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time of their origin, followed by long periods in which basic body plans and ways of life are retained. What is missing are the many intermediate forms hypothesized by Darwin, and the continual divergence of major lineages into the morphospace between distinct adaptive types. The most conspicuous event in metazoan evolution was the dramatic origin of major new structures and body plans documented by the Cambrian explosion10,11. Until 530 million years ago, multicellular animals consisted primarily of simple, soft-bodied forms, most of which have been identified from the fossil record as cnidarians and sponges. Then, within less then 10 million years, almost all of the advanced phyla appeared, including echinoderms, chordates, annelids, brachiopods, molluscs and a host of arthropods. The extreme speed of anatomical change and adaptive radiation during this brief time period requires explanations that go beyond those proposed for the evolution of species within the modern biota.

Towards a new evolutionary synthesis

Robert L. Carroll
New concepts and information from molecular developmental biology, systematics, geology and the fossil record of all groups of organisms, need to be integrated into an expanded evolutionary synthesis. These fields of study show that large-scale evolutionary phenomena cannot be understood solely on the basis of extrapolation from processes observed at the level of modern populations and species. Patterns and rates of evolution are much more varied than had been conceived by Darwin or the evolutionary synthesis, and physical factors of the earths history have had a significant, but extremely varied, impact on the evolution of life.

Robert Carroll is at the Dept of Biology and is Curator of Vertebrate Paleontology, Redpath Museum, McGill University, 859 Sherbrooke St. West, Montreal, PQ, Canada H3A 2K6 (

arwins theory of evolution was based on the primarily uniformitarian concept that the processes of genetic variation and natural selection, studied in modern populations, are sufficient to explain the large-scale patterns of diversification that have occurred throughout the billions of years of life on earth. The persistence of this viewpoint is evident in recent editions of numerous university textbooks, three of which were reviewed by Moore1. Moore specifically cited the uniformitarian approach of Ridley in bridging the gap between population level phenomena and larger scale patterns in the history of life. Large-scale phenomena continue to be treated in a primarily historical manner, with little consideration for the forces that are responsible for the origin and long-term perpetuation of basic body plans, major changes in structures and ways of life, or the influence of abiological factors on critical events in the history of life. The focus of these textbooks, and the majority of papers published in the journal Evolution, on modern species belies the great advances in other areas of science that contribute to the understanding of large-scale, long-term evolutionary phenomena. Research in many disciplines over the past 40 years has demonstrated that the patterns, processes and forces of evolution are far more diverse than hypothesized by Darwin2 and the framers of the evolutionary synthesis3: (1) Increasing knowledge of the fossil record and the capacity for accurate geological dating demonstrate that large-scale patterns and rates of evolution are not comparable with those hypothesized by Darwin on the basis of extrapolation from modern populations and species4. (2) Knowledge of plate tectonics indicates that changes in the position and configuration of the
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continents, and their influence on climate and the capacity for dispersal have been major forces in driving evolutionary change5. (3) The elaboration of phylogenetic systematics has provided a specifically evolutionary methodology for establishing relationships6. (4) The most spectacular contributions have come from the field of molecular developmental biology, making it possible to understand the specific manner in which major changes in the anatomy and physiology of organisms have occurred, and how such changes can be influenced by natural selection7. It is now necessary to incorporate this rapidly increasing body of information into an expanded evolutionary synthesis.

Empirical evidence from the fossil record The most obvious contrasts between the darwinian view of the patterns and the rates of evolution, and the evidence that has since been documented by the fossil record, are illustrated in Fig. 1. Darwin used the only illustration in the first edition of The Origin of Species to explain his hypothesis that the patterns of evolution over hundreds of millions of generations were the same as those at the level of populations and species. In fact, they are clearly distinct in all taxonomic groups4,8. Evolution at the level of populations and species might, in some cases, appear as nearly continuous change accompanied by divergence to occupy much of the available morphospace9. However, this is certainly not true for long-term, large-scale evolution, such as that of the metazoan phyla, which include most of the taxa that formed the basis for the evolutionary synthesis. The most striking features of large-scale evolution are the extremely rapid divergence of lineages near the

