toproposals (13). Several isolation.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. 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. 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. Darwin’s mentor in geology. left adaptive evoin seeing that biogeography must become challenged the beliefof original and disturbing. Darwin’s was undermined to vision contributions todid not produce an orderly pattern of in 1859.Species and Wallace (Fig.sciencemag. Such a world view species.it hard to see environment.adaptedpeoplebased creation environment. from Darwin’s notebooks again. first proposed in 1859. The to aH. Lamarck’s realized that itin the life on earth. Drinker Cope and Alpheus Hyatt theory. Many of tained five species cosmic teleology. School of BT7 1NN. Charles constructAlfred Russel Wallace. HULTON-DEUTSCH COLLECTION/CORBIS. Darwin’s vision challenged the beliefof naturalscience. but evenanicdid not share Darwin’s followed Lyell ended. explaining present distribushaped gressive evolution was widelyto predict an orderly pattern of branchingLamarckian effect). althoughexplained why naturalists were able to arrange of aptation. 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. BT7 1NN.local (14). 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.ology. variation was certainly caused hisdepicted was of the role played adaptation.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). the Chambers— evidence forthat species (Fig. publishedevolutionhad been widelywere subject in a of scientific interests view alerted divine to cosmic teleology. 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. somehow “in the in at the time. Here. vision during as Herbert Spencer as its tion. Closely related combination forcedinspiration in a that alerted off andthat variations way of This addition to “struggle for scientific scientific interests to cussed. James toto was perhaps the first was the onlyifmechanism the localinitiated a permitted that evolution was that the world was designed supposedeffect). model and the variation shaped the world in designed the organdistributionsand terms of past Archipelago supposedcalled Lamarckian effect). 2) nomic relations might made good alternative of branching based on geographical America and the Malay Archipelago cies to changes in their environment.ain addition ancestry.” Chambers’s of in of theas naturalists dis. Darwin had conceived its basic out. Darwin’s vi.accept theofclaimother on earth. (This assumption somehow “in thetion.from descenttheon ideas widely discussed at He cosmic teleology.223of subvertward an evolutionary Darwin explanation of adaptation. SelectionErnstbenevolent to that the creation and was proposed independently by Wallace in tially irregular and unpredictable.Wallace. 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.during the “eclipsecontroversy. 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. Darwin’s vision challenged the belief Lyell) evolutionary Desmond andPopulahave this too revolution somehow “in thedepicted astime. was worked20 years. isolation.of classification supposed that every genus con. centered model and letters 20 years earlier.his move the Natural History of Creation depicted Wallace formulated their ideas. articulated by thinkers such provided theof evolution that Darwin as Herbert Spencer to any other naturalistgood comparison: Spencer contributions to between science.M.by by the organisms’ own as genetic mutascience. whereas others came to dead end generate generate much controversy. first the Many species sole over and over again. 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. B. Darwin had conceived return from the including Jean-Baptiste Lamarck Lyell) evolutionary adaptations. Darwin approached the Darwin was certainly not the first to sug.plain that it be instituted a on at the Creation of 1844from a a debate over the posmeant local achievements.benevolence parasitic way of life each a perfectly to the influence of highly orig. In others came lating in his his again. even by those who accepted the general idea of evolution. so creation of ofhis contemporaries. explaining present appreciate just open-ended. Bowler Spencer (Fig. in his think. Many of the be traced further back down the wanted to show that changing created the Wallace. through extinction.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.the air”the thegroups. it was widely rejected recognition widely terms of share on a good comparison: He selection.lection was the Darwin was acertainly God. prompted in to anyone embeddedain a vision (modern Indonesia). Darwin’s new in the late 1830s. from a common ancestor pos. Darwin followed Lyell in seeing (for Darwin but not and. of natural not justwas both idea notnatural Darwin’s seeing that bio. Unlike Macleay series of parallel lines moved through the same School of Philosophy and Anthropological School of Philosophy and Anthropological Studies. So it was. Populations natural order.”in implications of the principle of common descent original drew tive Darwin discussed the natural inter.uk from family but was extent. Selection to it of to exthe disturbing tospecies byproposedB. until the took it for granted thator goal-directedness lifeand independentlyfrequent theevolution. It was as evidence for treated as populations sometimes 1858 is taken asof possiblefor this position. each family five genera. By andanticipating9Darwin did 2009 Macleay Chambers. useless a parasitic essentiallyinwas anot seem of 1844 similarities. Chambers’s (Fig. although generally rejected in 1855. posprovides toby other naturalist on the Beagle voyagePeter J. however. ofwaynomic efforts being made to ex. (2–4). in terms of parallel lines advancing through toward a model of branching evolution based on Darwin. the species to This instituted byenvironment.19th-century evolutionists were gest accept variations in a ruthless “struggle for scientific a world cussed. but this too permitted stages within each family. As ments (10). the idea of profor Lyell) evolutionary adaptations. (22). this case present shaped something (later identified activities (the so. Charles multiple Alfred Russel Wallace. been argued that by geographical of of the individual population positive that relations. there would be major implications on the Sharpirregular and unpredictable. although sparked debate within Rob. for in clearly The that the black coherent separately centered on the 20 that earlier. When first proposedthe 1859. possibility that barriers slaveholders argued (1)].distributions).ent because he argued that the an becomecould have been proposed tobarriers. althoughlying sparked a producedRobert speciesthosewas of on theby his scientific interests especially because existence. whereas the ancestry of more distantlyway. Most thinkers— (modern Indonesia). Robert combination sibility that species response inal whereas adaptation. theJANUARYnot expect www. provided by articulated by 1). J. The idea of common descent now seems so Macleay Natural selection replaced divine benev. He workedwas.estimated the rapidity with which other think verged recently of more commonrelated forms must tive model in Darwin was he was more his alterna. Populations thein its of pro. kingdom. isolation. be was extinctions multiple vectors idea (modern selection the Origin of perhaps in first is environment. Natural selection a highly orig.depictedsamebranching tree intheory undermined At the as a time. He made to ex.ology.Vestiges ofinto groups within groups. but even he of branching Darwin’s didhow share occurred including his studies of biogeography andthis score. 2) that the history of life on earth might be essen.existence.ology. self (14).converted to the theory. barriers gained on the (Fig.) for fact branchoutlines treated theory the as created wanted towhite.other natural.sciencemag. evolutionistswas so radical thatargued that Adrian Desmond and James to the local environment was the only mechanism changes in their environment.ent because he argued that the his thinking. Northern use those sources his time. a kind argued it the creation 1844generallyarejectedover thegroups. (later identified as genetic muta. 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. Closely related species have diof evolution. called Lamarckian effect). its basic outline universally accepted at the time. family tree to estedinfluence of William cosmic teleology. light wise and benevolent God. this it during his to Theprocess. Darwin theory of natural selection challenged this vision ferences between of this ing. and he realized become divided by geographical barriers. the migrations of species Herbert Spencer. depicted asby branching treeown activities (the soa the organisms’ in which each act of an evolutionary vision during the years he worked science.over the next paper in 1858 basicflurry of universally predetermined goal. it was widely rejected five genera. The image the first to sug. (Fig. But if new. but if much controversy. Belfast. Both realized that it plan. Wallace One innovation at and and how aimed Here. It was by approaching the share that Darwin on letters to assumption theory of natural selection 20 years earlier. a benevolent response byidea circumstances. branches adapting to Herbert Spencer.S. Darwin unrolling of aan orderly pattern of relations. 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. The who accepted articulated good comparison: He too moved toward ing process individuals. this essay. E-mail: p. MICHAEL NICHOLSON/CORBIS CREDIT: SYNDICS OF CAMBRIDGE UNIVERSITY LIBRARY CREDIT (LEFT TO RIGHT): STAPLETON COLLECTION/CORBIS. Charles changingthat weRussel Wallace.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. The Queen's “ahead ested time.g. 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. adapted specieskilling accept the claim that evolution by governed by a cause of transmutation. orderly system natural sedivine plan. the idea of proin progressive tions hasPopulations divided Darwin’s move called It in terms of past migrations. so ology.of how theH. in I think to overBecause many slaveholders argued Charles Lyell. Darwin may have been be traced Northern obvious that we might wonder More seriously for the idea of cosmic stages. but sources of his interests highly orig. Evolution had to Darwin had conceived its basic idea of by a not accepted at idea of Most thinkers— merely widely Wallace. after his from the vision challenged the of teleology world was designed supposed air” few initiated a revolution Wallace. controversy. He structured This did not seem Selection process gest the ideaVestiges1809. and was proposedprocesses independently by species to models could have been proposed to nature diversity.number of key insights. He had a unique ever-changing This model was by paper published Darwin theory. and itself achievements. 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. 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. BT7 1NN. and it system most innovative gressive evolution wasbarriers will develop independently be crossed widely sibility that and the can recognized. Darwin share Lyell in and.could Herbert Spencer. to the publication ofit in Origin. quarried Darwin’s notebooks a coherentgranted the the a unrolling of of barriers the Charles Lyell. had to be time. This article insights the as Herbert gained (1831–36). of to was ing (Fig. 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. lying similarities. idea and was as been widely to from any the of anyone embeddednatural se. 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”. Darwin’s non-Darwinian was production merely “ahead of his time. thein a Road of more distantly related forms some extent. Chambers’s of species by God. Evolution hadbe major of how as together in the and way [for culture. Closely related time. As a basis for his thinksay. The identifies those depended on aspects of Darwin’s work that led him to develop thisthrough the taxonomic hierarchy.org This model was so radical that many late just in original was scientific developed his theory (6–9). of Charlesnotwork that any him directionones in a progressive sequence lead. of the individual variants in a population was the relations among species.God.org VOL 323 9 JANUARY 2009 9 JANUARY 2009 223 www. This article throws original and process of the disturbing. isolation.from individual development. whatHerbert Spencer. In this this es. (1)].S. and I support this(10). that animal breeders throws was supposedfor have initiatedDarwin’s On for variation not entirely new. plorations in South America and the Malay acceptedaccepted it would emphasize the it (modern Indonesia).evolutionLife. Yet there by up to humans (5).from the model of the branching evolutionarythinkers such the argued that Darwin’s move to a an tree (11). Selection adapted species to an Vestiges of into Natural Lamarck’s especially time. and so thinkersatsuch time.aimUniversity of Belfast.model in part becausebeenwas more adaptiveinstituted inthe because its essen. He worked on it in relative took it for granted thatBecause that the black race was separately theory would allow (1)]. both inthe “in the air”Species in 1859 is waiting ingWallace.and the posmined developmental trend. publication but it was Darwin’s in led one to develop this revolutionary theory. 1) indepen. But truly original and would notbut a aspects ianany other naturalist atof the Darwinian vision obvious goal toward which it theoryaimed. Fig. and evolution made good to their local environment was found related issuewasdefiningby notebooks theory sug. pos. The American neo-Lamarckians Edward thatMore seriously for the some of cosmic telewould be estimated benevolent which Creation of Creationof Belfast. But of H. and(13). circularBy more historical viewpoint of pro1). Unlike century were introduced with the aim of subvertextending throughout Darwin. vision during the years he University Road merely “ahead of his time. but was influence of William Paley’s natural theology. air.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. forms must Belfast. isolation.S.Charles1859 evolution essentially open. By the late 1850s. 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.”late 323 Ireland.isolationvary. out any possibilgressive evolution role widely recognized. published sparked ofwerebeen widelyfrom certainly historyon ideas widely discussedunique thatdependant environment. divided byown way. MICHAEL NICHOLSON/CORBIS CREDIT (LEFT TO RIGHT): STAPLETONSTAPLETON COLLECTION/CORBIS. But Darwin was the relations among made it Several ac. be crossed the development of the branching process of H. sified into groups. adapting speby a on the process both inthe Origin of Species inculture. Darwin Charles the common shown how his uniformitar. and Ibetween this claim by addressing the scientific work and others from currents circulatDarwin’s world separate en. havewas being biogeographical modern science. and the agent ofkilling either first Robert plain the history of life on earth. 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. but it of Darwin’s theoryit islands. his contemporaries.is widely sion of how process worked certainly was. explorations in South that the world was designed supposed shaped by the organisms’ own activities (the was not entirely new.) 1) independentlyevidence[forainstanceof theory of the leading formulated theory (1)].” may interests to Ireland. for a predetermined sequence of stages within each geographical diversity. University of ones ancestrydebate over the posUniversity a Belfast. whyan (2–4).localeven ofat the but even he Wallace modern science. with no fixed limit on the range Peter J. way [for Darwin’s how 1858 is taken asfixed elementsthis aposition. using descent ignored in part because he wasHe existence. driven that the adaptation.possible variation. have vious goal toward which it has aimed. butthe late 19th it would The would allow descent ferences between the ways in by geographical barriers. natural adaptive response in some circumstances.certainly was of ideas widely discussed ert Chambers’s Vestigescommonproduced to explain thethe drew forced by hisirregular had aunpredictable. had been 1855.Few would ulations totransmutation. termined developmental trend. dependant common in full. whereas adaptation.non-Darwinian theories of evolution proposed find Lyell. contained fiverejected that were truly were individualthe time.bowler@qub.divine benev. Darwin was led alerted his alternative were introduced with the aim of subverting the generally rejected (2–4). way. of left adaptive is widely pre-existing ones recognition of sequence lead. this thesis is sure to generthe in adaptation than Paley’s natural the. any Beagle voyage way. 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.ac. by his scientific have devel. Populationsin Wallace’s paper in 1858 precipitated the flurry of aimed at a predetermined1830s. Unlike centurythe idea of cosmic tele. Darwin in a highly existence.M. good comparison: He Darwiniantoward aspects of the species provided vision the It was of possible variation. 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. UK. thinking. an updated To some and Chambers. derived www. the cantogether in the rightsame time.uk proposed to account for SCIENCEtheVOL 1850s. 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. but additionMayr natural selection verged recently from a common species have di. of organisms isolation over the next eventually ing for Alfredright put a[for readily indepen. way. Darwin’sversion of the idea production in Chambers’s Darwin’s Originality Darwin’s Originality Darwin’s Originality REVIEW REVIEW REVIEW Darwin’s Originality T T T T T CREDIT (LEFT TO RIGHT): COLLECTION/CORBIS. claims that Darwinism On Although the he frequentin Western culture. Chambers’s Vestiges of ate much of Darwinism” in if accepted position. The fact that a old idea natural selectionBut Wallace’s 1830s. activity his return the the Origin.tested cieswas role forin Darwin’s On proposed that to changes time. There was no more practical incentive was Charles Darwin’s theory of natural selection was been hailed as one of theof classification supposedwere1). Beagle. UK. a Wallace formulated their ideas. Few would now theory ofto their local environment was the sole that what was once a single species could split family. Belfast.defined activity order.by lightThebreeders dependent acts of migration to oceanic islands. the 1830s. Most both in science putair” Westerninstance YetofThe in or lessof1830s.theB. He had a unique and local ad.was. and from But if the the role idea Origin of Species in even he did offollowed selection including publicationthus. thinkers such as Herbert Spencer ment idea geographical the branching that the resultwere more or less unold idea was species of a idealized types. At Charles Lyell.itself (14). world view was the animal kingdom. 2) Darwin’s notebooks ofhad proposed that there nomic relations andand wonder what sense of branching evolutionevolution based on geographical the late 1830s (Fig. 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. had shownbiogeographer to the casionally allows for life on together in the right way outlines of the natural naturalOrigin.to Both plain the history of air. Darwin did not expect his theory hierarchy of developmentalteleUniversity of Belfast. for someone migrationinto groups. including his studies of biogeography and animal breeding. I argue that defining was trulywhich heinand which his cultural environment.lection was of predictable. Beagle.development. explained by of new species through a study insight by the animal breeders throws by the struggle for existence. Many of the non-Darexistence.less “struggle for its in a ruthless did perfectly scientific interests that toward off useless variations in a ruthless “struggle for cussed. even by at the heartaccepted the theory idea of evolution.studies of biogeography new animal not radicaland his recognition of the role played adaptation. Bowler that evolution could be shaped by a predeter. afterworked certainlyin on itAl.William Sharp Macleay’s quinary or in isolation. Such world life made it difficult it in 19th-century argued that the theory of explained whygroups within groups. E-mail:tree to find the common point of origin. romanticism (12)].1844 sparked a debate over theto explain the under. VOL 323 force ing in he related issue of Darwinways why thebranches splitting over and and others from currents circu. in adaptation than cosmic teleology. whereas others came to a one embedded as a predictfrom theDarwin of species just whyJ.meant that a perfectly naturallife the a response diverged recently from a common ancestor.have occurred fixed elements in a clearly defined to a new order.hisin(5). whereas relations. Northern what alternative extent. thinking.ent because ing. in almost forand benevolent God. There was and James both in science andevolution. to at the a branching waiting Adrian adaptations. he developed thinker who synthesized a of nature as scroll.his opponents onon concerns of with no fixed limit this score. merely tree in which each actwas not entirely new. but if ended.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. to have initiated a limitedofatCharles their environment. Inessay.pre-existing ones in a progressive sequence leadthough by have beenpublication of Charles Darwin’s was too permitted theory progressive sequence lead. 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. Evolution would become a 9 JANUARY 2009 rigidly323 SCIENCE ofwww. published in 1809. B. his return from the voyage a God. There was no ob. so by killingcommonby variations in killing a paper published in widely Both realizedthe historythelife on earth.further back down the extent. Evolution had to be REVIEW opments that would push other naturalists toward geography must become a historical ended.taxo. 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). 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.him any drew cept that other naturalists. God.individual development. Here. merely waiting unpredictable Darwin’shisMost thinkers— hatred of in its evolutionism the at the time. Charles Darwin. with some branches splitting relations divine taxo. that Darwin appreciate just howthe heart was breeding. explaining to have initiated a revolution evolution sodeveloped a similarand the Malay migrations. variation was population became divided up. adaptation took it universally accepted Populations wider of H. but it was not aimed in any one direction opments that would push other naturalists toward tions to oceanic islands.2.theory of waymerelyinstance isolationofDarwinin 1858 precipitatedthe arrival of earth represents the unfolding asthat the develop-its new environ. I environment adaptation was related issue of defining just why whytheory was ing dead cultural environment.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. 1830s. had shown how his uniformitarian for the whole system by which species are clas. divergent evolution.at the was a life on of change.bowler@qub. and the proposals evolution was widely recognized.M. had been widely distheory. The undermined resibility that goal. aspects Tree of Life work that as genetic mutations). Al. part because led toward inter. But keythe late 1850s. perfectly possibility that new Anthropological Studies. especiallya rapidity withGod. driven animal the process of natural selection. [for waiting Wallace’s Wallace’s 20 years.ukof origin.sciencemag.estimated the rapidity with which the naturalcreated from the white. to any otherbut workexplained by share Darwin’s contributions to himself made clear.which highly creative his theory (6–9).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. reof evolutionathat Darwin conceived in the constructthat migrations of biogeographer fixed the that Alfred Russel Wallace (Fig. But Darwin at the time. on that would be it in full.olence as an explanation of adaptation. he including his The theory a progressive he publication of Charles Darwin’s On of he The theory one direction and. thus. adapting Wallace it predictable. 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. Lamarck had proposed that seems so obvious Archipelagowould emphasize the played played by toward a model These rigidly structured models of taxo. But activity leading to the publication of the Origin. BT7 1NN.supposing that an original pop. Lamarck’s by Wallace inthe tothat efforts being made a vision of nature as a diversity. until the arrival of earth represents the unfoldingcreated from plan white. Tree Life.orgisolation.” This itself (14). that humans (5). however.cause in 1809.” anticipating devel. contemporaries. This article by approaching the problem that by the contemporaries.) Darwin was Darwin had individuals. 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. Darwin did not expect ing nificant between was truly original in his think-andnumber of key insights.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. He allowedaa is widely developed a throws wasexistence. J. Lamarck had byBut Darwin The theory was both original in he publication wise and benevolent There was a wider the process worked certainly was.this claim could be defended by extending the the ancestry from a distantly ancestor.uk supposition that the production to his time. toward was of individual competition and the positive essentially to a articulated by Peter J.of nature as an orderly patternadaptation found it into multiple branches 19th-century evolutionists accept the claim thatenvironment. HULTON-DEUTSCH COLLECTION/CORBIS.combination Natural History of him to topics that was other naturalists. thattruly original and would not (12)]. 1. In this adapting to was a highly creative thinker who synthesized a of nature as an orderly pattern of relations.ac. Bowler moderneven by those accusation that the general idea of evolution. 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.” anticipating devel. As a baidea throughout theory. way.” anticipating devel. Lamarck hadisproposedusthat limited role evolutionhumans (5).sciencemag. Yet to be implications for someone to a few readily available earth represents the of a coherent fact been Russel Wallace (Fig. But Darwin had ian theory idea of commonthe biogeographer so ology. and the each adapts to as biogeographical insightsfor tion.bowler@qub. whereas otherscame to a dead end Fig.to put a few readily availableto a mentorlocation.S. evidence variation. 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. is still preserved in theavery term origin of new species through common ancestry. and itas the by able.” life“selfish” naturenatural selection rejected (2–4).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. so that Historians have quarried Darwin’s notebooks Latin evolutio refers to the unrolling of a scroll. some circumstances. Wil. in which which act of branching the to way that Darwinism was relative locadently formulatedair”At the same time.) The explanatory framework reconstruct that migrations of species on an ever.vancing through a predetermined sequence of ulation became divided up. Many profoundly sole Wallace if essay. Darwin’s ing the implications of the principle of common UK. tree to extent. whereas adaptation.S. the flurry of this position. and however. I could split into of Darwinism” in the ology. thehis studies of biogeography and animal breeding.The Tree of Life significant dif.in a vision of nature ulations to their achievements. had point of origin. were unable to accept synthesized a cause of their localview wasofpeoplemuchdifWallace formulated contemporaries. devel.interests system governed by todivine environment.instancethe theoryhis uniformitarianBeagle. sug.descent“selfish”anature of hazards of migration.M.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. Here.g.emphasize the was truly just Darwin’s world view was profoundly differargue that Darwin was truly original in his think. MICHAEL NICHOLSON/CORBIS 18 CREDIT: SYNDICS OF CAMBRIDGE UNIVERSITY LIBRARY 224 www.selection in arrival paper had conceived its precipitated Chambers—took it for the time. published in 1809.white. the time. the and he realized conceived in the late 1858 is taken cies haddivided by position.”an ever-changingadapted speciesandan species the groups (2–4).in 1859 revolution ingevolution was not entirelythe Darwin’s vision It was not just workbothidea of natural selection struggle ended. 1).selection present distribuscience and in Western 1859 Yet there of how the the process worked certainly Al. Natural selection replaced divine benev.on ideas widely discussed at the thanks to thebe instituted by a benevolent God.ac.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. Darwin ulations natural selection challenged this poptheory 9 JANUARY 2009 driven by SCIENCE from individual ferences support the with some process. Darwin’s which each act of It has been years he worked an evolutionary visionforGermaneach adapts to[e.challenged the was bothgoal-directedness almost America disturbing. theory.org Ernst Mayr argued that the theory of of either lection of key the air. E-mail: p.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. Darwin was led toward his alterna. the principle of common adaptation of popscientific work ing.natural selection Darwin but not somehow Origin of at the time. aIn this essay. toward Darwin’s insight that the moved of the work Darwin himself made clear.emphasize the crucial role of subvert.sciencemag. MICHAEL NICHOLSON/CORBIS CREDIT (LEFT TO RIGHT): STAPLETON COLLECTION/CORBIS.liam hazardsMacleay’s quinary or circular system share common wasnaturalof Darwin’s greatest his move toward evolutionism (13). there wouldwas the only mechanisma process worked certainly was.sciencemag.varying to the publication of the Origin. undersibility that new in 1809. Here. merely wait. 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. dis. have wasforced by hazards of migration. sources of inspiration innaturalists. have been proposed to account for could Populations could sometimes tion and Chambers.19th-century Because many unable to accept many late were slaveholders explained why naturalists were able to arrange plan.non-Darwinian theories of evolution proposed find the common point of origin. can be provides But keyThe by his contemporaries. When modern of Life not Here. some derived from his of relations. Darwin related was of definingoriginal 224 vironments (10).certainly drew adaptation than cosmic teleology. ina athis too permitted was thevariantsofbut more or less was result unhis theory recognized.visionthesis is sure to 224the ways in which he and which he developed his theory (6–9). 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. But key aspects of the DarwinPeter J.Darwin case light provides the process of natural too by his struggle for existence.revolution of how the theory was eventually paralleledAl. so disturbing I overtheir ideas. inal related as an explanation of adaptation.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. model as the agent of popthe air. 1. some derived from his hard of transmutation. thanks ists were converted to the theory. 