Liking the good guys: amplifying local adaptation via the evolution of condition‐dependent mate choice

Local adaptation can be strengthened through a diversity of mechanisms that reduce gene flow between contrasting environments. Recent work revealed that mate choice could enhance local adaptation when females preferentially mate with locally adapted males and that such female preferences readily evolve, but the opposing effects of recombination, migration and costs of female preferences remain relatively unexplored. To investigate these effects, we develop a two‐patch model with two genes, one influencing an ecological trait and one influencing female preferences, where both male signals and female preferences are allowed to depend on the match between an individual's ecological trait and the local environment (condition). Because trait variation is limited when migration is rare and the benefits of preferential mating are short‐lived when migration is frequent, we find that female preferences for males in high condition spread most rapidly with intermediate levels of migration. Surprisingly, we find that preferences for locally adapted males spread fastest with higher recombination rates, which contrasts with earlier studies. This is because a stronger preference allele for locally adapted males can only get uncoupled from maladapted ecological alleles following migration through recombination. The effects of migration and recombination depend strongly on the condition of the males being chosen by females, but only weakly on the condition of the females doing the choosing, except when it comes to the costs of preference. Although costs always impede the spread of female preferences for locally adapted males, the impact is substantially lessened if costs are borne primarily by females in poor condition. The abundance of empirical examples of condition‐dependent mate choice combined with our theoretical results suggests that the evolution of mate choice could commonly facilitate local adaptation in nature.     

ON THE EVOLUTION OF MIGRATION IN HETEROGENEOUS ENVIRONMENTS

Populations often experience variable conditions, both in time and space. Here we develop a novel theoretical framework to study the evolution of migration under the influence of spatially and temporally variable selection and genetic drift. First, we examine when polymorphism is maintained at a locus under heterogeneous selection, as a function of the pattern of spatial heterogeneity and the migration rate. In a second step, we study how levels of migration evolve under the joint action of kin competition and local adaptation at a polymorphic locus. This analysis reveals the existence of evolutionary bistability, whereby a low or a high migration rate may evolve depending on the initial conditions. Last, we relax several assumptions regarding selection heterogeneity commonly made in previous studies and explore the consequences of more complex spatial and temporal patterns of variability in selection on the evolution of migration. We found that small modifications in the pattern of environmental heterogeneity may have dramatic effects on the evolution of migration. This work highlights the importance of considering more general scenarios of environmental heterogeneity when studying the evolution of life‐history traits in ecologically complex settings.     

Quantitative genetic models of sexual selection by male choice

There are many examples of male mate choice for female traits that tend to be associated with high fertility. I develop quantitative genetic models of a female trait and a male preference to show when such a male preference can evolve. I find that a disagreement between the fertility maximum and the viability maximum of the female trait is necessary for directional male preference (preference for extreme female trait values) to evolve. Moreover, when there is a shortage of available male partners or variance in male nongenetic quality, strong male preference can evolve. Furthermore, I also show that males evolve to exhibit a stronger preference for females that are more feminine (less resemblance to males) than the average female when there is a sexual dimorphism caused by fertility selection which acts only on females.     

Genes as Cues of Relatedness and Social Evolution in Heterogeneous Environments

There are many situations where relatives interact while at the same time there is genetic polymorphism in traits influencing survival and reproduction. Examples include cheater-cooperator polymorphism and polymorphic microbial pathogens. Environmental heterogeneity, favoring different traits in nearby habitats, with dispersal between them, is one general reason to expect polymorphism. Currently, there is no formal framework of social evolution that encompasses genetic polymorphism. We develop such a framework, thus integrating theories of social evolution into the evolutionary ecology of heterogeneous environments. We allow for adaptively maintained genetic polymorphism by applying the concept of genetic cues. We analyze a model of social evolution in a two-habitat situation with limited dispersal between habitats, in which the average relatedness at the time of helping and other benefits of helping can differ between habitats. An important result from the analysis is that alleles at a polymorphic locus play the role of genetic cues, in the sense that the presence of a cue allele contains statistical information for an organism about its current environment, including information about relatedness. We show that epistatic modifiers of the cue polymorphism can evolve to make optimal use of the information in the genetic cue, in analogy with a Bayesian decision maker. Another important result is that the genetic linkage between a cue locus and modifier loci influences the evolutionary interest of modifiers, with tighter linkage leading to greater divergence between social traits induced by different cue alleles, and this can be understood in terms of genetic conflict.     

