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Adaptive Radiation: Contrasting Theory with Data

Sergey Gavrilets, et al.
Science 323, 732 (2009);
DOI: 10.1126/science.1157966

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Isaac. Benton. genetics. Phylogenetic comparative methods. Ruta. H. D. Schmidt.A. Bofarull et al. 8. 169 (2008). J. 17. 715 (2008). E. J. Brusatte. 275. 315 (2007). S. 23 (2007). R. Harvard University. methods are shared by paleontologists and neontologists. Sci. Biol. 2Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology. 1 (1973). and developmental factors and strongly dependent on historical contingencies. Evolution 62. Sepkoski Jr. Wills. Am. 4.1157719 tion of an underpopulated area (e. 23. A. empirical support is more tentative. Roy. Sci. Different evolutionary factors allowing the populations to take advantage of new ecological opportunity have been emphasized. Am. K. P. Science 314. 3. USA. 105. Purvis. Vert. Am. 2381 (2001). Taxic studies in paleontology continue to have great value in highlighting correlations between species richness and other factors. J. 99. Sci. on February 6. 52 (1995). Jablonski. P. 14. G. 165. Bollmann. E-mail: sergey@tiem. B. J. and this allows direct communication on the patterns and processes of macroevolution.A. The disadvantages of this approach are incompleteness of the fossil record. Sci. Evol. T. TN 37996. including genetic drift in small founder or peripheral populations (9). 8. Roy. 887 (1984). evolution is all about biotic interactions in ecosystems (Red Queen model). J. 6. 27. Emerson. 19. Science 321. Nat. S. local adaptation. Krug. J. 301 (2008). Adaptive radiation in such clades is not only spectacular. Lett. 39. and sexual selection— can elucidate much about the processes driving www. Knoll. S. Lloyd et al. Australian pygopodid lizards). 15. A. Nat. Jablonski. Sepkoski Jr. 6). Erwin. 20. 97 (2008). Empirical Approaches for Studying Adaptive Radiation Four main empirical approaches have been used: Fossils. Natl. Powell for drafting the figures. 47 (2008). g. Hawaiian silverswords. K. Jablonski. Natl. Walker. Finnegan. Evol. Purvis. Ecol. M. Paleobiology 10. opens opportunities for dialog.A. L. J. 5. W. Vrba. Phylogenetic approaches take advantage of increasingly complete phylogenies for many important groups and have the ability to integrate studies of the evolution of organismal function and ecology. 30. A. S1 (2007). A. Biol. 32. 211 (2001). we identify 10 general patterns concerning the temporal. Science 268. but is also an extremely complex process influenced by a variety of ecological. J. Bush. 21. T. Cambridge. 24. Valentine. Future progress in our understanding of adaptive radiation will be most successful if theoretical and empirical approaches are integrated. Mittelbach. 11. Roy. Palaeontology 50. J. ecological niches. Lloyd. Knoxville. Alroy et al. Barnosky. D. extinction of previously ecologically dominant groups. Acad. 2). The classic view of adaptive radiation focuses on ecological opportunity. J. Downloaded from www. 13. Natl. Donoghue. London B. D. Schiebel.g. Science 321. S. R. 25. 28. Mittelbach et al. Paleobiology 33. Braddy. S. M.. A. Natl. Thanks to S. 418 (1993). 29. to detect whether a clade has been more species-rich in the past. Proc. Geobios 32.S. D. Adaptive radiation has two components: the production of new species (speciation) and the adaptation of constituent species to a diversity of ecological niches. N. 124. whereas for others. and cichlids of the East African Great Lakes (Fig. M. One of these is adaptive radiation. Benton. Benton. Cronin. REVIEW Adaptive Radiation: Contrasting Theory with Data Sergey Gavrilets1* and Jonathan B. J. M.S. Losos2 Biologists have long been fascinated by the exceptionally high diversity displayed by some evolutionary groups. Z. D.S.sciencemag. J. Ecol. Hunt. 97 (2008). K. E. Thierstein. 