1. Evolution would become a divergent of biogeography that Darwin was One innovation at the heart of Darwin’s theory divergent evolution.selection. University Road Belfast. it evolution inrejected parallel lines ad-naturalisthe did time. Tree of notebooks (22). more interested This did not seem the kind of process process Chambers’s Vestiges ofrecently from aHistory ofancestor. By the late 1850s.crucial role in gest the idea of The image an alternative to selection was ing.full. the Darwinissuethrough extinction. 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. in explainingby in. so that to the influence of William Paley’s natural the. had Natural History plain but drew essentiallyearth. of change. When first proposed in 1859.isolation over the next 20 years. Darwin had conceived its basic outline universally accepted new environment towardown way. Darwin’s theory undermined wasforinto whole system by which species geology. B. So it was.org SCIENCE VOL 323 SCIENCE www. Closely related ancestor. the kind ofadapted that made in Darwin’s notebooks of the late 1830s (Fig. local achievements.Iseparate a highly creative thinker who synthesizedhis of nature as an orderly patternby relations. Bowlering the old idea that species were idealized types.tions wasterms of past migrations. both in science and Yet there it his explorations in South there might be natural processes if adaptation science and in Western culture. Belfast. Thereand (for was a isms’Speciesthe 1859to realize thatadapting to humans (5). using descent Moore have recently proposed that of evolution. from Darwin’s notebooks (22). The Queen's www. 2. By the late 1850s. and the more practical predictable migration of organisms natural locagressive evolution was widely [e. some derived from his people by natural so disturbing to histo his contemporaries. clearly defined natural order. him to topics ignored by the history of to ex.accept the claim that evolution approached se. ment at predetermined goal. some derived from Darwin’s world view was profoundly the argue that Darwin Fig. merely “ahead of of inspiration in a William Paley’s natural the-parasitic way of that theories of evolution proposed opments in some circumstances.Many people foundan God.organisms how his uniformitarian his moveBecause many can be toward evolutionism sified of had shown points in geology. Darwin’s mentor in geology. 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. The idea of Studies. It contributions The Tree science.vancing through a predetermined insight that the work of the animal divided up.sciencemag. University Road Belfast. by natural the These VOL structured models taxonomic it in full. and tosupport this claim by addressing was a highly creative thinker whoby natural se. J. obvious Alfred might wonder and alternative olence as an explanation of adaptation. however. ested in adaptation thanthat could be arranged in a were converted to thethe animal kingdom. ideas. Northern certainlyway. with no fixed limit Wallace’s paper in 1858 precipitated process of aimed at a predetermined goal. origin supposing that an original be to any other naturalistconceived in the late Wallace was at the time. even “random” who accepted the the con. Populations sometimes Fig. So it was. differ-idea Fig. was perhaps the first to realize that if adaptation mightpaper published in 1855. But if the general outline universally and benevolent God.adaptation. Speelements in the migrations of species on an everlate goal.(Thisthat show that all races proband there were significant difwanted to common ancestry.idea of evolution. 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 next 20 years. HULTON-DEUTSCH COLLECTION/CORBIS. Evolution models divided by geographical account so Macleay and Chambers. 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).response in“eclipse of Darwinism” in the late 19th common descent inal way.cosmic teleology. Few would Darwin’sferent because he argued thatgenerate the of the the theory now accept the claim that evolution from now Fig. dependant on winian theories of evolution proposed during the certainly of Creation of other by other naturalists.by a wise and benevolentAdrian Desmondarecently proposed will in Western culture. orderly system governed by a divine a paper published in 1855. Darwin from the construct clearly defined could sometimes (This assumption dently formulated a individuals. worked in supposition that the suggested merely “ahead of predict an orderly pattern of relations. an evolutionary vision during the years he worked extinctions and that biomultiple vectors of change. although explained rejected alternative to able to arrangewayplan. Darwin was ing up to humans general played It was selection. Robert combination ofignored by interests that alerted off uselessac. and there were sig. He and at the ever-changing off useless it did so by ruthspecies the ancestor dis.) 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.M.toAs of possible variation. Alfred Russeloutlines ofandand letters to establish the complex process by term “evolution”. and on an everDarwin. become divided which he and which he developed his theory (6–9). earth.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. 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). using descent essentially irregular andthe branchingearth (11). geography must becomeby historical a the struggle any seems so time.especiallyseriously its essentially of parasitic tele.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. As Darwin one recognitionthe the role played the idea toward the andevolution drivenevolution animal breeding. species But if Studies. but a ity that evolution could be shaped by a prede(Fig. a show become to be this geographical activity leading of so that lem of the “evolution”.by aThe theory belief thatGod. Wallace in theory ranged in a circle. He allowed a limited role for variation in isolation. use but diof Creation new generally were debate over the time.sole cause of transmutation. 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Natural selection replaced natural adaptive during the some circumstances. divergent evolution. from time.tocircle.environment. Beagle. all races share could is still preserved in the very term “evolution”. Darwin of race was the Historians Darwin had 1858 is the hadas evidenceindepen. but I natural-Mayr overthat the black race was separately theory would allow the biogeographer to resified into groups. Tree of of Life. driven by force derived dependent acts of migrationin terms of past migrations. ever-changing “eclipse of Darwinism” in the late theory. models could have been idea ology. Lamarck’s from any of the other efforts being made to ex. common the kind of process wayin So was species the Natural History of him to topics model by other naturalists. aDarwin’s mentorWallace. Belfast. But barriers. through extinction. Darwin’s supposition thatathe production leading up tonew Anthropological the general idea time.crossed oc1858 is taken put few Russel Wallace were in the types. Many peopleI foundMayr overestimatso disturbing to dead end through extinction.ent because he argued that a played by structured common divergent process. world view made it the hard to see natural selection as the agent of either naturalists were creation of species by not J. Darwin’s supposition that the production 223Ireland. butformulated their ideas. The Queen's now seemsthat would push other naturalists to. and so on through sis for his thinking. UK. But key aspects of the Darwinian within a 1830s. and dependant common descent to one selection from a common ancestor to explain the under. family p. to to topics ignored inspiration was led towardnatural adaptive did not seemlife bewas.number was in insights. insight that the work of the animal breederssimilar open. until the outline aimed at a accepted at granted each adapts to sified atthe time. Manythe agentfound it the Darwin’s world view was accepted it would argue that Darwincertainly not the first to sug.It waswise just that the the time. were produced because were idea sibility Philosophy andE-mail: p. Here. the Latin evolutio refers to the all races share to the taxonomic hierarchy.lection certainly not the Lamarck’s subject in a the that relationsFew would now cosmic teleology.Darwinian vision aspects of the the idea was inspired by German in isolation.ac. and he realized that lying similarities. HULTON-DEUTSCH COLLECTION/CORBIS. 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. centered of the changing earth. but this pre-existing ones in a was eventually paralleled element of teleology or original and disturbing.bowler@qub. Evolution would become a divergent his this thesis is thesis process.was environ-key insights. Wallace historical science. 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 from the voyage including Jean-Baptiste Lamarck and Chambers— (13).org SCIENCE VOL 323 9 JANUARY 2009 223 19 CREDIT: SYNDICS OF CAMBRIDGE UNIVERSITY LIBRARY . thus. 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.“selfish” nature meant that “selfish” nature lying similarities. in of biogeographydivergent evolution.

way sence. the called theattitude of the key insights onimpact Darwin based At the is what Mayr breeders’ process operated. 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. policies breeders Darwin turned to the based on struggle. Adaptation was not crucial once the basic individuals.realized that in process.among indefinitely over time. The expressed with artificial selection insight Darwin’s may have that they worked byinselectionlater writings. orthogenetic evolution oftime group20). This very when Galton argued that itclear be necessary huge Californiain structure by acbreeder’s activity as a selecting 3.tion from typological 2000). in structure by acthe to extinction—the thejust an up. time. Like Chambers. late 1830s. Stud. The similarities linking the species in a their artificially small populations.Univ. in this case with characters useful to by forcing even Darwin’s critics to think about descent (15). R. ofM. The analogy with artificial selection then the selection theory brought this implication out synthesis of the selection sence.. highlight the harsher aspects of York. Cambridge. could change ofenhanced under variants help to createalthough heD. Ithaca. with harmful charac. Darwinism’s Struggle for Survival: method of artificial selection offered on struggle as the motor of change.concept of the “inheritance to conform to their own pre-existing ideals. The idea of struggle was pervasive in thewho taught Darwin that variation is not ordismissing nature. late 19th century dem. The potential 2. their studies in the early by Cope and Hyatt. process. branching artificial selection helped toPress. A. in fact.with animal breeding even while “sports of Artificial Selection exploited in natural selection goal.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. the analogy with as the addition of preordained stages to ontog. It was the breeders by taught may have analogy. variation among individual to.artificial selection continued to play ato Darwin (Cambridge by predetermined trends.inated by the struggle for existence. 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. especially in point is Wallace did not take this win’s Notebooks p. in the terminology wild population. Bowler. We may well feel uncomfortable with was truly unique. Like Chambers. Adaptation was not crucial once the basic variation pushed Darwin toward degree of variabil. of of parallel natural process that changes Press. orthogenetic evolution of the of each group should be by this Thoseand although their ideas about (18). It was the who analogy early geneticists endorsed eugenics by saw selection working (Univ. Eds. The similarities linking the species in directed variation among individual organisms. Darwin introduced 8. J. undirected variation among individual organisms. as well as scientific. process driven by predetermineddevelopment. When Darwin linked this informasense of the theory proposed by Cope to a recent common ancestry. may have exaggerated the acter of the group was established. P. Hist. There was a well-developed network of breedtant the analogy between artificial ers by this time. traordinary Publication. P. Charles Darwin: The Power of bert Cope and Hyatt.org/. Barlater thinking. providing just the source fact that such normal than the human breeder. In the debates that followed the publication eny recapitulates phylogeny. Bowler. J. nition that their later 19th century. allowing working within the framework defined by this erature of the period. In social Lamarckism expressed in the terminology inspiration from social. Darwinism that the with artificial selection expressed theory is responsible for the affairs. the analogyclaim could produce this case with characters useful to the of of On ultimately endorsed Darwin’s with could not be essentially plure.tion from typological the Lamarckian process. Spencerian certainly have been different had he not drawn Natural Selection portfolio p.later generations. allowing working within the framework defined vision decision to investigate the work of the animal the population becomes paramount. the consequences ideas about sence. The insight generations.” Darwin could make no sense of the allowedHer. nevertheless. and many historians now 19. MA.aggerated the extent to which Darwin himself try. A. P. He then exploited by those who wanted the human race (Harvard Univ. fluences. L. thePrinceton.and selection working on large variations seen as bizarre nonadaptive could of nature. At For by proposing that evolution worked the revolutionary impact of Mendelian Quest for HuGenetic mutations seemed to be essentially pluCause: Race. netics. it does of the time. Darwin’s Century: Evolution and social Darwinism. Chicago. J. This later development high. 3. any animal or characters as a prelude same hierarchy of developmental stages. Ideas 36. Ed. accepted species Artificial Selection orthogenetic evolution of the group breeding individuals. London. Darwin exploited the about the world.Although convinced that the degree of variabil. MD. accepted that there development of the selection theory brought this they endorsed the recapitulation theory (ontog. He ulation becomes paramount. But the non-Darwinianby this analogy. and although of variation was clarified acter of the group was established. because he allel process in which knew that individuals.recognize that the theory. Herbert. Richards. of Population. theory proposed by Spencer would later refer to allel process a new a few variant individuals. of Wisconsin Press.of On the Origin of Species. 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. the breeders’ attitude for primarily man “hard” heredity London. J. vive and reproduce. 1838). of Creation (Univ.speciesmutation the Origin of Species. Berkeley. endorsed the recapitulation theory (ontogeny breeders certainly taught him one thing.troduced in opposition to Mayr “soft”the transithe addition of preordained stages ward char.was Spencer.notprocess.23. In this investigate the work of Wallace Darwin was truly unique. P. 631 (1976). buttime by historians a human there scale and that could be investigated how imporcan be little doubt of directly. in Darwin’s laterappearance of a whole range of unpleasant social set the traditional foundations of how we think writings. Stud.realized that in a domesticated population there variability becomes part of the species’ character. and a 6. London.to depictcreative force in nature.made the conceptual transition. of Californiapop. because eventhe animal breeders (Fig. late thinking. Victorian Sensation: The Exrecapitulates phylogeny. G. bizarre nonadaptive characters some popu7. Opponents such ashas reopened the material. Press. The analogy with artificial seintroduced by Ernst Haeckel) and saw evolution lection then allowed him to depict natural selec. Modern evoluonstrates just how radical the theory of open. The American for Existence The Struggle neo-Lamarckians scale and that for that transition in the late 19th century. Chicago clarify the nature of both But 13.” were. This was what the philosopher him self a natural selection as a par.more clearly.tion as a parallel process in which a few variant artificial selection continued to play a key role REVIEW eny. London (Univ. 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. paving the way theory and genetics ain the different.There was a well-developed network of breeders were treated as idealized types with a fixed esthe linear. Corsi. toward variation pushed to populathe genetics. this informatraditional belief in a benevolent genus were due not to“strugglecommon ancestry. the allowed from depict natural selection as geneticists. Hist. the G. was unique until paralleled by Wallace nearly population could be changed— here at least was 20 years later. it led not just to the 5. species the Men Who Discovered It (Doubleday. Desmond. J. andand natural selection became in his although their ideas about later thinking. might evenCentennial Retrospect (Princeton extent to which Darwin himself made the con. In 15. It wasquestion of whether variation and large variations opment highlights thethe time.but of both heredity and selection. 3) and his recogel of progress became immensely popular in the of Darwin’s key insights when used as a way 17.” were. 75 tigate the work ofprogress. Traditionally.REVIEW Vestiges. tion of his theory is much debated sional use of highly individualistic language al. of struggle popularized by Darwin. providing transition of in the formulation of Darwin’s mecha. ical (like Darwin’s own). F. Library. the transithinking Adaptation was hapscrucial once realize that it might represent Darwin’s the degree on variabil. theory and genetics theory proposed20th century. 2009). For supporters such as Francis Galton. 1 (1982). The natural range of tribal groups competing for limited resources. The exact role played by Dar. nevertheless. Press. 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. they had a very would could produce the same hierarchy of developmental stages. In to debates that followed the publication Genetic mutations seemed toimagine an evolutionary process driven inhuge changes in structure by ac.The ing. transcribers and Eds. 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. Spencer thought that all humans will turbing implications. same time. Darwin heredity and variation were distinctly pregenetiwas truly unique. 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.more clearly. ultimately him to build on his existing conviction that adapt. survive and that the only way the continued to play a key role theories flourished in the late 19th generations.inated by the struggle for existence. and Hyatt. Those stand or accept the details elim. M. But if we accept science’s power to upNY. The 14. 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. that linear. their artificially small populations. Radick.Darwin. 3.. divergent evolution was to the to ontogeny. 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.the problems of heredity and variation in a new Edward Drinker Cope and Alpheus Hyatt pro. he was wants. 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. The Agebeing trivial Evolutionary theory of its group to the struggle this time. 2003).forcing even Darwin’s Press. E. The breeders a few variantthey geneticists the accept the situation. But some of those Heredity and the Hypothesis of Natural Serely a useful way of understanding howconfused with the Darwinian mechanism. J. and in its most extreme manifestation 3. its social and physical environment. but the new form of speciesIdea (Univ. 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). and the species rather than the human breeder. Traditionally. the Long form of that the win created an a population of introduced of “random” variation that Darwin’s mecha.population was by selection. Opponents such as Fleeming Jenkin. Press. S. 1988). The exact role played by Darwin’s eventually acquire the faculties needed to inter.to biological evolution and so. insights came from sources with profoundly dislection (Cambridge Univ. Thissame time. selection offered a useful character. Sci. Eiseley. Moore. P. and impermanent. He where ized that in a domesticated population there bemodifications were actually is ing produced on a human time Fig. This was the eugenics concept in which the Press. ing. H. and although he may have exa genus were due not to a recent common ances. Browne. S. 2002).ceptual through the subsequent developmentthe Galton and transition. Hodge. 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). But the cumulating rather variations over a number of ralistic and undirected. that they (Univ. still breeders lit. variants. Slavery and the disturbing. because he as the “survival in which and profoundly disturbing insight into the In the debates that followed the Cape. Press. Biology on large variations 1983). UK.amnh. nevertheless. Kohn. alent natural process operated. Cambridge. The processDarwin.org SCIENCE VOL 323 9 JANUARY 2009 225 225 21 . Reception. 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. inthis case. The analogyItwith to be admitted that. J. For supporters such as Francis Galton. 10. C. This later devel. 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. Stocksfield.istic aspects of Spencer’s philosophy. an insight that seems to have resonated 9. F.moreimpermanent. In fact. Their theory certainly fed into a situation where the actually bemodifications were movements that led toward various kinds of References and Notes 1. J.in which the popthe new form of species concept paving the way same stage of trends. Desmond. 28. 1992).as the breeder will not permit they had a very clear “sports produce huge changesnevertheless.driven toward a Robert Malthus’s An Essay on the Principle health of the population.metaphor focused attention onto the individualAround 1900 (Johns Hopkins Univ. lowed him to be perceived as the apostle of free science being “misused” by social commentacan be little doubt of how impor2007). Bowler. nevertheless.thenmakingselection theory brought this implication out than Cape. R. J. theory an open-ended. the breeding studies of of as a prelude to extinction—the theory of “racial lation. Pigeons (23). The Meaning of Evolution: The Morphological Construction many models were In the 1850s. and the the specieswas artificially enhanced under domestication. Chicago. tant the analogy enterprise.the way those implications were developed by Joseph. Herbert Spencer and the Invention by historians (16–17). J.mation with his conviction that species could tionary developmental biology Fleeming Jenkin. Transmutation Notebook B. The breedersFrance. The Eclipse of Darwinism: Antiinvoked Lamarck’s lights the importance of another of acquired characteristics” to explain how these the same way. Gautrey. M. just as the the problems of heredity and variation in a new required as its raw ended. Vestiges.analogy with The Cambridge Companion key role requires But differential such rather than the with the thinking of many re. 1958). Secord. The Philosophical Naturalists: Malthus.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.only the fact that reproduction among human breeder. Chicago. leading 16. Dar. from between artificial as “social Darwinism” was. interbreeding individuals. 1985). 6.org SCIENCE VOL 323 9 JANUARY 2009 20 CREDIT: AMERICAN MUSEUM OF NATURAL HISTORY CREDIT: AMERICAN MUSEUM OF NATURAL HISTORY www. his decision tocase. The breeders knew that they ters are eliminated by the struggle for distinctly pregenet. R. ity is just a population of inter. in turn.those unfortunates deemed unfit by the state. Darwin. It individuals.” Strictly speaking. played into 20. and because it too seemed to of explaining countless otherwise mysterious 18. Voigt. 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.” were. The American neo-Lamarckians scale and that could be investigated directly.produce. J. at the hands of the Nazis. Darwin (Michael study of breeding in the formulaact harmoniously with one another. Place (Jonathan publication of the fittest. 339 (1975).changed— population could be but the breeders certainly taught at least was a situation realhere him one thing. J. 1991). Spencer had And the Nazis wanted to purify fixed racial These non-Darwiniandifferent ways. This is what the called form of of open-ended. it was aspects of the natural world. After all. Hodge. erations. This is what Mayr called of Chicago Press. 2003). Hist. 1987).elim. 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. branching a domesticated population there variability becomes part of thehereditycharacter. The similarities linking the species in a Creator. Fig.Although convinced that emphasis of the natural elimination a means by which the population ity was artificially maladaptive domestication. Darwin rett. nevertheless. undirected naturehe may have exaggerated the be extent to which Darwin himself made the conmight even. experts studying Darwin’s notebooks). 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.sciencemag. The insight generations. survive andwho did not underUniv. an open-ended. predictable range of variability becomes existing conviction that of marginalized by the synthesis of the selection ive evolution must be an open-ended. senility. Desmond. 1985).the same time. Richards. however. New York. fixed norm. Cambridge. Philos.Although convinced that the the view inheritance implied by thinking to population thinknaturalists of the time. The in order to prevent “unfit” individuals from When Darwin linked of Chicago Press. and in some respects less had evolved gradually from an ape ancestry.must be some equivalent variability in every implication out more clearly. S. some Themes in Fleeming Jenkin. Ideas 37. could not imagine an evolutionary process drivennaturalthis case withworld. 1983). 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. Charles DarThis step and important in the context of those aspects of his theory today. The natural lowers believed. 12. M. 36 (Cambridge and natural selection became in his Univ.sciencemag. Darwin’s Sacred into very early 20th century.toview chang. an up-agent. Browne.norm. still Artificial Selection directed toward some preordained goal. sur. just how phylogeny. The Darwinian Heritage: A worked by climate of opinion in which through the (19. But his occa.produce.by Darwincritics to think about theories flourished in the but Darwin thought that the pressure of with harmful characters areof his theory. This is not a simple matter of 21. that they workedwho selection Darwin been tionFor supporters such species couldGalton. his decision to inves.just the sourcefrom typological thinking Darwin toward his theory of natural selection. they allowing him to build on his exist. interbreeding descent (15). but there of Modern Life (Acumen. tion thinking. Madison. but to parallel trends independently reaching ity was artificially enhanced under domestica. but could be directed toward some preordainedas the mechanism of evolution. 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. ing produced on a human time but it was Pigeonsonly vehicle www. often the equiv1998).ceptual transition. The notion of “hard” heredity was ralistic and undirected. species character of the group was established. to population thinknot the first to the basic char. J. He ulation becomes paramount. 1876). 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. S.” Darwin of the idea suggested into reproduce if it does not have they characterchangesworking within normal variations over a numberthis Vestiges. ed. Opponents such as Early Nineteenth-Century British It seems that without naturalists ended. he or eugenics in any reproduce if way (18). P. NJ. 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. J. selection. R. 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. These non-Darwinian models breeders (Fig.. because even cal (like Darwin’s own). because even Smith. mechanism of progress (21). Did the addition of preordained stages to ontogeny. Mayr. Traditionally. 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. wants. London. J. providing just the source toward variation pushed Darwin toward the variants. Francis. 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. they experts studying Darwin’s notebooks). divergent evolution was to the naturalists breeder will not permit any animal to reproduce if way (18). divergent evolution was to thethe input frombreeder will not permit any animal tosimple way. J. Biol. Rehbock. and breed. who saw impermanent. although used in the context of program. because Darwin’s theorizing would almost 22. always a fund of apparently purposeless and un- could be investigated directly. ralistic and undirected. not the (23). competition was necessary to make it effective. 1991). would not have come up with the theory. Gayon. 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. breeders (Fig.notion ofOrigins (Allen Lane. self-improvements Baltimore. of understanding how the equivDarwin turned to alentbreedersprocess operated. But the endorsed the recapitulation theory (ontogeny breeders certainly taught him one thing. term 4. ism was not “responsible” for social Darwinism heredity and variation in a new onstrates just how radical the theory of open. Hist. Cornell Univ. Das Ganze der Taubenzucht (B. http://darwinlibrary.of Darwin’s did. we should also accept its po. branching artificial selection helped to clarify the nature the result of accidental deviations plan has both heredity and selection. Kohn. Much of what later became known tors. in selection characters useful to the species of On the Origin Species. just as the the problems of 11. same stage of development. theory is much debated by historians (16–17).heredity andA. 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). Although it took some time for the marginalized by thesenility. Press.and although their of struggle. available at the Darwin Digital Library.Berkeley. and the linear. Neumeister. in the terminology intro. Moore.and Ideological Reconstruction of Darwin’s Theory (Univ. Weimar. fixed norm. change indefinitelynot have time. the interaction between individuals through the elimination of useless genetics. the subsequent the same stage of development. not have the character he wants. A. Like Chambers.artificial selection environment could affect by predetermined trends. 3) and his recognition that theirwere ultimately him to build on hispart of the species’ adapt-evolution unfolding to an orderly. Spencer’s self-improvement modthe animal Modern science recognizes the importance cial (1997). his toward a newbreeders who taughtconceptthat variation is be quite “sports of nature. his popularization of the struggle Darwinian Evolution Theories in the Decades insight gained by Darwin in the accumulated over many gen. Darwin linked this infor.ical (like Darwin’s own). paving the way method of artificial theory and genetics in the early 20th century.a analogy. Ruse. Darwin.” Darwin could make no sense ofany variation him tothe norm being trivial a par. tion. posed that the evolutionwaseachappeal should be by for exis. In this case. D.

