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.     

CAN REINFORCEMENT OCCUR WITH A LEARNED TRAIT?

We use birdsong as a case study to ask whether reinforcement can occur via the spread of a genetically determined female preference for a socially inherited (learned) male trait. We envision secondary contact between two neighboring populations with different song dialects. An individual's ability to learn song is confined by a genetic predisposition: if predispositions are strong, there will be no phenotypic overlap in song between populations, whereas weak predispositions allow phenotypic overlap, or "mixed" song. To determine if reinforcement has occurred, we consider if an allele for within-population female mating preference, based on song, can spread, and whether population specific songs can concurrently be maintained at equilibrium. We model several scenarios, including costs to mating preferences, mating preferences in hybrids, and hybrids having the ability to learn pure songs. We find that when weak predispositions are fixed within a population reinforcement based on song cannot occur. However, when some individuals have strong predispositions, restricting phenotypic overlap between populations in the trait, reinforcement is only slightly inhibited from a purely genetic model. Generalizing beyond the example of song, we conclude that socially learned signals will tend to prohibit reinforcement, but it may still occur if some individuals acquire trait phenotypes genetically.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.     

Speciation by Reinforcement: A Model Derived from Studies of Drosophila

Reinforcement is an increase in premating reproductive isolation between taxa resulting from selection against hybrids. We present a model of reinforcement with a novel type of selection on female mating behavior. Previous models of reinforcement have focused on the divergence of female mating preferences between nascent species. We suggest that an increase in the level of female mating discrimination can yield reinforcement without further divergence of either male characters or female preferences. This model indicates that selection on mating discrimination is a viable mechanism for reinforcement and may allow speciation under less stringent conditions than selection on female preference. This model also incorporates empirical results from genetic studies of hybrid fitness determination in Drosophila species. We find that the details of inheritance, which include sex-linked transmission, sex-limited fertility reduction, and X-autosome epistasis, have important effects on the likelihood of reinforcement. In particular, X-autosome epistasis for hybrid fitness determination facilitates reinforcement when hybrid fertility reduction occurs in males, but hinders the process when it occurs in females. HALDANE's rule indicates that hybrid sterility will generally evolve in males prior to females within nascent species. Thus, HALDANE's rule and X-autosome epistasis provide conditions that are surprisingly favorable for reinforcement in Drosophila.     

Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

REPRODUCTIVE CHARACTER DISPLACEMENT OF MALE STICKLEBACK MATE PREFERENCE: REINFORCEMENT OR DIRECT SELECTION?

Reproductive isolation can evolve between species as a byproduct of adaptation to different niches, through reinforcement, and by direct selection on mating preferences. We investigated the potential role of direct selection in the reproductive isolation between sympatric species of threespine sticklebacks. Each sympatric pair consists of a small-bodied limnetic species and large-bodied benthic species. We compared the mate preferences and courtship behavior of males from one sympatric limnetic population and two allopatric populations. We used limnetic-like allopatric populations to control for the effects of ecological character displacement and adaptation to different niches on mate preferences. The sympatric limnetic males preferred the small limnetic females, whereas the allopatric limnetic-like males preferred the large benthic females, suggesting that adaptation to the limnetic niche does not automatically confer a preference for small limnetic females. This reproductive character displacement of male preference is consistent with the predictions of both reinforcement and direct selection on mate preferences. To test for direct selection, we assessed a prediction of one proposed mechanism: predation by benthic females on eggs guarded by limnetic males. The allopatric males come from populations in which there is no egg predation. Sympatric limnetic males were more aggressive toward benthic females than toward limnetic females, whereas the allopatric limnetic-like males did not treat the two types of females differently. The contrast in male behavior suggests that egg predation has shaped male preferences. Direct selection is potentially more effective than indirect selection via reinforcement, and it is likely that it has been important in building up reproductive isolation between limnetic and benthic sticklebacks.     

The relative importance of different direct benefits in the mate choices of a field cricket

Discussions about the evolution of female mating preferences have often suggested that females should express multiple strong preferences when different male traits are correlated with different mating benefits, yet few studies have directly tested this hypothesis by comparing the strength of female preferences for male traits known to be correlated with different benefits. In the variable field cricket, Gryllus lineaticeps, females receive fecundity and fertility benefits from mating with males with higher chirp rates and life-span benefits from mating with males with longer chirp durations. Although females prefer higher chirp rates and longer chirp durations when the other trait is held constant, it is possible that they give priority to one of these song traits when both vary. In this study, we examined the relative importance of chirp rate and chirp duration in female mate choice using single-stimulus presentations of songs that varied in both chirp rate and chirp duration. Females expressed both directional and stabilizing preferences based on chirp rate, responding most strongly to a chirp rate approximately one standard deviation above the population mean. Females did not express preferences based on chirp duration, and did not express correlational preferences. These results suggest that females may give priority to the reproductive benefits provided by males that produce higher chirp rates.     

