No evidence for a genetic association between female mating preference and male secondary sexual trait in a Lake Victoria cichlid fish

Sexual selection by female mating preference for male nuptial coloration has been suggested as a driving force in the rapid speciation of Lake Victoria cichlid fish. This process could have been facilitated or accelerated by genetic associations between female preference loci and male coloration loci. Preferences, as well as coloration, are heritable traits and are probably determined by more than one gene. However, little is known about potential genetic associations between these traits. In turbid water, we found a population that is variable in male nuptial coloration from blue to yellow to red. Males at the extreme ends of the phenotype distribution resemble a reproductively isolated species pair in clear water that has diverged into one species with blue-grey males and one species with bright red males. Females of the turbid water population vary in mating preference coinciding with the male phenotype distribution. For the current study, these females were mated to blue males. We measured the coloration of the sires and male offspring. Parents-offspring regression showed that the sires did not affect male offspring coloration, which confirms earlier findings that the blue species breeds true. In contrast, male offspring coloration was determined by the identity of the dams, which suggests that there is heritable variation in male color genes between females. However, we found that mating preferences of the dams were not correlated with male offspring coloration. Thus, there is no evidence for strong genetic linkage between mating preference and the preferred trait in this population [Current Zoology 56 (1): 57-64 2010].     

PARTITIONING THE EFFECTS OF SPATIAL ISOLATION,NEST HABITAT,AND INDIVIDUAL DIET IN CAUSING ASSORTATIVE MATING WITHIN A POPULATION OF THREESPINE STICKLEBACK

Assortative mating is measured as a phenotypic or genotypic correlation between mates. Although biologists typically view assortative mating in terms of mate preference for similar partners, correlations between mates can also arise from phenotypic spatial structure arising from spatial isolation or habitat preferences. Here, we test whether diet‐assortative mating within an ecologically variable population of threespine stickleback results from small‐scale geographic isolation or microhabitat preference. We find evidence for assortative mating in the form of a positive correlation between mated pairs’ diets (measured using stable isotopes). Stable isotopes reveal diet differences between different nesting areas and among individuals using different nest habitat within a nesting area. This spatial segregation of diet types should generate some assortative mating, but is insufficient to explain the observed assortment strength. Significant male–female isotope correlations remain after controlling for spatial variables. We therefore conclude that sticklebacks’ diet‐assortative mating arises from additional behavioral preference. More generally, our results illustrate the point that spatial segregation can only drive appreciable levels of phenotypic assortative mating when environment‐phenotype correlations are parallel and strong in both sexes. Consequently, intraspecific assortative mating may typically entail mating preferences rather than just spatial cosegregation of phenotypes.     

Mate sampling and the sexual conflict over mating in seaweed flies

The order in which females encounter, or sample, males in apopulation may have important consequences for mate choice,with the information gathered about males influencing boththe preference function and degree of choosiness of females.Sexual selection may be affected as a result. Sampling of particularsubsets of males may be a crucial component of individual variation in mate preferences within populations. However, the sequencein which males are sampled may also be important in specieswithout traditional, active mate choice, such as when sexualselection involves sexual conflict over mating. This wouldoccur if the likelihood of a female mating with a male of acertain phenotype changes as a result of previous encounters.We examined the effects of encountering males differing inbody size, a sexually selected phenotype, in the seaweed flyCoelopa frigida. Sexual selection occurs in this species asa result of a sexual conflict over mating. We show that theoutcome of the sexual conflict is independent of the orderin which males are encountered by female seaweed flies, withthe overall mating advantage to large males being unaffected.In addition, we explored female preference functions and evaluatethe heterogeneity in female willingness to mate. We suggestthat consideration of mate sampling theory is valuable whenexamining mate choice in species in which sexual selectionis driven by sexual conflict.     

