Sexual selection plays several intricate and complex roles in the related processes of local adaptation and speciation. In some cases sexual selection can promote these processes, but in others it ...can be inhibitory. We present theoretical and empirical evidence supporting these dual effects of sexual selection during local adaptation, allopatric speciation, and speciation with gene flow. Much of the empirical evidence for sexual selection promoting speciation is suggestive rather than conclusive; we present what would constitute strong evidence for sexual selection driving speciation. We conclude that although there is ample evidence that sexual selection contributes to the speciation process, it is very likely to do so only in concert with natural selection.
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Decades of theoretical work on the evolution of adaptive prezygotic isolation have led to an interesting finding—namely that stable partial reproductive isolation is a relatively common outcome. This ...conclusion is generally lost, however, in the desire to pinpoint when exactly speciation occurs. Here, we argue that the evolution of partial reproductive isolation is of great interest in its own right and matches empirical findings that ongoing hybridization is taxonomically widespread. We present the mechanisms by which partial reproductive isolation can be a stable evolutionary endpoint, concentrating on insights from theoretical studies. We focus not on cases in which hybridization results from constraints imposed by ongoing migration or mutation, but on the intriguing idea that partial reproductive isolation may instead be an adaptive optimum. We identify three general categories of selective mechanisms that can lead to partial reproductive isolation: context-dependent hybrid advantage, indirect selection due to the varying actions of sexual selection in different geographic contexts, and a balance of costs of choosiness with indirect selection for stronger mating preferences. By any of these mechanisms, stable partial reproductive isolation can potentially provide a robust evolutionary alternative to either complete speciation or population fusion.
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Predation plays a role in preventing the evolution of ever more complicated sexual displays, because such displays often increase an individual's predation risk. Sexual selection theory, however, ...omits a key feature of predation in modeling costs to sexually selected traits: Predation is density dependent. As a result of this density dependence, predator-prey dynamics should feed back into the evolution of sexual displays, which, in turn, feeds back into predator-prey dynamics. Here, we develop both population and quantitative genetic models of sexual selection that explicitly link the evolution of sexual displays with predator-prey dynamics. Our primary result is that predation can drive eco-evolutionary cycles in sexually selected traits. We also show that mechanistically modeling the cost to sexual displays as predation leads to novel outcomes such as the maintenance of polymorphism in sexual displays and alters ecological dynamics by muting prey cycles. These results suggest predation as a potential mechanism to maintain variation in sexual displays and underscore that short-term studies of sexual display evolution may not accurately predict long-run dynamics. Further, they demonstrate that a common verbal model (that predation limits sexual displays) with widespread empirical support can result in unappreciated, complex dynamics due to the density-dependent nature of predation.
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The pronounced and elaborate displays that often differ between closely related animal species have led to the common assumption that sexual selection is important in speciation, especially in ...geographically separated populations. We use population genetic models to examine the ability of Fisherian sexual selection to contribute to lasting species differentiation by isolating its effect after the onset of gene flow between allopatric populations. We show that when sexually selected traits are under ecologically divergent selection, the situation most favorable to speciation, mating preferences tend to introgress faster than trait alleles, causing sexual selection to counter the effects of local adaptation. As a consequence, the net amount of trait divergence often drops with stronger Fisherian sexual selection. Furthermore, alleles for progressively weaker preferences spread in this context until sexual selection is removed. The effects of pure Fisherian sexual selection on species maintenance are thus much more inhibitory than previously assumed.
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Sympatric speciation illustrates how natural and sexual selection may create new species in isolation without geographic barriers. However, recent genomic reanalyses of classic examples of sympatric ...speciation reveal complex histories of secondary gene flow from outgroups into the radiation. In contrast, the rich theoretical literature on this process distinguishes among a diverse range of models based on simple genetic histories and different types of reproductive isolating barriers. Thus, there is a need to revisit how to connect theoretical models of sympatric speciation and their predictions to empirical case studies in the face of widespread gene flow. Here, theoretical differences among different types of sympatric speciation and speciation‐with‐gene‐flow models are reviewed and summarized, and genomic analyses are proposed for distinguishing which models apply to case studies based on the timing and function of adaptive introgression. Investigating whether secondary gene flow contributed to reproductive isolation is necessary to test whether predictions of theory are ultimately borne out in nature.
Sympatric speciation means two different things to empirical and theoretical biologists. Recent genomic analyses of classic sympatric speciation examples reveal complex histories of secondary gene flow from outgroups. It is argued that reconciling diverse theoretical models with existing empirical examples requires investigating the role that gene flow played in the process.