Environmental change mediates mate choice for an extended phenotype,but not for mate quality

Sexual cues, including extended phenotypes, are expected to be reliable indicators of male genetic quality and/or provide information on parental quality. However, the reliability of these cues may be dependent on stability of the environment, with heterogeneity affecting how selection acts on such traits. Here, we test how environmental change mediates mate choice for multiple sexual traits, including an extended phenotype–‐the structure of male‐built nests – in stickleback fish. First, we manipulated the dissolved oxygen (DO) content of water to create high or low DO environments in which male fish built nests. Then we recorded the mate choice of females encountering these males (and their nests), under either the same or reversed DO conditions. Males in high DO environments built more compact nests than those in low DO conditions and males adjusted their nest structure in response to changing conditions. Female mate choice for extended phenotype (male nests) was environmentally dependent (females chose more compact nests in high DO conditions), while female choice for male phenotype was not (females chose large, vigorous males regardless of DO level). Examining mate choice in this dynamic context suggests that females evaluate the reliability of multiple sexual cues, taking into account environmental heterogeneity.     

Natural and Sexual Selection on Many Loci

A method is developed that describes the effects on an arbitrary number of autosomal loci of selection on haploid and diploid stages, of nonrandom mating between haploid individuals, and of recombination. We provide exact recursions for the dynamics of allele frequencies and linkage disequilibria (nonrandom associations of alleles across loci). When selection is weak relative to recombination, our recursions provide simple approximations for the linkage disequilibria among arbitrary combinations of loci. We show how previous models of sex-independent natural selection on diploids, assortative mating between haploids, and sexual selection on haploids can be analyzed in this framework. Using our weak-selection approximations, we derive new results concerning the coevolution of male traits and female preferences under natural and sexual selection. In particular, we provide general expressions for the intensity of linkage-disequilibrium induced selection experienced by loci that contribute to female preferences for specific male traits. Our general results support the previous observation that these indirect selection forces are so weak that they are unlikely to dominate the evolution of preference-producing loci.     

Recombination and the evolution of coordinated phenotypic expression in a frequency-dependent game

A long standing question in evolutionary biology concerns the maintenance of adaptive combinations of traits in the presence of recombination. This problem may be solved if positive epistasis selects for reducing the rate of recombination between such traits, but this requires sufficiently strong epistasis. Here we use a model that we developed previously to analyze a frequency-dependent strategy game in asexual populations, to study how adaptive combinations of traits may be maintained in the presence of recombination when epistasis is too weak to select for genetic linkage. Previously, in the asexual case, our model demonstrated the evolution of adaptive associations between social foraging strategies and learning rules. We verify that these adaptive associations, which are represented by different two-locus haplotypes, can easily be broken by genetic recombination. We also confirm that a modifier allele that reduces the rate of recombination fails to evolve (due to weak epistasis). However, we find that under the same conditions of weak epistasis, there is an alternative mechanism that allows an association between traits to evolve. This is based on a genetic switch that responds to the presence of one social foraging allele by activating one of the two alternative learning alleles that are carried by all individuals. We suggest that such coordinated phenotypic expression by genetic switches offers a general and robust mechanism for the evolution of adaptive combinations of traits in the presence of recombination.     

The genetic architecture of adaptation under migration-selection balance

Many ecologically important traits have a complex genetic basis, with the potential for mutations at many different genes to shape the phenotype. Even so, studies of local adaptation in heterogeneous environments sometimes find that just a few quantitative trait loci (QTL) of large effect can explain a large percentage of observed differences between phenotypically divergent populations. As high levels of gene flow can swamp divergence at weakly selected alleles, migration-selection-drift balance may play an important role in shaping the genetic architecture of local adaptation. Here, we use analytical approximations and individual-based simulations to explore how genetic architecture evolves when two populations connected by migration experience stabilizing selection toward different optima. In contrast to the exponential distribution of allele effect sizes expected under adaptation without migration (Orr 1998), we find that adaptation with migration tends to result in concentrated genetic architectures with fewer, larger, and more tightly linked divergent alleles. Even if many small alleles contribute to adaptation at the outset, they tend to be replaced by a few large alleles under prolonged bouts of stabilizing selection with migration. All else being equal, we also find that stronger selection can maintain linked clusters of locally adapted alleles over much greater map distances than weaker selection. The common empirical finding of QTL of large effect is shown to be expected with migration in a heterogeneous landscape, and these QTL may often be composed of several tightly linked alleles of smaller effect.     

