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PERSPECTIVES

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 earth’s 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 (robertc@shared1.lan.mcgill.ca).

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arwin’s 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
TREE vol. 15, no. 1 January 2000

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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(b) A diagram of the fossil record of the major metazoan phyla showing their first appearance in the late Proterozoic (Vendian) and early Paleozoic. Phoronida and the Tardigrada. four to five in cnidarians. Hox genes are uniquely arranged in a linear sequence along the chromosome. with one in sponges. what differentiates insects. The anterior boundary of Ubx/abd-A (the genes are co-expressed) is correlated with transitions in appendage morphology along the anterio–posterior axis (Fig. arranged in a cluster along a chromosome. 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. no. 3). vertical lines indicate stasis. as in the case of the distinct body forms of the deuterostome phyla Chordata and Echinodermata23. Priapulida. These genes control the position and the expression of the major structural features of the body. and among higher taxa. dependant on the evolution of Hox genes near the end of the Precambrian (late Neoproterozoic). include the Onychophora. Other phyla that are known from the Cambrian. but have a comparatively incomplete fossil record. arrayed in four Hox clusters on different chromosomes. The position along the horizontal axis indicates the degree of morphological difference. This is based on a distinct genetic category. The development of complex body plans. which are also recognized in unicellular eukaryotes and land plants. and thus they regulate a host of processes within the cell. the specific structures whose position they control can be different. which diverged independently from a single gene in the common ancestor of these phyla. and to some extent their anatomical diversity8. The origin of multicellularity and complex body plans among animals was a unique phenomenon. is broadly comparable to the degree of complexity of the organism. which in turn control different structures and cell types. Within the arthropods. Homeobox genes code for specific proteins that activate other genes. The Hox genes control segmental identity by regulating the expression of downstream target genes. the Hox gene17–20. and the persistence of basic body plans throughout the Phanerozoic. their subsequent duplication and divergent change in adaptively distinct lineages established the basis for the radiation of the many metazoan phyla24. 15. which corresponds with both the linear and the temporal sequence of their activation along the anterio–posterior axis of the embryo. in which the largest scale change occurred between the cephalochordates and early vertebrates. The angles of the lines represent the rate of evolution. (MADS-box genes have a comparable role in controlling the position of major structures in land plants21. Once evolved. absence of legs on the abdomen results from repression of the Distal-less (Dll) gene by the gene TREE vol. This is because the Hox genes act as switches to control the expression of a variety of genes. 2). in mammals22 (Fig. Most phyla have apparently retained a relatively constant number of Hox genes since the Cambrian. Hox genes are unique to metazoans but evolved from a more inclusive group.PERSPECTIVES Po r C i fe r ni a Pl dar a ia An tyh n e e lm M lid a in t he ol lu s sc a (a) a14 q14 p14 b14 f14 o14 e14 m14 (b) Cenozoic 23 65 Neogene Paleogene a10 a9 a8 a7 a6 a5 a4 a3 a2 a1 f6 d5 f7 f10 f9 f8 k8 k7 k6 k5 d4 i 4 i3 s2 m1 A B C D m10 e10 m9 l8 l7 m5 m4 m3 m2 m8 146 Mesozoic Cretaceous Million years ago (Mya) m7 m6 Jurassic Triassic 208 251 Permian 300 Carboniferous Paleozoic 363 409 439 Devonian Silurian Ordovician 490 Cambrian 544 Vendian 610 E Fig. myriapods and crustaceans is not the number of Hox genes but the control of their area of expression within the body. (a) Darwin2 used this figure to represent the patterns and rates of evolution at both the level of populations and species.) The number of Hox genes. Ctenophora. required a new system of genetic control that is not present in unicellular organisms. with diverse body plans is certainly not explicable by extrapolation from the processes and rates of evolution observed in modern species. The essentially vertical orientation of the clades indicates that each retained a basically similar body plan throughout its known history. 1. six to ten in most of the higher metazoan phyla. Although molecular homologies have been established for Hox genes throughout the metazoan phyla. Arthropods are distinguished from annelids by the presence of two different Hox genes26. with many distinct cell types and anatomical structures. 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. Ultrabithorax (Ubx) and abdominal A (abd-A). In insects. and up to 39. The width of the lines is proportional to the number of families known from each geological period. 1 January 2000 28 Br a Br chi yo op z o Ec oa da hi no de rm at a C ho rd at es Trends in Ecology & Evolution Ar th ro p od a . the homeobox genes. We can recognize a hierarchy of change associated with Hox genes between and within phyla25. but requires a succession of unique events. including the elements of the head and the sequence and nature of the appendages. A striking exception is the Chordata.