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Progress in science often begins with verbal hypotheses meant to explain why certain biological phenomena exist. An important purpose of mathematical models in evolutionary research, as in many other ...fields, is to act as “proof-of-concept” tests of the logic in verbal explanations, paralleling the way in which empirical data are used to test hypotheses. Because not all subfields of biology use mathematics for this purpose, misunderstandings of the function of proof-of-concept modeling are common. In the hope of facilitating communication, we discuss the role of proof-of-concept modeling in evolutionary biology.
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Theoretical models often have fundamentally different goals than do empirical studies of the same topic. Models can test the logic of existing hypotheses, explore the plausibility of new hypotheses, ...provide expectations that can be tested with data, and address aspects of topics that are currently inaccessible empirically. Theoretical models are common in ecology and evolution and are generally well cited, but I show that many citations appearing in nontheoretical studies are general to topic and that a substantial proportion are incorrect. One potential cause of this pattern is that some functions of models are rather abstract, leading to miscommunication between theoreticians and empiricists. Such misunderstandings are often triggered by simplifying logistical assumptions that modelers make. The 2018 Vice Presidential Symposium of the American Society of Naturalists included a variety of mathematical models in ecology and evolution from across several topics. Common threads that appear in the use of the models are identified, highlighting the power of a theoretical approach and the role of the assumptions that such models make.
Imprinting sets the stage for speciation Yang, Yusan; Servedio, Maria R; Richards-Zawacki, Corinne L
Nature (London),
10/2019, Volume:
574, Issue:
7776
Journal Article
Peer reviewed
Sexual imprinting-a phenomenon in which offspring learn parental traits and later use them as a model for their own mate preferences-can generate reproductive barriers between species
. When the ...target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate speciation
. However, in most models of speciation by sexual selection, divergent natural selection is also required; the latter acts to generate and maintain variation in the sexually selected trait or traits, and in the mating preferences that act upon them
. Here we demonstrate that imprinting, in addition to mediating female mate preferences, can shape biases in male-male aggression. These biases can act similarly to natural selection to maintain variation in traits and mate preferences, which facilitates reproductive isolation driven entirely by sexual selection. Using a cross-fostering study, we show that both male and female strawberry poison frogs (Oophaga pumilio) imprint on coloration, which is a mating trait that has diverged recently and rapidly in this species
. Cross-fostered females prefer to court mates of the same colour as their foster mother, and cross-fostered males are more aggressive towards rivals that share the colour of their foster mother. We also use a simple population-genetics model to demonstrate that when both male aggression biases and female mate preferences are formed through parental imprinting, sexual selection alone can (1) stabilize a sympatric polymorphism and (2) strengthen the trait-preference association that leads to behavioural reproductive isolation. Our study provides evidence of imprinting in an amphibian and suggests that this rarely considered combination of rival and sexual imprinting can reduce gene flow between individuals that bear divergent mating traits, which sets the stage for speciation by sexual selection.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
“Magic traits,” in which the same trait is both under divergent ecological selection and forms the basis of assortative mating, have been sought after due to their supposed unique ability to promote ...divergence with gene flow. Here, we ask how unique magic traits are, by exploring whether a tightly linked complex of a locus under divergent selection and a locus that acts as a mating cue can mimic a magic trait in its divergence. We find that these “pseudomagic traits” can be very effective in promoting divergence; with tight linkage they are essentially as effective as a magic trait and with loose linkage, and even no linkage, divergence can still be enhanced. Distinguishing between magic and pseudomagic traits in empirical cases may thus not be important when inferring their role in divergence. The ability of divergence in the mating trait to drive divergence in the ecological trait by lowering the effective migration rate, which occurs somewhat even without linkage, is particularly striking; magic traits are typically considered to have the other direction of causality. Our results thus suggest that divergence in a mating trait can at least modestly increase local adaption by allowing more ecological divergence, particularly with tighter linkage.
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The strength of mate choice (choosiness) often varies with age, but theory to understand this variation is scarce. Additionally, theory has investigated the evolution of choosiness in speciation ...scenarios but has ignored that most organisms have overlapping generations. We investigate whether speciation can result in variation of choosiness with age, and whether such variation can in turn affect speciation. We develop a population‐genetic model of the evolution of choosiness in organisms with overlapping generations in the context of secondary contact between two divergent populations. We assume that females choose males that match their phenotype, such that choosiness evolves by sexual selection. We demonstrate that speciation can result in the evolution of age‐specific choosiness when the mating trait is under divergent ecological selection and age is not used as a mating cue. The cause of this result is that allele frequencies differ between choosy females and males. However, we find that the evolution of age‐specific choosiness does not affect the overall level of reproductive isolation compared to a case without age‐structure, supporting previous speciation theory. Overall, our results connect life history and speciation theory, and the mechanisms that we highlight have implications for the understanding of the role of sex‐specific selection in the evolution of choosiness.
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