S. beginning There model (1) to Alice oceanographic and tectonic eventsdo. organismic and species level on short Scale (100 ky) Species body to hard times. P. Pg. marine the Paleozoic Paleozoic. as well as by and oceanographic eventsFurther. although present (Fig. excludingan outline of how of the paraphyletic.work convincingly Jurassic. and other evolution of species diversity. influences on evolution in their The taxic approach involves treat. rates are not dence of origination andthe equilibrium does noted as “multilevellevels (10. or food supply. taxicQueen. the Paleozoic been only modest increase as when fossiliferous localities) levels Based through after assumptions (11. perhaps 400 Ma. Traditionally. and els long logistic model (5) are Red three urt Jester model. or a mixture of both. Paleobiological studies suggestmonophyletic or pansion model (8–11). and by abiotic place. be future investigation versification are extinction global partly an artifact of taxonomic scale (Fig. a view that has More largely been Less dividuals. Cretaceous. 10) Lack of cohesiveness of the great “evolutionary faunas” (12) Species richness–energy relationship (18.Life on land man error. mostspectacles of was character. evo.portant not in export organism-level processes to 3500 million years ago (Ma) (Fig.some 400 Ma and there has (450 to 250 Ma) and has risen. 14). work convincingly (5–7). partly an the logistic data.logistic evidence may be so complexhave radiated data in explosively.uk E-mail: mike. Thediveras theterm saturation modelexpanOrdovician singlePermo-Triassic from of food Fig. biotic cancel each other. Pliocene two versions to the equilibrium through thousands Court Jester years. excluding some descendants h the spectacles theeither the Red model (2) global scales. coupled logistic model may curve). 7) identifies amodel standardized (corrected) analysis of the Paleobiology Database (blue line). It is im- 728 6 FEBRUARY 2009 Bristol Temporal scale Department of Bristol Earth Sciences. it has proved hard to teristics (short gestation period.Patterns of marine two linesgenus diversification through and the land witnessing continuing (dampthe Phanerozoic. but thebetween the Perhaps Cambrian. I that sister clades add rigor to analyses showing will explore the The Global global.of organthrough (uncorrected) Sepkoski database reached for increasing complexity at ordinal and familial to models. Tr. Theseinteracted rise. or adaptability to Fig. proach els cladograms or molecular trees the licensed fool of to Thecapricious behaviorMedieval times. and Triassic. 7).treating species.onpopulations. for a long time. similar patterns of ex2A). Ng. whether one considers plants. tion. red to extinction. extinctions andcurrent extinction events to the muchLatitudinal diversity similar patterns of exponential increase in climatefossil other displacement physical factors. and thewhereastimes as diverse as life in the sea. obviously separated. ortoday’s all descendants of families as ized evolution. differing in an area ester model (2) is that and Van Valen (1)uses cladogramsextrinsic evolution. likely in Court Jester. S. In both models.C. 25) Declining global extinction rates through time (1. 1. Queen. the beginning the Pliocene expansionist(My) (10). 11). 19) Evolutionary arms races (1) Coordinated turnovers. mayandso complex and Pg. climate andequilibria correspond to biodiversity the empirical (uncorrected) Sepkoski database (red Sepkoski sampling.here is the microevolutionary Red Queen.global paleontological studies to all de.sciencemag. red) Number of genera 400 600 (corrected. 1. differof operates in a pluralistic way of the The Red Queen evolution the licensed fool of (3). The200 lines 100 530 two compare current after each long-term replacement event. although moreout at ordinal considers 8–11). at time scales above by climatic of theseSciences. 24) equilibrium levels (8. J. andworld novelties own on lineagesversions of the equilibrium span was diversityinin and Red factors.across larger scales. Biotic and speciesparticularly in the with damping. or active predation. The Red Queen may prevail at Court Milankovitch to biodiversityApparent saturation in which depends will explore the largest-scale global. and multilevel globally. a view that has been rejected (31). facdifferent times. UK. intrinsic) or signals are not obviously models. fromthe scale Jester holds ability to hard In on Species on short time scales. S. and species Species allowed to Alicerecalling species. 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. the equilibria proposed There are two and can do.the extrinsic. divergenceBiotic interactions (Fig. vertebrates. The suggesting no controlling averaging of effect of the perhaps world think in a his own on larger course.show gradient (22–24) of the and record. life My) Much scale Queen that posits exphysical sponses along the red line separating Red Queen ic factors way. “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. somewhat dampened Red Queen (biotic. intrinsic) or Court Jester (25) and their turnovers. great dealcorrection regimes increase in mainly climate and other physical factors.span so cancel each other. and food supply. 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.ened)from extensive attempts to correct ever other physical factors. it out a predictable to export not dent proxies dependent has proved hardrises in di-theDensity depen. My) early Paleozoic.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. primarily biotic. dithe background assumption of that both origination and expansionist. and other correction marine ecosystem became saturated.could intrinsic. Tr. PhysicalJester much ofand local-scale successso cancel each may Physical-environmental disruptions or views QueenJester. blue) 2000 Number of genera (empirical. allowing pends um sea showand between on models. breadth of in where Red Queen effects might be d extinction rarely happen except physiological tolerance. red) 1000 tion T T T Temporal scale Temporal scale Table 1. it has proved hard to ical studies to all life. J.(2) isit that evolution. Cretaceous.evolution in independent causation) because it implies primarily A con. in the which geologic andorbiologic signals are is that ecosystem threeand extinction rates plants. macroevolution of spein species richness and some descendants of the paraphyletic. including all descendants of an REVIEW are rigor to analyses showing that sister clades outline some phymixed models (Table 1). provide some descendants these and other Comparative macroecological studies ancestor. whoDarwin. or food supply. ing species.or global organism-level processes (31). limiting rises in standardized (corrected) increases in the occupation novel dependent at generic or specific Cm.Jester and factors way. In real. such as body physical environment on evolution. others curve).holds RedIn reality.org SCIENCE VOL 323 6 FEBRUARY 2009 729 .sciencemag. such as solution tigation must determine appropriate indepen. viewedhere are two balance viewing pressures. in the Cam. to keep in the other Queen phylogenetic geographic and temporal scales Species ent (3-6 pends primarily on intrinsic factors. so it rapid most 2A). an species of how and and other studies correin outline richness A keytoquestion of evolutionary novelties across spond the predictions of theoriginQueen.seem to the ground assumption of a global carrying are themselves land and sea Alternative or space.” of takes and millions of a balance in biotic pressures. the interponential increase for global diverterm saturation model in species numbers (8. suggesting outcomes (B). diversity 2. regional responses to climate change fluctuations holdsGenus own on larger scales. logenetic studies of themorphospace occupation. Illustration based on (2). O. and distributions of and it is and A for global lineages in a explore Queen or Queen or the Court Jester. and promoting rapid recovery imposed. 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. least. 2. Paleozoic. environment.marine ecosystemmarine paleobiologists at modprimarily a primarily biotic evolution. diet. Comparative macroecological Ordovician and Permo-Triassic intervals. Two least. other correction regimes 7). and species (Red Queen). 1).entities and counting their occurrences against Paleozoic. (2) the 1): Biotic between opposite di. colonizing ability or ecologiResolution between extinction and somodels. Here. Thediversification through the past must encompass the independentdata. 2. there are problemssam. by limiting factors such as shortage on (6).levels some 400 Ma and there has been only modest increaseand samplinghave been since then. or active predation. 11). for a long time. P. Comparative macroecological studies lineages and subclades. 1). 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. stud. 30) Court Jester Nonconstant probability of extinction (3. but these are Geographical Court iews.prevailed. or adapt. and future investigation that both both extinction present (Fig. Sepkoski’s y be dominated by biotic factors. through the spectacles the such a climate. but extrinsic factors such as modelsto the predictions of the Red Queen. Devonian. 9. Triassic. because origination equilibria. 25) Declining global extinction rates through time (1. and timing of increases may vary whereas taxa may be monophyletic or ancestor. limitingand continuing to the present rises in diversity and promoting explosively. Ordovician. breadth of physiological tolerance. or a mixture of both. Large-Scale number of so it may be Species Diversity 7). climate change. Environmental scale (1-2 My) tinction risk. Bristol rejected (31). and species (Red Queen). by the past500 My. Earth Sciences.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. or higher equilibrium levels asthe 400 0 without correction (5. Cambrian.might seem Alternative models three sets of diversimay be wrong to generalize from marine straightforward. from scale effect ability size.ac. as well as by doubtful (8. 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burrowers have burrowed deeper. the crocodile-like crurotarsans and others. W. J.5 228 203. bars represent the Comparisons of sister taxa have allowed tests observed durations of major lineages. and many other modern groups radiated substantially. Major biotic replacements. the ability to occupy and exploit different levels in the habitat: At times. and each probably more Jurassic boundaries. This would link most increases in species diversity to particular large-scale radiation events. Ecol. Further. Further. K. each and Triassicoccupied by a species. Benton. and that evolution may be pluralistic (3). J. at theinto small patches. when flowering plants. W. M. two antelope subgroups. Science 321. that generalists are less speciose and have longer species durations than specialists. The slow dance of the continents as Pangaea broke up during the www. some 130 to 100 Ma. 223 (1999). Syst. T. S. incomplete trees have been used. S. 6. but differences reflect pendent aspects of present. 16. or that they dwindled to extinction because of “racial senility. Numbers at top refer to millions of years before the present. some 130 to 100 Ma. leaf-eating insects. Rh. Evol.their continuing diversification in the Late Jurassic and Cretaceous was mainly indistinguishable from a random walk. or different. T. 275. D. Simple to say. D. Walker. tribes Alcelaphini and Aepycerotini. Braddy. and this allows direct communication on the patterns and processes of macroevolution. 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. Phylogenetic relationships and morphospace occupation for Triassic archosaurs. Lloyd et al. any time. and anonymous referees for comments and to S. Biol. A. H. Species diversity may increase by the occupation of new ecospace. lution probably Numbers reflect top refer to indeat this phylogenetic signal of millions of years a common origin. and flew. Schmidt. 23. Biol. pterosaurs. Lloyd. Bush. jectories occupy the same phylogeny for (A) Framework amount of time. and if different. In particular. A. M. the tribes Alcelaphini and Aepycerotini. Alroy. L. smaller black dots. there are strong correlations between plankton morphology and diversity and water temperature: Cooling sea temperatures through the past 70 My. J. 715 (2008).08 Dinosaur morphospace Pterosaur morphospace 0. 24). giant size. tectonic. Science 303. stars. whereas the speciose alcelaphines show more dietary specialization. Science 321. J.36 -0. T. J. Proc. Crn. 5. Sepkoski Jr. R. The number of occupied guilds. Vert. 19. long species at lived. A. 12. C. and reef-builders have built taller and more complex reefs. “rauisuchids”. Wildman et al. 29. The dinosaurs seemed to be radiating actively in the Cretaceous. Ecol. wider studies of dinosauromorphs. Vrba. J. Schiebel.A. Scleromochlus. D. where equal chances of speciation and of extinction are shared by all species (4). A further study on Dinosauria explored the subsequent evolution of the clade (26). M. A comparative phylogenetic study (28) shows. based on the first two principal coordinates. shifts should mainly occur low in a clade’s history: Clade shapes vary from bottom-heavy to topheavy. 52 (1995). J. A. that there are higher rates of speciation and lower rates of extinction in the tropics than elsewhere. Natl. J. Biol. J. G. There is geological and paleontological evidence for a mixture of both hypotheses (23. Proc. A. poposauroids. even though niche subdivision may be less important than occupation of new ecospace in increasing biodiversity. L. More commonly. coinciding with relatively high origination and extinction rates. 11536 (2008). M. Early Jurassic. S1 (2007). Afrotheria in Africa. dinoonly one. Mittelbach. 7. and the latter is represented by two species. only one. Roy. “rauisuchids”. on the other hand.org has affected323 past 200 My SCIENCE VOL modern distribution patterns. two antelope ogene mammals (29). with some 7 living and 25 extinct species. 315 (2007). hard to achieve. Natl. G. and especially in their final 15 My. and the origin of novelties. Wang. “Dinosauromorphs” ORNITHISCHIA Dinosauria SAUROPODOMORPHA THEROPODA PHYTOSAURIA Crurotarsi AETOSAURIA CROCODYLOMORPHA “Rauisuchids” POPOSAUROIDEA ORNITHOSUCHIDAE B 0. Finnegan. plotted accurately against geologic time (4). suggesting that there was no insistent competition driving other groups to extinction but rather that the dinosaurs occupied new ecospace opportunistically. Acad. and South American mammals (30). that complexity has increased many times in parallel in separate lineages (27). D. M. E. J. the identification of diversification shifts across numerous taxa may provide evidence A 245. and there are more specialists in habitats that underwent recent environmental change (tropical rain forests and deserts). Large circles. 97 (2008). then the Court Jester model of macroevolution would prevail. 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. aetosaurs. The ecological crosses. J. Krug. Benton. However.12 -0. N. Purvis. A. R. Carnian.S. 3. social insects. however (Fig. species richness. L. 165. Sci. G. Comparing Sister Taxa A powerful element of the comparative phylogenetic 3.A. Lad. EJ. The circles. J. This would link most increases in species diversity to particular largescale radiation events.. and some subsidiary use hypothesis (28). Studying species as members of clades is a fruitful approach to understanding the drivers and controls on speciation. Any similarities in to the Triassic time scale. 2381 (2001). Purvis. Barnosky.24 -0. and geographic drivers. from 20 in the early Paleozoic to 62 in post-Paleozoic marine faunas (25).. Paleobiology 34. 32.S. and the second following the end-Triassic extinction 200 Ma that removed most of the crurotarsans. verof the resource-use hypothesis (29). Acad. Eble. the coordinates. Jablonski. but differences reflect independent aspects of their separate histories. Erwin. 25) and terrestrial (10) systems. evolution is all about biotic interactions in ecosystems (Red Queen model). then the Red Queen worldview might be considered. with the risk of error in calculations of evolutionary rates or comparisons of subclades. have been a focus of debate about the roles of competition and progress in macroevolution. 14395 (2007). Lett. with many new clades appearing through their last 55 My. Donoghue. by a process of competition in which they prevailed over their precursors. A. the Jurassic.32 and upland habitats of the later Paleozoic when land animals first burrowed. B. R. both on land and in the sea. 26. that generalists are less speciose and have longer species tical dashed lines denotethetwo extinction durations than specialists. M. temperature.dots. J. and the latter is represented by two species. hexagons. stars. and so occur as twigs on a great phylogenetic tree. Mayhew. Rhaetian. (B) Empirical morphospace for Late Triassic archosaurs. 17. or productivity. principalimpala Aepyceros. E. Evolution 62. on the other hand. and dinosaurs provide a classic example. D. M. J. 21. D. predictions confirmed: Specialists are more common than generalists. G. J. K. gray bars represent the observed durations of major lineages. that the Dinosauria expanded in two steps. Bambach. N. the large patterns of biodiversity are driven by the physical environment (Court Jester model). and at lower disparity than the crurotarsans they supposedly out competed. expansions of ecospace have occurred on land. the resourceBased onwas supported. methods are shared by paleontologists and neontologists. Ladinian. a phylogenetic tree that contains all species living and extinct. Sci. 172 (2001). associated with increasing body size (20). Edentata in South America. W. and geographic drivers.16 -0. J. 25 extinct spe. there is close tracking be- Fig. Large slowly evolving Aepycerotini consists of few saurs. 4. mean species number in communities (alpha diversity) has increased through time in both marine (15. endothermy. Am. Alroy. 1 (2007). J. Paleont. surviving.. Science 268. Valentine. and studies of terrestrial and marine ecosystems have shown that these factors may explain as much as 90% of current diversity. and consequent increasing ocean stratification. pterosaurs. Classic views that the dinosaurs arose with a flourish. J. Acad. A..24 -0. or recoveries after mass extinctions. Natl. E. Ecol. opens opportunities for dialog. Palaeontology 50. but comparative phylogenetic methods will illuminate questions about clade dynamics. tween temperature and biodiversity on the globOutlook al scale for bothand evolutionary ecologists have marine and terrestrial organisms Paleontologists debated generic largely independently. diverged 6 to (B) Empirical now highly 8 Ma. Classic examples in support of the resource-use hypothesis come from studies of Neogene mammals (29). diverged 6 to 8 Ma. 1 (1973). arose because those continents were islands for much of the past 100 My. squamates. G. 207 (2004). clades differ: The impala has a smaller black habits of both crocodylomorphs. Sci. at the Carnian-Norian and Triassic-Jurassic boundaries. climbed. If the majority of diversification shifts are coordinated. with some 7 living and based on Triassic archosaurs. Over long time spans. Science 314. and not coordinated temporally with others. 97 (2008). such as the Cretaceous Terrestrial Revolution (26).. Any similarities in their subsequent evolution probably reflect this phylogenetic signal of a common origin. one after an extinction event 225 Ma that removed dominant herbivores.12 0. London B. the ideal is a complete species tree. D. K. Jones. of the lineages Classic examples in supportof Neresource-use hypothesis come from studies Ladinian.the first two cies. 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). presumably triggered by the split of those continents 100 Ma (17). hexagons. L. 8. 739 (2005). and Triassic cruthey started with the same genotype and pherotarsans scaledtheir subsequent evonotype. U. such as the Cretaceous Terrestrial Revolution (26). of many short-lived species. Proc. Proc. then the Red Queen worldview might be considered. If. 318 (2008). B. 105. S.06 Principal coordinate 2 0 -0. Isaac. or (ii) the diversification rate hypothesis. J. Van Valen. 24 25 . aetosaurs. Crn. wherespecies diversity and familial richness were relatively2009 during warm “greenhouse” phaslow 6 FEBRUARY 731 es of Earth history. surviving. Further. 25. 36. 1 (2004). Lett. Stanley. arrowheads indicate lineages that survived the latter event. For example. nondilarger black celaphines show more dietary In nosaurianmany clades of Neogene African Scleromochlus. Powell for drafting the figures. Comparisons of sister taxa have allowed tests of the resource-use hypothesis (29). 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. In particular. Principal coordinate 1 Geographic and tectonic history has generated patterns of species diversity through time. 14. EJ Court Jester worldviews. Knoll. leaf-eating insects. J. Z.A. M. A much-studied manifestation of energy and temperature gradients is the latitudinal diversity gradient (LDG). through the introduction of herbivory. R. 275. Nat. Ecol. D. Paleobiology 34. and associated with particular climatic. Further. and there are more specialists in habitats that underwent recent environmental change (tropical rain forests and deserts). equivalent to tree growth after a random walk. Jablonski. their genersubject to environmental crises than arrowheads indicate alist relatives. 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. The standard view was that dinosaurs originated in the Late Triassic. Other splits in species trees may relate to dispersal events. 39. the majority of diversification shifts are unique to particular clades. T. Comparing Sister Taxa A powerful element of the comparative phylogenetic approach to species diversity through time is the opportunity to compare sister taxa. 2. and Boreoeutheria in the northern hemisphere. namely the greater diversity of life in the tropics than in temperate or polar regions. and each of those is long lived. phytosaurs. generalist diet. In the future. The former is now highly speciose. M. Sci. G. that is. Ruta. N. Wills. Phylogenetic through time Fig. 6. marine animals have shown several step increases in tiering. crosses. Brusatte. Ecology 82. 24. Cronin. 124. Res. D. 3). Geobios 32.. the identification of diversification shifts across numerous taxa may provide evidence for the relative importance of the Red Queen and Court Jester worldviews. and yet it is not clear how higher-level patterns relate to those at species level. for example. and so tropical clades have had longer to speciate. Rhaetian. the impala Aepyceros. 9. when flowering plants. 20. Outlook Paleontologists and evolutionary ecologists have debated species diversity largely independently.approach to species diversity relationships and moris the opportunity to compare sister taxa. This is hard to document because of the number of other factors that vary between ecosystems through time. B. dinosaurs. Palaeontology 50. Purvis. Purvis. dinosaurs did not participate in the Cretaceous Terrestrial Revolution. Evol. M. Bambach. 31. and each probably more subject to environmental crises than their generalist relatives. M. Benton.sciencemag. Lad. Bofarull et al.A. Adamowicz. where one clade replaces another. Viewed close up. 418 (1993). Rh.08 0 0. 169 (2008). The ecological habits of both clades differ: The impala has a broad. Roy. Jablonski. Sci. phytosaurs. patterns. and a comparative study of crustaceans shows. U. Many key questions can be tackled by comparing a real tree to a hypothetical tree that follows an equal-rate Markov (ERM) model. and diversification shifts may be concentrated low (dinosaurs and bats) or high (insects and ants) in a clade (26). 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. Rev. al. generalist diet. poposauovals. after it had been vacated.3 Crurotarsan morphospace -0. Dinosauria remained at moderate diversity and low disparity.S. Payne. and for Triassic archosaurs. 105. crocodylomorphs. Paleobiology 33. some 230 Ma. H. and diversification shifts may be concentrated low (dinosaurs and bats) or high (insects and ants) in a clade (26). G. whereas the speciose Alcelaphini consists roids. Proc. Acad. Soc.06 -0. social insects. J.16 0.specialization. 1485 (2008). In wider studies of many clades of Neogene African and South American mammals (30). and each of those issquares. U. The slowly evolving Aepycerotini consists of few species at any time. morphological complexity may be quantified. Supported by the Natural Environment Research Council and the Royal Society. and then finally gave way in the Cretaceous to the superior mammals. has increased in several steps through time. 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. 104. Carnian. EJ. R. then the Court Jester model of macroevolution would prevail. P. 13. Hunt. Sepkoski Jr. but from further away. each occupied by a species. Thanks to S. G. tectonic. Nat. S. because of superior adaptations. 3. Valentine. Soc. Annu. carnivores include more generalists than herbivores. whereas the speciose Alcelaphini consists of many short-lived species. Taxic studies in paleontology continue to have great value in highlighting correlations between species richness and other factors. 246 (1984). Sisters phospace occupation so their traarose from a single ancestor. C. A classic example of vicariance is the fundamental division of placental mammals into three clades. drove a major radiation of Foraminifera. London B. 28. Emerson. Alroy et al. larger black dots. U. and many other modern groups radiated substantially. Sisters arose from a single ancestor. S. Am. Unique terrestrial faunas and floras. Ruta. 2483 (2008). and associated with particular climatic. 102 (2006). 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. More widely. J. 23 (2007). Thierstein. G.18 -0. gray before the their separate histories. 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. 10. although relationships between species diversity and productivity change with spatial scale (19). Analogous. G. If the majority of diversification shifts are coordinated. K. S. If. Benton. ovals. Mittelbach et al. 887 (1984). The realization that the Red Queen and Court Jester models may be scale-dependent. broad. Sci. Early subgroups. J. the resource-use hypothesis was supported. or there may be no geographic component at all. Specialists divide physical environment Carnian-Norian events. Gittleman. The former is morphospace for Late speciose. In the future. or recoveries after mass extinctions. J. H. K. notably those of Australia and South America.” had long been abandoned. Valentine.9 237 232. 99. References and Notes 1. vertical dashed lines denote two extinction events. 301 (2008). P. that the tropical belt is older and larger than temperate and polar zones. and they started with the same genotype and phenotype. Geol. Roy. 4786 (2008). C. and some subsidiary predictions confirmed: Specialists are more common than generalists. 47 (2008). nondinosaurian dinosauromorphs. The other mode of species increase globally or regionally is by niche subdivision. Paleobiology 10. 293A.S. squamates. (21). 21. (A) Framework phylogeny for Triassic crurotarsans scaled to the Triassic time scale.24 0. R. K. Benton. 30. 11. 8. J. BMC Evol. Based on (28). J. Jenkins. Jablonski. T. The species richness–energy relationship (18) posits correlations with evapotranspiration. 10. A. and so their trajectories occupy the same amount of time.6 Anisian Lad Crn Norian PTEROSAURIA Rh.. 211 (2001). 600 (2005). Sci. and not coordinated temporally with others. whereas the speciose dots. 18. if even more dramatic. Specialists divide the physical environment into small patches. 6854 (2002). Am. or increasing specialization. Theory 1. from the water-margin plants and arthropods of the early Paleozoic to the forests Phylogenetic Studies of Clade Histories Species are not randomly distributed. 22. they have an evolutionary history. that survived the latter event. Species richness through time may correlate with energy. Natl. D. and intelligence among vertebrates. the majority of diversification shifts are unique to particular clades. during the 25 My between the events. 8. Bollmann. Schmidt. 27. In paleontology. A. dinosaurs did not participate in the Cretaceous Terrestrial Revolution. There are two explanations (22): (i) the time and area hypothesis. squares. with numerous stepwise additions of new habitats. Proc. M.For example. broad ecological groupings of organisms with shared habits. carnivores include more generalists than herbivores. 15.6 199.

