Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake

A recent study of a pair of sympatric species of cichlids in Lake Apoyo in Nicaragua is viewed as providing probably one of the most convincing examples of sympatric speciation to date. Here, we describe and study a stochastic, individual‐based, explicit genetic model tailored for this cichlid system. Our results show that relatively rapid (< 20 000 generations) colonization of a new ecological niche and (sympatric or parapatric) speciation via local adaptation and divergence in habitat and mating preferences are theoretically plausible if: (i) the number of loci underlying the traits controlling local adaptation, and habitat and mating preferences is small; (ii) the strength of selection for local adaptation is intermediate; (iii) the carrying capacity of the population is intermediate; and (iv) the effects of the loci influencing nonrandom mating are strong. We discuss patterns and timescales of ecological speciation identified by our model, and we highlight important parameters and features that need to be studied empirically to provide information that can be used to improve the biological realism and power of mathematical models of ecological speciation.

[1]  M. Kawata.  Invasion of vacant niches and subsequent sympatric speciation , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  A. Pomiankowski.  The costs of choice in sexual selection. , 1987, Journal of theoretical biology.

[3]  K. R. Mckaye,et al.  Evolutionary Biology: Evidence for sympatric speciation? , 2006, Nature.

[4]  A. Meyer,et al.  Sympatric speciation in Nicaraguan crater lake cichlid fish , 2006, Nature.

[5]  J. Baylis.  A Quantitative Study of Long-Term Courtship: I. Ethological Isolation Between Sympatric Populations of the Midas Cichlid, Cichlasoma Citrinellum, and the Arrow Cichlid, C. Zaliosum , 1976 .

[6]  T. Kawecki.  Sympatric speciation driven by beneficial mutations , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  S. Gavrilets,et al.  Issues of terminology, gradient dynamics and the ease of sympatric speciation in Adaptive Dynamics , 2005, Journal of evolutionary biology.

[8]  Fyodor A. Kondrashov,et al.  Interactions among quantitative traits in the course of sympatric speciation , 1999, Nature.

[9]  A. Meyer,et al.  SHAPE ANALYSIS OF SYMMETRIC STRUCTURES: QUANTIFYING VARIATION AMONG INDIVIDUALS AND ASYMMETRY , 2002, Evolution; international journal of organic evolution.

[10]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[11]  Mark Kirkpatrick,et al.  Sexual selection can constrain sympatric speciation , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[12]  T. Kawecki.  SYMPATRIC SPECIATION VIA HABITAT SPECIALIZATION DRIVEN BY DELETERIOUS MUTATIONS , 1997, Evolution; international journal of organic evolution.

[13]  A. Meyer,et al.  Body shape variation in cichlid fishes of the Amphilophus citrinellus species complex. , 2003 .

[14]  N. Barton.  Fitness Landscapes and the Origin of Species , 2004 .

[15]  F. B. Christiansen.  Hard and Soft Selection in a Subdivided Population , 1975, The American Naturalist.

[16]  Sergey Gavrilets,et al.  PERSPECTIVE: MODELS OF SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS? , 2003, Evolution; international journal of organic evolution.

[17]  Sergey Gavrilets,et al.  Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island , 2007, Molecular ecology.

[18]  J. Felsenstein.  SKEPTICISM TOWARDS SANTA ROSALIA, OR WHY ARE THERE SO FEW KINDS OF ANIMALS? , 1981, Evolution; international journal of organic evolution.

[19]  J. Coyne.  Sympatric speciation , 2007, Current Biology.

[20]  A. Meyer,et al.  The Midas cichlid species complex: incipient sympatric speciation in Nicaraguan cichlid fishes? , 2004, Molecular ecology.

[21]  Motoo Kimura,et al.  A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population*. , 1973, Genetical research.

[22]  S. Gavrilets,et al.  Sympatric speciation by sexual conflict , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Daniel J. Howard,et al.  Endless Forms: Species and Speciation , 1998 .

[24]  M. McPeek,et al.  The dynamics of evolutionary stasis , 2005, Paleobiology.

[25]  Sergey Gavrilets,et al.  PERSPECTIVE: MODELS OF SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS? , 2003, Evolution; international journal of organic evolution.

[26]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[27]  Daniel I Bolnick,et al.  Multi-species outcomes in a common model of sympatric speciation. , 2006, Journal of theoretical biology.

[28]  Laurent Excoffier,et al.  Analysis of Population Subdivision , 2004 .

[29]  M. Doebeli.  Adaptive speciation when assortative mating is based on female preference for male marker traits , 2005, Journal of evolutionary biology.

[30]  A. Meyer,et al.  Evidence for sympatric speciation , 2006 .

[31]  D. Tautz,et al.  Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon , 2001, Molecular ecology.

[32]  Sergey Gavrilets,et al.  “ADAPTIVE SPECIATION”—IT IS NOT THAT EASY: REPLY TO DOEBELI ET AL. , 2005 .

[33]  N. Eldredge.  THE ALLOPATRIC MODEL AND PHYLOGENY IN PALEOZOIC INVERTEBRATES , 1971, Evolution; international journal of organic evolution.