Evolution of a mating preference for a dual‐utility trait used in intrasexual competition in genetically monogamous populations

The selection pressures by which mating preferences for ornamental traits can evolve in genetically monogamous mating systems remain understudied. Empirical evidence from several taxa supports the prevalence of dual‐utility traits, defined as traits used both as armaments in intersexual selection and ornaments in intrasexual selection, as well as the importance of intrasexual resource competition for the evolution of female ornamentation. Here, we study whether mating preferences for traits used in intrasexual resource competition can evolve under genetic monogamy. We find that a mating preference for a competitive trait can evolve and affect the evolution of the trait. The preference is more likely to persist when the fecundity benefit for mates of successful competitors is large and the aversion to unornamented potential mates is strong. The preference can persist for long periods or potentially permanently even when it incurs slight costs. Our results suggest that, when females use ornaments as signals in intrasexual resource competition, males can evolve mating preferences for those ornaments, illuminating both the evolution of female ornamentation and the evolution of male preferences for female ornaments in monogamous species.     

Evolution of disassortative and assortative mating preferences based on imprinting

A two-locus haploid model of sexual selection is investigated to explore evolution of disassortative and assortative mating preferences based on imprinting. In this model, individuals imprint on a genetically transmitted trait during early ontogeny and choosy females later use those parental images as a criterion of mate choice. It is assumed that the presence or absence of the female preference is determined by a genetic locus. In order to incorporate such mechanisms as inbreeding depression and heterozygous advantage into our haploid framework, we assume that same-type matings are less fertile than different-type mating. The model suggests that: if all the females have a disassortative mating preference a viability-reducing trait may be maintained even without the fertility cost of same-type matings; a disassortative mating preference can be established even if it is initially rare, when there is a fertility cost of same-type matings. Further, an assortative mating preference is less likely to evolve than a disassortative mating preference. The model may be applicable to the evolution of MHC-disassortative mating preferences documented in house mice and humans.     

The consequences of heterogamy and homogamy on the similarity between spouses

Humans in many societies are known to mate, or marry, assortatively for a number of characters such as eye colour, height, IQ and place of birth. In this assortment an element of active choice may be involved. It is not known whether this choice is genetic. Two models of human mate choice are examined in which both males and females can express a mating preference. In the first, 'sexual' preferences can be expressed for any phenotype not necessarily one's own; in the second, preferences are only expressed for an individual's own phenotype. The results of the examination indicate how much active choice would be needed to account for the observed correlations between human mates, and suggest whether human mating preferences are more likely to be sexual or assorting.     

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.     

The effects of sexual selection on trait divergence in a peripheral population with gene flow

The unique aspects of speciation and divergence in peripheral populations have long sparked much research. Unidirectional migration, received by some peripheral populations, can hinder the evolution of distinct differences from their founding populations. Here, we explore the effects that sexual selection, long hypothesized to drive the divergence of distinct traits used in mate choice, can play in the evolution of such traits in a partially isolated peripheral population. Using population genetic continent‐island models, we show that with phenotype matching, sexual selection increases the frequency of an island‐specific mating trait only when female preferences are of intermediate strength. We identify regions of preference strength for which sexual selection can instead cause an island‐specific trait to be lost, even when it would have otherwise been maintained at migration‐selection balance. When there are instead separate preference and trait loci, we find that sexual selection can lead to low trait frequencies or trait loss when female preferences are weak to intermediate, but that sexual selection can increase trait frequencies when preferences are strong. We also show that novel preference strengths almost universally cannot increase, under either mating mechanism, precluding the evolution of premating isolation in peripheral populations at the early stages of species divergence.     

The limits of sexual conflict in the narrow sense: new insights from waterfowl biology

