Genetic analysis of female preference functions as function-valued traits

The genetic analysis of female preferences has been seen as a particularly challenging empirical endeavor because of difficulties in generating suitable preference metrics in experiments large enough to adequately characterize variation. In this article, we take an alternative approach, treating female preference as a function-valued trait and exploiting random-coefficient models to characterize the genetic basis of female preference without measuring preference functions in each individual. Applying this approach to Drosophila bunnanda, in which females assess males through a multivariate contact pheromone system, we gain three valuable insights into the genetic basis of female preference functions. First, most genetic variation was attributable to one eigenfunction, suggesting shared genetic control of preferences for nine male pheromones. Second, genetic variance in female preference functions was not associated with genetic variance in the pheromones, implying that genetic variation in female preference did not maintain genetic variation in male traits. Finally, breeding values for female preference functions were skewed away from the direction of selection on the male traits, suggesting directional selection on female preferences. The genetic analysis of female preference functions as function-valued traits offers a robust statistical framework for investigations of female preference, in addition to alleviating some experimental difficulties associated with estimating variation in preference functions.     

Breeding experience and the heritability of female mate choice in collared flycatchers

Background

Heritability in mate preferences is assumed by models of sexual selection, and preference evolution may contribute to adaptation to changing environments. However, mate preference is difficult to measure in natural populations as detailed data on mate availability and mate sampling are usually missing. Often the only available information is the ornamentation of the actual mate. The single long-term quantitative genetic study of a wild population found low heritability in female mate ornamentation in Swedish collared flycatchers. One potentially important cause of low heritability in mate ornamentation at the population level is reduced mate preference expression among inexperienced individuals.

Methodology/Principal Findings

Applying animal model analyses to 21 years of data from a Hungarian collared flycatcher population, we found that additive genetic variance was 50 percent and significant for ornament expression in males, but less than 5 percent and non-significant for mate ornamentation treated as a female trait. Female breeding experience predicted breeding date and clutch size, but mate ornamentation and its variance components were unrelated to experience. Although we detected significant area and year effects on mate ornamentation, more than 85 percent of variance in this trait remained unexplained. Moreover, the effects of area and year on mate ornamentation were also highly positively correlated between inexperienced and experienced females, thereby acting to remove difference between the two groups.

Conclusions/Significance

The low heritability of mate ornamentation was apparently not explained by the presence of inexperienced individuals. Our results further indicate that the expression of mate ornamentation is dominated by temporal and spatial constraints and unmeasured background factors. Future studies should reduce unexplained variance or use alternative measures of mate preference. The heritability of mate preference in the wild remains a principal but unresolved question in evolutionary ecology.     

Testing the correlated response hypothesis for the evolution and maintenance of male mating preferences in Drosophila serrata

Mate preferences are abundant throughout the animal kingdom with female preferences receiving the most empirical and theoretical attention. Although recent work has acknowledged the existence of male mate preferences, whether they have evolved and are maintained as a direct result of selection on males or indirectly as a genetically correlated response to selection for female choice remains an open question. Using the native Australian species Drosophila serrata in which mutual mate choice occurs for a suite of contact pheromones (cuticular hydrocarbons or CHCs), we empirically test key predictions of the correlated response hypothesis. First, within the context of a quantitative genetic breeding design, we estimated the degree to which the trait values favoured by male and female choice are similar both phenotypically and genetically. The direction of sexual selection on male and female CHCs differed statistically, and the trait combinations that maximized male and female mating success were not genetically correlated, suggesting that male and female preferences target genetically different signals. Second, despite detecting significant genetic variance in female preferences, we found no evidence for genetic variance in male preferences and, as a consequence, no detectable correlation between male and female mating preferences. Combined, these findings are inconsistent with the idea that male mate choice in D. serrata is simply a correlated response to female choice. Our results suggest that male and female preferences are genetically distinct traits in this species and may therefore have arisen via different evolutionary processes.     