Evolution and development Most of the history of life, from 3.5 to 0.6 billion years ago, was dominated by extremely slowly evolving unicellular organisms12,13. Their potential for increasing complexity was restricted by the small size of the genome and the limited capacity for genetic recombination. The low concentration of atmospheric oxygen constrained their size and precluded the formation of supporting skeletons. Aggregation of identical cells was possible, but the development of organisms with complex body plans composed of many kinds of cells was not possible. Within these constraints, the most significant evolutionary events to occur in the mid-Proterozoic (approximately 1.5 billion years ago) were the endosymbiosis between species of the Archaea and the Eubacteria, which led to the origin of the mitochondria and the chloroplasts of eukaryotes14. These were unique events, only vaguely comparable with other aspects of the horizontal transfer of genetic material that can be studied in living species15. Beginning approximately 600 million years ago, larger, soft-bodied animals appeared in the fossil record, including species resembling sponges and cnidarians, as well as trails and burrows formed by bilaterally symmetrical, worm-like forms with a unidirectional digestive track. Then, between 530 and 525 million years ago, all more advanced metazoan phyla appeared and the most rapidly radiating group, the arthropods, quickly reached a level of diversity approaching that of their modern marine descendants16. This explosive evolution of phyla
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0169-5347/00/$ see front matter 2000 Elsevier Science Ltd. All rights reserved.



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Fig. 1. (a) Darwin2 used this figure to represent the patterns and rates of evolution at both the level of populations and species, and among higher taxa. The intervals between the horizontal lines were given by Darwin as either thousands or tens of thousands of generations at the level of species or as millions to hundreds of millions of generations at the level of families and orders. The position along the horizontal axis indicates the degree of morphological difference. The angles of the lines represent the rate of evolution; vertical lines indicate stasis. (b) A diagram of the fossil record of the major metazoan phyla showing their first appearance in the late Proterozoic (Vendian) and early Paleozoic, and the persistence of basic body plans throughout the Phanerozoic. The essentially vertical orientation of the clades indicates that each retained a basically similar body plan throughout its known history. The width of the lines is proportional to the number of families known from each geological period, and to some extent their anatomical diversity8. Other phyla that are known from the Cambrian, but have a comparatively incomplete fossil record, include the Onychophora, Ctenophora, Priapulida, Phoronida and the Tardigrada.

with diverse body plans is certainly not explicable by extrapolation from the processes and rates of evolution observed in modern species, but requires a succession of unique events. The development of complex body plans, with many distinct cell types and anatomical structures, required a new system of genetic control that is not present in unicellular organisms. This is based on a distinct genetic category, the Hox gene1720. Hox genes are unique to metazoans but evolved from a more inclusive group, the homeobox genes, which are also recognized in unicellular eukaryotes and land plants. Homeobox genes code for specific proteins that activate other genes, and thus they regulate a host of processes within the cell. Hox genes are uniquely arranged in a linear sequence along the chromosome, which corresponds with both the linear and the temporal sequence of their activation along the anterioposterior axis of the embryo. (MADS-box genes have a comparable role in controlling the position of major structures in land plants21.) The number of Hox genes, arranged in a cluster along a chromosome, is broadly comparable to the degree of complexity of the organism, with one in sponges, four

to five in cnidarians, six to ten in most of the higher metazoan phyla, and up to 39, arrayed in four Hox clusters on different chromosomes, in mammals22 (Fig. 2). These genes control the position and the expression of the major structural features of the body, including the elements of the head and the sequence and nature of the appendages. Although molecular homologies have been established for Hox genes throughout the metazoan phyla, the specific structures whose position they control can be different, as in the case of the distinct body forms of the deuterostome phyla Chordata and Echinodermata23. This is because the Hox genes act as switches to control the expression of a variety of genes, which in turn control different structures and cell types. The origin of multicellularity and complex body plans among animals was a unique phenomenon, dependant on the evolution of Hox genes near the end of the Precambrian (late Neoproterozoic). Once evolved, their subsequent duplication and divergent change in adaptively distinct lineages established the basis for the radiation of the many metazoan phyla24. Most phyla have apparently retained a relatively constant number of