31. “Adaptive radiation” refers to those evolutionary groups that have exhibited an exceptional extent of adaptive diversification into a variety of ecological niches (2–4). Such resource availability may result from coloniza- 6 FEBRUARY 2009 VOL 323 SCIENCE 22. R. 246 (1984). Adamowicz. Gittleman. alternatively. Microevolutionary studies of extant taxa. J. Methods based on fossil data allow one to infer the history of the clade through time and to use information from extinct taxa. spatial. 2). Anolis lizards on Caribbean islands (Fig. *To whom correspondence should be addressed. Stanley. Viewed close up. and that evolution may be pluralistic (3). M. J. Science 303. Res. 26. Soc. 2483 (2008). Sci. Purvis. Bambach. References and Notes 1. M. this correlation is far from perfect: Some adaptive radiations have relatively low species richness (e. Darwin’s finches. U. 105. 11536 (2008). Valentine. 6.. W. Alroy. L. K. University of Tennessee. M. U.utk. and the origin of novelties.. but from further away. genetic. E. phenotypic characters. relaxed (9) or strong selection (2. phylogenetic inferences about character states in the past can be unreliable (13. 600 (2005). J. D. Studies focusing on traits of and processes affecting extant taxa—e. J. Further. 739 (2005). M. R. 8). Proc. 2009 Speciation . G. 4786 (2008). Acad. Lett. 1 (2004). G. Purvis. Valentine. G. but comparative phylogenetic methods will illuminate questions about clade dynamics. MA 02138. Schmidt. G.S. 223 (1999). 732 include Darwin’s finches on the Galápagos islands. Paleobiology 34. J.. BMC Evol. R. Proc. T. in which an ancestral species finds itself in an environment in which resources are abundant and underutilized. Theory 1. S. the large patterns of biodiversity are driven by the physical environment (Court Jester model). Soc. 1 (2007). G. which some consider of foremost importance and potentially responsible for much of the ecological and phenotypic diversity of life (1. 26 Oxford Street. USA. and the absence of ecological. G. Mayhew.g. 9. M.. he spectacular diversity of life on Earth that Darwin sought to explain in On the Origin of Species emerged through a variety of intricate biological processes. A. island or lake). 293A. 104. 1485 (2008). J. H. Jones. Classic examples of adaptive radiation T 1 Departments of Ecology and Evolutionary Biology and Mathematics. Palaeontology 50. 36. Bambach. among many others (1. 21.. Wang. Payne. C. some speciose clades contain little adaptive disparity and thus would not qualify as adaptive radiations (3. Alroy. Ecology 82.. C. or evolution of a character— sometimes termed a “key innovation”—that allows the lineage to interact with the environment in novel ways (1. National Institute for Mathematical and Biological Synthesis. more data are needed. A. 14). M. physiological. Benton. A. Biol. Geol. Rev. 207 (2004). T. 1). U. and anonymous referees for comments and to S. with such divergence often occurring extremely rapidly (5). Ecol. M. D. A. In almost all cases. Jablonski. 2. Benton. J. J.A. H. 318 (2008). D. Sci. Paleobiology 34. 12. J. J. B. Jenkins. Syst. 172 (2001). Proc. J. D. Acad. for example. Moreover. 10. and other types of data. Van Valen. Eble. Supported by the Natural Environment Research Council and the Royal Society. N. L. 12). Acad. species richness. J. C. U. 275. Proc. Annu. Sci. and hybridization (11. Wildman et al. London B. 10). 2).1126/science. W. G. G. 102 (2006). Some of these are strongly supported by empirical work. 7. Ruta. Paleont. J.. N. K.. as has happened in other areas of evolutionary biology. difficulty in assessing the adaptive significance of phenotypic variation among taxa. 16.The realization that the Red Queen and Court Jester models may be scale-dependent. competition. 2. 10. 6854 (2002).sciencemag. M. 14395 (2007). R. 18. Proc. G. 10. T. Although many classic adaptive radiations are both species rich and adaptively disparate (7). A. Ecol. spatial structure. Using modeling approaches. The main disadvantage of these methods is that extinct taxa are often not represented so that there is no way. 8. L. J. and genetic/morphological properties of adaptive radiation. K.