SEX‐SPECIFIC EVOLUTIONARY POTENTIAL OF PRE‐ AND POSTCOPULATORY REPRODUCTIVE INTERACTIONS IN THE FIELD CRICKET,TELEOGRYLLUS COMMODUS

Mate choice often depends on the properties of both sexes, such as the preference and responsiveness of the female and the sexual display traits of the male. Quantitative genetic studies, however, traditionally explore the outcome of an interaction between males and females based solely on the genotype of one sex, treating the other sex as a source of environmental variance. Here, we use a half‐sib breeding design in the field cricket, Teleogryllus commodus, to estimate the additive genetic contribution of both partners to three steps of the mate choice process: the time taken to mate; the duration of spermatophore attachment; and the intensity of mate guarding. Rather than each sex contributing equally to the interactions, we found that genetic variation for latency to mate and spermatophore attachment was sex‐specific, and in the case of mate‐guarding intensity, largely absent. For a given interaction, genetic variation in one sex also appears to be largely independent of the other, and is also uncorrelated with the other traits. We discuss how pre‐ and postcopulatory interactions have the potential to evolve as an interacting phenotype, but that any coevolution between these traits, due to sexual selection or sexual conflict, may be limited.     

No evidence for an indirect benefit from female mate preference in Arctic charr Salvelinus alpinus,but female ornamentation decreases offspring viability

Female mate choice is considered an important evolutionary agent, but there has been an ongoing debate over the fitness consequences it produces, especially in species that have a resource‐free mating system. We examined a potential fitness benefit resulting from the pre‐spawning mate preference in Arctic charr Salvelinus alpinus, a salmonid fish with no parental care. The females were first allowed to discriminate behaviourally between two males presented to them in a free choice test. We then tested with controlled fertilizations whether the females would accrue indirect genetic benefits for their offspring, as measured by embryonic viability, if they had mated with the male they preferred. Both parental identities influenced offspring survivorship, but the females did not consistently prefer the male which gave her the higher reproductive success. Neither was the degree of male red breeding coloration associated with female preference or the observable genetic quality. In contrast, there was a negative relationship between female coloration and her offspring survivorship, suggesting a significant trade‐off in resource investment between sexual ornamentation and reproduction. To conclude, the potential indirect fitness consequences arising from females' pre‐spawning mate preference seem to be negligible in early stages of development of Arctic charr. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 602–611.     

The dilemma of Fisherian sexual selection: Mate choice for indirect benefits despite rarity and overall weakness of trait‐preference genetic correlation

Fisher's mechanism of sexual selection is a fundamental element of evolutionary theory. In it nonrandom mate choice causes a genetic covariance between a male trait and female preference for that trait and thereby generates a positive feedback process sustaining accelerated coevolution of the trait and preference. Numerous theoretical models of Fisher's mechanism have confirmed its mathematical underpinnings, yet biologists have often failed to find evidence for trait‐preference genetic correlation in populations in which the mechanism was expected to function. We undertook a survey of the literature to conduct a formal meta‐analysis probing the incidence and strength of trait‐preference correlation among animal species. Our meta‐analysis found significant positive genetic correlations in fewer than 20% of the species studied and an overall weighted correlation that is slightly positive. Importantly, a significant positive correlation was not found in any thorough study that included multiple subgroups. We discuss several ways in which the dynamic, multivariate nature of mate choice may reduce the trait‐preference genetic correlation predicted by Fisher's mechanism. We then entertain the possibilities that Fisherian‐like processes sometimes function without genetic correlation, and that mate choice may persist in a population as long as genetic correlation, and therefore Fisher's mechanism, occurs intermittently.     

Genetic population structure in an equatorial sparrow: roles for culture and geography

Female preference for local cultural traits has been proposed as a barrier to breeding among animal populations. As such, several studies have found correlations between male bird song dialects and population genetics over relatively large distances. To investigate whether female choice for local dialects could act as a barrier to breeding between nearby and contiguous populations, we tested whether variation in male song dialects explains genetic structure among eight populations of rufous‐collared sparrows (Zonotrichia capensis) in Ecuador. Our study sites lay along a transect, and adjacent study sites were separated by approximately 25 km, an order of magnitude less than previously examined for this and most other species. This transect crossed an Andean ridge and through the Quijos River Valley, both of which may be barriers to gene flow. Using a variance partitioning approach, we show that song dialect is important in explaining population genetics, independent of the geographic variables: distance, the river valley and the Andean Ridge. This result is consistent with the hypothesis that song acts as a barrier to breeding among populations in close proximity. In addition, songs of contiguous populations differed by the same degree or more than between two populations previously shown to exhibit female preference for local dialect, suggesting that birds from these populations would also breed preferentially with locals. As expected, all geographic variables (distance, the river valley and the Andean Ridge) also predicted population genetic structure. Our results have important implications for the understanding whether, and at what spatial scale, culture can affect population divergence.     