Sexual conflict occurs when the evolutionary interests of the sexes differ and it broadly applies to decisions over mating, fertilization and parental investment. Recently, a narrower view of sexual conflict has emerged in which direct selection on females to avoid male-imposed costs during mating is considered the distinguishing feature of conflict, while indirect selection is considered negligible. In this view, intersexual selection via sensory bias is seen as the most relevant mechanism by which male traits that harm females evolve, with antagonistic coevolution between female preferences and male manipulation following. Under this narrower framework, female preference and resistance have been synonymized because both result in a mating bias, and similarly male display and coercion are not distinguished. Our recent work on genital evolution in waterfowl has highlighted problems with this approach. In waterfowl, preference and resistance are distinct components of female phenotype, and display and coercion are independent male strategies. Female preference for male displays result in mate choice, while forced copulations by unpreferred males result in resistance to prevent these males from achieving matings and fertilizations. Genital elaborations in female waterfowl appear to function in reinforcing female preference to maintain the indirect benefits of choice rather than to reduce the direct costs of coercive mating. We propose a return to a broader view of conflict where indirect selection and intrasexual selection are considered important in the evolution of conflict.     

Preference polymorphism for coloration but no speciation in a population of Lake Victoria cichlids

Female mating preference based on male nuptial coloration hasbeen suggested to be an important source of diversifying selectionin the radiation of Lake Victoria cichlid fish. Initial variationin female preference is a prerequisite for diversifying selection;however, it is rarely studied in natural populations. In clearwater areas of Lake Victoria, the sibling species Pundamiliapundamilia with blue males and Pundamilia nyererei with redmales coexist, intermediate phenotypes are rare, and most femaleshave species-assortative mating preferences. Here, we studya population of Pundamilia that inhabits turbid water wheremale coloration is variable from reddish to blue with most malesintermediate. We investigated male phenotype distribution andfemale mating preferences. Male phenotype was unimodally distributedwith a mode on intermediate color in 1 year and more blue-shiftedin 2 other years. In mate choice experiments with females ofthe turbid water population and males from a clearer water population,we found females with a significant and consistent preferencefor P. pundamilia (blue) males, females with such preferencesfor P. nyererei (red) males, and many females without a preference.Hence, female mating preferences in this population could causedisruptive selection on male coloration that is probably constrainedby the low signal transduction of the turbid water environment.We suggest that if environmental signal transduction was improvedand the preference/color polymorphism was stabilized by negativefrequency-dependent selection, divergent sexual selection mightseparate the 2 morphs into reproductively isolated species resemblingthe clear water species P. pundamilia and P. nyererei.     

MALE MATING PREFERENCES AND ASSORTATIVE MATING IN THE SOLDIER BEETLE

Mating preferences for a color characteristic were examined in three northern Georgia populations of the soldier beetle, Chauliognathus pennsylvanicus De Geer, by comparing observed and expected frequencies of matings to the same phenotype. The three populations are apparently in a zone of secondary contact between disparate color morphs. In the most northern population sampled, preferences were strong and were associated with positive assortative mating with respect to the color characteristic. In the southern population, neither assortative mating nor mating preference was strong, while in the middle population, preferences were expressed in the absence of assortative mating. Mating preferences cannot be attributed to host-plant choice, microhabitat choice, or simple conditioning on the phenotype of the last mate. However, they may represent part of a specific mate-recognition system which has been maintained in part of the zone of overlap but which has eroded in other areas.     

Females decide whether size matters: plastic mate preferences tuned to the intensity of male-male competition

Recent studies have indicated that mating success of large malesmay improve under increasing levels of mating competition. Thisoutcome is explained 1) if male mating competition is overridingfemale preferences for male traits that are unrelated to, ornegatively correlated with, male size and dominance and, inso doing, dictates the distribution of matings or 2) if femalesalter their preferences with respect to large males when male–malecompetition is intense. Under both hypotheses, one could expectlarge, dominant males to be more successful under intense competitionthan under weak competition. However, only the first explanationpredicts that male mating success under intense competitionshould be determined by dominance; traits that are unrelatedto male dominance should be uncorrelated to mating success.In contrast, if females change their preferences (explanation2), males with traits beneficial to females independent of thecompetitive environment can maintain a high mating success underall levels of male–male competition. We tested these alternativesusing a small marine fish, the sand goby, Pomatoschistus minutus.The mating success of large males increased under conditionsallowing intense male competition, whereas females showed apreference for good nest building independent of the level ofcompetition. These findings suggest that females are in controlof their choice by altering their preference for male size inresponse to the intensity of male–male competition ratherthan female preference being overshadowed by male dominance.This plasticity of preferences implies that the strength ofsexual selection is not constant at the population level.     