recombination. Our goal here is threefold. The latter have traditionally played a major role both in evolutionary biology and in ecology. trunk-ground specialist. In this classification.. mechanisms of speciation are discussed according to the level of migration between the diverging (sub)populations (9. 2009 Fig. However. and sympatric. Adaptive radiation in the laboratory. tion are allopatric. one can study taxa that may be in early stages of radiation (e. extrapolation from processes operating today to what happened early in the history of a radiation is problematic. Losos)..e. 1. 22). the ability to identify crucial parameters. “Selection gradient” models [e. adaptive radiation). we summarize recent theoretical findings on the dynamics of adaptive radiation. However. However. e. and less genetic canalization. grass-bush. by extension. sometimes very different biological mechanisms have underlying dynamic commonalities and therefore can be described by very similar mathematical models. anoles have diversified to produce the same set of habitat specialists. stickleback fishes). Mahler).. First. A quantitative theory of speciation. in the past. Spontaneous clusterization models describe the accumulation of Dobzhansky-Muller genetic incompatibilities. (15. Second. corresponding to zero. A. so that these models describe sympatric speciation. different processes may have operated or the outcome of these processes may have been different. emerging species specialize on relatively narrow parts of a continuous unimodal distribution of abundances of a particular set of resources. it is not clear whether these systems are good analogs to adaptive radiations in nature. In these models. speciation via divergence in the timing of life-cycle events related to reproduction). mechanisms of speciation can be classified according to biological mechanisms driving divergence and speciation. Losos). Hispaniola (photo: L. as well as to point to the gaps in biological knowledge and intuition.sciencemag. Shown here (clockwise from top left) are A. Losos). But some general patterns do emerge in models of speciation and adaptive radiation. In “sympatric diversification” models [e.. The advantage of studies of adaptive radiation in microbial microcosms [e. intermediate. including greater resource abundance. 24). or sexual selection (23.. the modern synthesis of the 1930s and 1940s was a direct result of the development of theoretical population genetics by Fisher. and random drift and then splits into partially or completely reproductively isolated groups [reviewed in (20)]. (29. (25. The process of local adaptation is opposed by deleterious gene flow from subpopulations adapting to alternative niches. and maximum migration. parapatric. an initially random mating population accumulates a substantial amount of genetic variation by mutation. we identify important areas of theoretical and empirical research where notable advances can soon occur and can contribute dramatically to improving our understanding of adaptive radiation and the generation of biodiversity. A.g. pulchellus. a few founders enter a new environment with a number of novel discrete ecological niches. ecological selection. chlorocyanus. 28)] are similar to “invasion of empty niches” models except that environmental conditions vary in a continuous gradient-like fashion and selection for local adaptation acts on a single quantitative trait. A. Hispaniola (photo: J. classifying mechanisms of speciation and adaptive radiation on the basis of similarity of the corresponding models can be more general and insightful than on the basis of particular biological factors. In “spontaneous clusterization” models. Wright. However. Therefore. less ecological specialization. trunk-crown. 3). Mathematical Modeling Adaptive radiation can also be studied by using mathematical methods. divergence in mating preferences. Alternatively. Dynamic Models of Adaptive Radiation—Extensions on Speciation Theory Adaptive radiation can be viewed as the processes of speciation and adaptation extended to larger spatial and temporal scales. details do matter and generalizations are often difficult to make. These differences might result because conditions may have been different early in a radiation’s history.. random drift. respectively (19–21). twig. has clarified many questions and topics hotly debated by generations of biologists. Puerto Rico (photo: J. a reinforcement-like process can result in the evolution of premating reproductive isolation between different locally adapted groups. 30)]. and relevant temporal and spatial scales. On each island in the Greater Antilles.sciencemag. factors. Here we re- 6 FEBRUARY 2009 733 . Adaptive diversification in Caribbean Anolis lizards. cybotes. Third. speciation by hybridization. 26)]. Most commonly.. different lineages become adapted to and simultaneously develop genetic preferences for different ecological niches. the basic modes of specia- www. we attempt to test theoretical predictions against existing data obtained using a variety of empirical approaches. the optimum value of which changes linearly across space. For example.. insolitus. Hispaniola (photo: M. diversification is driven by coevolutionary interactions [ on February 6. Under these conditions. (31)]. different approaches are possible. The main advantages of mathematical modeling are its generality.g. and Haldane (18). 16)] and digital cyberworlds (17) is experimental flexibility. the biological realism of models and their underlying assumptions can always be SCIENCE VOL 323 Downloaded from www. Alternatively. As selection acts on the new genetic variation supplied by mutation. Ecological and phenotypic diversification is accompanied by the growth in the densities of emerging species (Fig. Ten Patterns of Adaptive Radiation In mathematical modeling.g. a spatial component is not present.g.SPECIALSECTION adaptive radiation and sometimes even include manipulative experiments. In “invasion of empty niches” models [e. or allochronic speciation (i.g. (27. which has emerged over the past 40 years [reviewed in (19–21)]. Five partially overlapping sets of models can be identified. In classifying mechanisms of speciation (and. but such ecologically and morphologically nondisparate groups are not necessarily good models for the early stages of adaptive radiation. In the fifth set of models.g.