Hox genes since the Cambrian. A striking exception is the Chordata, in which the largest scale change occurred between the cephalochordates and early vertebrates, when the number of Hox clusters duplicated twice, resulting in four clusters by the time early bony fish (Osteichthyes) appeared some 415 million years ago. We can recognize a hierarchy of change associated with Hox genes between and within phyla25. Arthropods are distinguished from annelids by the presence of two different Hox genes26, Ultrabithorax (Ubx) and abdominal A (abd-A), which diverged independently from a single gene in the common ancestor of these phyla. Within the arthropods, what differentiates insects, myriapods and crustaceans is not the number of Hox genes but the control of their area of expression within the body. The anterior boundary of Ubx/abd-A (the genes are co-expressed) is correlated with transitions in appendage morphology along the anterioposterior axis (Fig. 3). The Hox genes control segmental identity by regulating the expression of downstream target genes. In insects, absence of legs on the abdomen results from repression of the Distal-less (Dll) gene by the gene
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Fig. 2. Hox clusters among multicellular animals, showing the degree of homology between selected phyla. Horizontal lines connect Hox clusters, resulting from tandem duplication of a single ancestral Hox gene. The hypothetical common protostome/deuterostome ancestor is thought to have given rise to all higher metazoans. HoxaHoxd indicate the four Hox clusters in vertebrates, resulting from two successive duplications of the ancestral chordate Hox cluster (data from Refs 17,22,26).

products of Ubx and abd-A, but this does not occur in centipedes or crustaceans because Hox-mediated repression has not yet evolved in these classes. Changes in the number of Hox genes and their control over the expression of other genes can explain how distinct body plans and appendages evolved in the late Neoproterozoic and early Paleozoic, but they also provide a basis for explaining other structural changes observed throughout the subsequent history of life. Among vertebrates, changes in the area of expression of specific Hox genes have been used to explain the transition between the fins of sarcopterygian fish and the limbs of Devonian amphibians27, and differences in the shape and relative number of cervical, thoracic and lumbar vertebrae in amphibians, birds and mammals28. Other studies have demonstrated that morphological differences between closely related species and even polymorphisms within populations can result from modification in regulatory genes that influence quantitative aspects of the expression of a variety of structural genes.29 More broadly, the study of Hox genes has revealed a far different pattern of genetic control over structural features, throughout metazoan evolution, than those hypothesized by either mendelian or population genetics. Long-term evolution is not simply the result of selection of alternative alleles controlling specific
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traits, or the progressive accumulation of new mutations in an additive fashion, as proposed by quantitative genetics. It is now recognized that development involves a hierarchy of genetic control, including the precise timing and the position of expression of the Hox genes themselves, and the regulation of a cascade of downstream genes, together with interactions with the products of other Hox genes, commonly producing broadly pleiotrophic results in many tissues and structures30,31. Evolutionary changes over a wide range of magnitudes can occur by mutations at any point in this genetic complex.




Changes in the physical environment The evolution of Hox genes was a precondition for the origin of multicellularity in the late Proterozoic, but additional factors are necessary to explain the abrupt radiation of advanced metazoan phyla in the Early Cambrian. Major environmental changes were occurring during this period, including substantial increases in the availability of atmospheric oxygen32, which would have enabled the achievement of larger body sizes and the formation of calcareous or phosphatic skeletons in many lineages. The position and configuration of the continents were also undergoing major changes: in the late Neoproterozoic, many of the continents were grouped near the South Pole. Between 750 and 570 million years ago

Fig. 3. Expression domains of two Hox genes, Ultrabithorax (Ubx) and abdominal A (abd-A), overlap (indicated by dark shading) in an onychophoran and several arthropods. The anterior boundary of Ubx/abd-A correlates with transitions in appendage morphology along the anterioposterior axis. In the Onychophora, the boundary lies between the second to last and last lobopod, in the centipede between the poison claw and the first walking leg, in Artemia between the gnathal and thoracic segments that bear distinct limbs, and in Drosophila between the last thoracic segment bearing legs and the abdomen. Insects are unique in lacking legs on the abdomen. This results from the repression of the gene Distal-less (Dll), by the genes Ubx and abd-A, which would otherwise regulate the formation of legs (from Ref. 26).