Any process result. larly of morphological traits but alsoeither eco. Environ. the study of From this point under the muand intrinsic hybrid inviability as well as extrin. Valentine. 1B) is likely to be mutation-order a while (7). in when tory. the speciation by polyploidy. is defined as a stage of the evolupostzygot producing at which physiological isolatdivergent selection are extrinsic and can include tionary process Dobzhansky-Muller incom. Schluter. as one arbitrarily best documented by instances of reproductive isolation resulting from intragenomic conflict. It predicts that ecological speciation if ecologically based diver. laboratory trials. Voyage 57. In those reproductive isoecology does not favor divergence as such. to different environments tween Drosophila species. D. Div of large fish is scarce or seasonal” (12). Ecology 87. at the to be the define mutation-order speciation as the habitat.ing bluehead in in the Bahamas has evolved a largerin their (16). Additional scenarios successful in identifying major genes implicated We now know of many real species that have. although it was tested onlygenerationsisolation by the fixation of than afterward. divergence experimental alleles.wrote Clarke (10). (1). abiotic and biotic factors such as food resources. J. Funct. but the study of speciation after the pubthat most of them do. but is defined as the evolution ofinstances when sterility. 7). In On the Origin of Species.. it was greater be. Marshall. Genetics 128. The chastic bu of reproductive isolation between populations is unlikely to figure fromby which mechanism key is to result out chance. tory.prevailed.sciencemag. C. B.. The basic idea has been around for homo.study showcased instances in which derived morevolution of reproductive isolation between pop. C. which drives to a chance individuals closely resembling each link between speciation and natural selection. Space. andevolution of reproductive isolation by came withthis Darwinian perspective. D.ductive extensive than morphology. this speciation by experimental and conceptual ad.. Ecological speciation can lead to the ing). nature is unknown. ecologically based pre. lacks the restorer. mutation-order spe. K. forms.. competition. and (iii) actions such as disease. S. Nature 368. Diver. H. The not acquire the same mutations or fix them in the although it is easiest when gene flow ing a47). divergence occurs when B. view. Male-fertile mutation-order speciation. Forde. and how do changes at these genes yield stronger premating The relative isolation once tions. as Darwin initially claimed. to a definition9). Skulason. with undevelopedhave M..in hybrids between specie In not between populations Laboratory experimentsaccordance with (10). 475 (2002).Annu. Subsequently. Step (iii) has been challenging undermutation-order spe of evolution by natural of reproductive mutation-order speciation. Supported by and life 59. aaspecial whether I 291 (2003). 62. its contributions uncertain under the between populations or subsets of a alleles. Evol.credit: on the left also but the process is distinct from genetic drift. The two most general flowerAndrea Case (47)] has the nuclear restorer. also ignore Dolph Schluter (2–5). 65. Speciation by sexual sexual isolation (ds2) beductive isolation. Danley. However. N. Jablonski. J. “that mystery of other such groups” (7).. 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. D. we still have not identified all aspects of selection. competition. Jablonski. Lhr. the cies? As a start. Under this the biological species concept took evolutionary biologists nearly 150 years. must have In this review. sterility (F Speciation species were defined as terference. Cambridge. guttatusnuclear restorer are theore flower on the related species (M. Brede.phenotypic traits werepopulations. 1947). and ofbecause gene flow. facilitates subsequent isola. inhabitbetween speciation and natural selection.natural “physiological” is interpretedAmerican selection. 6 FEBRUARY 2009 VOL 323 SCIENCE www. the mosquito fish.generally greater difficulty of studying concept and other incompatibilities different alleles be. D.tions to warrant their Iclassificationspeciation by as separate isolation has “As a result of our recent studies mysteries” (1). selection thought to Philos.and mutation-order. 14). 8. divergence of mate preferences. the set of occurrence and fixation of different speciation with adaptation was relatively straightdifferences (6. S. The lation. butas food on re. species were deand thabitat. only data same order. Vancouver. R334 (2006). Biogeogr. hybrid first evolved (3). speciationunder mutation-order speciation. nasutus) whereas the one on and a closelyleft also has the nuclear restorer.streams.. 9.org SCIENCE VOL 323 6 FEBRUARY 2009 737 27 . Nature 408. including a revision of the driven by divergent naturaladvantageous in one environment lution of species differences. really does occur by means of natural selection ulations or subsets of a single population by ad. trait-based assortative nisms. 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. and identifying the underlying that of natural selection. each advanta. lacks the restormechanism hypotheses involving selection are ecological and infinite) populations. Losos.logical and mutation-order mechanisms. 109 (1996). Nature 435. D. and intrinsic hybrid inviability as well as ences have accumulated b speciation. 366 different mutations arise and (grant DEB-0519777) and the NIH (grant GM56693). Joyce et al. pre54. Cambridge. arise and Appreciation of the connection between studies The point speciation adaptaof Originin separate populations 80 years after by C. (A) Example of ecological speciation. J. D. have isolation rather different advantaSpeciation agents of genetic selection are consistent geous phenotypic speciation because. each other. by chance. Price. Doebeli. The relative importance of speciation symposium [the last major symposium occurrence and fixation of that are the reproduc. linking reproductive isolation instead of morphological tion as the given for the sake of convenience Under it Darwinian to investigate any directions between environments. Evol. W. Schliewen. of whether arbitrarily that “I look at theonly become as one phenotypdeveloped” by bestlead to speciation? What are howmechanisms selection pressures. In contrast.Thedetected divergent divergence extrinsic and with the mutations in separate populations expe-themodels.phological and life history forms of fishes had because populations fix distinct mutations that between species (1). Div es the possibility that favorable mutaregion and smaller head in the presence of predators (top) tive isolation by the fixation of different advan. Fryer. (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. Todd Streelman.. each advantageous of species largely lution of species differences.with Streelman. tragenomi “physiological” is interpreted to mean evolved climate. Nature 426. J. 51. E.cases.ca conceptual ad. hybrid sterility.the chance occurrence andby which ofallopatric speciation separation is definedrelatively straightvailed. 11). 7). cally based pre. Vancouver.similar under divergent selection. Glor. Progress up toalleles. P. Reproductive isolation evolves ic differences between species were caused by Followingselection. [Photo The topic of natural selection in speciation is once 47). selection here because natural selection drives the type of reproductive isolation (3). Whittaker.have made itflow. O. 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. al scenario many from pursuing the connection. 50. J. U. Under this but at last we last we can agree with that the speciation. physiological. by c evolution of any type of reproductive isolation. 383.Dobzhansky (13) suggested that the genes under. I summarize progress barriers study showcased instances in which the connecmany ways by Reproductive isolation arise by tion pressures. features study of speciation tion.can be rapid under both mutationcause. such repetition of flow. Ecological 1Z4. by chance.theories of the process (8. to still have not identified all aspects selection. ries: ecological speciation and mutation-order rankedI as species or factors. (A) Example of ecological speciation. 629 (1994).. 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)].. Sims. that “I look define term species.these two categories of mechanism for the ignore on speciation before or varieties” (1). evenspeciation symposium be crucial 64. Lack. and behav. The ative imp Experiments with laboratory popu. ecologically based pre. 10. order speciation is difficult must there independently. Syst. given forof the processconvenience to aout distheories the sake of (8.Pääbo. S. behavioral. each selection between environments. Origin of G. but the evidence suggests that most of niches (2. in the study of speciation after the pubCanada. reproduc. Ecological speciation importancethe view. Webb.be advantageous in boththe basis of reproductive isolation. 434 56. reproductive importance of speciationin settling whether two forms should be criterion symposium [the last major the other incompatibilities that are the chemical. taxonomic species. The relative refers to of unlikelyselection defined to favor stronger preoriginthe species. Darwin understoodbe crucial polyploidy. Fishes 45. T. Mahler.once postzygotic mating by natural selection. ries: ecological speciation and mutation-order ranked as species physiological. Darwin un. London. 80 years after publication of On but not in the other. and only data can in the way order. I leave set of However. environmental years. Subsequently. 21.two broad categories: ecologicalC.independently. S. producing Dobzhansky-M populations adapting to contrasting environments preferences. selection between environments. in hybrid inviability (Hmr. Virtually no F2 hybrids between mutation-order mechanism. Iand mutation-order. R. for example by sensory drive (15). epistasis. selection fall into 847 (2000). W. the The main question today is how does selec. evolved by divergent natural seare elaborated in (5). J. A. 33. J. I at the mutation-order as one other phenotypic traits. 9). Clarke (10). at the isolation 63. on the Boogle (Collier. traits but also of behavioral and speciation itself. Donoghue.org SCIENCE VOL 323 6 FEBRUARY 2009 737 The biological species concept must surely vironmentsof the Species.speciation and adaptation in the early forgotten. The repeated. 1.tion as separate taxonomic species. al. Under36.referring to the origin of morphological species. 58. R. (7)].and postzygotic iso. whereas the key is to can occur in both small and large (though not lations of Drosophila and yeast dem. evolve by selection. Harmon. there isJ.(Odsh. forms should be mutation-order speciation when there is gene tttook evolutionary biologists nearly 150 years. Ackerly. mutation-order process. what genes are affected. ignore reinforcement. The approach has been hugely reproductive isolation [reviewed in (2. Trends Ecol.there is populations fix distinct mutationsgenes (here. body from than when they were from the same predaperiencing similar selection pressures. two other learn tions occurring in populations in ordinary absence (bottom) (29).one on the right. Syst. parallel origin of nonparasitic lamprey vailed. might be favored in one population gence as s and not the other because of epistatic ulations adapting to similar environments. Both flowers shown have M. M.. 47. S.reason.under the rigid Natural The effort leading up to this conclusion acting in contrasting directions between environthem do. tation-order process. ecological speciation. Hence. or without gene flow. It lation between populations by postmating re. and the anonymous 49. It again receiving attention. S. “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). When corlogical speciation is defined as the evolution related with environmental factors.understanding the link between morphological mutation-o population. its contributions uncertain under the new concept.sufficiently many differences between populaorigin of species. 9. Schwilk.selection commonly drives the origin of species. Newthe bio46. Divergence is therefore stochastic Models of Speciation by Selection is absent. single population by adaptation to different en. Adaptive Appreciation of the connection between adaptaare fixed in separate populations adapting to similar60. Whalley. Trans. Darwin new concept.under the rigid control of by either process. (Academic Press. speciaral selection is divergent. by divergent natural selection arising from dif. The a of reproductive isolation. subsequen measurable pre. D. the same alleles present. J. 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.phologicalwarrant their classification as separate (1). the same alleles greater difficulty of studying reproductivediver. M. H.standing the general but the of speciation by se. pp. 8. Mani and B. parallel Progress nonBiodiversity but the evidence suggests that most of and mutation-order leading up to this conclusion Appreciation mate directions between environ. mechanical. would be favored Two approaches investigate can lead would Speciation by sexual selection is mutation-order ioral interference. mechanical. Seehausen et al. 45.org 738 populations. 41. D. 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. an Oregon population of monkey flowers (M. I because populations fix distinct mutations that natural selection. many ways by which barriers betweenmysteries” mightthis crucial insummarize progress in under. P. I also the Advancement by (2007).” and “The amount of difference similar Dobzhansky (13) only a test of whethergenes unfixation of different alleles.B Mimulus Specia ing patibilities in hybrids between species mechanisms become developed” (6) (here.. Virtually no research effort followed that lection. 43.reproductive isolation (3). Nup96). in the early stages.and divergent natural can lead to the evolution of any type of repro.. 90 (2005). very important criterion in settling whether two derlying differences between populations in ortion lead one environment but not mechanisms selection pressures. provided that flict such as meiotic drive or cytoplasmic male environments.case is onlyand Adaptation origin of morphoecological speciation. H. For example. Repeatedly and fixation o for example by sensory drive (15). Tautz. P. 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. but the evidence suggests derstanding the general features of speciation thethe early that speciation is.divergence of of the preferences. their environments.on fishes.ments. For example. I define mutation-order speciaare fixed of of speciation itself. even though selection might the imIn this review. is the cultural equivalent of the at selected loci. including that (10).different alleles are favored between populations the mutation-order proces unlikely to be the same in separate populations. caused reproductive 2805 (2008).. this case is only contrasting environments but not between pop.discouraged many from pursuing derived morselection can be grouped into two broad catego. D. as by sexual conflict (16). vergence lection drives divergence of mating preferences. based on B. habitat.. (bottom) (29). C. Under do not differentiate speciation control of the environment” (12). mechanical. ecologi.with the modern conceptgenetic background interactions with of speciation “Species ductive iso tion of eco though it was tested only recently.in both the same i speciation was the study of the evolution of sic. selection pressures. Harrison. E. 715 (2008). 52. 977 (2008). Birand. Nature 455. because alleles ar approach involves identifying (i) include abiotic and biotic factors such effects riencing traits selection pressures. and (iii) identifying the phenotype Evidence for ecological speciation has accumumolded by selection for efficient signal trans.selection arising isolation evolved. particu. 620 (2008). Darwin wrote in streams from the same migratory.evolved. 21).of reproductive isolation evolving under the [Photo credit: tion than morphology. Eds. London Ser. advances. D. Evolution 54. the Origin or ecological niches (2. 356 (2004). what genes habitat. differenceshave demonstrated that ecological in. really does occur by means of natural selection ulations or general features of speciation by ad. where a suitable food supply determine plausible. Graham. C. 9)]. Speciation resulting from intragenomic con. to mating. 53. 201–226. are life in small mutations ecological and mutation-order speciation. vances. 1983).” but for reproductive isolation remains challenging. ciation is defined as the evolution of reproduc. Not all species appear to evolve by aptation to different environments or ecological taxonomic species. Garant. 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. the populations do adaptation in speciation. Natural selection is divergent.between populations of mechanism forclassifica. adapting to similar either ecological Tests of parallel evolution the the notionthe Species. straightforward. would be favored in every lation. A. U.then but lamprey in streams from the same migraUniversity of British Columbia.logical environments (2. such repetition their relative importance in nature. He later changed how do changes at these genes yield the evolu.were from opposite predation environments. Tautz. and other species? As a start. The effort leading up to by selection. 443 (1991).correlated resembling eachspeciationand cussion of closely with allopatric other. phenotypic differences between stronger were natural Schwenk. For example. divergence is driven by divergent(2005). linking R. T. Selection can be ecologi. postzygotic isolation has evolved. W. Press. 8. but at can agree with Darwin Darwin their environments. Not all species appear to selection. 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.parasitic of Speciation by from the same migraUniversity of British Columbia.. S.is defined as the evolution of reproductive reproductive or mutati on various microbes maintained under ciation fixation occurred before complete either ecological sterility (Fig.parasiticunderstanding the link between morphoacting in contrasting connection by either ecothem do. D. I ignore reinforcement.sciencemag.these genes reproductive isolation should evolve between gent selection drives divergence of mating background (10). with undeveloped anthers. Time and 44. A. productive isolation have not been explored. S50 (2006). I of reproductive isolation. adaptation Kocheer. For this reason. Hendry. 11). 35. the Both flowers shown anthers. Schemske.. D. D. Ladle. chemical.ubc. T. Research Centre and Zoology portance The repeated. JYAlpha). which new species might evolves derstood the importance of reproductivein under.but conditions (20. 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. I leave out discussion of sympatric and allopatric speciation but SPECIALSECTION Under this Darwinian of ecological and instead identify the likelihoodperspective. cial type of natural selection thought both of evolved reproductive isolation between populafor do changes these genes yield the are afhowreproductive atselection.Tests of parallel evolution history forms of fishes had arisen over and over selection pressures. in most The topic of natural selection thatspeciation is REVIEW Speciation Evidence for Ecological Speciation and Its Alternative I I Evidence for Ecological Speciation and Its Alternative I way becau Both models of have evolved into nononce again receiving attention. and interspecies interactions reproductive result from eitherpopulations. speciation is thought as the accumulation of natural to result from chance. and theincluding tion environment (and similar body shape)(29)].having neither (46. parallel origin of nonBiodiversity Research Centre and Zoology Department. Darwin understood evoluinto two broad categories: ecological Department. E-mail: schluter@zoology. speciation comparative and are the reproductive new species might arise by new spelations that are reproductively isolated from In be review. smaller holes the presence of predators (top) than caudal ulations.” and at the individuals closely resembling nisms of natural isolation remains challenging. right. American Association for ignore speciation of isolation has evolved. Dieckman. guttatus) hav. Annu.these two categories to warrant their the origin on speciation before the biological species reprotive barriers between new species? As a start. guttatus cytoplasm. the (2000). B. Biol.weight is constantly being added to the have accumulated between populations mutationshould evolve between populations adapting to theory that speciation is. R. selection’s role (3). (left)Example of reproductiveflowers of mutation-o mechanism.alleles between populations adapting to is one forward. 8. Hered. their environments.lying differences between one population will than in their absence In laboratory trials.1126/science. R. BC V6T spe. Metz.isolation. B. must have discouraged Brian Langerhans (29)]. mating. The The turning point for speciation studies came evolution basic idea has been around for a while (7). BC V6T 1Z4. C. Whereas those traits tions causing drive and those countering it are can mutation-order process (22). Price. divergence not in the other. whereas under mutation-order speciation.extrinsic. and behavioral in. Ecol. selection here because natural selection drives the on the evolution of species differences. J.sciencemag. “As aearliest genetic differences can be ec 8. Bradshaw. that tested speciation guttatus) having a cytoplasmic flowers of element and nuclear Both anyway because.of species. physiological. Ecol. 48. 519 Speciation and Adaptation from L. can isolation between ecological or otic drive such as disease. 18. Smith. The agents of separationHence. Ecological speciation isolation. gene mutation-order speciation when was relatively 61. Most of because of epistatic inte tween lines subjected 14). T. L.approaches but is needed to understand how sealternative advantageous mutations in different ping of reproductive isolation between closely lection has led to reproductive isolation. Evolution 60. Press. at least was largely stages of cal speciation if ecologically based divergent se. 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. sterility at least in part. [Photo credit: Brian Langerhans than when they different alleles are favored between populations but ing in time this viewpoint. Dolph Schluter Science 1939 though selection might [the last polyploidy. chemical. really does occur by means of gin of species in nature is unknown. (1995). T. A. T. as distinct from geographical symposium behavioral. We thank A. 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.other. for the sake of convenience to mean However.In On the Originat Species. special type is took evolutionary biologists nearly 150 would nevertheless be advantageous in both of with environmental varieties”a (1). nasutus) having neither (46. inhabiting In accordance with (10). acting in contrasting arbitrarily evolution of reproductive isolation by have made thismore difficultperspective. Gillespie. 2311 (2006). an isolation comparative and biogeographic tween populations adapting to similar selec. the same then in Speciation if present. with the exception of ecologi. adapting to similar proving natural mutation-order spe. habitat.ca ioral and other phenotypic mechanisms. major symposium of speciation before York. what genes are affected. G. mutationThe biological species concept when surely Fig. requiring suggested that the phenotypgeous in to speciation? What are thein the other.sufficiently many differences betweenthe cause of origin “that mystery of mysteries” these two categories of isolation between ori. Rev. J. ignore reinforcement. O. origin of up to speciation to Dobzhansky Natural selection is divergent. He later changed his mind. Darwin’s Finches (Cambridge Univ. The top-down can be rapid geneous conditions for many recently. credit: Andrea Case (47)] cally based under mutation-order speciation. the many ways broad categoselection can be grouped into twoby which new standing thesubsets of a single population by se.1157966 (2003). 11). C. an extensive comspeciation by D. Natural selection commonly drives 2166 origin of species.or mutation-order mecha. Mechanisms of 1909). J. E. However. in Evolution.ecological and from intragenomic conflict. Streit. logical species. Reproductive isolation evolves isolating mechanisms documented by today is the does selec. 18). Rev. tion (12). Ecol. 176 Speciation (Cambridge Univ. Mechanisms of (1). Seehausen. speciation J. requiring only test of type of flow. would nevertheless be advantageous in to favor Association forof difference is one very important “The amount the Advancement of Science 1939 barriers to fected. A. (B) Example efficient s under ecological speciation.other andturning traits. Lande. as Darwin initially claimed. I summarize progress in un. It predicts that reproductive isolation fishes. Repeatedly and gamete re divergence. in reproductive isolation by active reproductive of On the instead of the Species.on. J.and postzygotic either process.under ecological speciation. not selection.and source of fitness effects of alternative alleles lated from top-down studies of adaptation and mission (5). parasitic ancestor showed in “Again and Canada. the initial muta. including a revision tion drives the divergence of mate preferences. E-mail: schluter@zoology. of speciation. “that mystery of evolution of reproductivemechanism for thepop. parasitic arise. Triantis. Divergence occurs research effort followed ecological the role of (left) and male-sterile (right)male sterility F2 hybrids between (19). Whereas reproductive isolation.and postzygotic isolation. but at the time this viewpoint. [Photoincluding premating isolation. “groups of interbreeding natural populations that speciation models. Eco. 9). between adap. C. Clarke (10). speciation. Mani and morphological www. natural Darwin in which derived morphologicalthe NSF stances to Dobzhansky reviewers for useful comments. J. O. Evolution 62. logical species concept (7)]. the of species in nature is unknown. Speciation by sexual selection is ecologi. Under this view.weight is constantly being added to natural selection (2–5). 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. generally environments. 42.related species. and identifying the underlying genes sitic lampreys have evolved into nonparasitic REVIEW individuals sympatric and life in small streams. Curr. environmental from gene reproductive isolation first evolved (3). J. Crespi. D. Science 303. particularly of vances. From this point on. 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).correlated with theoretically cal and mutation-order.type (12). Parent. by of behav. the mosquitoevolved a larger caudal region and geous mu is gene more difficult to investigate any link blue holes in the Bahamas has fish. K. selection. are driven to fixation by natural selection countering groups” (7). 2004).ecologica can proceed with restorer and a closely related species (M. D.mutation-orderthe plausibility of ecological er. and interspecies inter.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. Following G. associated with reproductive isolation. and forms should be ranked as species or varieties” dinary phenotypic traits were unlikely American of natural G. p. and reproductive isolation by active 10. not m at the low levels of gene flow. I also origin interbreeding). Fig. A.. In On the FollowingSpecies. Coyne. parative and biogeographic study showcased inD Jablonski.Models lamprey in streams Selection logical or mutation-order traits.physiological arise. e than between lines raised under homogeneous show molecular signatures of positive selection. Gambusia hubbsi. Trends Ecol.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. Webb.of reproductive barriers between species niches (2. 1. (ii) natural selection in both resources. subsequent mutations ecology d the environment” (12).were shape) different populations having opposite predation tion. Divergence occurs any..selection pressures must therefore be populamating reproductive isolation once postzygotic that (1). K. M. and selection is favored in one populatio productive from differences between eco. However. Evidence for mutation-order (6. C. 126 (2003). because gene flow increas. 66.. cytoplasmic male sterility element and cytoplasm. Darwin. I the early stages. both gamete recognition occurs by the fixation of bottom-up approach involves (i) genetic map. Ackerly. Albertson. Gambusia hubbsi. Biol.94. 8. 26 www. to a definition based on B.distinct from geographical barriers to interbreedmutation-order speciation. and the behavioral. (1).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. 16. Wiens. B 363. R. R. The effort speciation. because alleles are tions cau reproductively isolated from other such including premating isolation. 7). R. trait-based assortative morphological concept of species largely preselection have demonstrated that ecological speciation is a common means by which new species peated. tion and speciation began with Darwin whenreagain from the same ancestral type (12). a spe. D. portance of reproductive barriers between species in theory stages. The two most again the parasitic lampreysspeciation. 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. In the probability of the individuals mating was higher when they were from different tageous mutations in separate populations ex. Once the onstrate speciation. an extensiveis defined as the accumulation of barriers between new incompatibilities the speciation. McPeek.A Gambusia ulations d general hypotheses involving selection are parasitic forms.ubc. A.alleles betweeninstead identify the likelihood of evolutionary process a testwhich The morphological differences does requiring term species. climate. Natu. mutation-order is the cul selection.favor species Soc. 55. selec. as (3).

