Predation drives complex eco-evolutionary dynamics in sexually selected traits.

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.

Inferred Attractiveness: A generalized mechanism for sexual selection that can maintain variation in traits and preferences over time.

Sexual selection by mate choice is a powerful force that can lead to evolutionary change, and models of why females choose particular mates are central to understanding its effects. Predominant mate choice theories assume preferences are determined solely by genetic inheritance, an assumption still lacking widespread support. Moreover, preferences often vary among individuals or populations, fail to correspond with conspicuous male traits, or change with context, patterns not predicted by dominant models. Here, we propose a new model that explains this mate choice complexity with one general hypothesized mechanism, "Inferred Attractiveness." In this model, females acquire mating preferences by observing others' choices and use context-dependent information to infer which traits are attractive. They learn to prefer the feature of a chosen male that most distinguishes him from other available males. Over generations, this process produces repeated population-level switches in preference and maintains male trait variation. When viability selection is strong, Inferred Attractiveness produces population-wide adaptive preferences superficially resembling "good genes." However, it results in widespread preference variation or nonadaptive preferences under other predictable circumstances. By casting the female brain as the central selective agent, Inferred Attractiveness captures novel and dynamic aspects of sexual selection and reconciles inconsistencies between mate choice theory and observed behavior.

Imprinting sets the stage for speciation.

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 species1. When the target of imprinting is a mating trait that differs among young lineages, imprinted preferences may contribute to behavioural isolation and facilitate speciation1,2. 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 them3. 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 species4. 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.

The Evolution of Mate Attachment.

AbstractWhether natural selection leads to attachment in monogamous pair bonds has seldom been addressed. Operationally defining attachment as a behavioral modifier that decreases divorce probability with pair duration, we develop a model for the evolution of attachment. If divorce (the ending of a pair bond when both individuals survive to the next breeding season) is more likely to occur out of poor-quality reproductive opportunities (i.e., poor territory or low-quality mate), individuals in experienced pairs are more likely to be found in high-quality opportunities. Consequently, when divorce decisions occur using imperfect information from reproductive success, pair duration provides individuals with information about the quality of their reproductive opportunity and attachment can evolve. We show that high survival rates, divorce propensities, and probabilities of nest failure favor the evolution of attachment. Attachment is also more likely to evolve when individuals can directly assess the quality of their reproductive opportunity (as opposed to relying on imperfect information from reproductive success), when the quality of the reproductive opportunity has adult survival ramifications, and when divorce coevolves with attachment. We show that our core conclusions are robust to a variety of assumptions using individual-based simulations. Our results clarify how attachment can be adaptive and suggest that studying pair bonds as dynamic entities is a promising avenue for future work.

The evolution of fear-acquisition strategies under predation.

Fear is a taxonomically widespread behavioral response that functions to keep individuals out of danger. Empirical research has demonstrated that a diverse set of strategies are used in order to acquire a fear response across animals. Animals often use a mixed strategy: fear is acquired both innately and through learning. Despite the ubiquity of the fear response, and its established importance for shaping predator-prey interactions, little is known about why different fear acquisition strategies evolve or why mixed strategies appear common. Here, we model the evolution of fear acquisition (learning versus innate) under predation. We assume a tradeoff where individuals that learn fear are at higher risk from predators initially, but eventually obtain a lower risk as they survive predation attempts. We find that frequent predator encounters, predators that are not very dangerous, and effective learning favor the evolution of learned fear. Only pure strategies of fear acquisition evolve unless individuals suffer from either a cost to fear or, especially, a cost to learning, either of which can lead to the evolution of mixed strategies. Our results thus shed light onto the evolution of mixed fear acquisition strategies and open the door to further research on the evolution of fear acquisition.

Indiscriminate Mating and the Coevolution of Sex Discrimination and Sexual Signals.

AbstractThe presence of same-sex sexual behavior across the animal kingdom is often viewed as unexpected. One explanation for its prevalence in some taxa is indiscriminate mating-a strategy wherein an individual does not attempt to determine the sex of its potential partner before attempting copulation. Indiscriminate mating has been argued to be the ancestral mode of sexual reproduction and can also be an optimal strategy given search costs of choosiness. Less attention has been paid to the fact that sex discrimination requires not just the attempt to differentiate between the sexes but also some discernible difference (a signal or cue) that can be detected. To address this, we extend models of mating behavior to consider the coevolution of sex discrimination and sexual signals. We find that under a wide range of parameters, including some with relatively minor costs, indiscriminate mating and the absence of sexual signals will be an evolutionary end point. Furthermore, the absence of both sex discrimination and sexual signals is always evolutionarily stable. These results suggest that an observable difference between the sexes likely arose as a by-product of the evolution of different sexes, allowing discrimination to evolve.

The effectiveness of pseudomagic traits in promoting premating isolation.