Limits to environmental masking of genetic quality in sexual signals

There is considerable debate over the value of male sexual ornaments as signals of genetic quality. Studies alternately report that environmental variation enhances or diminishes the genetic signal, or leads to crossover where genotypes perform well in one environment but poorly in another. A unified understanding is lacking. We conduct a novel experimental test examining the dual effects of distinct categories of genetic (inbred vs. crossed parental lines) and environmental quality (low, through high to extreme larval food stress) on a condition‐dependent male ornament. We find that differences in genetic quality signalled by the ornament (male eyespan in Diasemopsis meigenii stalk‐eyed flies) become visible and are amplified under high stress but are overwhelmed in extreme‐stress environments. Variance among independent genetic lines increases with environmental stress in both genetic quality classes, but at a slower rate in high quality outcrossed flies. Individual genetic lines generally maintain their ranks across environments, except among high quality lines under low environmental stress, where low genetic variance among lines precludes differentiation between ranks. Our results provide a conceptual advance, demonstrating a unified pattern for how genetic and environmental quality interact. They show when environmental conditions lead to the amplification of differences in signals of genetic quality and thereby enhance the potential indirect genetic benefits gained by female mate choice.     

FEMALE PREFERENCE FOR MALE COURTSHIP EFFORT CAN DRIVE THE EVOLUTION OF MALE MATE CHOICE

The evolution of male mate choice is constrained by costs of choice in species with a male‐biased operational sex ratio (OSR). Previous theoretical studies have shown that significant benefits of male choice are required, for example, by mating with more fecund females, in order for these costs to be offset and a male preference to spread. In a series of population genetic models we show the novel effect that male mating preference, expressed as a bias in courtship, can spread when females prefer, and thus are more likely to mate with, males who court more. We explore two female preference functions for levels of male courtship, one representing a threshold and the other a weighted female preference. The basic finding generally holds for both preference functions. However, the preference function greatly affects the spread of a male preference allele after the addition of competing males who can court more in total. Our results thus stress that a thorough understanding of the response of females to male courtship is a critical component to understanding male preference evolution in polygynous species.     

Why do ovigerous females approach courting males? Female preferences and sensory biases in a fiddler crab

Perceptual biases explain the origin and evolution of female preference in many species. Some responses that mediate mate choice, however, may have never been used in nonmating contexts. In the fiddler crab, Uca mjoebergi, mate‐searching females prefer faster wave rates and leading wave; however, it remains unclear whether such responses evolved in a mating context (i.e., the preference has effect on the fitness of the female and her offspring that arise from mating with a particular male) or a nonmating contexts (i.e., a female obtains direct benefits through selecting the male with a more detectable trait). Here, we compared the preferences of mate‐searching with those of ovigerous females that are searching for a burrow and do not concern about male “quality.” Results showed that as both mate‐searching and ovigerous females preferentially approached robotic males with faster wave rates. This suggests that wave rate increases detectability/locatability of males, but the mating preference for this trait is unlikely to evolve in the mating context (although it may currently function in mate choice), as it does not provide fitness‐related benefit to females or her offspring. Wave leadership, in contract, was attractive to mate‐searching females, but not ovigerous females, suggesting that female preference for leadership evolves because wave leadership conveys information about male quality. We provide not only an empirical evidence of sensory biases (in terms of the preference for faster wave), but the first experimental evidence that mating context can be the only selection force that mediates the evolution of male sexual traits and female preference (in terms of the preference for leading wave).     

Female mate choice in relation to heterozygosity in Tribolium castaneum

Abstract Female mate choice, both before and after copulation, is pervasive among insect species. It is often hypothesized that females would preferentially mate with males that are genetically dissimilar to promote the genetic variability of the offspring. We used various strains of red flour beetle, Tribolium castaneum, and tested the effect of male and female genetic backgrounds on precopulatory and post‐copulatory female mate choice. Simultaneous mate choice experiments using previously well established pheromone assays did not detect female preference for males of different strains. Post‐copulatory female mate choice was examined through paternity analysis. Two parameters were used to measure post‐copulatory female mate choice, including male defence capacity (P₁, proportion of offspring sired by the first male when a female mated with two males consecutively) and offence capacity (P₂, proportion of offspring sired by the second of two males to mate with a female). When female and male beetle strains were same, defence capacity was significantly higher than when female and male strains were different. However, such a pattern was not observed for offence capacity. The results suggest that female precopulatory mate choice is not affected by genetic background, but the outcome of post‐copulatory processes depends on the genetic background of male and female beetles.     