8. 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. Nosil. 17. 42. thus the process leads to divergence. 29. How and Why Species Multiply: The Radiation of Darwin’s Finches (Princeton Univ. Hered. and it also constitutes direct reproductive isolation because it is an evolved barrier to gene flow between parental populations. S. Willis.indicates that hybrids had higher fitness than the parental species competition. Ecol. C. 6527 (2005). 31)]. M. Trends Ecol. 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). Proc. Schluter. 103 (2007). Soc. pollen ypic dif. 20. s when components include intrinsic hybrid inviability. if built by selection and not genetic drift. B Biol. R. Joseph. J. 176 (2003). he would most likely be staggered by the discoveries of genes and molecular evolution and astonished at the prospect that evolutionary conflict C. Trends Ecol. compared l perenDivergent selection components include those attributable to under divergent selection between environidentifiable Divergent selection s of the active selection causes (bottom). Borland. Whitlock. of mutation-order divergence. In these studies. Rogers. N. 31) (table S1). R. Evol. Ecol. Swapping alleles of this QTL between the species with repeated backcrossing resulted in shifts in pollinator preference and. Sci. These examples indicate a growing knowledge of the mechanisms of selection and its consequences for reproductive isolation. Anderson. 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. 3009 (2008). 1372 (2006).A. 37.8 1 migrant in insects. London Ser. Funk. C. Ecol. E.1126/science. J. 336 (2005). C.4 0. The connections between selection on ordinary phenotypic traits and reproductive isolation are often strong and straightforward. 330 (2001). B. 363. Nagel. J. Nature 447. 34. D. K. Grant. 25. The Ecology of Adaptive Radiation (Oxford Univ. H. separate components may not be independent. We have strong signatures of positive selection at genes for reproductive isolation without enough knowledge of the mechanisms of selection behind them. H.S. B Biol. The unattributed components hybrid fecundity. M. It is unclear how much reproductive isolation typically evolves by ecologically based divergent selection in nature. 435 (2005). W. 41. One example. D. P. H. J. 336 (2008). L. Wu. Am. L. Sexual conflict is also expected to lead to mutation-order speciation. CO. 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). 2008). and to trait-based assortative postzygotic isolation) and breeding time). Evolution 60. Evolution 62. 15. 102. A. L. Lett. H. Sci. J. Egan. Rundle. Hostert. It may be that the mutation-order process is more difficult to detect. and a reviewer for assistance and comments. G. 2008). Mol. Schemske. Rieseberg. 198 (1940). Schluter. S. London Ser. Between 1859 and the present.1160006 28 29 . 146. 267. L. Coyne. uttatus) postzygotic isolation) and to trait-based assortative mating (habitat selection on and extrinsic Ecologically based divergent selection North preference. If he were here to witness. Via. 2. perhaps indicating genomic regions under divergent selection. the general acceptance of the biological species concept altered the focus of speciation studies. that hybrids had higher fitness than the parental species [extrinsic postzygotic isolation (33)]. Evolution 57. is also prematComponents – divergent selection plants (28). 68 (2007). H. M. Estimates the magnitude of reproductive isolation specific phenotypic floral traits. 30. H. Distorter and restorer mutations are unlikely to be the same in different populations regardless of environment. The unidentified component of speciation. 41). R. compared isolation resulting from divergent selection components 3)]. 43). W. J. compilation of the data shows that the amount of reproductive isolation attributable to active selection and traitbased assortative mating is at least as strong. J. Evol. This is really what On the Origin of Species was all about. Mol. 1637 (1993). 312 (1940). multiple origins are supported in several examples of parallel speciation. The mismatch between the distorter in one population and the restorer in the other can result in hybrid sterility or inviability and. J. as the amount from components of reproductive isolation lacking identifiable causes (Fig. partial reproductive isolation generated by meiotic drive has been identified in Drosophila [reviewed in (3. 30. S.66 was Number of studies lection between environments. Multiple traits are probably involved.S. Evolution 62. 5. such as those observed in cytoplasmic male sterility of plants. Sirjusingh. 1423 (2007). The most obvious shortcoming of our current understanding of speciation is that the threads connecting genes and selection are still few. 151 (2003). 98. W. Philos. Gifford. Princeton. Evolution 55. A. Barton. B. Sci. S125 (1992). Littorina marine snail ecotypes n which rentially inhabiting different zones of the intertidal 15 basis of (24). Langerhans. 1A). Via. Evol. Whitlock. B Biol. Blount. Sci. R. W. Martin. A. 45. One line of evidence comes from tests of parallel speciation. 36. Evolution 47. 32)] Cumulative reproductive isolation beak size in birds. Proc. Rieseberg. B. D. 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). R. Beaumont. whereby greater reproductive isolation repeatedly evolves between independent populations adapting to contrasting environments than between independent populations adapting to similar environments (20. Am. T. Bradshaw. 1026 (2008). 11. However.y to mate if they are of nents of reproductive isolation lacking identifiable less of relatedness as causes (Fig. including flowering time and tolerance of salt and drought. Lowry. Masly. Modliszewski. or other incompatibilities must arise that interact with these genes to prevent their spread after secondary contact. C. Nat. S. and mosquito fish inhabiting blue e under 10 holes with and without fish predators in the nt selecBahamas (29) (Fig. for these mechanisms to contribute to speciation. T. The contribution by these mechanisms to speciation is still uncertain. E. P. T. N. Z. the most glaring deficiency is our knowledge of the impact of selection on genes. West. 6 value of –2. 16. These scans compare allelic variation within and between populations at many marker loci spaced throughout the genome (37). P. E. Levin.. which may strengthen the barrier to gene flow (20). sets of genes that diverged under a mutation-order process can produce the same pattern (17. 26). places selection on mutations in other genes that counter the selfish element’s effects and restore more equal genetic representation in gametes. For for at least one component of postzygotic isolation. Nature 426. hence. Science 287. 910 (2007). We can approximate an answer from estimates of the combined contribution of active selection on traits and trait-based assortative mating.. U. 19. C. Examples 0 he enviinclude assortative mating by host choice -0. Markers that show excessive differentiation between populations (outliers) may indicate selection on nearby genes. paradoxus) mapped strongly to a QTL identified as the salt tolerance gene CDPK3 (36). I expect that he would be chuffed by mounting evidence for the role of natural selection on phenotypic traits in the origin of species. Hubbs. M. 292 (1995). L. 381 (2001). 40). D. Noor. body size and coloration in fish. J. Trends Ecol. Lenski. Darwin. petiolaris transplanted to the salt marsh habitat of their hybrid descendent species (H. We still do not know much about the selective factors causing mutation-order speciation. as shown mating (habitat preference. I expect that we will have that much more to celebrate. Another form of investigation involves the analysis of genome scans of ecologically different populations and species. 24). Components – unknown cause flowerEcological speciation is also supported 15 be under by examples of premating reproductive environ10 isolation in which individuals choose or 30. J. S. Nosil. 316 (2008). 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. 32. lewisii (35). H. S. H. C. Clarke. Presgraves. Funk. R. Mimulus cardinalis and M. B. 2056 (2007). Nat. McKinnon et al. McPhail. Science 317. G. active selection favors the evolution of ever-greater differences between populations. 16. S. 13. 9. D. These estimates are incomplete because individual studies may lack data on components of reproductive isolation. New York. 26. 5 (2003). 363. MA. Yet. and genetic elements conferring meiotic drive. personal communication (2008). 46. J. 28. 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. 2997 (2008). Galindo. In addition. regardless of relatedness as indicated notypic by phylogenetic affinity. 705 (2005). Soc. T. R. Curr. New Phytol. A. N. Lai. 1942). Examples include the yup QTL. H. reviewed in (31. M. thus. preferentially encounter mates on the basis vergent 5 directly of phenotypic traits that are under ecologiuced fitcally based divergent selection. Second. indirectly affected premating isolation. D. Arnegard. 225 (2004). This type of reproductive isolation is context-dependent and is weakened in intermediate environments. 139. A. and varia[extrinresulting from divergent selection components (top). 7. But we still know little about the genetics of ecological speciation. 31. H. M. 24. Kohn. K. Under both mechanisms. Willis. 372 (2001). 31. Hoekstra. 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). Barrett. tion in flowering time—traits inferred to be lacking identifiable causes lacking (top). 28. if built by selection and not genetic affinity. Bot. include intrinsic vironment of the other [immigrant inviabilA negative value hybrid inviability. 48. Press. For with other componentswith other components (bottom). H. Butlin. J. Nosil. Rogers. Biol. 294 (2004). J. T. L. H. D. M. Fishman. E. J. R. Ortiz-Barrientos. Schluter. This. 585 (2007). On the other hand.sciencemag. Proc.2 0 0. A. Turelli. Mol. A. between genes could generate reproductive isolation (45). 40. Nosil. 4. Heredity 57. 23). 6. 41)]. 14. Acad. L. This work was supported by grants from the Natural Sciences and Engineering Research Council of Canada and the Canada Foundation for Innovation. Syst. Trends Ecol. The method is particularly informative when applied to populations with ongoing hybridization. It follows that much of the genetic basis of reproductive isolation should involve ordinary genes that underlie differences in phenotypic traits. C. A negative value indicates ness of hybrids in the parental environments because of –2. 375 (2009). in turn. Am. Via. a mutation arises that can distort representation in gametes and spreads in a selfish manner. Bengtsson. 47. however. Supporting Online Material www. R125 (2007). 43.4 -0. but there are few compelling examples (3). even though such an element reduces overall fitness of the organism that bears it. A. L. 2). which affects flower color differences between the monkey flowers. E. S. 21. including the sympatric benthiclimnetic species pairs of threespine stickleback in young lakes of British Columbia (25. Grahame. 2. eliminating that component of reproductive isolation (43). L. 18). So many new model systems for speciation are being developed that the filling of major gaps is imminent. 12. D. Kondrashov. 18. Philos. Coyne. W. Dobzhansky. Z. M. 22. H. We thank M. Mani. P. Sci. We have many cases of ecological selection generating reproductive isolation with little knowledge of the genetic changes that allow it. Rieseberg. Rice et al. However. each of the coastal perennial and 739 VOL 323 dataFEBRUARY 2009 left out of the bottom panel. Orr. Press. R. Data were ity. B. floral of the against hybrids. Willis. Nat. Rundle.2 0. J. At this point. 74. E. 16. Willis. A. A. such as cytoplasmic male sterility in hermaphroditic plants (Fig. 2000). Proc. 35. A. 17. Taylor. R. P. London Ser. B Biol. Speciation (Sinauer Sunderland. J. M. 1B). M. 2. Endler. it ortative 5 was shown that males and females are more insects.A. D. 17. J. H. 18. 24. Nature 429. Acad. Trans. C. or perhaps we have not looked hard enough at species with only small ecological differences (5). D. 31)]. Evol. Hence. Nat. 74. 2 and table S1). References and Notes 1. 240. likely to mate if they are of the same ecoin fish. 4334 (2008). L. Soc. 161. Presgraves. pollen competition. if divergent populations come into secondary contact. Press. 32)] and by reduced fitutes di. Murray. Genetics and the Origin of Species (Columbia Univ. Bernatchez. Willis. 0 or preftype. 16. Phadnis. J. Price. H. Evolution 61. Willis. support these hypotheses (42. J. Case. 38. The unidentified component of speciation. sexual selection has also been directly measured. and reduced hybrid fecundity. H. 2). Am. O.for at least one component of postzygotic isolation. Nagel. Systematics and the Origin of Species (Columbia Univ. J. 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. D. and the strength of barriers between species may not be symmetric (34). 20. 39. 33. On the Origin of Species by Means of Natural Selection (J. Boughman. J. 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. R. Biol. Oxford. London. 2004). L. mple of Data were taken from (32. Vines.org/content/full/323/5915/737/ DC1 Tables S1 to S3 References 10. S. Wright. Dobzhansky. D. Barton. D. Natl. B. E. 8. R. H. 357 (1986). floraltraits (immigrant inviabilityThe unattributed isolation. on average. NJ. Evol. London Ser. 7899 (2008). 39. Nosil. S.6 -0. Orr. Nevertheless. Rieseberg. Evolution 59. D. the fitness of hybrids must be reduced to very low levels. But we hardly have time to complain. Schluter. 24.66 was left out of the bottom panel. One data value taken from (32. 29 (1990). Evolution 61. As genomic resources increase for more species. J. This is an example of active selection on phenotypic differences. Schluter. H. Sci. Additional references are available as supporting material on Science Online. 10. D. 27. Speciation in Birds (Roberts & Company. Lexer. Estimates of of the magnitude of reproductive Fig. sexual selection against hybrids. Press. 31) (table S1). P. New York. which makes analysis of such studies more difficult. reproductive isolation (3. 105. B. 23. 1859). O. P. D. 306 (2000). Z. Otto. A. D. N. could be the result of either ecological or mutation-order mechanisms. Rundle.6 0. inviability and extrinsic components on traits (immigrant include those attributable to active ments [see examples in (8. 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. U. pollinator preferences for ybrids in Fig. as compared with other forms of reproductive isolation (Fig. Optimistically. Mayr. By the time we reach the bicentennial of the greatest book ever written. Mostly. D. Dettman. Natl. C. L. Case. Trans. Survival and salt tolerance of second-generation hybrids between the sunflowers Helianthus annuus and H. D. the repeated origin of divergent marine and stream populations of threespine stickleback around the Northern Hemisphere (27). 3. Royal Soc. Trends Genet. Price. 198 (2001). 2375 (2000). 1937). P. andisolation. and breeding by reduced fitness of each ecotype in the enreduced time). Funk. 44. because outlier markers may identify points in the genome that resist the homogenizing influence of gene flow. Greenwood Village. Numerous examples of selfish elements. J. Grant. Rice.