Upon the secondary contact of populations, speciation with gene flow is greatly facilitated when the same pleiotropic loci are both subject to divergent ecological selection and induce non-random mating, leading to loci with this fortuitous combination of functions being referred to as 'magic trait' loci. We use a population genetics model to examine whether 'pseudomagic trait' complexes, composed of physically linked loci fulfilling these two functions, are as efficient in promoting premating isolation as magic traits. We specifically measure the evolution of choosiness, which controls the strength of assortative mating. We show that, surprisingly, pseudomagic trait complexes, and to a lesser extent also physically unlinked loci, can lead to the evolution of considerably stronger assortative mating preferences than do magic traits, provided polymorphism at the involved loci is maintained. This is because assortative mating preferences are generally favoured when there is a risk of producing maladapted recombinants, as occurs with non-magic trait complexes but not with magic traits (since pleiotropy precludes recombination). Contrary to current belief, magic traits may not be the most effective genetic architecture for promoting strong premating isolation. Therefore, distinguishing between magic traits and pseudomagic trait complexes is important when inferring their role in premating isolation. This calls for further fine-scale genomic research on speciation genes.

Evolutionary rescue under demographic and environmental stochasticity.

Populations suffer two types of stochasticity: demographic stochasticity, from sampling error in offspring number, and environmental stochasticity, from temporal variation in the growth rate. By modelling evolution through phenotypic selection following an abrupt environmental change, we investigate how genetic and demographic dynamics, as well as effects on population survival of the genetic variance and of the strength of stabilizing selection, differ under the two types of stochasticity. We show that population survival probability declines sharply with stronger stabilizing selection under demographic stochasticity, but declines more continuously when environmental stochasticity is strengthened. However, the genetic variance that confers the highest population survival probability differs little under demographic and environmental stochasticity. Since the influence of demographic stochasticity is stronger when population size is smaller, a slow initial decline of genetic variance, which allows quicker evolution, is important for population persistence. In contrast, the influence of environmental stochasticity is population-size-independent, so higher initial fitness becomes important for survival under strong environmental stochasticity. The two types of stochasticity interact in a more than multiplicative way in reducing the population survival probability. Our work suggests the importance of explicitly distinguishing and measuring the forms of stochasticity during evolutionary rescue.

The ecological stage maintains preference differentiation and promotes speciation.

Influential models of speciation by sexual selection posit either a single shared preference for a universal display, expressed only when males are locally adapted and hence in high condition, or that shared loci evolve population-specific alleles for displays and preferences. However, many closely related species instead show substantial differences across categorically different traits. We present a model of secondary contact whereby females maintain preferences for distinct displays that indicate both male condition and their match to distinct environments, fostering reproductive isolation among diverging species. This occurs even with search costs and with independent preference loci targeting independent displays. Such preferences can also evolve from standing variation. Divergence occurs because condition-dependent display and female preference depend on local ecology, and females obtain different benefits of choice. Given the ubiquity of ecological differences among environments, our model could help explain the evolution of striking radiations of displays seen in nature.

Better to Divorce than Be Widowed: The Role of Mortality and Environmental Heterogeneity in the Evolution of Divorce.

AbstractDespite widespread interest in the evolution and implications of monogamy across taxa, less attention-especially theoretical-has been paid toward understanding the evolution of divorce (ending a socially monogamous pairing to find a new partner). Here, we develop a model of the evolution of divorce by females in a heterogeneous environment, where females assess territory quality as a result of their breeding success. Divorce results in females leaving poor territories disproportionally more often than good territories, while death of a partner occurs independent of territory quality, giving an advantage to divorce. Increasing environmental heterogeneity, a decreasing benefit of pair experience, and moderate survival rates favor the evolution of higher divorce rates, even in the absence of variance in individual quality and knowledge of available territories. Imperfect information about territory quality constrains the evolution of divorce, typically favoring divorce strategies that remain faithful to one's partner whenever successful reproduction occurs. Our model shows how feedbacks between divorce, widowhood, and the availability of territories are intricately linked in determining the evolutionary advantage of divorce. We detail testable predictions about populations that should be expected to divorce at high rates.

Evolution of sexual cooperation from sexual conflict.

In many species that form pair bonds, males display to their mate after pair formation. These displays elevate the female's investment into the brood. This is a form of cooperation because without the display, female investment is reduced to levels that are suboptimal for both sexes. The presence of such displays is paradoxical as in their absence the male should be able to invest extra resources directly into offspring, to the benefit of both sexes. We consider that the origin of these displays lies in the exploitation of preexisting perceptual biases which increase female investment beyond that which is optimal for her, initially resulting in a sexual conflict. We use a combined population genetic and quantitative genetic model to show how this conflict becomes resolved into sexual cooperation. A cooperative outcome is most likely when perceptual biases are under selection pressures in other contexts (e.g., detection of predators, prey, or conspecifics), but this is not required. Cooperation between pair members can regularly evolve even when this provides no net advantage to the pair and when the display itself reduces a male's contributions to raising the brood. The findings account for many interactions between the sexes that have been difficult to explain in the context of sexual selection.