Female mate choice of male signals is unlikely to promote ecological adaptation in Enchenopa treehoppers (Hemiptera: Membracidae)

A key question in speciation research is how ecological and sexual divergence arise and interact. We tested the hypothesis that mate choice causes local adaptation and ecological divergence using the rationale that the performance~signal trait relationship should parallel the attractiveness~signal trait relationship. We used female fecundity as a measure of ecological performance. We used a species in the Enchenopa binotata treehopper complex, wherein speciation involves adaptation to novel environments and divergence in sexual communication. We used a full‐sibling, split‐family rearing design to estimate genetic correlations (r_G) between fecundity and signal traits, and compared those relationships against population‐level mate preferences for the signal traits. Animal model estimates for r_G between female fecundity and male signal traits overlapped zero—rejecting the hypothesis—but could reflect sample size limitations. The magnitude of r_G correlated with the strength of the mate preferences for the corresponding signal traits, especially for signal frequency, which has the strongest mate preference and the most divergence in the complex. However, signal frequencies favored by the population‐level mate preference are not associated with high fecundity. Therefore, mate preferences do not appear to have been selected to favor high‐performance genotypes. Our findings suggest that ecological and sexual divergence may arise separately, but reinforce each other, during speciation.     

Insect mating signal and mate preference phenotypes covary among host plant genotypes

Sexual selection acting on small initial differences in mating signals and mate preferences can enhance signal–preference codivergence and reproductive isolation during speciation. However, the origin of initial differences in sexual traits remains unclear. We asked whether biotic environments, a source of variation in sexual traits, may provide a general solution to this problem. Specifically, we asked whether genetic variation in biotic environments provided by host plants can result in signal–preference phenotypic covariance in a host‐specific, plant‐feeding insect. We used a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) to assess patterns of variation in male mating signals and female mate preferences induced by genetic variation in host plants. We employed a novel implementation of a quantitative genetics method, rearing field‐collected treehoppers on a sample of naturally occurring replicated host plant clone lines. We found remarkably high signal–preference covariance among host plant genotypes. Thus, genetic variation in biotic environments influences the sexual phenotypes of organisms living on those environments in a way that promotes assortative mating among environments. This consequence arises from conditions likely to be common in nature (phenotypic plasticity and variation in biotic environments). It therefore offers a general answer to how divergent sexual selection may begin.     

Temperature coupling of mate attraction signals and female mate preferences in four populations of Enchenopa treehopper (Hemiptera: Membracidae)

Variation in temperature can affect the expression of a variety of important fitness‐related behaviours, including those involved with mate attraction and selection, with consequences for the coordination of mating across variable environments. We examined how temperature influences the expression of male mating signals and female mate preferences—as well as the relationship between how male signals and female mate preferences change across temperatures (signal–preference temperature coupling)—in Enchenopa binotata treehoppers. These small plant‐feeding insects communicate using plantborne vibrations, and our field surveys indicate they experience significant natural variation in temperature during the mating season. We tested for signal–preference temperature coupling in four populations of E. binotata by manipulating temperature in a controlled laboratory environment. We measured the frequency of male signals—the trait for which females show strongest preference—and female peak preference—the signal frequency most preferred by females—across a range of biologically relevant temperatures (18°C–36°C). We found a strong effect of temperature on both male signals and female preferences, which generated signal–preference temperature coupling within each population. Even in a population in which male signals mismatched female preferences, the temperature coupling reinforces predicted directional selection across all temperatures. Additionally, we found similar thermal sensitivity in signals and preferences across populations even though populations varied in the mean frequency of male signals and female peak preference. Together, these results suggest that temperature variation should not affect the action of sexual selection via female choice, but rather should reinforce stabilizing selection in populations with signal–preference matches, and directional selection in those with signal–preference mismatches. Finally, we do not predict that thermal variation will disrupt the coordination of mating in this species by generating signal–preference mismatches at thermal extremes.     