The evolution of postpairing male mate choice

An increasing number of empirical studies in animals have demonstrated male mate choice. However, little is known about the evolution of postpairing male choice, specifically which occurs by differential allocation of male parental care in response to female signals. We use a population genetic model to examine whether such postpairing male mate choice can evolve when males face a trade‐off between parental care and extra‐pair copulations (EPCs). Specifically, we assume that males allocate more effort to providing parental care when mated to preferred (signaling) females, but they are then unable to allocate additional effort to seek EPCs. We find that both male preference and female signaling can evolve in this situation, under certain conditions. First, this evolution requires a relatively large difference in parental investment between males mated to preferred versus nonpreferred females. Second, whether male choice and female signaling alleles become fixed in a population versus cycle in their frequencies depends on the additional fecundity benefits from EPCs that are gained by choosy males. Third, less costly female signals enable both signaling and choice alleles to evolve under more relaxed conditions. Our results also provide a new insight into the evolution of sexual conflict over parental care.     

The evolution of preference strength under sensory bias: a role for indirect selection?

Evidence suggests that female preferences may sometimes arise through sensory bias, and that males may subsequently evolve traits that increase their conspicuousness to females. Here, we ask whether indirect selection, arising through genetic associations (linkage disequilibrium) during the sexual selection that sensory bias imposes, can itself influence the evolution of preference strength. Specifically, we use population genetic models to consider whether or not modifiers of preference strength can spread under different ecological conditions when female mate choice is driven by sensory bias. We focus on male traits that make a male more conspicuous in certain habitats-and thus both more visible to predators and more attractive to females-and examine modifiers of the strength of preference for conspicuous males. We first solve for the rate of spread of a modifier that strengthens preference within an environmentally uniform population; we illustrate that this spread will be extremely slow. Second, we used a series of simulations to consider the role of habitat structure and movement on the evolution of a modifier of preference strength, using male color polymorphisms as a case study. We find that in most cases, indirect selection does not allow the evolution of stronger or weaker preferences for sensory bias. Only in a "two-island" model, where there is restricted migration between different patches that favor different male phenotypes, did we find that preference strength could evolve. The role of indirect selection in the evolution of sensory bias is of particular interest because of ongoing speculation regarding the role of sensory bias in the evolution of reproductive isolation.     

THE EVOLUTION OF MATE PREFERENCES FOR MULTIPLE SEXUAL ORNAMENTS

Males of many species use multiple sexual ornaments in their courtship display. We investigate the evolution of female sexual preferences for more than a single male trait by the handicap process. The handicap process assumes that ornaments are indicators of male quality, and a female benefits from mate choice by her offspring inheriting “good genes” that increase survival chances. A new handicap model is developed that allows equilibria to be given in terms of selection pressures, independent of genetic parameters. Multiple sexual preferences evolve if the overall cost of choice is not greatly increased by a female using additional male traits in her assessment of potential mates. However, only a single preference is evolutionarily stable if assessment of additional male traits greatly increases the overall cost of choice (more than expected by combining the cost of each preference independently). Any single preference can evolve, the outcome being determined by initial conditions. The evolution of one preference effectively blocks the evolution of others, even for traits that are better indicators of male quality. Comparison is made with sexual selection caused by Fisher's runaway process in which male traits are purely attractive characters. This shows that sexual preferences for multiple Fisher traits are likely to evolve alongside preference for a single handicap trait that indicates male quality. This is a general difference in the evolutionary outcome of these two causes of sexual selection.     

Sexual selection when the female directly benefits

Why do females of many species mate with males on the basis of traits apparently detrimental to male survival? The answer may lie in the fact that these male traits are correlated with male condition. We consider the argument that high male condition directly benefits female fecundity and/or viability (e.g. through lower transmission of parasites, improved control of resources, or better paternal care). Using a quantitative genetic model we show how female preferences for male traits that indicate condition can evolve, even if the male traits themselves have deleterious effects on both the male and the female's fecundity. So-called ‘arbitrary preferences’ can spread in this way because male traits subject to sexual selection are often under additional selection to become correlated with condition. At equilibrium the positive effects of male condition on a female's fecundity and the negative effects of the male trait on her fecundity are balanced and the female preference is under stabilizing selection. The male trait will often be correlated with viability, but not with fecundity, even though the preference evolved as a result of differences in male fecundity. The mean fecundity of females is not maximized, and can steadily decline as the male trait and female preference evolve. If the male trait has no direct deleterious effects on female fecundity, as may happen in species with no paternal care, female preferences are under continuous directional selection to increase.     