V.0% for and Harvard University. a very interesting obserREVIEW Speciation lyt icu s r ua ia s i nu ge lo ri/ e ch The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity V.2% diversity. J. Thus.tion are defined as the same species (2. Mol.furtherTaxonomists that in the water fixed level of sequence divergence limitedonly about a human desire forcedthis pur. 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. taxa too similar to be distance between S. Cambridge. which showed repeated selective sweeps which the whole (4. 16. but environment.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. Massachusetts Institute of TechnolGenetic Clustering anismsspecies. T. 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M. 98. limitations and can.framework within which to conditions in cheof clusters related groups of bacteria can be eco. inspection of the clusterstodoes not tion to defined industry. ficulties. those Rogers.uk categories cannot easily be thus used variety of relatedness life. 2Department of Civil have all fueled the controversy of how one de. 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. pneumoniae to strains to species (e. C.2% the concatenated sequences offor S. p. Clusters associated with named species are evident. but environment. Hoekstra. S. and of taxonomic uncertainty more DNA work a reviewer for assistance and comments. The tree was built using concatenates of six housekeeping loci. One common measure of neutral cies. Habitats were defined using (rRNA) fueled have helped of how species. strains to species (e. pseudopneumoniae. 1A has beenS. J. The overall genetic pneumoniae genotypesmay be measuredimplies (2). 21). evolutionary cal difficulties.2 Brian G.ability of there are several sweeps to limit the based life forms. 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.Genetic Clustering ogy. shape. H. Whitlock. Willis.g. was supported recently same species (2. these theory.the ecotype model. Among Darwin commentedFig. the phylogenetic structure pseudopneumoniae reveals about our ignorance of how evolutionary More recently. J. This is clearly superimposed relatedness of isolates and observations by the differentiated populations was unsatisfactory. Cohan re. ization are defined as thedescribed organism of pneumoniae is aby grants from the Natural Sciences10). the details of the evolutionary forces or ecologi. To the right.org discern clustering 323 through that the use of a each other. fundamental than any For example. the There are striking a distinctive evolutionary forces form. This pseudo41. lack of studies also show that of vast a species of its own. 1 forces form. The limit the effective population rates than DNAthatWhat do thevariation wastell us about mech. Such cutoffs imply nonetheless corresponds to Engineering Research Council of Canada that Canada 42. clearly unsatisfactory. 176 (2003). Naturally. H. C.sciencemag. 4Broad Institute of MIT As an example. however. ecologically almost all genetic diversity in the population be monophyletic). Asterisk denotes that trees based on additional loci indicate that the placement of V. however. they colleagues (4. 1) (7). Crucially. 2). ranging Christophe Fraser. Habitats (colored dots) were estimated as differential distributions of groups of closely related strains among samples (size fractions enriched in different environmental resources). ity or inability to interbreed. fine-scale re. patterns among populations of closely related for exploring that diversity are only just becoming widespread. per se.of the ecologically characteristics convenience of taxonomists. rRNA se. rRNA sequences are too to call species. J. but such Thetraits and by their abil. them from close and up to Among cies are defined by Cambridge. D. coding regions or results in synonymous sub. 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. mitis(11). N. Case. the numbers of those niches but not in other niches. per se. E-mail: value is applicable to all groups of bacteria or variety of surfaces. To put this into context. H. evolutionary theory should be able to explain why species that the use of a fixed level of a species. H. speciation. Rieseberg. Thus. 1372 (2006). categories cannot easily help ordinary variety of microbial theories of resulting data may be interbreed. W. however. In this way put this into context. This by the relatedness of isolates (5. Vines. whereas others are conserved to resolve similar true classification 3. these homologous recombination—mean that we still do not understand what a bacterial species is. mitis. pneumoniae to 3. Department of cannot reliably assign a large collection of similar evolutionary housekeeping genes we these named ment. inspection ancestral population (13). Nosil. 1. and in 8 many cases are congruent perate coastal regions range from 108 to 109 (19). these data (12). H. morphological and be.005 Fig. ordalii orvegic us lg in o st ae is V. that this cutoff value is applicable to all groups www.. To specific niches cause selective sweeps within for classifying species. The overall genetic or break up S. oralis 0.Habitats and Ecological Thus.too similar tothe and zooplankton in the water column (13). 32. as of many to each natural regularly purge the population notable exception and splits into numerous closely low 20). where genes adapted to versity as is actually observed.clearly closelywhich level in randomly seindicatesThe distance betweengroups ofhierarchy Animal species are defined by their ecology one defines a have. pseudotance or same between S. 2A). p. D.observed scale resource partitioning shows the relationships among multiple populations coexisting many eukaryotic microbes). D. three implies cannot easily be applied to the Bacteria or Ar. How would one detect the magnitude between recent ecological radiation size and population of any size (true of most (Fig. panecida within V. one can population. and observations homologous pathogens constitutein thesedescriptor of of overall bacterial for S. J. Ecol. including organic particles lected S. Habitats were Niches and Ecotypes defined using measure of neutral diversity is the Niches and Ecotypes One common an empirical modeling approach. and medicine.Habitats and Ecological Differentiation of the 1PG. H. 198 (2001).values that place two bacterial isolates into the same or different species. Most of the (14–18). defined as the size To extend this model. This advantages they confer to specific genes.average logical and behavioral As an example. and (2007). Brian G. and this the differ. E-mail: c.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.Polz. The vation. much of it lected S.3.metagenomic studies (1). 103 33. and this diversity needs is a commensal bacteria S. MA 02139. taxa which use be distance between S. N. 5. Bernatchez. Recent MLSA studies.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. Evol. time (17. 1A shows classification evolutionary history of close microbes in quesand Harvard University. H. Instead. Rieseberg. A. ture of the ecologicallyevident in noncoding re. 35.clusters that characterizes a species. Willis. these data (12). 4Broad of life. of Price.1%) cutoff or descripshow that there is no universal is not merely a semantic question.org/cgi/content/full/323/5915/737/DC1 diversity observed within homologous house46. but differences inRNA distinguish them species to relatives. 336 (2008). genetic clusters and Environmental Engineering. Spratt. 24). what observe is predicted to be associated with adaptfromcensus population size (true of (13). Mol. 161. and the is the amount of and thus landscape. USA. However. Schemske. 20.process of adaptation to new homologous importance. Cambridge.bacterial diversity onto environmental resources cies arenew niches and changing environments. Nature 426. D. and techniques evolutionary importance. 2 Collegelineages.the same species.1126/science. 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). D. 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. practi. (2004). The exception is V. Trends Genet.sciencemag. Fig.selective constitute a candidate mechanism the types are coherent self-contained genemechalandscape. Orr.4 Martin F. always clearly revealas the same species pseudocombine genetic diversity and distinct ecology in an attempt to define species in a coherent and pneumoniae.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. and pose. Willis. traordinary variety of microbial P. This sequence different species. C.(rRNA) sequencing] have(1). J. samples. Hered.2A.005 Vibrio splendidus 0. Biol.in an attempt to bacterial speciesrevealed the extra. P. 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. The first proposed mechanism was makes reference to the neutral diversity. This the amount ofhistorically been used to within show that there is no universal cutoff or named is not merely semantic question. 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.genome was ecologicaltodifferentiation. ferentiation while maintaining relatively low levels regions range from 10 to 109 (19).distinguished and circumscribed by rRNA se. Tables S1 to S3 of bacteria or archaea. Streptococcus he species debate in Alm.1%) (2). diversity through related streptococcal (13). and of between subpopulations sharing theory should beassignof theory.nomic uncertainty so that nearly every isolate was selected fundamental argument because of what it to be or diversity in theory.g. 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. Multilocus sequence analysis of closely related species.Epidemiology.uk thus used sequence relatedness define cutoff ease has historically been used to define species. from which selection) (22).0% for applications in by their agriculture. stitutions. London W2mechanisms of differen. finecan be ecologically divergent. mitis genotypes used to to the average interbreed. Case.distinguish pseudopneumoniae relatives.populations consisting of clusters which showed extended periods under stable discuss bacterial logically divergent. Partitioning was have been indeed to rely oneukaryotic microbes). revealed the ex. Evol. and in many cases rRNA sequences are too multilocus of closely related (MLSA) (2) and for differentiating named species. MA 02139. Recent to resolve emphasized the need se. and ecology.2.bacteria studied to (Fig. de. ranging from 1.pneumoniae genotypes isolates (2). whereas others are absence of selection that would generate as much a mechanistic understanding of the evolutionlection that would generate as much neutral di. Recent MLSA studies. Crucially. UK. of the mechanisms of differen. extent is a commensal bacteria with them. USA.diversity studies fueled the species). f ri he sc . named species. of A clear natural criterion to identify clusters fines a clusters species (3–8). bio. Massachusetts Institute of of the bacterial does not always clearly reveal that correlate with ecology can be discerned.Darwin commented that “all true classification among coastal Vibrio (5. these observations of repeated per cubic meter of seawater in temperate coastal way the population will undergo adaptation from each other.. Lexer. Presgraves. of related orga. New Phytol. H.distinguish them from the relatives. USA. purple.the true different species. Beyond this. keeping genes in these Recent MLSA studies. 23).microbiology is not allow bacteria to use different life.and differentiation while maintaining relatively selective sweeps were made in chemostats. irrespective of stable conditions in chemostats. 10). A. which sug. 225 together withforaInnovation.1* Eric J. taxonomists have been to catalog bac. to call of population differentiation and the ogy. those characters Department ofbacthat allow Civil those that showthe or more DNA hybridiza. shape. Evolution 55. A.0% for S. agriculture.g. The resulting data may help to discriminate among the many theories of every isolate was certain1A shows own. Beyond this. USA. 1B) and can colonize a wide neutral diversity as is actually observed. their morphological USA. pneumoniae to exist at all changing the tree process and we need to be ablespeciesof asspecies for practicalare too species. pseudopneumoniae. many or most only a of a fraction of not. tiple housekeeping genes to discern clustering is also abacterial diversity in abecause ofgeneticallythedistinguished and circumscribed by rRNA se. References which1. and tor of clusters that characterizessequence diverexist at all levels of the tree of life. Ecol. Evolution 59. mitis related groups with distinct However.nisms. a very interesting observation. was thought to source partitioningA more substantial observa. mitis. taxonomists concatenated sequences of multiple housekeep. The distance to cause a distinctive sehavioral correspondence is genealogical”have. as selective sweeps confined gests vast census population sizes (>1020).colleagues structure Because it links patterns of nisms that can explain this mismatch question? for Whatever mechanisms are drivingmodel has population(4. Differentiation College London. H. they correspond to well-resolvedThus. This implies many eukaryotic microbes).As a result. human J.species is.sequence clusters. splendidus is a which suggests vast census population sizes of neutral diversity. 5 (2003). toStreptococcus clusters is not. H. and of the MA 02139. and extinguish bacterial ge.0% mul48. other (Fig. Beaumont. pneumoniae and pseudoprokaryotic species that Archaea produced to Genetic Clustering applied to the Bacteria orhave been(orcategories date. sequence clusters. Furextent of DNA hybridization between them. ecologically informative samples. 36. 2A). they same explained by this superkingdom of life. which mutate at much highersize has been recdiscerned. many or strict the accumulation of unifying biological overall bacterial diversity. a V.nomic uncertainty (11). 34. Schluter. or break up S. T. ordalii is only found as Biological Engineering.of the human influenza vievolutionary history of the microbes in(Fig.advantages they confer to specific genes.To extend this the ancestral consider multiple effective population e for a population evolving V. practical dif. 2). P. Whitlock. of MIT true diversity with a certain amount of similarity must be from single free-swimming cells). hybrid40. This high levels of specialization diversity is the effective population size Ne. is also a for the for this purpose. 37. conservedhave allhavesimilar controversy of how 3. 16.. pneumoniae and S.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. 435 (2005). was superimposedin synonymous substitutions. Naturally. counter claims of neutrality and instead argue to be associated with adaptive traits. and S. Via. lack of theory. quence surveysconvenience of taxonomists. pneumoniae andstudies also clusters. which we might want which level in the hierarchy is more fundamen. and techniques (2007). 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. Technology. Nosil. resulting in a total of 2751 positions in the final data set (2). 68 (2007). 705 (2005).have all sequencing]controversy to defineone de. pneumoniae and S. Christophe about a 1* Eric desire to catalog bac. Masly. 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. and only capture a small fraction of the cutoffs imply that sequences that cluster together populations (e. and in most cases species show a clear predilection for one of the habitats. Streptococcus chaea (or speciesto manyinbiochemical tests and is genealogical” [(9). studies (1). and this rates of homologous recombination—mean that we still not understand what a serious Thus. irrespective sweeps in which evolution. Beyond this. Massachusetts Institute of Technolspecies. D.1%) of This closely he forced debate microbiology is not reflect only a revealed 404]. Hanage of bacteria is archaea. mitis 5% divergent um V.ac.of the predicted Vibrio (5.sciencemag. 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. 24.0% for S.3. However. P. must be differences in the amount of moreover Supporting Online same species. the numbers of Vibrio cells those niches but not in other niches. Neutral diversity is for ulation and thus constitute a candidate pools.fraser@imperial. but uncultured (1). it has neutral variation that ecotypes polymorphism that is differentiated populations reducing neutral variation (23).repeated selective of the details of the the whole evolution.to be explained by theory. splendidus.strains to to define yet unclassified microbial fraction ranging from 1.genetic differentiation driven by repeated selecThat bacteria are organized intoare driving the been substantially developed bythey mustand rus is predominantly with adaptation.g. Alm. West. Nosil. havioral traits anddiversity and distinct morpho. is populations of uncertain status of what it into species inour ignorance of way multilocus hybridization and ribosomal and taxa. with named species. Phadnis. M. such selective different mechanisms ognized for some It has been established from However.g. these studies also bacterial genetic lineages. R.may be measured of vast a species of its own. r vibrio n Entero V. as well as an organizing principle variety of surfaces. J. Partitioning was discovered because neutral diversity inSelective sweeps of microbes. (B) Ecological associations of Vibrionaceae sequence clusters (13). USA. mitis. and on their habitats. is to find ecological features that niches and changing environments. suggest corresponds defined by taxonoorganisms reveals and much the same ge.evolutionarythe genetic data tell us about mechBiological Engineering. Evolution 60. A more in The ecotype modelgenome 24) predicts that cal differentiation. 3Department of What do importance.relationtogether with a aFig. and of the niches and thermore. and this diversity cases rejoin S. which in might want descent. the ability between two randomlydis*To whom traits and by their ability or inability to DNA hybridization andshould be addressed. C. and Darwin commented that “allspecies). pneumoniae and with a history of taxoon biochemical tests in a consistent manner.1Evolution 62. 17.S. and population size Ne (<100) is very much smaller 742 6 FEBRUARY 2009 VOL 323 SCIENCE www.amount of polymorphism that is evident in non. Barrett. rRNA se. a small similar to A clearuse the criterion with sequences of taxowhich natural bacteria to a history of multerial diversity in a consistent manner. In this mental observations of bacterial populations. Imperial characterizes a species. H. but differences in their taxa. UK. 17. some time (17. Lai.1 Williamresources in1 the pneumoniae or a major human pathogen. Animal spe. V. Levin. suggest that species defined by taxonoS. R125 (2007). A. 16. Rundle. convincing fashion. Rogers.2% divergent B nsis s V. 21). 38. The mean distance within the clusters. convincing fashion. Funk.of vast amounts (e. and sequence striking from the Material 45. andwhich we might want fundamental argument consistent manpatterns among to find ecological features that ner. 1B) and can colonize a wide quence surveys [(9). Martin.Taxonomistsextra. L.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. p.2% for S. Hanage1 47. pneumoniae and S.mostats. able a explain why species differentiationa the process of adaptation to new cannot reliably lack to large collection of similar species. which breaks up into many closely related ecological populations. Ortiz-Barrientos. S. D. pseudopneumoniae and up 5. rRNA to always that reveal related two the bacteria combine genetic by their ability or inability to quence surveysdefine however. depending on the level of genetic differThis analysis revealedsize N . L. William 1026 (2008).thus used sequence analysis (MLSA) (2) and discovered because strains were tend toS. molecular methods [particularly is a recently described organism of uncertain status chemical characters have been selected for the ficulties. MA 02139. life. nism for reducing been suggested (23). 23).in(3–8). ordalii is only of se. and of DNA hybridization between a history mitis S. much of it sequencing] have helped to define (or indeed to archaea. Rieseberg. is clearly unsatisfactory. 910 (2007).pathogens.populationssequence analysis taxa. of adapta. 4334 (2008). Syst. limitations and A clear natural criterion to identify clusters of teria to use different resources in 3the environ. J. Because it links patterns tive sweeps (25) and that the resulting effective must restrict the accumulation of neutral of genetic differentiation with adaptation. Bot. M. mitis so that nearly is more fundamental than sequences (Fig. species. 1) (7). molecular methodsthese through is acall species. is shown. Selective sweeps in many populations of microbes. however. Willis. Funk. 24). Cambridge. quences have tiny subset of those charactershave thatthe use of a column species. berecently. mitis only Fraser. and putative subclusters are indicated in dark gray. fi V oi en si s A S. but housekeeping genes only a minute descent. amount of similarity As an example. sweeps confined to each effective population stable and diverse. 10). 375 (2009). mitis Instead.DNA-DNA eukaryotes. and makes differentiation of bacteria into clusters. L. but such indeed to uncultured (1). pseudothese methods have serious Instead. c. L. much of it Habitats and Ecological Differentiation only about a human desire to catalog uncultured (1). Noor. Taxonomists classify these The distance between two randomly selected organisms into species in much the same way as they classify eukaryotes. from terial diversity and limited morphological values that place two capture a small fraction of distinct. all genetic variation was adaptive (20.0% for S. uncertain status that that sequences and thecluster Foundation 43. London W2 1PG. 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. Science 317. revealed further diversity reveals about ourfundamental argument because More recently. S. Evolution 61. Cambridge. 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. shape. However. similarity in these 44. Presgraves. in the absence found ecological niches characterized evolving in the ecological niches characterized by the selective as single free-swimming cells).the population will undergo adaptation and difHowever. and green. population differentiation mecha. Z. S. but such ribosomal RNA (rRNA) ordinary sequence microbial to define cutoff ease has historically beenis similardefine species. many populations can purge mutation (periodic within niches (which should strains were collected from distinct. 1423 from 10. D. Fishman. biochemical characters have been metagenomic and only bacterial isolates into the rejoin S.org www. MA 02139.numerous closely so that nearly every isolate was selected for the have. and medicine. and observationsthere is ecological preferences. amount of There are a distinct cluster certain data (12). pseudopneumoniae diverse superkingdoms superkingdom of life. the a major be measured by S. Whatever mechanisms genetic clusters is entiation of bacteria into clusters. Furthermore. that “all true the relation. showing clusters among 97 isolates of four Streptococcus species identified as indicated. 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. V. terial populationsselection) (22). predicted Vibrio populations are deeply divergent Vibrio cells per cubic meter of seawater in tem.to discriminate among the manylife. Curr. and moreover that this cutoff more generalist (Fig. u rs pe teu s a* p V. species of its the This is prokaryotic species that have been produced to date. inspection ofor species would tend applications in industry. rRNA sequences common descent.fined as the size of a populationby the selective model therefore has the advantage of providing of some populations (e. practical dif. splendidus may be an artifact of horizontal gene transfer at the Hsp60 locus. There are striking differences in netic London. Naturally. pneumoniae 3% divergent 1. L. Willis. J. S. is genealogical” [(9). Mol. Esti. Bradshaw. (A) Radial minimum evolution tree constructed using MEGA4. or break up any other that cluster Such cutoffs imply that S. calvie S. M. This is more generalist (Fig.. 24. H. Furlevels of environments. pseudopneumoniae S. Estimates of Ne is the ecotype model.an empirical modeling approach. P. that A. Via. 404]. that is based on experizooplankton in the water column (13). Recent studies have emphasized the need to to either rejoin S.. species a coherent and is more mitis genotypes is similar to the 1) (7). S. and S. D.characteristics for this pur.4 Martin F. Mapping of of life. This (>10 levels of neutral diversity. use for S. V. We thank M. the pneumococcal cluster is shown at larger scale. e an cid T T The Bacterial Species Challenge: Making Sense of Genetic and Ecological Diversity S. Imperial amounts of as yet unclassified between them. Polz. and this model all genetic genetic data adaptive (20.should be considered as putative or actual spegions or results on their habitats. The overall genetic relatedness of isSPECIALSECTION pneumoniae isolates mayhuman pathogen. 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). Trends Ecol. L.2. Taxonomists have pathogens. Otto. where genes adapted to ary processes. 39. Distances were calculated as the percentage of variant nucleotide sites. is to find ecological features that tal than any other (Fig. Cambridge. Among forces form.hierarchy ization are defined which level in the (2. 28. biochemical species). tiple housekeeping genes to discern clustering The Bacteria and Archaea are the most genetically diverse superkingdoms pseudopneumoniae and up to 5. one can consider multiple entiation from model. taxonomists distinguished and circumscribed by rRNA se. Animal spe.show 70% or (11).org SCIENCE VOL 323 6 FEBRUARY 2009 741 31 . Spratt. calculated by MEGA4. T 30 but pathogens constitutemodelsminutepopulation diversity.ac. J.fraser@imperial. Massachusetts common finesthese methods have(3–8).cases correspond to differences in netic lineages. Most applied to the Bacteria or Archaea 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. 18.

” they will continue to diverge from each other.53 threshold explain low predictions than neutrality) pro(or. which can colonize a host but are then forced to move on because the host develops immunity or dies (17). Choosing Between Models It has proven difficult to discriminate between models of population differentiation that focus on ecotypes or metapopulations.sciencemag.is another unusual feature of bacteria. recombination—that validate competing models more systematically.Bottlenecks. one current view is that process that reduces the rate of recombination Illegitimate Recombination and Gene they do not form species because they recom. is changes in their environment (33). However.g. In 0 (or. The ecotype model. However.converge. 37). As re. does not involvesegment from reassortment of When the rate of change is positive. the fate of the that populations will depend on how genetically distinct they are at the outset. Diversity lost by a local selective sweep in one patch may be rescued and reintroduced from other patches. 2.the host strain. Selective sweeps are predicted to be inevitable in simple. observed using established 1 ecological than were a model-based can be is needed if we wanthypothesis thatmethods 1 ecological criteria.differences at neutral lociathan at association with a very low estimate of popula. Bacterial reproduction When the rate of change isbetween the clusters as a function of the genetic distancenegative.criteria.small. (A) The ecotype model of bacterial population differentiation. recombination does occur in phase-spacedynamicsthe cluster divergence. For low recombination rates. held together by recombination. As the recombination rate increases.e. 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. In this case. Selective to new resource patches (e. The speciation Illegitimate recombination or gene acquisition In asexual clonal organisms.sweeps are predicted be inevitable in from a ral bacterial metapopulation well as is fundamen. which occur in (green line). a hypothesis that can be tested. but were suggests that established the model criteria. These creasing sequence divergence between the donor If they away than this “speciation point. which shows the rate at which two clusters diverge over time—that els based on the assumption that genetic varia. with recombination occurring bebacteria and archaea (29) and feature of involves tween them at a rate that is varied for the three different simulations. followed by dispersal effects of complexity and instability of actual population structure driven by selective sweeps tive bottleneck population structure. This metapopulation model is fundamentally different from the ecotype model because it does not predict an association between neutral diversity and adaptive traits. 31). The importance of this phenomenon tain circumstances recombination can prevent hypothesized that two related Campylobacter is evident in the clear and ubiquitous signature this. Because another strain. B new and empty colonization Metapopulation structure. The figure summarizes some key results from (15) in a Homologous Recombination One specific challenge to models that invoke Fig. which can colonize a host but are diversity and adaptive traits. when negative. a hypothfrom establishede ecological It hasdisconnected Recombination rate relative to mutation from census to find esis that can be tested. but the importance ofthat more work is -1 systematically. this simple model is an adequate effective description of the more complex processes represented in (A). However. can generate very low effective population sizes if patches turn over (i.. For low recombination rates. and archaea (29) and typically reduces donor and the recipient (30.org 744 cies in the eukaryotic sense because they do not 6 FEBRUARY 2009 VOL 323 SCIENCE www. The direction of change for each scenario is shown by arrows color-coded to each increasing sequence divergence does occur in scenario.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. bottlenecks will also restrict neutral diversity. 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). even in the point is the amount of divergence between clus. Otherin (28)]. in which the population is divided into patches and where individuals disperse between patches. different 0% 10% 20% 30% we have not yet discussed.00 sexual simple better predictions than models based on very general problem in population genetics that 2 2. but rather the effecintensively for short bursts. 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.level. 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. 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. and diversity generated only by neutral drift. problem of low power to detect selection This plausible explanations of genetic data.53 threshold viding neutral drift.involved in virulence. Patches of varying size (gray circles) are vacant (empty) or may be colonized by a single genotype randomly acquired from another patch. 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. characteristics of the acquired DNA and that of The above insights were reached using mod.. change of genetic distance positive.10 clonal This low to of low values of Ne while pro3 explain problem find models to detect selection 0. level.Content Variation bine too much (5). of two populations. Different genotypes (different colors) arise by mutation or recombination and increase or decrease in the population by random drift. we held a distinction be.” because the new bination between the clusters. a power to detect selection Table 1 we proposeto reject neutrality) is a very 0 (or. the increase in the mean genetic distance tion is neutral. 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. to reject neutrality)that does is a very general that could be used to test. 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). as ssifying bserva- * * * * stable ecotype concept * * * colonization old and void C D 20 Population size 15 10 5 0 0 20 40 Time 60 80 100 Bacteria Phage ated sewhereas ble and ence of lations? ot from utate at orms. Regular population bottlenecks can drastically shrink the effective population size. Hence. A metapopulation may evolve. The ganisms. 35). In Table 1 we proexplanations of genetic data. This problem of low scheme for performing more accurately. estimates of effective combination increases. they Recombination becomes in most higher orga. whichcharacteristic of farther away than this “speciation described in (15). Each ecotype can therefore diverge to become separate species.or codon usage.more on the accumulation of differences at neu. are within the “speciation point. 31). whereas it curves are derived using the model described in (15). This structure well describes the situation for parasites. organic particles in seawater by Vibrio popula. any inference of a niche adaptation per se. with its predicted monophyletic relationship between niche and genotype. the populations will diverge genetically. 2B) Fig. 31). in most cases. and the recipient (30. 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.assumed a homogeneous distribution of poly. which may colonize empty patches as described above. the cohesive effects of recombination slow the increases. and adapt without global selective sweeps. However. and (D). Different models of microbial evolution that lead to low values of Ne.geneous distribution of polymorphisms across population size N are often grossly proven very Recombination rate relative to mutation using census population sizes. when itself (x they the have not yet discussed. estimates of effective population size Ne are often grossly disconnected combination increases. all other param. that proven very 0. For “sexual” processes (34. and if a small number of bacteria are dispersed to colonize empty patches) (Fig. may therefore not be an appropriate model of speciation in complex ecosystems.genomic barriers to recombination will depend functions encoded by the imports were often eters being held constant.between them—for example. and thus that in an unstable landscape. but a better term is “gecreases. If they are creasing sequence divergence reduces but does some genetic material that isbetween the donor curves are derived using the model point. However. the divergence of clusters requires a in this fashion—such as a new metabolic capa- 33 . it may capture some of the effects of complexity and instability of actual ecosystems on population structure. although highly idelong pedigree in eukaryotic a limited (26).all other parameters being see constant. the replacement of a shortfrom of such inter. If this becomes negative. This version of the model was dismissed because of its association with a very low estimate of population size (14). stable environments but not in complex metapopulations [a point partly addressed in (28)]. 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 three examples shown in Fig. The largest of these (which converge. under cer.farther 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. recombination does involves rate of divergence. in base composition summarized in Fig. Although it is verge (the green line) and a “sexual” organism morphisms across the genome. then always an appropriate assumption. colonization of organic particles in seawater by Vibrio populations). differentiate. develop. Strains may diversify within a patch (as shown by different colors representing distinct genotypes). A recent study ent strain. As re.adaptive loci.. the populations are effectively clonal and always diverge genetic material recombination higher the scenario. the occasional ability to gain a new adaptation species.org 744 recombine at all (32). followed by dispersal to new resource patches (e. periodic selection in one sublineage does not influence diversity in the other sublineage and vice versa. The models also nomic islands” as the phenomenon is far from organism in which clusters are predicted to di. which can generate oscillations in population size of any amplitude. As the two populations are ecologically distinct (i. Metapopulations. to rejectof Ne while ison viding better estimated values models based a 0.Fig. it is plau. genetic models karyotic alogies. Bacterial reproduction we homologous the obligate another strain. These and the recipient (30. For some purposes. In this absence of any selective pressure. The use of longitu. 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. the ecotypic structure of a soil Bacillus has been modeled to predict a priori which sequence clusters were ecotypes. iven by ngitudions. and of other more complex evolutionary models not described in this review.10 clonal 3 challenging estimated power that successfully 0. mulation of differences at neutral on the accuversion of the model was dismissed because of its homologous recombination between the clusters. for example. we see a distinction between a “clonal” tral loci than at adaptive loci. andanalyses that could evolution—homologous and validate different -3 be used to test. develop. 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. as model observations stable individual and the resulting extinction of episodic crashes the diversitymodel because it of all other [a point partly 2A). a period of allopa. 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. However. more accurately. Some clusters are associated with certain phenotypic traits. dentiation l therehanistic sses. species recombination. of merging into a single species as a result of data. The dynamics of cluster divergence. clusters will ters that needs to accumulate to prevent them case. Although this is obviously not DNA in question is unknown. This effect. It ollected cture of y driven hat the 100) is acteria. estimates of effective population size Ne are often grossly disconnected from census population sizes. (C) A neutral model with small population size. addressed mechaated with genetic changes and not associated nisms that induce or involve regular population with changes in ecological covariates.” then recombination will cause them to each other. to discriminate among different biologically tested.SPECIALSECTION A E1 E2 cts that ng bacould be cotypes As a reshould ies. Gene acquisition between them. in which patches occasionally become unable to support colonization and their inhabitants are removed (solid gray circles). The analysis of Bacillus 2.sciencemag. It also describes any situation where bacteria use a limited resource intensively for short bursts.sexual in the sense two the populations no longer diverge. although highly idealized and simplified. However. the populations will diverge genetically.all other parameters being held constant. 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. (B) A metapopulation. (D) Predator-prey dynamics and population bottlenecks.the whole populationtoby descendants simple. clonal and always diverge nisms.g. ecotypes).axis). 3 in adaptive ecological differentiation will be may be many kilobases in length) were initially differ only in the rate of homologous recom. 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.to recombination are removed. 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).(green line).of its homologous in Fig. any from another within If theythe fate of the two populations will then recombination will cause themtheymerge.single environments but not in complex metations). lution. These are identified by differences in the described at greater length elsewhere (15). 3. This structure well describes the situation does not predict an association between neutral than observed for bacteria. bacteria-phage predator-prey dynamics are simulated with a classical Lotka-Volterra model.geneous loci. (B). which is shown by the dashed branches (diversity purged by periodic selection) or solid branches (existing diversity) on the tree. 3.sciencemag. if patches are only intermittently able to support bacterial growth. 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. 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. On with respect to limitingmay capture some is not situation where bacteria use biology resource alized and simplified. For example.. the outset. evolution—homologous piece of DNA with we have not yet discussed. 3. Reproduced from (24) with permission.” they will continue to diverge from merge. the cohesive effects bacteriaHowever.populations lineages (Fig. more accurately. As recombination in. try or ecological differentiation. The tree shows a single bacterial lineage that differentiates into two sublineages (E1 and E2) that differ in some aspect of their ecology. As the recombination rate the populations are effectively of recombination slow the nisms. and Local for parasites.observed in mostbetweenorga. tally different from in ecotype causally associ. 3 differbetween the clusters. mulation of The models also assumed homoassociation with a very low estimate of popula. termed “pathogenicity islands. This ples shown in Fig. The modelspolymorphisms homotion size (14). as shes in changes ological (27).e.limited to pathogens (36. A characteristic of this sort of metapopulation is patch turnover. This populations. 2B) (27). The analysis of Bacillus partly did this by predicting more ecotypes in the model than were observed 32 Relative rate change in d distance between Relative rate of of change inistance between r r clusters per generation (x10 clusters per generation (x10-9)-9) iples of ype has within ciation. For recombination rates above this the homologous segment piece of DNA with closely related species. 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. Recombination becomes less probable with in. which reduces but does other closely related species.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. we see a distinction be. Bacterial reproduccompeting models more systematically. and hence which ones should be associated with specific ecological properties (16). The relevance of the metapopulation model to the species question is that.00 sexual simple did this by predicting more ecotypes in neutral drift. it neutral diversity of the the basis of these analogies. the donor of the is. such as a propensity to grow on shady north-facing slopes or sunny south-facing slopes. It also describes any the species question is that. 743 ww. was once thought that bacteria do not form spe6 FEBRUARY 2009 VOL 323 SCIENCE www. Population sizes and time axes are in arbitrary units for illustrative purposes only. colonization of ecosystems on caused by the replacement of would require good longitudinal data from natu.models It has successfully challenging population sizes. analysesproblem in population genetics develop. For recombination rates above this the homologous segment given isolate strain.adaptive distribution of also assumed a across tion size (14).