resulting from tandem duplication of a single ancestral Hox gene. the boundary lies between the second to last and last lobopod. than those hypothesized by either mendelian or population genetics. and the regulation of a cascade of downstream genes. Hoxa–Hoxd indicate the four Hox clusters in vertebrates. overlap (indicated by dark shading) in an onychophoran and several arthropods.31. in Artemia between the gnathal and thoracic segments that bear distinct limbs. as proposed by quantitative genetics.22. The hypothetical common protostome/deuterostome ancestor is thought to have given rise to all higher metazoans. Insects are unique in lacking legs on the abdomen. 26). no. products of Ubx and abd-A. 2. Hox clusters among multicellular animals. but additional factors are necessary to explain the abrupt radiation of advanced metazoan phyla in the Early Cambrian. In the Onychophora. Between 750 and 570 million years ago Onychophora Fig. and differences in the shape and relative number of cervical. Among vertebrates. This results from the repression of the gene Distal-less (Dll). 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. 1 January 2000 traits. the study of Hox genes has revealed a far different pattern of genetic control over structural features. showing the degree of homology between selected phyla. including substantial increases in the availability of atmospheric oxygen32. The anterior boundary of Ubx/abd-A correlates with transitions in appendage morphology along the anterio–posterior axis. 29 Trends in Ecology & Evolution . Ultrabithorax (Ubx) and abdominal A (abd-A). resulting from two successive duplications of the ancestral chordate Hox cluster (data from Refs 17. and in Drosophila between the last thoracic segment bearing legs and the abdomen. 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. Long-term evolution is not simply the result of selection of alternative alleles controlling specific TREE vol. but this does not occur in centipedes or crustaceans because Hox-mediated repression has not yet evolved in these classes. Evolutionary changes over a wide range of magnitudes can occur by mutations at any point in this genetic complex. Expression domains of two Hox genes. which would otherwise regulate the formation of legs (from Ref. 3. or the progressive accumulation of new mutations in an additive fashion. commonly producing broadly pleiotrophic results in many tissues and structures30. Drosophila Artemia Centipede Changes in the physical environment The evolution of Hox genes was a precondition for the origin of multicellularity in the late Proterozoic. Major environmental changes were occurring during this period. Horizontal lines connect Hox clusters. thoracic and lumbar vertebrae in amphibians. 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. 15.26). 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. birds and mammals28. The position and configuration of the continents were also undergoing major changes: in the late Neoproterozoic. together with interactions with the products of other Hox genes. many of the continents were grouped near the South Pole.PERSPECTIVES Annelid ancestor Lox7 pb Hox3 Lox6 Lox1/20 Lox5 Lox2 Lox4 Lox21 Onychophora/arthropod ancestor Protostome ancestor Common protostome/ deuterostome ancestor Ancestral chordate Mouse Hox clusters A Hoxa B Hoxb C Hoxc D Hoxd Hox groups in vertebrates lab pb Hox3 Dfd Scr ftz Antp Ubx AbdA AbdB 1 2 3 4 5 6 7 8 9 10 a-1 b-1 a-2 b-2 a-3 b-3 a-4 b-4 c-4 a-5 b-5 c-5 a-6 b-6 c-6 a-7 b-7 b-8 c-8 d-8 a-9 b-9 c-9 d-9 9 a-10 a-11 a-13 b-13 c-10 d-10 10 c-11 d-11 11 c-12 d-12 12 c-13 d-13 13 Paralogous genes d-1 1 2 d-3 3 d-4 4 5 6 7 8 Trends in Ecology & Evolution Fig. throughout metazoan evolution. which would have enabled the achievement of larger body sizes and the formation of calcareous or phosphatic skeletons in many lineages.29 More broadly. by the genes Ubx and abd-A. but they also provide a basis for explaining other structural changes observed throughout the subsequent history of life. in the centipede between the poison claw and the first walking leg.

