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Theory and Speciation 330 Review TRENDS in Ecology & Evolution Vol.16 No.7 July 2001 Theory and speciation Michael Turelli, Nicholas H. Barton and Jerry A. Coyne The study of speciation has become one of the most active areas of selection, and the relative rates of evolution of evolutionary biology, and substantial progress has been made in documenting premating and postmating isolation, is more likely to and understanding phenomena ranging from sympatric speciation and emerge from empirical than from mathematical reinforcement to the evolutionary genetics of postzygotic isolation. This analyses4–6. However, some important questions are progress has been driven largely by empirical results, and most useful mathematically tractable, such as the plausibility of theoretical work has concentrated on making sense of empirical patterns. reinforcement7,8 and the evolutionary consequences Given the complexity of speciation, mathematical theory is subordinate to of genetic incompatibilities that cause postzygotic verbal theory and generalizations about data. Nevertheless, mathematical isolation9,10. theory can provide a useful classification of verbal theories; can help determine We first discuss ALLOPATRIC SPECIATION, and then the biological plausibility of verbal theories; can determine whether alternative proceed to PARAPATRIC and sympatric speciation. Given mechanisms of speciation are consistent with empirical patterns; and can the recent flurry of empirical and theoretical studies occasionally provide predictions that go beyond empirical generalizations. We of sympatric speciation11–13 (Via14, this issue) and of discuss recent examples of progress in each of these areas. rapid PHENOTYPIC DIVERGENCE driven by DISRUPTIVE SELECTION (Schluter15, this issue), our traditional This review covers both verbal and mathematical biogeographical approach requires some defense. We theories of SPECIATION (see Glossary) in sexually offer two rationales, one conceptual, the other reproducing diploid organisms. Adopting the empirical. BIOLOGICAL SPECIES CONCEPT, we equate speciation to the The conceptual rationale is simply that, given evolution of reproductive isolating mechanisms that enough time, speciation is an inevitable consequence essentially prevent gene exchange between newly of populations evolving in allopatry. Because there arising taxa. However, our use of this definition does are no forces acting to enforce reproductive not imply that we believe REPRODUCTIVE ISOLATION to be compatibility between geographically isolated essential for morphological, ecological or genetic populations, they will eventually become divergence, or that we regard other aspects of reproductively incompatible. Thus, in contrast to the divergence between sympatric or allopatric groups as balance of forces required to produce sympatric or being less interesting than the evolution of parapatric speciation, allopatric speciation requires reproductive isolation. only geographical isolation and time. As with most areas of population biology, theories In addition, several lines of empirical evidence of speciation are generally verbal, describing support the view that allopatric speciation is conditions or mechanisms that are thought to cause pervasive; whereas current data suggest that the reproductive isolation. Classic examples include opposite extreme, sympatric speciation, is far less Dobzhansky’s suggestion1 that evolution in ALLOPATRY common. First, we have many empirical examples of leads to POSTZYGOTIC ISOLATION through the allopatric speciation (e.g. geminate sister pairs and accumulation of incompatibilities between alleles in island endemics). Second, despite recent data and different LINEAGES, and Mayr’s idea2 that population theory indicating that sympatric speciation almost BOTTLENECKS can produce rapid speciation through certainly occurs, few examples are unambiguous or ‘genetic revolutions’. Mathematical analyses serve widely accepted. Because it is harder to demonstrate mainly to test the plausibility of such conjectures. sympatric than allopatric speciation, these first two Recent treatments of SYMPATRIC SPECIATION and lines of evidence are compromised by an Michael Turelli* Section of Evolution and REINFORCEMENT are obvious examples. ascertainment bias. However, recent comparative Ecology, University Discussions of molecular evolution have been analyses5 (Barraclough and Nee16, this issue) show of California, Davis, dominated by mathematically based theory. By that, in several taxa, the most recently evolved CA 95616, USA. contrast, speciation is dominated by verbal theories species generally have allopatric ranges, supporting *e-mail: [email protected] because the process involves so many complex Mayr’s view that allopatric