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gressive cooling in the Cenozoic, resulting in long-term changes in the diet and dentition of Northern Hemisphere mammals, culminating in the origin of the arctic and tundra fauna of the Pleistocene37. Rifting of continental plates in the Pliocene and Quaternary produced the East African Great Lakes, within which occurred the explosive radiation of cichlid fish over periods ranging from 5 million to as short as 12 000 years38. The Milenkovitch cycles (i.e. changes in the earths axis of rotation and the eccentricity of its orbit) are associated with significant climatic changes over intervals of between 20 000 and 100 000 years, and El Nio produces measurable evolutionary changes at time scales of less than a decade (e.g. changes in the length and height of the bill of avian predators, associated with feeding on different types of prey, which have differing abundance depending on the amount of rainfall).


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Fig. 4. The changing distribution of continents between the late Precambrian (late Neoproterozoic) and the Cenozoic. (a) During the late Neoproterozoic, the continents were grouped close to the South Pole and the earth underwent a series of continental glaciations (shaded areas), with the ice sometimes approaching sea level, even at tropical latitudes, suggesting severe cooling of the entire world. (b) In the Permian, most of the continents were joined into a single land mass, resulting in great similarity of land animals throughout the world. The coalescence of the continents might have restricted the heat flow from the earths core, leading to explosive volcanism at the end of the Permian, which contributed to the most drastic period of mass extinction in the history of life. (c) By the Late Cretaceous, the continents had drifted apart resulting in far greater endemism of terrestrial faunas, few barriers to oceanic circulation and an equable climate over the entire earth. (d) By the middle Oligocene, Antarctica had separated from both South America and Australia. This resulted in the formation of the Antarctic circumpolar seaway, which isolated Antarctica thermally and led to the formation of the Antarctic icecap. In the late Cenozoic, the Arctic ocean became effectively isolated from the Atlantic and Pacific oceans, which might have contributed to the formation of the continental ice sheets that spread over North America and Eurasia in the Pleistocene. [Maps (a), (c) and (d) from Ref. 5; map (b) from Ref. 45.]

there were several episodes of continental glaciation affecting many areas of the world (Fig. 4a)5,33,34. However, at the end of the Proterozoic, the southern continents began to move away from one another and the world climate began to ameliorate. Not only higher temperatures but also the increase in the coastlines and the areas of the continental shelf, would have augmented the space available for marine life. These physical factors might have culminated, over a relatively short time, in conditions that fostered the differentiation of a multitude of distinct adaptive strategies and body patterns that we see in the distinct metazoan phyla. What distinguished this time further was the absence of any pre-existing complex multicellular animals that could act as predators or competitors of

the early members of the modern phyla. The entire aquatic world was open for them to conquer. The latter was a unique phenomenon, but major changes in the position of the continents have been a continuing factor in the reshaping of the physical environment and climate. As stated by Knoll35: On the geological time scales on which evolution is played out, the physical development of our planet may be a major engine of evolutionary change. Changes in the position and configuration of the continents have influenced the patterns of evolution at many different time scales. The coalescence of the continents in the Permian is thought to have been a major factor in the mass extinction at the end of the Paleozoic36. Changes in global circulation led to pro-