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F. and its evolu. a program grant from the Wellcome Trust (B. 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. Environ. the donor or incorporate it forand fashion that Nonea they are mainis example. J. N. J.A. Soc. 745 Speciation 22. e77 (2007). the occasional ability to to testing the ability ofneed theoretical background. A. 1 (1981). FEMS Microbiol. R. taxonomic practicality. Natl. G. E. Soc. U.Identifyingloosely coupled with that of any par. R. 4686 (2004). and the Moore Foundation (M. The part of the ecological space where the shared in red. It tained framework? or or selection. Polz. 29. S.S.. M. 30. B. thatVibrio the same species. And if genetic groups do not map exclusively onto sampling categories (as is likely to be the case). 18.sciencemag. portance in terms terms all speciation. 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In the case of very mobile question of defining least. Dobrindt. 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. 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. other related testing the ability of different models background. including the extent of variation in The importance of this phenomenon is evident in between them by mobile elements. 36. N. an acidencodes “core” which mine drainage this or other theoretical concepts areas of alternatives.. of interest. Genetics structure (1999). Focus on longitudinal studies. B. 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A least. 28. Atwood. 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. Pickerill. Rev. Majewski. genotypes] in different habitats” (17). To test the hypothesis of ecotypic structure. Trans. Connor and S. 10. “auxiliary” bolted species). Andwould denygroups do not populations that are a group but as little as 40% of genes genes may be distributed across using house.tant. data distribution of genetic and ecological (without ecological covariates) and test on new data. Genome Biol. K. 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. Microbiol. Acad. without tions concerning detailed will not saying. N. 11. 4. little choice geneticists may the terms of speciation. Natl.. Genetics 176. P. Microbiol. described above for indithe samethe organism. 1093 (2007). C. the donor of is unknown. of and thus how likely ecological differentiation. 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. 4.A. K.P. we need to know the distribution of electrophoretic types [i. J. Sci. to genes compete dividual a group of related Leptospirilbe (13). H. Sci. Sci. 55. B. E. that guidegenome. 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.S. how to that structured environments (40). 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Proc. onto observe. which shared by fundamental of agenes) and heavy metal resistance in environmental organisms. 2.F.in alloperons It seems ranging from highly resistance core functions to suggest types of application of principles case of very mobile elements—for exam.1).S.different genera on the basis of their specific charin the growing body of genomic data. even at the a for a measure the dynamics are. 37). and between genetic-ecological clusters 5.sciencemag. K. T. Milkman.. A. Biol. G. F. 2. Curr. and real populations. some guidetic to of very mobile strain is specificity.A. In the foregoing we have emphasized ecotype and metapopulation models.or interbreed enough. statistical that shuffling of thatnamed species as being characteris. more complexpopulation gebe only Mechanisms within chromosome segments enriched in to taxonomists. the mobile gene may be speciesvariant to define populations prisinglyrecently been hypoth. Spratt.). entire populations of strains likely growing inare available. A. Examples of such distributed ical commitment to a strong these is now commonplace to speakdifferent loci include drug resistance determinants in pathogens (e. Goldenfeld. H. D. 2009 3. J. F. Genetics 99. but as little as 40% of genes ofconcept and chemical gradients affecting arena within speciesKimura. Annu. Retchless.lying niche structure. G. 1. 37. 433–455. and E. U. Rev. 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). it should gospecies). J. hitch-hiking. Hacker. onto are tested and refined on a wide should. C. Welch et al. One clear either of these include drug resistance resistance in in pathogens organisms. 44. Rambaut et al. K. 14. Natl. vary. See supplementary information in (16) for a statistical comparison of the ecotype model with an effective neutral model and an implicit estimate of Ne. MLSA. in base composition orof the host strain. 99. D. W. Appl. L. Heredity 1. Feil.F. 33. “clonal” and provide a F. A. 1459patterns 28. Nonethe DNA usage. 2009 growth. 476 (2007). Trends Biochem. Microbiol. 16. 253 (1977). rectly making a strong theoretlum has high frequency. S. Denef et al. Proc. however. Microbiol. G. Cohan. Majewski. 21. A. Popul. 22. F. J. pp. plasmids encodingconserved to antibiotics or lines for thean ad hocecological studiessomewill ecological not be genes a isolates. the ecological data collected must be relevant to the niche boundaries of the populations studied. available. populations. Biol. G. for a pathogen—may mission in they are theless.” becausetermednew species. 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. Acad. McCarthy. asas described above for Vibrio is if define populations gene acquisition occurs at a sur.P.taxonomists. or species. (Fig. purple mobile element for all isolates. and mobile gene common to all three. such as the presence of other SCIENCE VOL parasitic FEBRUARY R. 31. Ford. Rev. Microbiol. London. schematic toexplain highly variable expense the patterns species). Theor. even likely. D. Rev. in Microbial Classification. M. Wilson. J.be most informative are emerging. If after this process it emerges that some model or models are consistently validated for different study systems. Press. Hoffmann et al. 146 (1951). Lawrence. 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. Department of Energy Genomes to Life program (M. likely thatspecific ecological propertiesto determine heavyloci by these accessory loci specificityno to a tant. composed of genes orand also leadthat habitatcasewhich each hostecologicaladapted. Washington. 34. Proc. C. 3. Sci. tions concerning species will not be saying. H. F. species no link test for may have definitions functions encoded a locussequence we observe using often involved in virulence. Longitudinal or. 7332 (2005). depending on to genomes (2004). is that the model is sufficiently flexible to explain almost anything. C. Spratt. K. toof bacteria ple. Hunt et al. C. Wilmes.undergoes a selective sweep or goes extinct. Most importhe suchin structured environments (40). These genome. In any case. answered in the absence of it may be sensible which genome. B. B 361. to define populations without making bacterial species concepts. We should. Soc. It is still unclearGenetics 152. Cowan. L. M. U. R. the specific ecological properties of on the genomes specific habitat. Denef.

species to identify temporally stable (refugial) andWe apply this approach to one of regions for unstable (recently colonized) the world’s most species-rich. H. 1920 14. they lead to London Ser.forAls. the mohaveH. Rio Claro. persistence and population structure. R. yet notoriously endangered and understudied ecosystems: the Brazilian multispecies molecular data. Am. the approachpredicts cur. which documents a replacement of forests by grasslands in the southern Atlantic forest during the LGM (14. 53 (2004). conservation (1965).1126/science. Materials and methods are available as supporting Fig. 49.89]. and 21 kybp) overprediction (fig. Schönrogge et al. 21 kybp). Entomol. Ecol. A. a third. C. D. P. Building onthe model material on Science Online. 2 and figs. ateTravassos. Soc. albomarginatus of predicted unstable areas.785 cause of conflicting evidence (2. Proposed method of model-based hypothesis formulationstages arehypothesis testing and reflecting the forest. Tautz. W. Ital. Field sampling is driven by them. scenarios suggested by the climate-based models. Fiedler. faber in 2 (Fig.1 Michael J. Evol. divergent clades are also represented divergence times (HABC) relative to unstable areas. hypothesis phylogeography diversity within and among populations in phylogeography diversity within and among populations in refugia refugia divergence times (HABC) H. 32.989. C. W. Markl. lecular analyses contrast the fit of assemblageversity within and among populations in refugia 17. Recent studies from sub. University of California. (iii) absence of new D. Queens College. Entomol. Rodrigues. G. 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. Schönrogge. Whereas H. DNA chondrial786 (mtDNA) lineages found in this FEBRUARY 2009 VOL 323 SCIENCE www. as opposed to post-LGM evidence for stability in both areas under the noH. but historical pro. traditional species-by-species approach. N.4 Craig Moritz1 108. NY 11367. 60. while explicitly accounting ties (22) reflects high geographic structure with. species-rich regions. isolation by distance is not model [B(Z2 = 3. T. In the tropics. K. we and species diversity (5. Hickerson. Vgl. faber (0. faber has a broader altitudinal range and also inhabits mixed and deciduous areas. 387 (2008). we region as a hotspot within the Atlantic rainforest putation (HABC) method (24) allows us to use compare mtDNA sequences between the pre. Metrics of genetic diversity confirm the To test for assemblage-wide colonization well as under a postisolation migration model above patterns (Table 1). semilineatus. particularly unstable (recently temporally stable (refugial) Ana F. or 6 kybp. 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. genetic patterns of isolation-by-distance in unprediction in otherMus. Berkeley. A. G. because ofpredictions of in the São Paulo region. Using Bayes factor (25). Brown. Aust. These palaeomodel results are congruent with the fossil pollen record. A. In Descriptive Descriptive predictions of species should show (i) higher genetic genetic a large refugium in show (i) higher stability/expansion. Diversity of H.g. Fig.model validation (bottom). sparse ators. Rather. City University of New York. faber. Zool. as well as some adjacent refugial populations since the LGM. T. Combining data sets from several sites located outside (south of) the refugia are Mybp. we group mtDNA [B(Z2 = 0. (ii) genetic molecular data. 1). faber. Flushing. although the central refugium extends farther south in the frog-based models. Elmes. Acoust. 14). N. cover both predictedis driven Fig. The hierarchical approximate Bayesian com. 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. Fiedler. SP 3526-4100. ternsWe thank N. semilineatus. Experientia 52. Anim. Biol. As predicted. 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. we and species diversity (5. and establishes a validated approach to biodiversity 1 Science 319. If the approachdivergent clades withall taxa there are multiple. accepted 28 November temporally stable endemic species to identify 2008 10. faber. C. Elmes. Schurian. 2). Soc. In allpersistence highhence diregional differences in species. USA.994. Fanfani. Rolff. 21. By signature of population expansion in the south. Fig. J. faber). 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. USA. 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). A.6%). 2Biology Department. climatic extremes of the Late Pleistocene. 1392in the face of rapid environmental change. Brazil.compare alternative hypotheses of assemblage-scale response to late 19. Exp. and 0. 110. Grasso. progeneral Downey. 47. Hickling. despite the more extensive (preclearing) range of the forest in southern and southeastern Brazil. B. within refugial areas for H. City University of New York. Flushing. our method benefits from a mulaverage net nucleotide differences across locali.nized from refugial population 1 subsequent to gruence across species.from an ancestral population prior to the LGM for the stochasticity of a single-locus coalescent in refugia (2. even comparisons of species-specific analyses. Nachr. involved: biodiversity disreflecting across in southernmost low genetic diversity multispecies colonizationareas. 1 (1991).. USA. first map the cover both predictedof endemic predictions to palaeodistribution refugia and 12. 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). G. predict for all species a large central refugium throughout the Late Quaternary (“Bahia refugium”) (Fig.all three species (Z2 = 0. depicting the intersection of distribution models for each taxon under current. 7). and boreal systems 14.org/cgi/content/full/323/5915/782/DC1 of high endemism (5. providing a tifying putative refugia (4). Departamento de Zoologia. J. Thomas. and 21 kybp) to predict areas of stability (regions in which species are predicted to occupy irrespective of time period) and unstable areas (7. Going beyond the Atlantic rainforest. level data to the spatially because demographic relative to unstable areas.94 in H. reflecting assemblage-wide. and 21 kybp climates. A. 3A)] to lacked forested habitats in the late Pleistocene: model-driven hypotheses of (i) simultaneous. Behav. climate fluctuations helped refugia models have been dismissed because of 11367. Diversity of H.multispecies colonization from yet notoriously endangered and We show that the southern Atlantic forest was climatically unstable relative to the central region. long-term 27.when allowing for postisolation migration (Fig. S2)]. Am. Sociobiol. B 266.all three species (Z2 = 3) under the no-migration at patterns of historical community assembly in cies. albomarginatus and [B(Z2 = 3. The lack of the number of species evolved under H2). H. mito.925. Z2 < 3) = 35. Hölldobler. in identifying putative refugia (4). Rio Claro. Our ultimate goal is to Biociências. Given their life history traits. 1. When Bayes factor is used (25). Akino. CA 94720–3160. semilineatus. C. HABC will offer the possibility of looking ally low levels of diversity observed in this spe. ays the nt’s hicue has ate and Berlin.org biodiversity patterns323 with the the acoustical equipment. J. A. 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. S2) (14). 3A)] to contrast two alternative historical to environmental modification (1). larger. Going beyond the traditional species-by-species palaeoclimate models of species and habitats to approach. semilineatus. 109. R. the long-term persis. of endemism. for neotropical species in the late Pleistocene. ecies of icularly Diptera. 103 (1968). 3025. ancolonization from Glacial Maximum model validation (bottom). B. Berkeley. Rev. Furthermore.2% divergence). E-mail: carnaval@berkeley. adjacent 1. If correctly correctly predicts rent patterns region. understudied. Museum of Vertebrate Zoology. DeVries.climatic 283 (1993). migration model [B(Z2 = 0. and M. reflecting 14. Hill. with most species-rich. 3Departamento de Zoologia. R. it mimics adult ant acoustics (particularly queens) to advance its seniority toward the ’s hiermimicry lack the and of.tence model. but historical aim of informing conservation. 7). Am. London Ser. ElfferichIn the J. Universidade de São Paulo. Chem. albomarginatus and indicate that all three species colonized the ple (24).curpled areas. The results from the full comparative phylogeographic samin the unstable area for H. The population persistence in isolated areas. stable areas. Nash. 3A). NY 3 too recent to permit restoration of equilibrium (1996). Using frogs as indicators. Roces. been Z. assemblage-wide responses to Late Quaternary 3A)] and adjacent (northern) populations from This is not to say that southern areas entirely climate change. Because the stability maps raise specific hypotheses about regional differences (AUC) values (16) 0. region. Inclimatic extremes of the Late Quaternary (putative refugia) data tions and H. multispeciesregions after the Last adjacent tribution modeling (top). the recent colonization codistributed groups into a single hierarchical genetically more similar to each other. they lead to to S5). B and C). R. matching structure. Markl.16]. faber. B. R. albomarginatus and H. This can translate into higher analytical H. particularly emphasizingH. migration and genetic drift (15). semilineatus occur in low and mid altitudes and are mostly restricted to the evergreen or semideciduous components of the Atlantic Forest in eastern Brazil.grasslands in the southern Atlantic forest during relative to the less stable (southern) portion of the assemblage-scale responses to former climates (7). large refugial populations after the LGM.000 km2 along the Brazilian coast and lecular analyses contrast the fit of assemblagereaching into Paraguay and Argentina. we also detect region are shared with adjacent refugia FEBRUARY 2009 VOL 323 SCIENCE www. respectively (fig. 13. H. in pled areas. for effectiveScience 149. Proc. palaeoclimate models of species and habiTable S1 tats to provide insights about processes shaping References genetic and species diversity (5. C. Linn. J.1126/science. amphibians are useful indicators of environmental changes through time (12). Soc. Fig. as opposed to long-term persistence of popu. 733 (2002). and between UNESP. but is detected support under a postisolation migration model barcode-type DNA sequence information (e. DeVries. Appl. 14 Queens College.. Entomol. In contrast. Stability maps. mtDNA data are and H. Mus. In contrast to the central and northern regions. Z2 > 0) = 4. which are then validated with have usefully employed post hoc tropical biomesmultispecies molecular data. two contemporary populations split titaxon approach. Instituto de Biociências. 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. understudied ecosystems: after the LastAtlantic adjacent refugial regions the Brazilian Glacial 21. J.6 to 6. explicit of long-term 18. Because the in persistence and rainforest Atlantic hence diregional differencesBrazilian raise specific hypotheses about the stability maps spatial-temporal patterns (Fig. multispecies molecular data. Physiol. the lations in unstable areas. This sets J. B. refugium which 22. . A. J. given that this species occupies a broader environmental niche. A. The palaeomodeling method intersects predicted species’ distributions under current conditions and climatic extremes of the Late Quaternary (6000 years before present. to shape present-day diversity in temper. semilineatus may reflect 3.Universidade de São Paulo. contrast alternative historical models H1 and H2. SP 055008-090. Soc. two in isolated refugial areas. species and assemblages (codistributed taxa. orSão Paulo refugium 6 kybp.1163583 (refugial) and unstable (recently colonized) regions for species occurrence. and referees for refugia models have been dismissed be. Brazil. 1). USA. 3A). DeVries Pleistocene Distribution models developed under current rent patterns of endemism. J. ate Quaternary climate fluctuations being described (8. species are predicted to occupy irrespective of Spatially explicit hypotheses Re: Models of to unstable areas stability (regions habitat stability (7. i. which are then validated with species occurrence. and moderate codistributed nonmodel organisms for which observed in unstable regions. areas. much smaller refugium is predicted in the northeasternmost portion of the forest (“Pernambuco refugium”). H. D phylogeographically validated palaeomodels Model Validation Hypothesis Formulation Distribution Modeling 6 FEBRUARY 2009 36 785 37 . given that colonization has been 24. Bull. yet species in endangered and understudied and even genera Brazilian Atlantic many species ecosystems: the of vertebrates still 1 Museum of Vertebrate Zoology. occupying interior and coastal sites in the Atlantic Forest south to Paraguay and Argentina (figs.968. The existence of species and genera endemic multispecies colonization of unstable areas from In this case. M. 3) or circularity in iden. 1). nsect y. Wardlaw. and P. H. 6 kybp. J. Ecol.of described and undocumented diversity. Yet. long-termlong-term perbecause of perrelative to unstable areas. (120. toceneLa Morgia. Bonsall. faber).selection (26).81. albomarginatus. 4). 1895 (1998). G. A. although model. W. E. they lead to and/or vicariance of colonization genetic diversity across taxa for both individual species corrected distributed taxa. species occurrence. Knapp.edu We use molecular genetic data from multiple.is admitted and accepted as a member of a host society. 3. populations south of the Bahia or São Paulo refugia appear much less stable. 14). 0. species pot. A second. and 0. Z1 = 3). and H. E. the HABC results infer long-term to the southern forests (27). 229 (1993). Instituto de Biociências. representing regions with high species endemism and conservation threat. faber and H. 65. Thomas. F. capturing the historical signal that emerges from ernmost localities of H. Wardlaw. E-mail: context 1 (1973). Haddad. 183 Biodiversity hotspots. Three stages are involved: biodiversity disnature of this area. Going beyond the of biodiversity at the regional scale. J. this biome level data to the spatially explicit demographic has been reduced to by the climate-based models. in ot hreat. J. 3080 (2001). which are then validated with the approach correctly predicts current patterns (2000). Giovannotti. Allyn. viding a general context for understanding cur. 3)for designing comments and advice. J. species to identify colonized) areas. Thomas. If Miguel T. nu. 14).hotspot and a refuge for biodiversity during data from all three species at once to test for dicted Pernambuco refugium [population 1 (Fig. and unstable previously colonized) regions for emphasizing (recently undersampled areas. combined multispecies molecular data low statistical power because of the exception. UNESP. his sets ty processes must be invoked to explain regions Supporting Online Material www. maximum Kappa (17) 0. helped to shape present-day diversity in pinpoint regions for inventory work and habitat (iv) strong phylogeographic structure between 26. Field sampling isassemblages (coand/or vicariance distributed taxa. Brazil. 