speciation might be most mechanisms, including ecology, behavior and common. These tests are conservative, because Nicholas H. Barton ICAPB, Division of interactions between multilocus genotypes. related sympatric species might falsely appear to be Biological Sciences, Moreover, speciation focuses on a composite trait – sister species because of genetic homogenization University of Edinburgh, reproductive isolation – that is a property of pairs of resulting from hybridization after divergence in Edinburgh, UK EH9 3JT. taxa and hence is inherently more complex than are allopatry. Third, if sympatric speciation were Jerry A. Coyne traits evolving within a single lineage3. Because of extremely common, we would expect to often see Dept of Ecology and this complexity, progress on major issues, including sister taxa of highly mobile species on islands, but the Evolution, University of 6,17 Chicago, 1101 E. 57th St, the biogeography of speciation, the frequency of few existing studies do not show such a pattern. An Chicago, IL 60637, USA. reinforcement, the roles of sexual versus natural alternative review of speciation could be based on a http://tree.trends.com 0169–5347/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(01)02177-2 Review TRENDS in Ecology & Evolution Vol.16 No.7 July 2001 331 Box 1. Evolution of prezygotic isolation via sexual selection Sexual selection can produce sexual females who mate with males possessing prezygotic isolation. As in other ‘quasi- isolation between allopatric populations ‘good genes’. There can often be multiple neutral’ models, many combinations of because female preferences can evolve for stable states that produce sexual isolation. trait and preference are compatible, and arbitrary male characteristics. In Lande’s Slight perturbations (e.g. the effect of transitions between them can be produced seminal modela, both trait and preference environmental differences between by natural and/or sexual selection. Paths of are additive polygenic traits. The female isolated populations) might then lead to high fitness that connect incompatible preference is assumed to have no direct rapid evolutionary changes in trait and genotypes also occur in the effect on fitness, evolving solely through preferencec,f. However, natural selection Dobzhansky–Muller model of epistasisn its association with the male trait. When need not be involved in speciation via and in Gavrilets’ ‘holey landscapes’o. the mean trait value is plotted against the sexual selection: examples are changes in References mean strength of female preference, this male genitalia or post-mating, prezygotic a Lande, R. (1981) Models of speciation by sexual model produces a line of neutral reproductive isolation (e.g. sperm–egg selection on polygenic traits. Proc. Natl. Acad. equilibria, corresponding to the infinite incompatibility), both of which can be Sci. U. S. A. 78, 3721–3725 number of ways that natural and sexual driven by male–male competition or by b Lande, R. (1982) Rapid origin of sexual isolation and character divergence in a cline. Evolution selection on the male trait can female behavioral or biochemical 36, 213–223 counterbalance. Isolated populations can ‘preference’. c Lande, R. and Kirkpatrick, M. (1988) Ecological move freely along the line, leading to ‘Arms races’ set off by a divergence speciation by sexual selection. J. Theor. Biol. sexual isolation. between the reproductive interests of 133, 85–98 d Payne, R.J.H. and Krakauer, D.C. (1997) Sexual Many models have built upon Lande’sa, males and females can also cause non- selection, space, and speciation. Evolution 51, invoking various mechanisms to drive ecological sexual selection that yields 1–9 populations to different points on the speciationk,l. However, other types of arms e Pomiankowski, A. and Iwasa, Y. (1998) equilibrium line; these mechanisms race (e.g. host–parasite coevolution) could Runaway ornament diversity caused by include genetic drift, selection on the male also drive divergence, and if sexual Fisherian sexual selection. Proc. Natl. Acad. Sci. U. S. A. 96, 5106–5111 trait, and changes in the intensity of female selection is important in speciation, one f Price, T. (1998) Sexual selection and natural a–g preferences . In many of these models, must explain why it is especially likely to selection in bird speciation. Philos. Trans. R. however, the evolution of reproductive be involved in such coevolutionary arms Soc. London Ser. B 353, 251–260 isolation is facilitated by the unrealistic races. One might argue that the arbitrary g Schluter, D. and Price, T. (1993) Honesty, assumption that female preferences are nature of sexual signals facilitates perception and population divergence in sexually selected traits. Proc. R. Soc. London
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