[34]  Axel Meyer,et al.  Incipient speciation in sympatric Nicaraguan crater lake cichlid fishes: sexual selection versus ecological diversification , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  Y. Michalakis,et al.  Polymorphism in heterogeneous environments, evolution of habitat selection and sympatric speciation: Soft and hard selection models , 1993, Evolutionary Ecology.

[36]  S. Gourbière.  How do natural and sexual selection contribute to sympatric speciation? , 2004, Journal of evolutionary biology.

[37]  S. Gould.  The Structure of Evolutionary Theory , 2002 .

[38]  D. Bolnick.  WAITING FOR SYMPATRIC SPECIATION , 2004, Evolution; international journal of organic evolution.

[39]  U. Dieckmann,et al.  Adaptive dynamics as a mathematical tool for studying the ecology of speciation processes , 2005, Journal of evolutionary biology.

[40]  K. R. Mckaye,et al.  COMPETITION FOR BREEDING SITES BETWEEN THE CICHLID FISHES OF LAKE JILOA, NICARAGUA' , 1977 .

[41]  S. Gavrilets.  The Maynard Smith model of sympatric speciation. , 2006, Journal of theoretical biology.

[42]  MULTILOCUS MODELS OF SYMPATRIC SPECIATION: BUSH VERSUS RICE VERSUS FELSENSTEIN , 2003, Evolution; international journal of organic evolution.

[43]  D. Gíslason,et al.  Rapid and coupled phenotypic and genetic divergence in Icelandic Arctic char (Salvelinus alpinus) , 1999 .

[44]  D. Tautz,et al.  Sympatric speciation suggested by monophyly of crater lake cichlids , 1994, Nature.

[45]  Ulf Dieckmann,et al.  Adaptive Speciation , 2004 .

[46]  H. Rundle,et al.  Ecological speciation: Ecological speciation , 2005 .

[47]  M. Higashi,et al.  Sympatric speciation by sexual selection , 1999, Nature.

[48]  Axel Meyer,et al.  Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae) , 1990 .

[49]  G. Barlow,et al.  Competition Between Color Morphs of the Midas Cichlid, Cichlasoma citrinellum, in Lake Jiloá, Nicaragua , 1976 .

[50]  Andrew P Hendry,et al.  The speed of ecological speciation. , 2007, Functional ecology.

[51]  U. Dieckmann,et al.  On the origin of species by sympatric speciation , 1999, Nature.

[52]  G. Barlow.  Competition between Color Morphs of the Polychromatic Midas Cichlid Cichlasoma citrinellum , 1973, Science.

[53]  Sergey Gavrilets,et al.  Dynamic patterns of adaptive radiation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[54]  F. Hoppensteadt,et al.  Conditions for sympatric speciation: A diploid model incorporating habitat fidelity and non-habitat assortative mating , 1996, Evolutionary Ecology.

[55]  Mark Kirkpatrick,et al.  Speciation by Natural and Sexual Selection: Models and Experiments , 2002, The American Naturalist.

[56]  G. Turner.  The Ecology of Adaptive Radiation , 2001, Heredity.

[57]  Daniel Pauly,et al.  The Cichlid Fishes : Nature ' s Grand Experiment In Evolution , 2001 .

[58]  T. Kawecki,et al.  The Maintenance (or Not) of Polygenic Variation by Soft Selection in Heterogeneous Environments , 2004, The American Naturalist.

[59]  D. Tautz,et al.  WHAT WE HAVE ALSO LEARNED: ADAPTIVE SPECIATION IS THEORETICALLY PLAUSIBLE , 2005, Evolution; international journal of organic evolution.

[60]  U. Schliewen,et al.  Reticulate sympatric speciation in Cameroonian crater lake cichlids , 2004, Frontiers in Zoology.

[61]  G. Barlow,et al.  The R ed Devil-Midas-Arrow Cichlid Species Complex in Nicaragua , 1976 .

[62]  Nicolas Salamin,et al.  Sympatric speciation in palms on an oceanic island , 2006, Nature.

[63]  D. Udovic.  Frequency-Dependent Selection, Disruptive Selection, and the Evolution of Reproductive Isolation , 1980, The American Naturalist.

[64]  Ernst Mayr,et al.  ECOLOGICAL FACTORS IN SPECIATION , 1947 .

[65]  N. Eldredge,et al.  Punctuated equilibrium comes of age , 1993, Nature.

[66]  J. Maienschein.  Growth of biological thought , 1994, Nature.

[67]  A. Meyer,et al.  Cost of morphological specialization: feeding performance of the two morphs in the trophically polymorphic cichlid fish, Cichlasoma citrinellum , 1989, Oecologia.

[68]  S. Gavrilets,et al.  20 Questions on Adaptive Dynamics , 2005, Journal of evolutionary biology.

[69]  D. Tautz,et al.  Adaptive Speciation: Epilogue , 2004 .

[70]  A. Meyer.  Morphometrics and allometry in the trophically polymorphic cichlid fish, Cichlasoma citrinellum: Alternative adaptations and ontogenetic changes in shape , 1990 .