even at tropical latitudes. information and concepts from molecular developmental biology is already resulting in extensive cooperation with paleontologists. leading to explosive volcanism at the end of the Permian. 45. most of the continents were joined into a single land mass. to guide evolutionary research and teaching in the next century (Box 1). 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. 4. 5. within which occurred the explosive radiation of cichlid fish over periods ranging from 5 million to as short as 12 000 years38. In the late Cenozoic.40. no. Changes in global circulation led to pro- Integration From the time of Darwin. The entire aquatic world was open for them to conquer. The Linnean Society of London. few barriers to oceanic circulation and an equable climate over the entire earth. The present generation of evolutionary biologists. changes in the length and height of the bill of avian predators. As stated by Knoll35: ‘On the geological time scales on which evolution is played out. now has the opportunity to integrate this information into a new synthesis. The Milenkovitch cycles (i. (a) Late Neoproterozoic (late Precambrian) (b) Late Permian Baltica Siberia Siberia Baltica South America South Pole North America North America Arm 60 °S Antarctica Africa South America Africa 3 Eq 0°S ua tor alia str Au India Antarctica Australia (c) Late Cretaceous (d) Middle Oligocene North America Euroasia North America Euroasia Africa South America Africa India South America India Antarctica Antarctica Trends in Ecology & Evolution Fig. but major changes in the position of the continents have been a continuing factor in the reshaping of the physical environment and climate.33. molecular biologists or population biologists. plate tectonics and mass extinctions39 (Evolution on Planet Earth: The Impact of the Physical Environment.’ Changes in the position and configuration of the continents have influenced the patterns of evolution at many different time scales. resulting in long-term changes in the diet and dentition of Northern Hemisphere mammals. the southern continents began to move away from one another and the world climate began to ameliorate. suggesting severe cooling of the entire world. which have differing abundance depending on the amount of rainfall). and El Niño produces measurable evolutionary changes at time scales of less than a decade (e. (c) By the Late Cretaceous. The fossil record documented the history of life. This resulted in the formation of the Antarctic circumpolar seaway. (b) In the Permian. Not only higher temperatures but also the increase in the coastlines and the areas of the continental shelf.5 billion years. These physical factors might have culminated. TREE vol. More recently. the physical development of our planet may be a major engine of evolutionary change. (c) and (d) from Ref. However. (a) During the late Neoproterozoic. The coalescence of the continents might have restricted the heat flow from the earth’s core. over a relatively short time. [Maps (a). which isolated Antarctica thermally and led to the formation of the Antarctic icecap.g. the continents had drifted apart resulting in far greater endemism of terrestrial faunas. in conditions that fostered the differentiation of a multitude of distinct adaptive strategies and body patterns that we see in the distinct metazoan phyla. resulting in great similarity of land animals throughout the world. with the ice sometimes approaching sea level. The changing distribution of continents between the late Precambrian (late Neoproterozoic) and the Cenozoic. associated with feeding on different types of prey. 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. 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. which contributed to the most drastic period of mass extinction in the history of life. knowledge of the succession of fossils covering 3. reflected in joint studies of major morphological changes and the origin of new structures. would have augmented the space available for marine life. 6–7 May 1999) showed that physical changes during the history of the world have had a profound impact on its biota. whether trained as paleontologists. Evolution and Development.34. the continents were grouped close to the South Pole and the earth underwent a series of continental glaciations (shaded areas). Rifting of continental plates in the Pliocene and Quaternary produced the East African Great Lakes.] there were several episodes of continental glaciation affecting many areas of the world (Fig. Antarctica had separated from both South America and Australia. which might have contributed to the formation of the continental ice sheets that spread over North America and Eurasia in the Pleistocene. The flood of new techniques. A new journal. 15. culminating in the origin of the arctic and tundra fauna of the Pleistocene37. The latter was a unique phenomenon. 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.PERSPECTIVES gressive cooling in the Cenozoic. 1 January 2000 30 . knowledge from molecular biology has revealed how genes control development and how modifications in these genes can result in evolutionary changes of all magnitudes. at the end of the Proterozoic. large-scale evolutionary processes. the Arctic ocean became effectively isolated from the Atlantic and Pacific oceans. (d) By the middle Oligocene. 4a)5. Subsequently. map (b) from Ref. but provided few unique concepts to explain long-term.e. changes in the earth’s 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.