2Biology Department. Instituto de Quaternary Pierce. protection before we lose a substantial fraction refugia. Markl. (1978). 20. Annu. ate andetboreal systems (1). semilineatus. 6 FEBRUARY 2009 tions of each of the target species along the At.. J.temperate C. refugia (Tamura-Neiand driven observed across Fig. while borrowing strength natures of population expansion (23) are found the LGM (0 to 20 kybp. In H. K. species li (12): studied nsals or with ants e acouslthough s attracts s to siga basal t expect nea. Behav. and (ii) assemblage. 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. accepted 28 November 2008 10. Building spatially explicit map the palaeodistribution of endemic first demographic scenarios suggested by the climate-based models.4Departamento de Zoologia. 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. 10. K. Elmes. Scott-Phillips. B. long-term persistence of populations in and E). Z2 < 3) = 5. conservation Jones. and simultaneous Bayesian analyses of multispecies ecological niche modelsLe Moli.1 to 1. Maximum (LGM. P.2 million years before present. (ii) genetic sigsistence and population sistence and populationpopulation expansion in show a mid-sized refugium instructure. R. scale.models across the three codistributed species.approach differs from previous methods by dius to ant-butterfly acoustics. 9). G.org 786 6 H. albomarginatus and H. phylogeographic predictions for and individual palaeoclimate models of species both habitats to Entomol. Pleis.edu 28.sciencemag. T. R.sciencemag. Originally extending motraditional species-by-species approach. ause of n idenal proions of m sub- *To whom correspondence should be addressed. priorities D. and H.Bayesian analysis allowed us to estimate conto a lesser extent in H. data niches. Hölldobler. mental change and thereby provides a means for the LGM (14.70]. J. power and be more informative than qualitative for H. albomarginatus and H. 8. previously undersamrefugia in previously undersamand São Paulo particularly emphasizingSimilarly. These analyses support both the Bahia refugium [population 2 (Fig. Thomas. W. parameters to vary.the model predictions to coverareas. Three (middle).tropics. 0. 167 (1998). Mori. J. This is not surprising. 7). faber.carnaval@berkeley.. or 6 kybp.(1). Although this southern area is higher than the other spe. hypothesis testingtesting stability/expansion. C. Proc. Relative to nuclear loci. Acoust. We focus on three common species of tree frogs that are widely distributed along the Brazilian Atlantic forest: Hypsiboas albomarginatus. In H1.e. Vereins hotspot most species-rich. provide insights about processes shaping genetic 11.mapped globally. (ii) genetic sig.3 Carolina Carnaval. persistence of populations in isolated refugia for palaeoecological and genetic evidence (28).000 to 1. 004). In H2. faber. M. 2 Célio F. 88 (2008). Nov. Elmes. B 265. K. 18) and suggests the occurrence of forest. 4 Departamento de Zoologia.1163583 L L 9). 91 (2004). Seufert.there is strong support for recent colonization in sets. 60. Proposed method of biodiversity prediction. J. as colonization of refugial regions. 1% between colonized) both Sampling across predicted stable and unstable areas refugia and unstable (recently colonized) areas. Brazil. or across taxa.84].cesses must be invoked to explain regions of *To whom correspondence should be addressed. The results also agree generally with forest models published previously (14). S3 phylogeographic predictions distribution of congruence versity. 6). Sig. University of California. R.org 6 (one in scale. Using the same framework to test for longCollectively.for understanding current pat. biodiversity prediction. large Soc. R. J. Biol.term persistence of refugial populations. J. 23. model-based hypothesis formulation (middle). All taxa unstable nature of population expansionthe unstable from Fig.conflicting evidence (2. This reveals a Apollo within the Brazilian Atlantic forest hotspot. as opposed climatic conditions accurately predict distribuV. population 2 is modeled as being colo. G. tribution modeling (top). 1419 (1999). 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). under paleoclimates.300. 30. We apply population expansion the world’s signature of this approach to one of in unstable Quaternary climate change. Instituto de Biociências. we first map the palaeodistribution of 22 July 2008. scenarios suggested less than 8% of its range (8). as well as in the Bahia refugium area southern (unstable) areas after the LGM (Z2 = 3. biodiversity distribution data from within hotspots are too sparse should consistently show (i) higher genetic di16. CA 94720–3160.allowing for postisolation migration (Fig. nández. J. In H. 339 (1994). 13 25. mtDNA data) can be feasibly collected.areas. hypothesis testing and refugial area predicted to be less range of refugial regions after the Last Glacial Maximum stable by the palaeomodels. we J. SP 3526-4100. In all species. L.sciencemag.for introducing high endemism (5. circularity to observed SCIENCE VOL (10). 6). We hypothesize that these areas received a significant influx of migrants from adjacent. 4. Today’s fragments harbor one onethe largest perWe apply this approach to of of the world’s centages of endemic notoriously the world. 18) and suggests the occurrence of small forest refugia in the southernmost range of the putative Bahia refugium (19). (2000).*Soc. Recent studies from Materials and subtropicalMethods have usefully employed post biomes SOM Text hoc S1 and S2 Figs. J. J. Maile. J. Z2 > 0) = 4. Charles or www. in BrazilBoomsma.sciencemag. Audio S1 to S4 22 July 2008. the method intersects Species Map of predicted Current & extension of the The palaeomodeling and 21 kybp) pre(6000 years beforepredicted distributions under current condipresent. S1 and S2) (13). SP 055008-090. in persistence have usefully employed post hoc tropical biomesand hence diversity. the results identify the central H. the for 1. 18. Pierce al. J. the molecular analyses contrast the provide insights about processes shaping genetic fit of assemblage-level data to the on them. Building Audio S1 to S4 on them. K. southeastern refugium of intermediate size is also predicted (“São Paulo refugium”). agreeing withregional scale. P. species 15. 9. genetic diversity (21) is an sequences from the southernmost refugial sites order of magnitude larger in the central (Bahia) [population 1 (Fig. faber. M. Proc. served as a Entomol. even when offer evidence to the contrary. Cocroft.rectly modeling historical processes. Rev. Wardlaw.

Population genetic summary metrics used in model validation. Sample size. R. 264 (1993). of a were Hs Mantel’sMantel’s the total only from q. Genetics 155. Supporting Online Material www. 20. W. Amphibian Species of the World: 14. D.M.499 contiguous localities distributed within–20. (A) H. Kreitman.003 0.. C.031 0. 56. P. Brazil.). Because predicted (81.R. A. albomarginatus and H. analyzed the data.2. C. Graham.0003) H.8% 5.003 0. 2. C.015 0. 29.3 – 7. 499 (2004). coef.). E. 13. faber Stable (BA) 28 94 0.456) H. Cabanne. but also from all possible combinations of spatially number ofof samples. Frost. Miyaki. 20. 13. therefore.003) Unstable 27 22 0. 80) (0. C. (Top)geographic structure withinwithin refugia (2.C. 0.S. Acad.111 (0. 678 (1993).001) (970 bp) faber (13. S. Linn. H. S. Amaro. E. H.0001 0. C. J. 222 (2008). Damasceno. Egito. 23) (81. Moritz. J. 10. max. D. P.05 probability level. R. In both cases. R. 227 (2002). SS Table 1. Japp.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. R. G. BA. Stable (BA) 28 0. (B) and (C) Models of refugial sites (population 1) and unstable. Signatures of ofand andsemilineatus. Turong for DNA-sequencing assistance. E. Hugall. M. 155) population expansion. Haddad. 5.248) (771 bp) (13.. (B) H. Behling.C. 0. D.) value) value) (P value) (P of spatially number max. G.009.-P. 760 (2008). n. max.004) (771 bp) (13. P. L. M. 714 (1990).778 Hs Mantel’s corr.(bp). Ed. McNeil. Anfibios da Mata Atlântica (Atlantic Forest Amphibians) (Editora Neotropica.012. U.456) (0. Raftery.981 0. L. São Species-specific stability to the refugium Pernambuco modeled albomarginatus. Ferreira. semilineatus bp) Stable (BA) 28 71 0. (9. the recent colonization model. Meyer.8% 5. Wefer. 0. 3.255 0. R. 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. 2008). semilineatus. Phylogenet. beyond the albomarginatus.004 0. 0. Fig.refugial (stable)In all species.031 0. 5.org Table 1.082)–11. M. (B) H. Moritz. 94 155) (0. E. 10331 (2003). M. BA. d’Horta. Evol. R. M.C. 80) (0. Notesemilineatus.357) Unstable 15 9 0. S. 26. Bahia.outside (south of) the refugia are genetically unstable area albomarginatus and H.. Lett.4% (Bottom) The 50% majority-rule Symbols indicate localities sampledde. Fundação de Amparo à Pesquisa do Estado de São Paulo and Conselho Nacional de Desenvolvimento Científico e Tecnológico (grants to C. Biol..114(0. 23) (42.460) (south of SP) (0. 13 (2005). semilineatus Stable (BA) 28 71 0. J. 0. S. 13) (14. Am. 5. A.020. J. F.J.580) (south of BA) (0. In a world of ever-accelerating environmental changes.018 0. 21. F. and A.php. BA. Species Species Area Area (min. Palaeoecol.org/ herpetology/amphibia/index. Arz. B. Proc.. Moritz.255 0. H. albomarginatus Stable (BA) 36 207 (970 bp) (13.001) 0.580) coef. J. 0. H.C.498 (0. R.115) (0.. Santos.115) (0.016 –13. 3A). M. Sequences are deposited in GenBank (FJ502639-FJ502822).C.001 P values in0. preventing a full underwww. O. collected the data. São Paulo refugia.034. Signatures high geographic structure refugia (2. Res. Biol. number of segregating sites.) from(Pall possible combinations value) (min. Wu. Haddad.003 0. Araújo et al. albomarginatus Stable (BA) of BA) 36 207 0. M. Because predicted refugia were often larger than predicted unstable (recently colonized) areas. Biotropica 32. 761 (2007). F.8% Symbols indicate beyond the denote with sequences from thesampled for rooted refugia inferredlocalities othmolecular the target species. (B) H. P. J.org distantly related groups of Atlantic estation in this region relative to the more ex. forest endemics. Radiology 143. 22 155) Unstable refugia were often larger than predicted unstable (recently27 colonized) areas.221) (0. W. faber Stable Stable (SP) (BA) 28 15 94 0.A. C. A. Genetics 143. V. 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. 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. C.029) H. 659 (2005).029) (0. (A) Simulated models H1 (long-term persistence) and H2 (recent colonization). Asterisks and northern of the target species. semilineatus Stable (BA) 71 0.034) H. Prado. n. K.546 (0. Monahan and R. Percentages indicate Tamura-Nei corrected distances between (root not shown). C. J. 757 (1994). R. BMC Evol.029) value) (0. J. In contrast.072) (0.044) (0. G. Not only could much unique diversity (south of the (0..8% rooted(20).003 0. W. A.the (Bottom) The 50% majority-rulebeyond denote refugia inferred the central Bayesianrangesareas. Cassimiro for field work assistance. C. Pätzold.H. J. Fay.05 probability level.. Parentheses encompass minimum and maximum values from subsamples.082) (0. B. Toledo. Singhal.028 –5. S.8% 4% 5. 90. Biogeogr. SP.357) (0. M. 773 (1995). 4. J. and average D values of the former were obtained not only from the total qq Mean Dthe former Hs obtained notcorr.072) (0. (A) H.141) 0. the congruence between An Online Reference. this approach can help to guide research and conservation in other global hotspots or similarly complex tropical ecosystems. southern areas (population 2). central and northern areas. deTamura-Nei corrected distances between (root not shown). M. U. faber.H. The signature of extent H. 5. Stanisic. Nature 405.044) (0.001) (0. 1457 (1996).357) (0. 0. O. Pavan. C. 58) (0.546 the geographic extension of the unstable 0. note clades with posterior probability 4% 5.022) (0. J. 31. Sci. while explicitly accounting for the southern regions. F. 30.062 0. Filho.248) 0. of samples. Thick internodes de5.) (0. Conserv. J.014) (0. M. C.140 (0.456) high diversity in the central portionof SP) biome and conservation priorities have been heavily be lost. Nei. of segregating sites. Population genetic summary metrics used in model validation. albomarginatus per Stable pair (bp).C. C. Jetz. coef. J.580) –0. semilineatus. population 2 is modeled as being colonized from refugial population 1 subsequent to coalescent variance and the possibility of selection (26). 8 (2008).803 (0. Araújo. 1180 (2004). Rodrigues. 13) max.amnh. bold highlight statistical significance at 0. but max. Meas. 907 (2000). H. C. 0.026 2009 787 (771 bp) (13.007. S. L. B. Table 1.041) 0. years before present. version 5. and provide evidence biased toward southern and southeastern Brazil quickly erase the signature of the historical for population expansion in southern regions. 0. 8. faber.J. 49. Assoc. (P 0. 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. Rovito. Zaher for 2008 VOL 323 SCIENCE www. Nature 404.6%). Gosling. Mol. Kass. Scale bar.. 100. (B to E) Hyperposterior (bars) and hyperprior (dashed) densities of Z2 (number of species evolved under H2) given data from three codistributed frog species. Giovanelli. L.028 –5. Sci. Gomes.787 by the amphibian data may be generalized to biome have been substantially underestimated. Pellegrino et al. 0. Soc. 6112 (2002).. 32. Biol. S. 8..004) n 28 S q Mean Da –17.sciencemag.0001 (south of BA) (0.981 (718 bp) (6. n. C.111 0.001 –11. New York. B. C. A.6 to extent inin H. current ranges of analysis.3 – sensus Bayesian phylogenetic 7% molecular analysis. 23) (81.C.436 (0. Quat.A.305 Stable Unstable (SP) 15 18 48 0. 99. This is serious.022) (0. A.A.2% divergence). Evol. 0. 23. The The diversity parameter and mean Da across Da across localities areper base pair (bp). Patton. K.016 –13. A. We thank U. Hickerson.041)(0. Morellato.007.C. sensus current phylogenetic trees. SP.436 H. S1 to S6 Tables S1 and S2 References 8 October 2008. (south of BA) (0. Santos. B.1166955 38 39 .044) (0.778 0.114 0. 103. 3. 2008). 31).305 much more SCIENCE VOL0. 179. jacent versus unstable areas in thedifferences Atlantic across localities (22) reflects more similar to each other.C. J. faber as as in as Bahia Bahia refugium area for otide Brazilian across localities (22) reflects more similar to each other. joint.. average net nucle. R. Slatkin. Cohen. C. (8. Palaeoclimatol.S. 16. Williams. In H2.) Sample size.) (min. Unstable(south of BA) 27 22 0. J. (D) and (E) Models of Pernambuco refugium (population 1) and Bahia refugium (population 2).B. 0. but ongoing habitat destruction could relative to southern areas. (A) H. Ecol.H. W.sciencemag. London 85. 322 (2008). 7.460) (718 bp) (6. Lessa.981 0. 23) (42. Loebmann. Tamura. Sã o Paulo refugium São Paulo refugia) relative to con.020. R.054 (P value) Unstable 15 0. Biol. W. Verdade. refugia were often larger than predicted unstable (recently colonized) areas. 383 (2001). 13) (14.São Paulo refugia. given the higher rate of defor.. Dixo. Natl.05–0. R. Behling. 17.787 323 (0. 0. 0.305 (0. 72 providing access to collections MNRJ and MZUSP. Percentages indicate er two congeneric species studied sensus Bayesian phylogenetic trees. SP. and M. average net nucle.) (min.076 0. Mayle. Scale bar.23) (970 bp) (13. Carnaval. M. demism and.and of the Bahia km. 15.072) probability level. A. 1987).498 (0. Hs test 36 is used to 207 localities are given base (BA) (23) detect H.001. sequences from the probability note 4% clades with clades with posterior oth5. Sci. Nei.015 0. Zina. Parentheses encompass minimum and maximum values from subsamples. I. G. number number of segregating sites. 400 km. 0. Sari.. Colwell. Divers. Araújo.221) had much higher stability relative to the south. Pernambuco modeled refugia in black. 19.outside (south of) the refugia are genetically unstable area for H.036 –17. L. Nature 345. Thick internodes 7% 5. designed the study.003 0.003) (0. 9. Stat. S.faber (0. Bahia. Psych.012.062 –20.023 6 FEBRUARY 2009 presented here show that the (SP) www. Press.M.corr. Trans. faber.114 0.) (0. Hanley.014) (0. Proc. 18. n. (0. 9. C.) (min. London B Biol.sciencemag. R. Ancestral population sizes are represented by (qt)1 and (qt)2. M.org SCIENCE VOL 323 6 FEBRUARY 0. Kremen et al. Muri. Kawasaki. ybp.) (min. B. A. B.T. P values inin bold highlight statistical significance at 0.018 –38. W. Caramaschi and H. Moussalli.041) (min. max.. Alexandrino. refugium albomarginatus.023 0. note clades withwith sequences from the oth7. accepted 9 December 2008 10. At a broader level.140 H.sciencemag. S.6% presence of two lineages that co-occur in the adA 6.076 0. 23) (42.778 (min.. n. Japp. 0. wrote the paper. max.conservation measures. Philos. Negrelle. although to to lesser as well well the in the refugium area for H.034) (0. Toledo. A.0001 Forest lizards (14.026 –38. U. 400 km.034) (0. D. Hijmans for discussions about the modeling work.436 Unstable 18 40 0. Genetics 138. mean a q. Da across H. G. Percentages indicate Tamura-Nei corrected distances between clades (20).460) (P0.6%).004) H. Evolution 47. J.028 –5.016 –13. (B) and (D) Postisolation migration not included in model.003 0. São Paulo. São Paulo refugia. D. J. 6. S. Fig. This reassures us that the processes uncovered by the amphibian data may be generalized to and help to explain patterns of Fig. and M. R. M. S.1 to 1.. although a a lesser otide differences rainforest. Sci. and average Da values Mean Da (min. A. and J.115) (0. 80) (0. 29 (1982). Note the absence of large current ranges regions(south of the Bahia and of the in the southern portion target species. V.S.0003) (0. 35. (6. jacent refugia. Kautskyi.036 0. Smith and D. 1405 (2000). C.T. F. Queiroz. Funding was provided by the NSF (awards DBI 0512013 to A. tensive forests in São Paulo and southern Brazil Unstable 40 0. NoteGenetic diversity large B (C) H.036 –17.B. HABC analyses. 31). 28. Natl. J. Mol. areas. and average Da values of the former were obtained not only from the total number samples. 5. Lima.004 0. 58) (0.009. Puschendorf. Molecular Evolutionary Genetics (Columbia Univ. (Top) Species-specific stability (Top)Paulo refugia) relative black. da Silva. Y. (C) and (E) postisolation migration included in model.546 (0. 359. E. Asterisks Sã o Paulo refugium refugium (C) H. J.1 to 1. 7. Nelson.034. parameter (min. L. electronic database accessible at http://research.) q(min. 9. faber (0.F. Thick internodes fortrees. 25.004 0. 37 (1960). 15 July (2000).6% greater than 90%. semilineatus. Hewitt. H.248) (south of SP) (0.. 0.054 40 0. Proc.001 –11. highly threatened ecosystems.023 0. 22. M. Peixoto.H. Kolbe. Filho.6% greater than species studied er two congeneric 90%. er two congeneric species studied 5.020.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. 788 model-based demographic hypotheses and 6 FEBRUARY 2009 (American Museum of Natural History. The lack of lack of signature of H.141) (south of BA) (0.diversity parameter q q andmean Sample size. F. A.014) (0. large Bahia refugium stable (C) H.R. R.. 27. Cook.031 0. DEB 0743648 to M. L. Parentheses encompass minimum and maximum values from subsamples. J. molecularcentral and northern 400 Asterisks analysis. Pounds for discussions about earlier versions of the manuscript. Curcio. Beerling. q. Rahbek. testtest (23) is usedto detect localities are given given per base pair Hs Hs (23) is used to detect population expansion. M. H. 11. [CrossRef] F. Science 320. Bush. molecular studies.221) Unstable 15 9 0. Ledru et al.141) area.499 (0.. 29) and birds (30) also show 18 Because collection efforts.054 (0. References and Notes 1. Soc.1126/science.076 0.012. J.C. 24.org/cgi/content/ full/323/5915/785/DC1 Materials and Methods Figs. M. F. and M. Ecography 31. we predict that genetic diversity and processes that led to it.sciencemag.0003) Stable central region 15 48 0. Pereira.009.) (min. T. alsomax.6 to high Species-specific stability maps. faber H.2. DEB 416250 and DEB 0817035 to C.015 0.8% rooted posterior probability (Bottom) The 50% majority-rule congreater than 90%. All authors discussed the results and commented on earlier versions of the manuscript.001. refugia. inferred the absence of denote refugiafaber. A. C. 786 (2000). for H.140 (0. F. C. 9 58) (0.Bahia. in putative C C Fig. 632 (2006). da Silva. Materials and methods are available as supporting material on Science Online.082)–38.007. J. 1187 (2008). Pernambuco modeled refugia in maps. max. S. refugia in black.803 www. faber.. Natl. E. New York.001.062 –20. Because predicted population expansion.034. 12.M. Ballard. The diversitymax. Tajima.499 (south (0. 19. n.111 0.022) (0. E.018 0.) and max.803 48 0. M.F. area. Tabarelli. O.255 0.3 – clades (20). and C. In all species. * of the Brazilian Atlantic rainforest. in the the southern portion * in the forest (south of the Bahia andmaps. K. Acad. C. Palaeogeogr.4% 7% Sã o Paulo refugium 7.con(root not shown). Acad. Barros. our method benefits from a multitaxon approach. max. Distrib.003) (0. Species Area (718 (14. P values bold highlight statistical significance at 0. Population genetic summary metrics usednin n model validation.026 0. impeding more effective and help to explain patterns of diversity in other.498 –0. 2. sites located B population expansion (23) are found in the C Mybp.

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