The evolution of flower longevity in unpredictable pollination environments.

Pollination requires a flower to remain open for long enough to allow for the arrival of pollinators. However, maintaining flowers costs energy and resources. Therefore, flower longevity, the length of time a flower remains viable, is critical for the outcome of plant reproduction. Although previous studies showed that the evolution of flower longevity depends on the rates of pollen deposition and removal, whether plants should increase or decrease flower life span when the pollination environment is unpredictable has not been explored. Moreover, the common hypothesis that an unpredictable pollination environment should select for increased flower longevity may be too simplistic since there is no distinction drawn between the effects of spatial and temporal variation. Adopting evolutionary game theory, we investigate the evolution of flower longevity under three types of variation: spatial heterogeneity, daily fluctuations within a flowering season and yearly fluctuations between flowering seasons. We find that spatial heterogeneity often selects for a shorter flower lifespan, while temporal fluctuations of fitness accrual rates at both daily and yearly time scales tends to favour greater longevity, although daily and yearly fluctuations have somewhat different effects. However, the presence of correlation between female and male fitness accrual rates seems to have no effect on flower longevity. Our work suggests that explicit measurements of spatial and temporal variation in both female and male functions may provide a better understanding of the evolution of flower longevity and reproduction.

Searching for Sympatric Speciation in the Genomic Era.

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.

An Effective Mutualism? The Role of Theoretical Studies in Ecology and Evolution.

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.

Grey zones of sexual selection: why is finding a modern definition so hard?

Sexual selection has long been acknowledged as an important evolutionary force, capable of shaping phenotypes ranging from fascinating and unusual displays to cryptic traits whose function is only uncovered by careful study. Yet, despite decades of research, reaching a consensus definition of the term 'sexual selection' has proved difficult. Here we explore why arriving at a unifying definition of sexual selection is so hard. While some researchers have argued about whether sexual selection should be considered a form of natural selection, we concentrate on where the line between sexual selection and other forms of selection falls. We focus on identifying the 'grey zones' of sexual selection by illustrating cases in which application of the term 'sexual selection' would be considered controversial or ambiguous. We believe that clarifying why sexual selection is so difficult to define is an essential first step forward towards greater clarity, and if possible towards reaching a consensus definition. We suggest that a more nuanced perspective may be necessary, particularly one that specifies for cases of 'sexual selection' why the term is used or whether they fall into a grey zone.

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice.

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.

Mechanisms of Assortative Mating in Speciation with Gene Flow: Connecting Theory and Empirical Research.

The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.

Theory Meets Empiry: A Citation Network Analysis.

According to a recent survey, ecologists and evolutionary biologists feel that theoretical and empirical research should coexist in a tight feedback loop but believe that the two domains actually interact very little. We evaluate this perception using a citation network analysis for two data sets, representing the literature on sexual selection and speciation. Overall, 54%-60% of citations come from a paper's own category, whereas 17%-23% are citations across categories. These cross-citations tend to focus on highly cited papers, and we observe a positive correlation between the numbers of citations a study receives within and across categories. We find evidence that reviews can function as integrators between the two literatures, argue that theoretical models are analogous to specific empirical study systems, and complement our analyses by studying a cocitation network. We conclude that theoretical and empirical research are more tightly connected than generally thought but that avenues exist to further increase this integration.

The Roles of Sexual and Viability Selection in the Evolution of Incomplete Reproductive Isolation: From Allopatry to Sympatry.

In recent years, theoretical models have introduced the concept that ongoing hybridization between "good" species can occur because incomplete reproductive isolation can be a selected optimum. They furthermore show that positive frequency-dependent sexual selection, which is naturally generated by some of the underlying processes that lead to assortative mating, plays a key role in the evolution of incomplete reproductive isolation. This occurs, however, through different mechanisms in sympatric versus allopatric scenarios. We investigate the evolution of incomplete reproductive isolation by sexual selection in scenarios ranging from sympatry to allopatry, to examine how these mechanisms interact. We consider an ecological scenario in which there are two habitats used during foraging and individuals can breed either within a habitat or in a common mating pool. We find that when trait divergence is maintained, sexual selection drives the evolution of choosiness in opposite ways in the common mating pool versus within each habitat. Specifically, strong choosiness is favored in the common mating pool, whereas intermediate choosiness is favored within habitat; the interaction of these forces determines whether intermediate reproductive isolation ultimately evolves in the system. We further find cases where the evolution of stronger choosiness occurs but leads to the loss of divergence. Overall, our study shows that contrasting forces on the evolution of reproductive isolation can occur in different mating areas, and we propose a new avenue for understanding the diversity in levels of reproductive isolation within and across species.

Not just a theory--the utility of mathematical models in evolutionary biology.

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.