The Role of Courtship Behavior and Size in Mate Preference in the Sex‐Role‐Reversed Gulf Pipefish,Syngnathus scovelli

In sex‐role‐reversed species, sexual selection acts more strongly on females than on males, a situation that can result in the evolution of secondary sexual traits in females and strong mating preferences in males. While some research exploring mating preferences in sex‐role‐reversed species has been conducted, overall, this topic remains relatively unexplored. The Gulf pipefish, Syngnathus scovelli, is a highly polyandrous pipefish species. Sexual selection is significantly stronger in females than in males, which has led to the evolution of both morphological and behavioral female secondary sexual traits. However, because males gestate the offspring in specialized pouches and make a substantial investment in embryos during development, females may also benefit from being choosy. The goal of this study was to examine both male and female mating preferences in this species. We found that male mating preference was significantly associated with female courtship behavior. Larger females were also able to maintain these behaviors for longer intervals than smaller females. No evidence of female mating preference in regard to male size was observed but the data suggest that male behaviors may be providing positive reinforcement to courting females. This research provides further insight into how mate preferences vary among sex‐role‐reversed species.     

Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids

Disruptive sexual selection on colour patterns has been suggested as a major cause of diversification in the cichlid species flock of Lake Victoria. In Neochromis omnicaeruleus, a colour and sex determination polymorphism is associated with a polymorphism in male and female mating preferences. Theoretical work on this incipient species complex found conditions for rapid sympatric speciation by selection on sex determination and sexual selection on male and female colour patterns, under restrictive assumptions. Here we test the biological plausibility of a key assumption of such models, namely, the existence of a male preference against a novel female colour morph before its appearance in the population. We show that most males in a population that lacks the colour polymorphism exhibit a strong mating preference against the novel female colour morph and that reinforcement is not a likely explanation for the origin of such male preferences. Our results show that a specific condition required for the combined action of selection on sex determination and sexual selection to drive sympatric speciation is biologically justified. Finally, we suggest that Lake Victoria cichlids might share an ancestral female recognition scheme, predisposing colour monomorphic populations/species to similar evolutionary pathways leading to divergence of colour morphs in sympatry.     

The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

The evolution of male and female mating preferences in Drosophila speciation*

The relative importance of male and female mating preferences in causing sexual isolation between species remains a major unresolved question in speciation. Despite previous work showing that male courtship bias and/or female copulation bias for conspecifics occur in many taxa, the present study is one of the first large‐scale works to study their relative divergence. To achieve this, we used data from the literature and present experiments across 66 Drosophila species pairs. Our results revealed that male and female mate preferences are both ubiquitous in Drosophila but evolved largely independently, suggesting different underlying evolutionary and genetic mechanisms. Moreover, their relative divergence strongly depends on the geographical relationship of species. Between allopatric species, male courtship and female copulation preferences diverged at very similar rates, evolving approximately linearly with time of divergence. In sharp contrast, between sympatric species pairs, female preferences diverged much more rapidly than male preferences and were the only drivers of enhanced sexual isolation in sympatry and Reproductive Character Displacement (RCD). Not only does this result suggest that females are primarily responsible for such processes as reinforcement, but it also implies that evolved female preferences may reduce selection for further divergence of male courtship preferences in sympatry.     

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.     

Mechanisms of species divergence through visual adaptation and sexual selection: Perspectives from a cichlid model sys-tem

The theory of ecological speciation suggests that assortative mating evolves most easily when mating preferences are directly linked to ecological traits that are subject to divergent selection. Sensory adaptation can play a major role in this process, because selective mating is often mediated by sexual signals: bright colours, complex song, pheromone blends and so on. When divergent sensory adaptation affects the perception of such signals, mating patterns may change as an immediate consequence. Alternatively, mating preferences can diverge as a result of indirect effects: assortative mating may be promoted by selection against intermediate phenotypes that are maladapted to their (sensory) environment. For Lake Victoria cichlids, the visual envi-ronment constitutes an important selective force that is heterogeneous across geographical and water depth gradients. We investi-gate the direct and indirect effects of this heterogeneity on the evolution of female preferences for alternative male nuptial colours (red and blue) in the genus Pundamilia. Here, we review the current evidence for divergent sensory drive in this system, extract general principles, and discuss future perspectives.     

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.     

