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Ecology and the Origin of Species 372 Review TRENDS in Ecology & Evolution Vol.16 No.7 July 2001 Ecology and the origin of species Dolph Schluter The ecological hypothesis of speciation is that reproductive isolation evolves direct selection on premating isolation ultimately as a consequence of divergent natural selection on traits between (REINFORCEMENT). Distinguishing the ways in which environments. Ecological speciation is general and might occur in allopatry or divergent selection has led to reproductive isolation is sympatry, involve many agents of natural selection, and result from a among the greatest challenges of the empirical study combination of adaptive processes. The main difficulty of the ecological of ecological speciation. hypothesis has been the scarcity of examples from nature, but several potential In what is perhaps the classic scenario for cases have recently emerged. I review the mechanisms that give rise to new ecological speciation (Fig. 1), reproductive isolation species by divergent selection, compare ecological speciation with its between two populations starts to build in allopatry as alternatives, summarize recent tests in nature, and highlight areas requiring populations accumulate adaptations to unique aspects research. of their environments. Premating isolation then evolves to completion by reinforcement after sympatry ECOLOGICAL SPECIATION (see Glossary) occurs when is secondarily established. The timing of SECONDARY DIVERGENT SELECTION on traits between populations or CONTACT is flexible, however, and the extremes of subpopulations in contrasting environments leads possibility lead to departures from this classic model. directly or indirectly to the evolution of REPRODUCTIVE At one extreme is pure ALLOPATRIC SPECIATION, in which ISOLATION. The concept of ecological speciation dates the sympatric phase is entirely absent. New species back to the 1940s, from the time the BIOLOGICAL SPECIES might eventually become sympatric, but this occurs CONCEPT was developed. Dobzhansky1 believed that after reproductive isolation is complete. The other ‘SPECIATION in Drosophila proceeds mainly through extreme is full-blown SYMPATRIC SPECIATION, which evolving physiological complexes which are successful completely lacks the allopatric stage. Although debate each in its environment’. Mayr2 recognized that many about the plausibility of these extremes has long of the accumulated genetic differences between polarized research on speciation, from an ecological populations ‘particularly those affecting physiological perspective, the more fundamental issue concerns the and ecological characters, are potential isolating mechanisms that drive the evolution of reproductive mechanisms’. Acceptance of this perspective by many isolation, which is the focus of this article. evolutionists in the mid-20th century resulted from the inherent appeal and simple plausibility of By-product mechanisms ecological speciation. However, until recently, neither In the simplest models of ecological speciation, was there evidence to support ecological speciation, reproductive isolation builds between populations nor had tests been devised and applied to distinguish incidentally as a by-product of adaptation to ecological speciation from other mechanisms that alternative selection regimes2,3. Reproductive might also cause speciation in the wild, such as isolation is not directly favored by selection, but is a GENETIC DRIFT (BOX 1). secondary consequence of genetic differentiation driven by selection on other traits. This BY-PRODUCT Mechanisms of ecological speciation MECHANISM could lead to premating isolation and to ‘Ecological speciation’ is a concept that unites various forms of postmating isolation. speciation processes in which reproductive isolation Several laboratory experiments with Drosophila evolves ultimately as a consequence of divergent have simulated the early stages of by-product (including DISRUPTIVE) selection on traits between speciation (reviewed in Ref. 4), and these hint at how environments. ‘Environment’ refers to biotic and the process might work in nature. Kilias et al.5 raised abiotic elements of habitat (e.g. climate, resources different lines of Drosophila melanogaster for five and physical structure) as well as to interactions with years in either a cold–dry–dark or a other species (e.g. resource competition, predation, warm–damp–light environment. Dodd6 examined mutualism and various forms of interspecific mating preferences in replicate lines of Drosophila interference). A diversity of evolutionary processes pseudoobscura raised for one year on either starch- might be involved. Ecological speciation might occur based or maltose-based larval medium. In both Dolph Schluter