Integration From the time of Darwin, through the formulation of the evolutionary synthesis, evolution was studied and taught primarily on the basis of what can be learned from modern populations and species. The fossil record documented the history of life, but provided few unique concepts to explain long-term, large-scale evolutionary processes. Subsequently, knowledge of the succession of fossils covering 3.5 billion years, plate tectonics and mass extinctions39 (Evolution on Planet Earth: The Impact of the Physical Environment, The Linnean Society of London, 67 May 1999) showed that physical changes during the history of the world have had a profound impact on its biota. More recently, knowledge from molecular biology has revealed how genes control development and how modifications in these genes can result in evolutionary changes of all magnitudes. The present generation of evolutionary biologists, whether trained as paleontologists, molecular biologists or population biologists, now has the opportunity to integrate this information into a new synthesis, to guide evolutionary research and teaching in the next century (Box 1). The flood of new techniques, information and concepts from molecular developmental biology is already resulting in extensive cooperation with paleontologists, reflected in joint studies of major morphological changes and the origin of new structures. This has proven especially effective in understanding the radiation of metazoans in the Cambrian and the origin and modification of appendages in both arthropods and vertebrates27,40. A new journal, Evolution and Development,
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has just been inaugurated and a new division, with this name, has been added to the Society for Integrative and Comparative Biology. Numerous recent books have dealt with this subject7,20,30,41. The needs and the benefits of this association were summarized by Schlichting and Pigliucci42: The time is ripe for evolutionary theory to actively integrate development into its conceptual and experimental arsenal, lest we squander a second opportunity at a true synthesis. However, as yet, there is relatively little integration of new evidence, from either molecular genetics or paleontology, into the publications on population genetics. This is especially conspicuous in the area of quantitative genetics, which continues to treat polygenic traits in a statistical manner, as if they resulted from the additive effects of a large number of essentially equivalent genes43. Population genetics has also been slow to deal with the enigma that evolutionary changes that are rapid in terms of geological time (such as the origin of tetrapods and the evolution of horses) appear so slow, in comparison with the rates measured in living populations, that they are indistinguishable from a random walk. Rapid rates of morphological change can be observed from generation to generation as a result of rapidly changing selection coefficients44, but unidirectional selection is rarely maintained for a sufficient time to result in continuing morphological or physiological modification. Over the duration of most species, the intensity and direction of selection change repeatedly, either in an oscillating manner or in what appears to be a random walk. Over short intervals, the rates of change accord well with examples of the selection of alternative alleles emphasized in most textbooks. But, for much of the duration of the majority of species there is relatively little net change, even over hundreds of thousands of years. The relatively rare events involving the origin of major new taxa or significant morphological divergence at the species level require much greater than normal consistency of directional selection. Cooperation between population geneticists and paleontologists is necessary to provide a realistic bridge between the rates and forces of evolution among organisms at the level of modern populations and the patterns observed within genera, families and orders. Researchers could make use of field observations to establish models that incorporate parameters such as: the duration of essentially unidirectional selection, which is necessary for establishing recognizable changes in the morphology and the physiology of a variety of traits in species with different generation periods, population
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Box 1. Requirements for an expanded evolutionary synthesis

Recognition of the importance of physical events in the history of the earth as a driving force of evolution, over time scales ranging from a decade or less (e.g. El Nio), through tens and hundreds of thousands of years (Milankovitch cycles and episodes of continental glaciation), to unique events that re-set the pattern of evolution for the rest of the history of life (a progressive increase in atmospheric oxygen leading up to the Cambrian explosion and tectonic events associated with the end-Permian extinction). Utilization of information, generated by molecular developmental biology, to investigate the wide range of evolutionary phenomena from the genetic control of body form in different phyla, through establishing the position and configuration of appendages in different clades within specific phyla, to the regulation of anatomical and physiological differences that are subject to selection within species. Employment of emerging knowledge of the mutual interaction of genes controlling quantitative traits to formulate a truly descriptive, rather than a statistical, methodology for understanding how natural selection controls their evolution. Establishment of quantitative models to investigate the changing patterns of selection and structural modification in well known fossil lineages that record significant morphological change associated with adaptation to different environments and/or ways of life over varying time scales (e.g. the explosive differentiation of placental mammals in the early Cenozoic and the continuing changes in the dentition of rodents associated with progressive cooling and drying in the late Cenozoic). Recognition of the importance of horizontal genetic exchange throughout the history of life.

sizes, habitats and ways of life; and the range of intensity of selection for various traits that can act more or less continuously on species for hundreds or thousands of generations without leading to extinction. These factors could be estimated over a wide range of time scales in a variety of organisms for which there is an extensive and well dated fossil record, such as many lineages of late Cenozoic metazoans. Other models would be necessary for unicellular and clonal organisms. However, over increasingly longer periods of time, any model would break down because the nature of the organisms and their genetic systems changed beyond the original parameters. Over the entire history of life, the nature of the earth and its atmosphere have changed to such an extent that none of the original types of organisms could survive today. No general model could account for the mass extinctions at the end of the Paleozoic and Mesozoic, or the subsequent changes in the earths biota. A new evolutionary synthesis requires: the integration of knowledge from all forms of life that have ever existed on earth; a thorough understanding of the geological history of our planet; detailed knowledge of the changes in the biology of development throughout all multicellular organisms; and an appreciation of the processes of genetic change, natural selection and speciation as they can be observed in modern populations.
I thank David Green for discussion and comments on the manuscript, and Elena Roman for preparing the illustrations. The referees provided many useful suggestions for improvement of the manuscript. Support for research was provided by the Natural Sciences and Engineering Research Council of Canada.