SELECTION FOR RECOMBINATION IN SMALL POPULATIONS

Abstract The reasons that sex and recombination are so widespread remain elusive. One popular hypothesis is that sex and recombination promote adaptation to a changing environment. The strongest evidence that increased recombination may evolve because recombination promotes adaptation comes from artificially selected populations. Recombination rates have been found to increase as a correlated response to selection on traits unrelated to recombination in several artificial selection experiments and in a comparison of domesticated and nondomesticated mammals. There are, however, several alternative explanations for the increase in recombination in such populations, including two different evolutionary explanations. The first is that the form of selection is epistatic, generating linkage disequilibria among selected loci, which can indirectly favor modifier alleles that increase recombination. The second is that random genetic drift in selected populations tends to generate disequilibria such that beneficial alleles are often found in different individuals; modifier alleles that increase recombination can bring together such favorable alleles and thus may be found in individuals with greater fitness. In this paper, we compare the evolutionary forces acting on recombination in finite populations subject to strong selection. To our surprise, we found that drift accounted for the majority of selection for increased recombination observed in simulations of small to moderately large populations, suggesting that, unless selected populations are large, epistasis plays a secondary role in the evolution of recombination.     

Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata)

Under the indicator models of mate choice, female preferences evolve to exploit the condition-dependence or "indicator value" of male traits, which in turn may cause these traits to evolve to elaborate extremes. If the indicator value of a male trait changes, the payoff function of the female preference for that trait should change and the preference should evolve to a new optimum. I tested this prediction in the guppy, Poecilia reticulata, a species in which the indicator value of a sexually selected male trait, carotenoid coloration, varies geographically. Carotenoid coloration is thought to be an indicator of foraging ability and health because animals must obtain carotenoid pigments from their diet. The primary dietary source of carotenoids for guppies is unicellular algae, the abundance of which varies among natural streams because of variation in forest canopy cover. Carotenoid availability limits male coloration to a greater extent in streams with greater forest canopy cover. Thus, the indicator value of male coloration covaries positively with canopy cover. To test the indicator model prediction, I measured genetic divergence in the strength of female preferences for carotenoid coloration between high- and low-carotenoid availability streams in each of three river drainages. Second-generation laboratory-born females were given a choice between full-sib males raised on three different dietary levels of carotenoids. For all six populations, male attractiveness (as determined from the responses of females to male courtship displays) increased with dietary carotenoid levels. However, the strength of female preferences differed between populations in the predicted direction in only one of three river drainages. These results fail to support a crucial prediction of the indicator model. More studies taking an interpopulation approach to studying mate preference evolution are needed before the explanatory value of the indicator models can be rigorously assessed.     

The evolution of female mating preferences: differentiation from species with promiscuous males can promote speciation

Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.     

Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement

Male mate choice, expressed through courtship preferences, sometime occurs even under the mating system of polygyny, when the operational sex ratio is skewed toward males. The conditions under which male mate choice may be expected during polygyny are not well established. Servedio and Lande (2006, Evolution 60:674-685), assuming strict polygyny where all females have equal mating success, show that when having a preference does not increase the amount of energy that a male can put into courtship, male preferences for "arbitrary" female ornaments should not be expected to evolve; direct selection acts against them because they place males that carry them into situations in which there is high competition for mates. Here I explore in detail two situations under which logic dictates that this effect may be overcome or reversed. First I determine the contributions that direct and indirect selection place on male versus female preferences for traits that increase viability, using notation that allows the exact expression of these measures of selection. I find that direct selection against male preferences still predominates in the male mate choice model, causing less evolution by male than female preferences under these conditions. Second I address whether male mate choice is likely to evolve as a mechanism of premating isolation leading to species recognition, driven by the process of reinforcement. Reinforcement is compared under male and female mate choice, using a variety of models analyzed by both analytical techniques assuming weak selection and numerical techniques under broader selective conditions. I demonstrate that although under many conditions stronger premating isolation evolves under female mate choice, reinforcement may indeed occur via male mate choice alone.     