in ALLOPATRY or in SYMPATRY. It might lead to mainly studies, some premating reproductive isolation Zoology Dept and The Center for Biodiversity premating isolation, mainly postmating isolation, or a evolved between lines that had experienced Research, The University combination of both. It includes several (but not all) contrasting environments, but no premating isolation of British Columbia, modes of speciation involving SEXUAL SELECTION. evolved between independent lines raised in the same Vancouver, BC, Canada Ecological speciation might come about indirectly as a environment (Fig. 2). The populations in these V6T 1Z4. e-mail: consequence of natural selection on morphological, experiments were fully allopatric, as in the first part [email protected] physiological or behavioral traits, or it might include of the classic scenario (Fig. 1). http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02198-X Review TRENDS in Ecology & Evolution Vol.16 No.7 July 2001 373 Box 1. The major modes of speciation, according to initial causes Speciation modes have been classified mutations arise in separate populations References historically by the geographical occupying similar environments (Turelli et al.e, a Schluter, D. (1996) Ecological speciation in arrangement of populations undergoing the this issue). Reproductive isolation between postglacial fishes. Philos. Trans. R. Soc. London Ser. B 351, 807–814 process (allopatric, sympatric or parapatric), populations brought about by conflict and b Schluter, D. (1998) Ecological causes of a classification that focuses on the inhibitory coevolution between the sexes within speciation. In Endless Forms: Species and effects of gene flow on the evolution of populationsf–h is an example of this second Speciation (Howard, D. and Berlocher, S., eds), reproductive isolation. Some have argued mode. pp. 114–129, Oxford University Press that an alternative classification centering If populations are in contact before the c Orr, M.R. and Smith, T.B. (1998) Ecology and speciation. Trends Ecol. Evol. 13, 502–506 on mechanisms that drive the evolution of evolution of reproductive isolation is d Via, S. (2001) Sympatric speciation in animals: reproductive isolation would be more completed, natural selection might be the ugly duckling grows up. Trends Ecol. Evol. productivea–c (Viad, this issue). TableI breaks involved at a late stage of all four modes of 16, 381–390 modes of speciation events into four speciation, during reinforcement of e Turelli, M. et al. (2001) Theory and speciation. categories according to initial cause, and premating isolation (Turelli et al.e this Trends Ecol. Evol. 16, 330–343 f Palumbi, S.R. (1998) Species formation and the compares some other principal features of issue)i. Similarly, sexual selection might be evolution of gamete recognition loci. In Endless those categories. involved in every speciation mode, Forms: Species and Speciation (Howard, D. and Natural selection is involved at an early depending on the cause of divergence in Berlocher, S., eds), pp. 271–278, Oxford stage of two different modes of speciation. mate preferences. For this reason, the University Press Under ecological speciation, populations in presence of natural or sexual selection g Rice, W.R. (1998) Intergenomic conflict, interlocus antagonistic coevolution, and the different environments, or populations per se is probably not a good basis for evolution of reproductive isolation. In Endless exploiting different resources, experience classifying speciation events. Nevertheless, Forms: Species and Speciation (Howard, D. and contrasting natural selection pressures on the classification in Table I is coarse, and Berlocher, S., eds), pp. 261–270, Oxford traits that directly or indirectly bring about finer subdivisions are necessary to highlight University Press the evolution of reproductive isolation. differences in the roles of natural and sexual h Gavrilets, S. (2000) Rapid evolution of reproductive isolation driven by sexual conflict. However, divergence might also occur selection within each mode, as well as Nature 403, 886–889 under uniform selection, for example, if different roles for genetic drift in speciation i Dobzhansky, T. (1951) Genetics and the Origin different advantageous (but incompatible) initiated by that mechanism. of Species (3rd edn), Columbia University Press Table I.Modes of speciation Mode of speciation Mechanism of initial Initial form of Proximate basis of Examples of the roles of Example roles of divergence reproductive reduced hybrid natural selection sexual selection isolation fitness Ecological speciation Divergent natural Prezygotic or Ecological selection, Initial: Drive divergence in Amplify selection postzygotic genetic incompatibility
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