Female dark‐eyed juncos Junco hyemalis thurberi produce male‐like song in a territorial context during the early breeding season

Reports of female song, once considered a rarity, have recently increased across a variety of avian taxa. Females of many species can be induced to produce male‐like song with exogenous testosterone, but observations of female song in free‐living birds remain limited by incomplete sampling of females. Here, we report three independent observations of female dark‐eyed juncos Junco hyemalis producing male‐like song early in the breeding season (i.e. post‐territory establishment, pre‐nesting) in a recently established non‐migratory, urban population. To elicit song, we presented 17 free‐living junco pairs with a live, caged female conspecific. Three unique females responded to our trials by diving at the intruding female, chasing their (male) mate, fanning their tail feathers, and singing a trilled song similar in structure to male long‐range (broadcast) song. We compared male and female songs quantitatively and found that the two sexes were statistically similar in many spectral and temporal characteristics, but female songs had significantly lower minimum and peak frequencies than males. This result is particularly surprising, as males in this urban population are known to sing at a significantly higher minimum frequency than males in a nearby montane population. Both the seasonal and social context in which these songs were observed suggest a potential function for female song in mate guarding and polygyny prevention, but more data are needed to test this hypothesis. Whether female song is common in all dark‐eyed juncos during the early breeding season or if it is restricted to this particular urban and non‐migratory population remains an important question for future research.     

Pheromone Blend Does not Explain Old Male Mating Advantage in a Butterfly

In several insect species, male mating success is higher in older than in younger males, although condition diminishes dramatically with age. Two hypotheses are under debate to explain the counterintuitive pattern of old male mating advantage: first, an increased eagerness of older males to mate, driven by their low residual reproductive value, and second female preference for older males based on chemical cues such as sex pheromones (female choice hypothesis). In a series of experiments, we manipulated female olfaction, male pheromone blend and female age to test whether old male mating advantage prevails when the influence of male sex pheromones is controlled for, using the tropical butterfly Bicyclus anynana as model. We found that older males had a higher mating success than younger ones irrespective of female scent‐sensitivity and irrespective of male pheromone blend. Interestingly, older males were found to court more often and for longer time bouts than younger males. These results were independent of female age, although younger males courted younger females more often and for longer bouts than older females. Taken together, our results indicate that male courtship activity (1) is higher in older compared to younger males and (2) increases the mating success of older males. Olfaction and sensing pheromones, in contrast, were not a necessary prerequisite for old male mating advantage to occur and may use other cues than pheromones to assess male quality.     

An evolutionary limit to male mating success

The well-known phenotypic diversity of male sexual displays, and the high levels of genetic variation reported for individual display traits have generated the expectation that male display traits, and consequently male mating success, are highly evolvable. It has not been shown however that selection for male mating success, exerted by female preferences in an unmanipulated population, results in evolutionary change. Here, we tested the expectation that male mating success is highly evolvable in Drosophila bunnanda using an experimental evolution approach. Female D. bunnanda exhibit a strong, consistent preference for a specific combination of male cuticular hydrocarbons (CHCs). We used female preference to select for male mating success by propagating replicate populations from either attractive or unattractive males over 10 generations. Neither the combination of CHCs under sexual selection (the sexual signal) nor male mating success itself evolved. The lack of a response to selection was consistent with previous quantitative genetic experiments in D. bunnanda that demonstrated the virtual absence of genetic variance in the combination of CHCs under sexual selection. Persistent directional selection, such as applied by female mate choice, may erode genetic variance, resulting in multitrait evolutionary limits.     

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.     

The Disruption Hypothesis Does Not Explain Mate‐Choice Copying in the Guppy (Poecilia reticulata)

In some species, female mate choice is non‐independent as, under certain circumstances, females may copy the mate choice of other nearby females. One standard experimental protocol used to test for mate‐choice copying is the mate‐choice ‘reversal’ protocol. In this protocol, a focal female is allowed to choose between two males as potential mates and then is presented with an opportunity to see another female (i.e. the model female) choose the male that she did not initially choose. The focal is subsequently allowed to again choose between the same set of males. An observed reversal of her initial choice in this second preference test has been previously interpreted as evidence for mate‐choice copying. Alternatively, it has recently been proposed that environmental events, such as seeing the mate choice of nearby females that occur within the visual field of a female actively engaged in mate assessment, may ‘disrupt’ her decision‐making behavior and consequently alter the consistency of her mating preference, and may thus cause mate‐choice reversals. The disruption hypothesis predicts that if a model female is placed near the male that the focal female initially chose, the latter's mate preference would be disrupted and she would subsequently and consistently prefer the male that she initially rejected. Here we examined whether the disruption hypothesis explains mate‐choice copying in the guppy (Poecilia reticulata). Our results do not support this hypothesis, but rather provide further support for mate‐choice copying in the guppy.