mathematical models and generalizations from data have suggested the same patterns independently. 2. (ii) evolution of microhabitat choice and divergence with respect to microhabitat. appears to be L-shaped [figure 2d in (38)].view and evaluate with empirical data 10 patterns concerning temporal. 1) Early burst of evolutionary divergence: Typically. and genetic/ morphological properties of adaptive radiation. Taking this approach. 2009 Speciation . An alternative approach is to compare related clades of different ages. The radiation of placental mammals is a classic example. Adaptive diversification in cichlids. followed by a decline and then leveling-off of diversity (40). Some clades do. Phylogenetic studies also indicate that major ecological differences often evolve early in clade history. Coupling of studies of species diversification and the evolution of adaptive disparity is an important new direction (39). phenomenological null models of clade diversification (32. once corrected for lake surface area. Gillespie (43) hypothesized that in time. (Lower left) Cyprichromis sp. (Center) Hemitilapia oxyrhynchus. Among African Rift lakes. This hypothesis is mostly based on generalizations from the mathematical theory of speci- Fig. (Lower right) Petrotilapia nigra occurs in the upper part (>10 m) of the sediment-free rocky habitat of Lake Malawi. an assumption that probably is often. Konings] 6 FEBRUARY 2009 VOL 323 SCIENCE www. alternative interpretations exist to explain these patterns (41). as expected under overshooting. 36). The rate of speciation can decrease because fewer niches remain empty (reduced ecological opportunity) and species become more specialized (increased genetic constraints). [Photographs by A. Many fossil groups experience a peak in morphological disparity relatively early in their history and subsequently decline (35). such as tree versus ground Darwin’s finches or the “ecomorph” habitat specialists of Anolis (12. the ranges of such species expand and come into on February 6. which is found in shallow vegetated habitats in Lake Malawi. 734 There are several ways to examine these ideas. and (iv) divergence with respect to other traits controlling survival and reproduction. correct. This finding is often discussed in the context of adaptive radiation as evidence for the early burst model of diversification. 38).org Downloaded from www. Both paleontological and phylogenetic comparative data indicate that ecologically important morphological variation often arises early in a clade’s history. at which point competitive exclusion occurs. the dependence of cichlid species diversity on time. In some cases. 26). This pattern is also seen in the fossil records for some groups. overshooting has also been demonstrated in a comparison of the Tetragnatha spiders of the Hawaiian islands. Mathematical models provide only partial support because overshooting is predicted only under some conditions (25). (Upper left) Gnathochromis permaxillaris occurs in the deeper (>35 m) intermediate (rock-sand interface) habitat with sediment-rich bottoms in Lake Tanganyika. but not always.sciencemag. The most direct is to follow a radiation through history. the following sequence of the diversification events is expected: (i) divergence with respect to macrohabitat. exhibit an early peak in species richness. implicit in this discussion is the assumption that species diversity is correlated with adaptive diversity. the high diversity is attained by having several niches occupied by sets of allopatric species. 2) Overshooting: An early increase in species diversity is followed by a decline that plateaus (or substantially decelerates). “Leptosoma Jumbo” (Nkondwe) occurs in open water in Lake Tanganyika. (iii) divergence with respect to traits that simultaneously control the degree of local adaptation and nonrandom mating. leading to a decrease in species richness on older islands. This happens because the rate of speciation declines as fewer niches remain empty (reduced ecological opportunity) and species become more specialized (increased genetic constraints). Mathematical models of adaptive radiation that explicitly describe microevolutionary processes predict a burst of speciation soon after colonization (25. however. An increasingly common theme in molecular studies of speciation is the finding of a burst of species diversification early in a clade’s history (37. there is a burst of speciation and morphological diversification soon after the beginning of the radiation rather than similar rates through time. in fact. Overshooting can result if speciation rate is decreasing and/or extinction rate is increasing in time. 33) predict that morphological disparity grows more rapidly than species diversity early in the clade history due to the structure of multidimensional phenotype space and contrasting effects of speciation and extinction on disparity and diversity. with most modern orders appearing in the fossil record within a short period (34). In addition. in which the relatively young (but not youngest) island of Maui has the most species. Several examples of cichlids that use different habitats. 3) Stages of radiation: All else being equal.sciencemag. with the assumption that all else is equal [but see (42)]. However. spatial. (Upper right) Lethrinops furcifer is found in sandy environments near beaches in Lake Malawi.