1 Moore, W.S. (1999) Teaching neo-darwinism; weak selection among evolution texts. Evolution 53, 635638 2 Darwin, C. (1859) On the Origin of Species by Means of Natural Selection, Murray 3 Mayr, E. and Provine, W. (1980) The Evolutionary Synthesis: Perspectives on the Unification of Biology, Harvard University Press 4 Carroll, R.L. (1997) Patterns and Processes of Vertebrate Evolution, Cambridge University Press 5 van Ander, T.H. (1994) New Views on an Old Planet (2nd edn), Cambridge University Press 6 Ax, P. (1987) The Phylogenetic System, John Wiley & Sons 7 Arthur, W. (1997) The Origin of Animal Body Plans, Cambridge University Press 8 Benton, M.J., ed. (1993) The Fossil Record 2, Chapman & Hall 9 Greenwood, P.H. (1974) The cichlid fishes of Lake Victoria, East Africa. Bull. Br. Mus. (Nat. Hist.) Zool. Suppl. 6, 1134 10 Valentine, J.W. et al. (1999) Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development 126, 851859 11 Conway Morris, S. (1998) The Crucible of Creation: The Burgess Shale and the Rise of Animals, Oxford University Press 12 Schopf, J.W. (1995) Disparate rates, different fates: tempo and mode of evolution changed from the Precambrian to the Phanerozoic. In Tempo and Mode in Evolution (Fitch, W.M. and Ayala, F.J., eds), pp. 4161, National Academy of Sciences 13 Knoll, A.H. (1995) Proterozoic and Early Cambrian protists: evidence of accelerating evolutionary tempo. In Tempo and Mode in Evolution (Fitch, W.M. and Ayala, F.J., eds), pp. 6383, National Academy of Sciences 14 Katz, L.A. (1998) Changing perspectives on the origin of eukaryotes. Trends Ecol. Evol. 13, 493497 15 Lake, J.A. et al. (1999) Mix and match in the tree of life. Science 283, 20272028 16 Will, M.A. (1998) Crustacean disparity through the Phanerozoic: comparing morphological and stratigraphic data. Biol. J. Linn. Soc. 65, 455500


17 Carroll, S.B. (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376, 479485 18 Meyer, A. (1998) Hox gene variation and evolution. Nature 391, 225228 19 Erwin, D. et al. (1997) The origin of animal body plans. Am. Sci. 86, 126137 20 Raff, R.A. (1996) The Shape of Life, University of Chicago Press 21 Purugganan, M.D. (1997) The MADS-box floral homeotic gene lineages predate the origin of seed plants. J. Mol. Evol. 45, 392396 22 Finnerty, J.R. and Martindale, M.Q. (1998) The evolution of the Hox cluster: insights from outgroups. Curr. Opin. Genet. Dev. 8, 681687 23 Wray, G.A. and Raff, R.A. (1999) Body builders of the sea. Nat. Hist. 107, 3846 24 Valentine, J.W. et al. (1996) Developmental evolution of metazoan body plans: the fossil evidence. Dev. Biol. 173, 373381 25 Gellon, G. and McGinnis, W. (1998) Shaping animal body plans in development and evolution by modulation of Hox expression patterns. BioEssays 20, 116125 26 Grenier, J.K. et al. (1997) Evolution of the entire arthropod Hox gene set predated the origin and relationship of onychophoran/arthropod clade. Curr. Biol. 7, 547553 27 Shubin, N. et al. (1997) Fossils, genes, and the evolution of animal limbs. Nature 388, 639646 28 Burke, A.C. et al. (1995) Hox genes and the evolution of vertebrate axial morphology. Development 121, 333346 29 Purugganan, M.D. (1998) The molecular evolution of development. BioEssays 20, 700711 30 Hall, B.K. (1998) Evolutionary Developmental Biology, Kluwer Academic Publishers 31 Nagy, L. (1998) Changing patterns of gene regulation in the evolution of arthropod morphology. Am. Zool. 38, 818828 32 Canfield, D.E. (1998) A new model for Proterozoic ocean chemistry. Nature 396, 450452 33 Kennedy, M.J. (1998) Two or four Neoproterozoic glaciations? Geology 26, 10591063 34 Hoffman, P.F. et al. (1998) A Neoproterozoic snowball Earth. Science 281, 13421346 35 Knoll, A.H. (1989) Evolution and extinction in the marine realm: some constraints imposed by phytoplankton. Philos. Trans. R. Soc. Lond. B Biol. Sci. 325, 279290 36 Bowring, W.A. et al. (1998) Tempo of the endPermian mass extinction. Science 280, 10391045 37 Martin, R.A. and Barnosky, A.D., eds (1993) Morphological Change in Quaternary Mammals in North America, Cambridge University Press 38 Keenleyside, M.H.A., ed. (1991) Cichlid Fishes: Behaviour, Ecology, and Evolution, Chapman & Hall 39 Chaloner, W.G. and Hallam, A., eds (1989) Evolution and extinction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 325, 239488 40 Coates, M.I. and Cohn, M.J. (1998) Fins, limbs, and tails: outgrowths and axial patterning in vertebrate evolution. BioEssays 20, 371381 41 Gerhart, J. and Kirschner, M. (1997) Cells, Embryos, and Evolution, Blackwell Science 42 Schlichting, C.D. and Pigliucci, M. (1998) Phenotypic Evolution, Sinauer Associates 43 Lynch, M. and Walsh, B. (1998) Genetics and Analysis of Quantitative Traits, Sinauer Associates 44 Grant, B.R. and Grant, P.R. (1989) Evolutionary Dynamics of a Natural Population, University of Chicago Press 45 Ziegler, A.M. et al. (1997) Permian world topography and climate. In Late Glacial and Postglacial Environmental Changes (Martini, I.P., ed.), pp. 111146, Oxford University Press