such as many lineages of late Cenozoic metazoans. This is especially conspicuous in the area of quantitative genetics. 455–500 31 . (1998) Changing perspectives on the origin of eukaryotes. 1–134 10 Valentine. 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. to the regulation of anatomical and physiological differences that are subject to selection within species. eds).J. E. Over the entire history of life. Oxford University Press 12 Schopf. National Academy of Sciences 14 Katz. to investigate the wide range of evolutionary phenomena from the genetic control of body form in different phyla. J.30. families and orders. (1980) The Evolutionary Synthesis: Perspectives on the Unification of Biology.W. Numerous recent books have dealt with this subject7. F. population TREE vol. W. over time scales ranging from a decade or less (e. Development 126. In Tempo and Mode in Evolution (Fitch. et al. • 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. S. which is necessary for establishing recognizable changes in the morphology and the physiology of a variety of traits in species with different generation periods. • Utilization of information.) Zool. or the subsequent changes in the earth’s biota.. a thorough understanding of the geological history of our planet. as yet. 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. El Niño).L. P.H. Harvard University Press 4 Carroll. W. The referees provided many useful suggestions for improvement of the manuscript.J. into the publications on population genetics. (Nat. 635–638 2 Darwin.W. P. the intensity and direction of selection change repeatedly. J. through establishing the position and configuration of appendages in different clades within specific phyla. the rates of change accord well with examples of the selection of alternative alleles emphasized in most textbooks. L. as if they resulted from the additive effects of a large number of essentially equivalent genes43. habitats and ways of life. Chapman & Hall 9 Greenwood. generated by molecular developmental biology. References 1 Moore. Other models would be necessary for unicellular and clonal organisms. natural selection and speciation as they can be observed in modern populations. pp. But.A. Science 283. there is relatively little integration of new evidence. rather than a statistical. which continues to treat polygenic traits in a statistical manner. 41–61. Soc. different fates: tempo and mode of evolution changed from the Precambrian to the Phanerozoic. in comparison with the rates measured in living populations. Over the duration of most species. F.g. W. over increasingly longer periods of time. 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.PERSPECTIVES has just been inaugurated and a new division. et al. Cambridge University Press 6 Ax. 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. (1998) The Crucible of Creation: The Burgess Shale and the Rise of Animals. (1974) The cichlid fishes of Lake Victoria. Bull.’ However. Suppl.A. 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. R. (1999) Mix and match in the tree of life. (1999) Teaching neo-darwinism. 493–497 15 Lake.g. Cambridge University Press 8 Benton. 63–83. ed.H.S. 15. 6. A. (1995) Proterozoic and Early Cambrian protists: evidence of accelerating evolutionary tempo. either in an oscillating manner or in what appears to be a random walk. Br. M. C. T. (1993) The Fossil Record 2. 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. has been added to the Society for Integrative and Comparative Biology.20. (1995) Disparate rates. Trends Ecol. Support for research was provided by the Natural Sciences and Engineering Research Council of Canada. from either molecular genetics or paleontology. lest we squander a second opportunity at a true synthesis. any model would break down because the nature of the organisms and their genetic systems changed beyond the original parameters. Evolution 53. and Ayala. (1998) Crustacean disparity through the Phanerozoic: comparing morphological and stratigraphic data. J.. through tens and hundreds of thousands of years (Milankovitch cycles and episodes of continental glaciation).41. Researchers could make use of field observations to establish models that incorporate parameters such as: the duration of essentially unidirectional selection. eds). and Ayala. 65. and Provine. No general model could account for the mass extinctions at the end of the Paleozoic and Mesozoic. 851–859 11 Conway Morris.H. no.A. • Recognition of the importance of horizontal genetic exchange throughout the history of life. for much of the duration of the majority of species there is relatively little net change. J. (1997) The Origin of Animal Body Plans. • Employment of emerging knowledge of the mutual interaction of genes controlling quantitative traits to formulate a truly descriptive. and Elena Roman for preparing the illustrations. (1999) Fossils. 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. (1859) On the Origin of Species by Means of Natural Selection. (1994) New Views on an Old Planet (2nd edn). However. Biol. 13. and an appreciation of the processes of genetic change. 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).M. molecules and embryos: new perspectives on the Cambrian explosion. (1997) Patterns and Processes of Vertebrate Evolution. A new evolutionary synthesis requires: the integration of knowledge from all forms of life that have ever existed on earth. even over hundreds of thousands of years. Murray 3 Mayr. Cambridge University Press 5 van Ander. Rapid rates of morphological change can be observed from generation to generation as a result of rapidly changing selection coefficients44. detailed knowledge of the changes in the biology of development throughout all multicellular organisms.M. 1 January 2000 Box 1. Acknowledgements I thank David Green for discussion and comments on the manuscript. 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). In Tempo and Mode in Evolution (Fitch. Linn. National Academy of Sciences 13 Knoll. 2027–2028 16 Will.. Hist. W. pp. sizes. John Wiley & Sons 7 Arthur. 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. East Africa. methodology for understanding how natural selection controls their evolution. weak selection among evolution texts. with this name. Mus. (1987) The Phylogenetic System. that they are indistinguishable from a random walk. Over short intervals. Evol. M.J. W. but unidirectional selection is rarely maintained for a sufficient time to result in continuing morphological or physiological modification.