Female discrimination thresholds frequently exceed local male display variation: implications for mate choice dynamics and sexual selection

Among the factors that can influence female mate choice decisions is the degree to which females differentiate among similar displays: as differences decrease, females are expected to eventually stop discriminating. This discrimination threshold, in conjunction with the magnitude of male trait variation females regularly encounter while making mate choice decisions, may have important consequences for sexual selection. If local display variation is above the discrimination threshold, female preferences should translate into higher mating success for the more attractive male. But if display variation is frequently below the threshold, the resulting increased pattern of random mating may obscure the existence of female mate choice. I investigated the interplay between female discrimination and male display variation in green treefrogs (Hyla cinerea) and found that call trait differences between nearest neighbour males were frequently smaller than what females are expected to discriminate. This finding has two important consequences for our understanding of sexual selection in the wild: first, low display variation should weaken the strength of selection on male display traits, but the direction of selection should mirror the one predicted from females choice trials. Second, caution is needed when interpreting data on realized mating success in the wild: a pattern of random mating with respect to male display traits does not always mean that female preferences are weak or that conditions are too challenging for females to express their preferences. Rather, insufficient display variation can generate the same pattern.     

Reinforcement in the banded darter Etheostoma zonale: The effect of sex and sympatry on preferences

Reinforcement occurs when selection against hybrid offspring strengthens behavioral isolation between parental species and may be an important factor in speciation. Theoretical models and experimental evidence indicate that both female and male preferences can be strengthened upon secondary contact via reinforcement. However, the question remains whether this process is more likely to affect the preferences of one sex or the other. Males of polygynous species are often predicted to exhibit weaker preferences than females, potentially limiting the ability for reinforcement to shape male preferences. Yet, in darters (Percidae: Etheostoma), male preference for conspecific mates appears to arise before female preferences during the early stages of allopatric speciation, and research suggests that male, but not female, preferences become reinforced upon secondary contact. In the current study, we aimed to determine whether the geographically widespread darter species Etheostoma zonale exhibits a signature of reinforcement, by comparing the strength of preference for conspecific mates between populations that are sympatric and allopatric with respect to a close congener, E. barrenense. We examined the strength of preference for conspecifics for males and females separately to determine whether the preferences of one or both sexes have been strengthened by reinforcement. Our results show that both sexes of E. zonale from sympatric populations exhibit stronger conspecific preferences than E. zonale from allopatric populations, but that female preferences appear to be more strongly reinforced than male preferences. Results therefore suggest that reinforcement of female preferences may promote behavioral isolation upon secondary contact, even in a genus that is characterized by pervasive male mate choice.     

Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata

The nature of male mating preferences, and how they differ from female mating preferences in species with conventional sex roles, has received little attention in sexual selection studies. We estimated the form and strength of sexual selection as a consequence of male and female mating preferences in a laboratory-based population of Drosophila serrata. The differences between sexual selection on male and female signal traits (cuticular hydrocarbons [CHCs]) were evaluated within a formal framework of linear and nonlinear selection gradients. Females tended to exert linear sexual selection on male CHCs, whereas males preferred intermediate female CHC phenotypes leading to convex (stabilizing) selection gradients. Possible mechanisms determining the nonlinear nature of sexual selection on female CHCs are proposed.     

MAPPING INDIVIDUAL VARIATION IN MALE MATING PREFERENCE SPACE: MULTIPLE CHOICE IN A COLOR POLYMORPHIC CICHLID FISH

Sexual selection theory largely rests on the assumption that populations contain individual variation in mating preferences and that individuals are consistent in their preferences. However, there are few empirical studies of within-population variation and even fewer have examined individual male mating preferences. Here, we studied a color polymorphic population of the Lake Victoria cichlid fish Neochromis omnicaeruleus , a species in which color morphs are associated with different sex-determining factors. Wild-caught males were tested in three-way choice trials with multiple combinations of different females belonging to the three color morphs. Compositional log-ratio techniques were applied to analyze individual male mating preferences. Large individual variation in consistency, strength, and direction of male mating preferences for female color morphs was found and hierarchical clustering of the compositional data revealed the presence of four distinct preference groups corresponding to the three color morphs in addition to a no-preference class. Consistency of individual male mating preferences was higher in males with strongest preferences. We discuss the implications of these findings for our understanding of the mechanisms underlying polymorphism in mating preferences.     

The evolution of premating isolation: local adaptation and natural and sexual selection against hybrids

Although reinforcement is ostensibly driven by selection against hybrids, there are often other components in empirical cases and theoretical models of reinforcement that may contribute to premating isolation. One of these components is local adaptation of a trait used in mate choice. I use several different comparisons to assess the roles that local adaptation and selection against hybrids may play in reinforcement models. Both numerical simulations of exact recursion equations and analytical weak selection approximations are employed. I find that selection against hybrids may play a small role in driving preference evolution in a reinforcement model where the mating cue is separate from loci causing hybrid incompatibilities. When females have preferences directly for purebreds of their own population, however, selection against hybrids can play a large role in premating isolation evolution. I present some situations in which this type of selection is likely to exist. This work also illustrates shortfalls of using a weak selection approach to address questions about reinforcement.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.