Laboratory selection experiments using Drosophila: what do they really tell us?
Lawrence G. Harshman and Ary A. Hoffmann
Laboratory selection experiments using Drosophila, and other organisms, are widely used in experimental biology. In particular, such experiments on D. melanogaster life history and stress-related traits have been instrumental in developing the emerging field of experimental evolution. However, similar selection experiments often produce inconsistent correlated responses to selection. Unfortunately, selection experiments are vulnerable to artifacts that are difficult to control. In spite of these problems, selection experiments are a valuable research tool and can contribute to our understanding of evolution in natural populations.

Lawrence Harshman is at the School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, NE 68588, USA (; Ary Hoffmann is at the Dept of Genetics and Evolution, La Trobe University, Bundoora, Victoria 3083, Australia (

istorically, it was recognized that laboratory selection experiments would be valuable for testing evolutionary hypotheses1,2 considerable progress has been made in their design. For example, the importance of adequate line replication (multiple independent sub-populations treated in the same manner) and of sufficient population size to avoid inbreeding when selecting on fitnessrelated characters has been established3. Although there are other useful genetic

approaches, selection experiments have advantageous features; these features include replication of selection treatments and controls, and a relatively high degree of control of the conditions under which the experiment is conducted4. Selection provides a genetic approach to magnify phenotypic differences between selected lines and control lines, and it can be used to measure direct and indirect (correlated) responses to selection5. Moreover, because selection experiments

allow for a relatively high degree of control over the evolutionary process, they provide an opportunity to observe evolution as it occurs and they can contribute to an understanding of physiological mechanisms involved in the response to selection4. From an evolutionary perspective, the ability to study correlated responses to selection is particularly valuable, because these responses can indicate the pleiotropic basis of evolutionary constraints resulting from trade-offs between characters6. Watson and Hoffmann7 selected for increased resistance to cold stress in adult D. melanogaster and adult D. simulans, and found that an increase in adult cold resistance was accompanied by a decrease in early fecundity in all replicate lines of both species, thus suggesting the presence of a trade-off. Indirect responses to selection experiments can be used to understand the mechanistic basis of tradeoffs by combining information on correlated changes in traits with correlated changes in potential mechanisms underlying the selection response. Importantly, correlated responses to laboratory selection can reveal traits and mechanisms whose association with the response to selection was not anticipated at the start of the experiment. In spite of the perceived value of laboratory selection experiments, their use in some contexts is limited; this article will address two areas of general concern.
TREE vol. 15, no. 1 January 2000


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