sexually selected the population’s spread into unoctraits). leadThis prediction follows both from ing to increased selection efficiency classical results on patterns of geoand more advantageous mutations graphic variation in neutral loci infor selection to act upon. Matching of the color of the corresponding square and circle extraordinary divergence of cichlids species diversity in Galápagos snails (observed in most cases) means that most individuals in the patch prefer the in the great lakes of Africa. islands suggests that geographic isolation may be needed for during species divergence. Third. including strong disruptive cichlids in African rivers (54). Phylloscopus leaf identified a number of conditions promoting non. 28) show that itat elevation first. geographic 4) Area effects: Speciation drivareas that can approximately be en by ecological factors is promoted viewed as one-dimensional (such as by larger geographic areas (e. As a result. diet. 50). some types of speciation and evodoes not occur. In all mating preferences. The radius of the circle is proportional to the popeffect may have contributed to the example. 46. and absence of costs of lutionary diversification occur more readily in the threshold are environmentally quite hetero. Recent years have seen a resurgence of inter. but isolated.phenotypic change. Each local population is (20).sciencemag. 735 . as discussed above. of selection gradients are most conthese hypotheses have been proposed ducive for speciation. 21). close correlation of traits ex. 8) Least action effect: Speciation occurring 5) Nonallopatric diversification: Speciation (20. 47). 26). during adaptive radiation can occur in the abThe strongest evidence for nonallopatric adapt.. In addition. In the case shown. and continental areas). However. SCIENCE VOL 323 6 FEBRUARY 2009 Downloaded from www. are two-dimensional (such as lakes. such as strength of acter displacement). Mathematical models have if selection gradients are too shallow. thus con. it does patric speciation (25. The color of the square (53)] and from speciation models defines the ecological niche assigned to the patch.est in nonallopatric modes of speciation driven by tingencies such as the ancestral starting condition divergent natural selection pressures (19.Fig. This predicon the basis of phylogenetic analyses tion is supported by a recent study of that may be incapable of accurately divergence in male coloration and identifying character states during female preferences in cichlids (52). Moreover. erogeneous in larger areas. intermediate slopes [reviewed in (44. these conditions are in nature is controversial tinental shelves (56). extent of 6) Selection gradient effect: Selection graenvironmental heterogeneity. differences foraging techniques. lation sizes can be achieved. 26). and African cichlids). size. high levels ation of other lacustrine taxa is not limited to dieffect results in part because a threshold island/ of genetic variation. How common open. ecological opportunity. many factors can interfere forcement of incomplete reproductive isolation some groups on relatively large and environmenwith the order in which niche axes are partitioned and enhancement of ecological differences (char. microclimate) tion. and Anolis lizards (body size. havior.g.Each square represents a unit spatial area (patch). of rivers or shores of lakes and oceans) islands or lakes).org on February 6. two-dimensional habitats than along congeneous (38. 2009 In the traditional view [e. Models of parapatric speciation in which In line with these theories.allopatric phase. An illustration of an adaptive radiation in a mathematical model (25. For represented by a circle.sciencemag. promote more speciation and tend to Both mathematical models (20. Stages hypotheses have been proposed for diation as the expected outcome of sympatric or spatially heterogeneous selection for local adapmountain New Guinea birds (divergence in hab. However. Subsequent sympatry could lead to rein.g. the area the oceans.. 49)].these groups is composed of two or three different species differentiated by line and have extremely restricted dispersal abilities. All else being equal.tally heterogeneous. Each of tively narrow band along the shoreopportunity for allopatric or para. a metric of niche availaulation size. divergent tion in areas in which it is hard to envision an ation (20). 