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The Roles of Divergent Selection and Environmental Heterogeneity in Speciation of Lake Victoria Cichlid Fish

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The Roles of Divergent Selection and Environmental Heterogeneity in Speciation of Lake Victoria Cichlid Fish Eawag 05573 The roles of divergent selection and environmental heterogeneity in speciation of Lake Victoria cichlid fish Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern vorgelegt von Isabel S. Magalhães von Portugal Leiter der Arbeit: Prof. Dr. Ole Seehausen Institute of Ecology and Evolution Division of Aquatic Ecology Universität Bern The roles of divergent selection and environmental heterogeneity in speciation of Lake Victoria cichlid fish Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern vorgelegt von Isabel S. Magalhães von Portugal Leiter der Arbeit: Prof. Dr. Ole Seehausen Institute of Ecology and Evolution Division of Aquatic Ecology Universität Bern Von der Philosophisch-naturwissenschaftlichen Fakultät angenommen Bern, 17 February 2009 Der Dekan: Prof. Dr. Urs Feller Contents Chapter 1 - Introduction and synthesis________________________________________5 Chapter 2 - Sympatric colour polymorphisms associated with non-random gene flow in cichlid fish of Lake Victoria ____________________________________27 Chapter 3 - Eco-morphological but not genetic differentiation within cichlid fish populations correlates with the slope of resource gradients_______________________59 Chapter 4 - Speciation through sensory drive in cichlid fish_____________________101 Chapter 5 - Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish_____________________________________145 Chapter 6 - Genetics of male colour in a Lake Victoria cichlid fish species pair and its role in sympatric speciation________________________________________179 Chapter 7 - Summary and conclusion______________________________________201 Affiliations of co-authors________________________________________________209 Acknowledgements____________________________________________________211 Erklärung____________________________________________________________213 Curriculum Vitae______________________________________________________215 3 4 Chapter 1 Introduction and Synthesis 5 6 Chapter 1. Introduction and Synthesis Introduction and Synthesis This thesis wants to contribute to the understanding of the environmental conditions under which (ecological or sexual) selection can cause phenotypic divergence and speciation. It starts with an introduction to the problem of speciation in the presence of gene flow. This is followed by theoretical support and empirical evidence for the role of disruptive ecological and sexual selection as mechanisms of speciation in sympatry and for the role of environmental heterogeneity in this process. I then introduce the study system and provide a summary of the chapters. This is followed by five chapters, followed by a summary and conclusions. 1. Speciation in the presence of gene flow One of the least well understood problems in evolutionary biology is why some taxa have speciated while others often closely related and superficially similar fail to do so. The advent of molecular techniques combined with increasingly powerful computer simulations and the development of a mathematical framework for speciation genetics (Gavrilets, 2004) have in recent years led to several paradigm shifts in speciation theory. One of these shifts is that speciation is no longer considered to be exclusively a by-product of drift and ecological adaptation in geographical isolation (Mayr, 1942). For many decades empirical evidence in animals failed to produce convincing evidence for speciation other than in geographical isolation. However, more recently empirical evidence for speciation in the absence of geographical isolation has accumulated (Bush 1994; Schluter, 2000; Via 2001; Dieckmann et al., 2004). Speciation in the presence of gene flow is now receiving a great deal of attention, and an intensive scientific debate has emerged about conditions leading to it. Two questions are central to this debate: one is how commonly and under which genetic and environmental conditions can divergent selection lead to speciation when gene flow is frequent (Nosil & Harmon, 2008; Rasanen & Hendry, 2008; Nosil et al., in press); the second is whether assortative mating evolves in response to ecological selection exerted by competition for ecological resources, competition for mating opportunities or by subtle interactions of the two. Increasingly sophisticated models of speciation by disruptive ecological and sexual selection or divergent selection along environmental gradients have been explored (Doebeli, 1996; Dieckmann & Doebeli, 1999; Kondrashov & Kondrashov, 1999; van Doorn et al., 2004; Kawata et al., 2007), but empirical testing of theory and model assumptions are lagging behind. 