J. Oxford University Press Laboratory selection experiments using Drosophila: what do they really tell us? Lawrence G. BioEssays 20. and McGinnis. Nature 391. Blackwell Science 42 Schlichting. B.R. M. eds (1993) Morphological Change in Quaternary Mammals in North America.A. C. and it can be used to measure direct and indirect (correlated) responses to selection5.R. J. Biol. (1998) The evolution of the Hox cluster: insights from outgroups. J. (1997) Fossils. 126–137 20 Raff. M. no. (1998) Genetics and Analysis of Quantitative Traits. PII: S0169-5347(99)01756-5 . 7. All rights reserved. (1995) Hox genes and the evolution of vertebrate axial morphology. B Biol.). Science 280.. 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. et al. limbs. Nature 376. Trans. Moreover. 1059–1063 34 Hoffman. the ability to study correlated responses to selection is particularly valuable..PERSPECTIVES 17 Carroll.A. R. Ary Hoffmann is at the Dept of Genetics and Evolution. Curr. Philos. (1998) Evolutionary Developmental Biology. B.2 – considerable progress has been made in their design. selection experiments are vulnerable to artifacts that are difficult to control. 107. A. et al. Science 281. R. Kluwer Academic Publishers 31 Nagy. (1997) Permian world topography and climate. 173. M. ed. (1998) The molecular evolution of development. Am. In spite of the perceived value of laboratory selection experiments. R.edu. (1989) Evolution and extinction in the marine realm: some constraints imposed by phytoplankton. eds (1989) Evolution and extinction. 86. P.latrobe. J. pp. Cambridge University Press 38 Keenleyside. I. From an evolutionary perspective. (1998) A Neoproterozoic snowball Earth. 325. and Raff. 239–488 40 Coates. Mol. Nature 396. 639–646 28 Burke.B. A. et al. this article will address two areas of general concern. Lond. and Cohn. Soc. Evol. (1998) Fins. Watson and Hoffmann7 selected for increased resistance to cold stress in adult D. (1991) Cichlid Fishes: Behaviour. such experiments on D. et al. B Biol. Ecology. (1998) Two or four Neoproterozoic glaciations? Geology 26. 325. selection experiments are a valuable research tool and can contribute to our understanding of evolution in natural populations. D. (1997) Evolution of the entire arthropod Hox gene set predated the origin and relationship of onychophoran/arthropod clade. W. it was recognized that laboratory selection experiments would be valuable for testing evolutionary hypotheses1. However. 1 January 2000 32 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. (1997) The origin of animal body plans. (1998) Phenotypic Evolution. Development 121.A.F. and Martindale. et al. M. Although there are other useful genetic approaches.K. Sci. Genet. and Grant. Hoffmann Laboratory selection experiments using Drosophila. 700–711 30 Hall. and found that an increase in adult cold resistance was accompanied by a decrease in early fecundity in all replicate lines of both species. 8. and tails: outgrowths and axial patterning in vertebrate evolution. Soc. (1998) Changing patterns of gene regulation in the evolution of arthropod morphology. 1342–1346 35 Knoll.C. 479–485 18 Meyer. In spite of these problems. Nat. Bundoora. (1996) Developmental evolution of metazoan body plans: the fossil evidence. (1998) Hox gene variation and evolution. R. are widely used in experimental biology. A. Lincoln. 333–346 29 Purugganan. and Evolution. University of Chicago Press 45 Ziegler. et al. 225–228 19 Erwin. USA (lharsh@unlserve. TREE vol. Am. 116–125 26 Grenier. Victoria 3083. G.D.edu). et al. M. similar selection experiments often produce inconsistent correlated responses to selection. Lond. In particular. Unfortunately.J. S. thus suggesting the presence of a trade-off. Harshman and Ary A.unl. Trans. Dev. (1999) Body builders of the sea.H. Philos.W. Zool.D.. Hist. (1996) The Shape of Life. Sinauer Associates 44 Grant. M.I.A. Curr.H. (1989) Evolutionary Dynamics of a Natural Population. and Hallam. G. W. M. (1998) A new model for Proterozoic ocean chemistry. et al. University of Nebraska-Lincoln. (1998) Tempo of the endPermian mass extinction. 38–46 24 Valentine. 392–396 22 Finnerty. 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.K. and Kirschner. 45. 38. 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. 279–290 36 Bowring.D. 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