3. ive radiation comes from examples of diversifica. some see adaptive raof a clade (2.speciation to occur. larger areas imply that larger popuoceans. The classic case is the clade of 11 scribing the evolution of various types of traits tions that adapted to different ecological niches cichlid species found in a small and environmenfor a sufficiently long time.tally homogeneous crater lake in Cameroon simulations did support the above hypothesis lation. duced by isolation by distance [e. the lack of speciation in (25. 50). (9.versification in shoreline habitats (55).(51). 45)]. most than does island area (46). First. allopatric speciation.. cupied areas with different selecstructural selection experienced in different parts of the species range are not strong enough warblers (order of divergence: body to drive divergence and speciation. there are eight species of which inhabit the relalarger areas may allow for more different groups of species utilizing eight different ecological niches. early stages of a radiation for traits 7) Spatial dimensionality effect: that are evolutionarily labile (45). 48). Second.SPECIALSECTION www. ecological conditions they experience. or historical con.parapatric speciation in the context of abundant tation acts on an additive trait (27. However. the environment may be more het. radiGalápagos snails. foraging morphology and beIf selection gradients are too steep. followed by segregation in diet. even though some islands below ling nonrandom mating. At the same time.after the initial burst usually involves a minimum sence of allopatry. habitat). But in these cases. and thus incidentally evolved reproductive iso. available genetic variation. The color of the circle defines the niche preferred by most bility better explains the extent of individuals. not account for the low diversity of three cases in which this hypothesis has been examined (Caribbean Anolis lizards. lake area exists below which in situ cladogenesis periencing disruptive selection with those control. This spatial dimensionality taining more ecological niches. Only a limited amount of theoretical work has so far been done with models de. 20).adaptive evolution occurred in allopatric popula. selection. cichlids and parrotselection is so strong that it prevents fish (habitat. strong nonrandom mating. dients of intermediate slopes promote speciation. 25) maintain higher species richness and and verbal theory show that several phenotypic and genetic diversity per factors might contribute to increasunit area than geographic areas that ing speciation rates with area. and size).g.being choosy in mating (19.

Soc. S. Ecol. Biol. 436 (2007). environmental perturbations can negate these isolating mechanisms. Harmon. 33. have shown that a similar pattern also occurs in many species of animals (62). Kirkpatrick. P. Simpson. J. Gavrilets. A. intimately related group of birds.sciencemag. A. Hunter. Grant. Pie. we are left with a haphazard set of studies that happen to be relevant. Christensen. E96 (2007). J. one species has been taken and modified for different ends. J. www. Losos. R. the homogenizing effect of gene flow has classically been considered an impediment to evolutionary divergence (9). Some workers add to the definition that divergence occurs unusually rapidly (2) or is unusually great (3) to emphasize the difference between adaptive radiation and standard processes of evolutionary diversification. Science 301. Ito. 1977). New York. Proc. T. NJ. (Princeton Univ. 23 (1981).. Biol. Fukami. R. 734 (2006). 2197 (2003). Seehausen. NJ. 133 (2005). Press. 48. S22 (2002). Princeton. Science 305. Princeton.This pattern is explained by the joint action of genetic constraints and selection for local adaptation: As each lineage gets more specialized for a particular ecological niche. J.. For example. 1997). 28. 133 (1992). C. Press. Evol. S. At the same time. 99 (2007). (Cambridge Univ. D. Biol. The complexity of the processes of adaptive radiation is reflected in the complexity of corresponding mathematical models. the cause of which requires explanation. Hall. Theor. A related prediction is that during earlier stages of diversification. Botanists have long been aware that sympatric and ecologically differentiated taxa can maintain their distinctiveness in the face of ongoing hybridization. 7. 216. D. Moreover. all of which indicate the existence of a small number of loci underlying traits involved in ecological interactions and reproduction (59–61). S. 38. 6. Natl. Janis. Molecular Evolution and Adaptive Radiation (Cambridge Univ. A. of California Press. R. Stud. 2004). 26. Bridle. and monkeyflowers. Darwin was confronted with the fruits of adaptive radiation throughout his 5-year journey around the world. Press. is consistent with this pattern (57. Nature 421. Downloaded from www. Annu. G. 21. 