2. Ecological and sexual selection as mechanisms of sympatric speciation Sympatric speciation in its strict definition is speciation in a population in which the site where an individual reproduces is independent of its site of birth (Gavrilets, 2004). As mating is random with respect to birth place, the proportion of members of the two parental populations that is exchanged per generation (i.e. migration rate) is expected to be 0.5. Sympatric speciation requires disruptive selection of some kind that places intermediate phenotypes at a fitness minimum and can generate the evolution of assortative mating. In terms of the biology, two main classes of theoretical models have emerged on sympatric speciation: models based on disruptive ecological selection involving competition for resources and models based on disruptive sexual selection. 7 Chapter 1. Introduction and Synthesis Both types of models have been subjected to several criticisms (Arnegard & Kondrashov, 2004; Coyne & Orr, 2004; Turelli et al., 2001). Empirical examples of sympatric speciation by sexual or ecological selection also suffer from difficulties in proving themselves as such. The most important difficulty is showing that population divergence is initiated by sexual or ecological selection in sympatry and was not preceded by an allopatric phase (Schluter, 2001). Nonetheless evidence for sympatric speciation by sexual or ecological selection is no longer negligible. However many empirical studies also illustrate that there are several alternative outcomes of ecological or sexual selection and speciation is only one of them (reviewed by Panhuis et al., 2001; Rueffler et al., 2006). 2a. Ecological selection - models - Theoretical models of sympatric ecological speciation can be usually divided in two types: discrete-habitat models (Maynard Smith, 1966; Felsenstein, 1981; Rice, 1984; Rice, 1987; Diehl & Bush 1989; Johnson et al. 1996a; Kawecki, 1996; Kawecki, 1997; Fry, 2003; Gavrilets & Vose, 2007; Gavrilets et al., 2007) and continuous-resource models (Doebeli, 1996; Dieckmann & Doebeli, 1999; Kondrashov & Kondrashov, 1999; Doebeli & Dieckmann, 2000; Ito & Dieckmann, 2007). In the first type models sympatric populations, exploiting different niches, are most fit in their own niche and mate preferably with members of their own population. Therefore, they require the evolution of niche preference, niche adaptation and assortative mating. Sympatric speciation requires the development of at least two of these traits and there are models for all three pairwise combinations of them (reviewed by Coyne & Orr, 2004). The second type of models assumes the simultaneous coevolution of ecological traits and assortative mating that splits the population into sympatric groups, each using different parts of an initially continuous resource distribution (Doebeli, 1996; Dieckmann & Doebeli, 1999; Kondrashov & Kondrashov, 1999; Doebeli & Dieckman, 2000; Ito & Dieckman, 2007). In these models competition between similar phenotypes produces negative frequency-dependent selection that confers higher fitness to the individuals at the extremes of the resource distribution. This can create intraspecific polymorphisms but if mating stays random, the population will not split into genetically differentiated subpopulations. Speciation is possible through the development of assortative mating, either based directly on the ecological trait that is under selection or based on a marker trait that may become associated with the ecological trait (Dieckmann & Doebeli, 1999; Kondrashov & Kondrashov, 1999). An alternative to this scenario is assortative mating exerted by females carrying genes that affect their preference for different types of the marker trait. A female’s willingness to mate depends on the difference between their preference and the marker trait (Kondrashov & Kondrashov, 1999). - Empirical data - Good empirical examples supporting that disruptive ecological selection can initiate speciation in the absence of geographical isolation remain few. In vertebrates, examples of sympatric speciation come from cichlid fishes (Schliewen et al., 1994; Barluenga et al., 2006), palm trees (Savolainen et al., 2006) and more recently Neospiza finches from the Tristan da Cunha Archipelago (Ryan et al. 2007). However there is no conclusive evidence for disruptive ecological selection having initiated speciation. 8 Chapter 1. Introduction and Synthesis threespine sticklebacks (Gasterosteus aculeatus) from coastal lakes in British Columbia, Canada (McPhail, 1994; Schluter 1996a; Schluter 1996b; Rundle et al. 2000; Bolnick 2004; Bolnick & Lau, 2008) and Darwin’s finches (Grant & Grant, 2006; Hendry et al., 2008), on the other hand, are prominent examples of disruptive ecological selection as an important agent in divergence with
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