Direct detection of male quality can facilitate the evolution of female choosiness and indicators of good genes: Evolution across a continuum of indicator mechanisms

The evolution of mating displays as indicators of male quality has been the subject of extensive theoretical and empirical research for over four decades. Research has also addressed the evolution of female mate choice favoring such indicators. Yet, much debate still exists about whether displays can evolve through the indirect benefits of female mate choice. Here, we use a population genetic model to investigate how the extent to which females can directly detect male quality influences the evolution of female choosiness and male displays. We use a continuum framework that incorporates indicator mechanisms that are traditionally modeled separately. Counter to intuition, we find that intermediate levels of direct detection of male quality can facilitate, rather than impede, the evolution of female choosiness and male displays in broad regions of this continuum. We examine how this evolution is driven by selective forces on genetic quality and on the display, and find that direct detection of male quality results in stronger indirect selection favoring female choosiness. Our results imply that displays maybe more likely to evolve when female choosiness has already evolved to discriminate perceptible forms of male quality. They also highlight the importance of considering general female choosiness, as well as preference, in studies of “good genes.”     

Is Preening Behaviour Sexually Selected? An Experimental Approach

Elaborate or colourful feathers are important traits in female mate choice in birds but little attention has been given to potential costs of maintaining these traits in good condition with preening behaviour. Recent studies indicate that the time and energy required to maintain ornamental plumage in good condition reinforces the honesty of plumage trait. It has been proposed that some behaviours, whose primary function is not to transfer information, can also evolve as signalling components. Here we investigate whether the preening behaviour intensity has a signalling component: we hypothesized that if only high quality males can invest a lot of time in preening, this behaviour may be used by females as a quality signal (attractive preening hypothesis). We tested this hypothesis by using female budgerigars in mate‐choice tests in captivity. We tried to experimentally manipulate the preening behaviour of two groups of budgerigar males (treatment and control group). The proportion of time in which treated males preened in front of females was statistically higher than for control males, however, females spent similar amounts of time with treated males and control males. Moreover, males did not show significant quantitative changes in preening (for both groups) when females were present, suggesting that male budgerigars did not use this behaviour to convey information. These results are inconsistent with the ‘attractive preening’ hypothesis which predicts that preening behaviour itself provides information on condition and is used in female choice.     

Female soldier beetles display a flexible preference for selectively favored male phenotypes

In Georgia (USA) the soldier beetle, Chauliognathus pennsylvanicus (Coleoptera; Cantharidae), exhibits clinal variation in the length of the spot on its elytron. This suggests that the viability of phenotypes varies by habitat. Evidence of viability selection comes from within-site changes in the spot length distribution across a breeding season. When males with spots of intermediate length became less frequent, they became disproportionately less likely to mate, consistent with either a loss of vigor among remaining males or female rejection of disfavored phenotypes. Persistent, daily courtship by males provides females with the opportunity to track changes in male phenotype frequency and to exercise choice for phenotypes favored under natural selection. A laboratory experiment in which the frequency of one spot morph (long) or the other (short) was increased from 25% to 75% over a period of 30 days revealed that females possess a flexible preference that leads them to prefer whichever spot type has become more common over time. A haploid genetic model demonstrates that a flexible female preference for the locally favored male phenotype can be selected for when different viability alleles, genetically correlated with the male trait, are favored in different habitats that are linked by gene flow. Thus, migration between different kinds of habitat patches of a metapopulation could maintain the variation in male quality. This variation favors female choice for any trait that is directly or indirectly favored by natural selection. Such choice imparts positive frequency-dependent selection that could rapidly fix traits pleiotropically linked to viability. Rapid fixation would cause differentiation between populations of colonizing species as females exercise choice for mates favored under new ecological conditions.     

Sexual selection when fertilization is not guaranteed

Abstract Much of the theory of sexual selection assumes that females do not generally experience difficulties getting their eggs fertilized, yet sperm limitation is occasionally documented. How often does male limitation form a selection for female traits that improve their mating rate? The question is difficult to test, because if such traits evolve to be efficient, sperm limitation will no longer appear to be a problem to females. Here, we suggest that changes in choosiness between populations, and in particular between virgin and mated females, offer an efficient way to test this hypothesis. We model the “wallflower effect,” that is, changes in female preferences due to time and mortality costs of remaining unmated (for at least some time). We show that these costs cause adaptive reductions of female choice, even if mate encounter rates appear high and females only rarely end their lives unfertilized. We also consider the population consequences of plastic or fixed mate preferences at different mate encounter rates. If mate choice is plastic, we confirm earlier verbal models that virgins should mate relatively indiscriminately, but plastic increase of choosiness in later matings can compensate and intensify sexual selection on the male trait, particularly if there is last male sperm precedence. Plastic populations will cope well with unusual conditions: eagerness of virgins leads to high reproductive output and a relaxation of sexual selection at low population densities. If females lack such plasticity, however, population‐wide reproductive output may be severely reduced, whereas sexual selection on male traits remains strong.