15. Acad. This effect has been observed in many different models (25. A. and how it differs among taxa and in different settings. J. Vose. CA.sciencemag. it becomes more and more difficult to establish adaptations for alternative niches (25. 7. 1987 (2006). Chow. similar evolutionary outcomes can be achieved via alternative paths. Ecol. 166. Schluter Eds. Eldredge et al. Cambridge. 35. Gavrilets. Rainey. 26) assume that mating occurs in the ecological niche that a species exploits. Am. Evolution 51. D. D. 39. 1953). Lenski. 73 (2002). 3) We need studies of general models aiming to capture the most widespread patterns of adaptive radiation. 129 (1997). 19. H. Jensen. B. 2363 (2008). R. 22. Schluter. 6. The Major Features of Evolution (Columbia Univ. R. Press. B. 8. R. Ofria. Weitz. Syst. whereas the term “diversity” is reserved for quantification of species richness.. U. 4. A. J. Science 283. are still unclear. Rev. Sci.A. 160. MA. de Collobiano.. 26). L. 159. this assumption is true for some taxa. J. London B. 27. T. we need models that are more closely tailored to the biology of particular taxa. 2. BMC Evol. 13. Larson. various evolutionary factors act simultaneously. Butlin. 25. in Speciation and Patterns of Diversity. B. Speciation. A. Mooers. J. D. a role that it probably plays in many cases (63). Valentine. Nat. 16. Doebeli. But how exactly radiation occurs. O. On the other hand. W. 12. T. Soc. 2008). Dieckmann. Cambridge. the number of genetic changes necessary for divergence is smaller. Foote. P. Vose. J. 26). J. 28. Zhang. Press. 1985). Cunningham. Gavrilets. Coyne. R. M. Losos. H. Schulte II. Recent years. Sci. 9) Effect of the number of loci: Rapid and extensive diversification is most likely if the number of underlying loci is small. A. 2) More generally. 198 (2004). 817 (1999). 37. 12). A. J. 32. V. O. evolutionary biology is an inductive science in which we establish generalities by the accumulation of case studies. 30. Sepkoski Jr. New York. Animal Species and Evolution (Belknap. adaptive radiations have continued to astonish and inspire scientists and the public alike. new traits (ecological or involved in mating) that emerge in some lineages can spread to other lineages as a result of hybridization. C. 2009 Speciation . P. A. 40. O. Grant. S. J. in which closely related species are ecologically and phenotypically similar. NJ. 2. Sci. Sytsma. Kassen. 18040 (2005). K. NJ. S. as well as why some lineages radiate and others do not.S. 102. X. Gavrilets. R. but we believe that such an interpretation makes “adaptive radiation” nothing more than the product of evolutionary diversification. S. More detailed studies. M. C. B. Press. Proc. is needed to build a reservoir of case studies from which generalizations can be drawn. Sunderland. Paleobiology 31. M. D. Indeed. New York. Sytsma. Soc. General Conclusions This brief survey suggests the following: 1) More empirical studies are needed specifically aimed at assessing the predictions 736 discussed above. Gavrilets. 34. 1963). I. References and Notes 1. 6 FEBRUARY 2009 VOL 323 SCIENCE 5. S. Foote. The Ecology of Adaptive Radiation (Oxford Univ. Press. Am. W. on February 6. Princeton. D. Seehausen. Evolution 57. M. 19. H. the effect of selection on each locus is stronger. U. Proc. T. J. Trends Ecol. Sepkoski Jr. Kawamura. Press. 961 (2003). 170. and the contingencies of place and time play a large role in guiding the evolutionary process. 18. Endler. E. Kawata. 259 (2003). J. 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J. leading previously genetically distinct taxa to interbreed and even “de-speciate” (64). Lovette. Ludwig. but not for other classic adaptive radiations. Ed. Biol. 14. 266. Oxford. At present. Syst. Miles. 23. 273. he wrote in The Voyage of the Beagle: “Seeing this gradation and diversity of structure in one small. H. 241. one might really fancy that from an original paucity of birds in this archipelago. D. Schluter. 36. The extent to which relaxing these assumptions or tailoring them to other biological situations (e. 147 (2002). recent work has suggested that such interspecific gene flow can be an important source of genetic variation that enables adaptive diversification in early stages of radiation (11. Ravigné. Biol. M. J. 10) Porous genome effect: Species can stably maintain their divergence in a large number of selected loci for very long periods despite substantial hybridization and gene flow that decreases or removes differentiation in neutral markers. Hist. 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