Variation between and within the sexes in body size preferences

Although it is often assumed that males and females have mating preferences for larger individuals of the other sex, potential underlying differences between male and female preferences for body size are not commonly investigated. Here, sexual differences in body size preferences are examined in the poeciliid fish, Brachyrhaphis rhabdophora. Females preferred larger males to smaller males, but preference did not appear to be affected by female size. One population-level analysis for males did not indicate an overall preference for larger females. A closer examination, however, revealed an effect of male size on preference; larger males preferred larger females, while smaller males preferred smaller females. It appears then that females, regardless of size, share a preference for large males, but males differ in their behaviour, depending on their body size. In addition, while the degree of difference in size between paired females did not appear to affect male preference, the degree of difference in size between paired males strongly affected female preference; the greater the difference, the more strongly females preferred the larger male. Thus, intersexual selection is found to operate in both sexes, but how it operates appears to differ. Intrasexual and intersexual differences in mating behaviour may be missed when evaluating population-wide preferences. That is, there can be underlying differences in how the sexes respond and the consequences of such differences should be considered when investigating mate choice. The results are considered in terms of the evolution of mating preferences, alternative mating strategies, assortative mating, the maintenance of trait variation in a population, and current methods to evaluate mating preferences.     

MATE PREFERENCE FOR A PHENOTYPICALLY PLASTIC TRAIT IS LEARNED,AND MAY FACILITATE PREFERENCE‐PHENOTYPE MATCHING

Fixed, genetically determined, mate preferences for species whose adult phenotype varies with rearing environment may be maladaptive, as the phenotype that is most fit in the parental environment may be absent in the offspring environment. Mate preference in species with polyphenisms (environmentally dependent alternative phenotypes) should therefore either not focus on polyphenic traits, be polyphenic themselves, or learned each generation. Here, we test these alternative hypotheses by first describing a female‐limited seasonal polyphenism in a sexually dimorphic trait in the butterfly Bicyclus anynana, dorsal hindwing spot number (DHSN), and then testing whether male and female mate preferences for this trait exist, and whether they are seasonally polyphenic, or learned. Neither naïve males nor naïve females in either seasonal form exhibited mating preferences for DHSN. However, males, but not females, noticed DHSN variation and learned mate preferences for DHSN. These results suggest that individuals may accommodate environmentally dependent variation in morphological traits via learned mate preferences in each generation, and that learned mate preference plasticity can be sexually dimorphic.     

Runaway sexual selection when female preferences are directly selected

We introduce models for the runaway coevolution of female mating preferences and male display traits. The models generalize earlier results by allowing for direct natural selection on the preference, arbitrary forms of mate choice, and fairly general assumptions about the underlying genetics. Results show that a runaway is less likely when there is direct selection on the preference, but that it is still possible if there is a sufficiently large phenotypic correlation between the female's preference and the male's trait among mated pairs. Comparison of three preference functions introduced by Lande (1981) shows that open-ended preferences are particularly prone to a runaway, and that absolute preferences require very large differences between females in their preferences. We analyze the causes of the runaway seen in a model developed by Iwasa and Pomiankowski (1995).     

Treat ’em Mean,Keep ’em (sometimes) Keen: Evolution of Female Preferences for Dominant and Coercive Males

How should females choose their mates if choice is not completely free, but at least partly dictated by outcomes of male–male competition, or sexual coercion? This question is of central importance when evaluating the relationship between sexually antagonistic ‘chase-away’ scenarios and models of more traditional female choice. Currently, there is a mismatch between theories: indirect benefits are seen to play a role in conventional mate choice, whereas they are not predicted to have an influence on the outcome if matings impose direct costs on females. This is at odds with the idea that resistance and preference are two sides of the same coin: either leads to a subset of males enjoying enhanced mating success. In the same way as choosy females benefit from mating with sexy males if this yields sexy sons, females could benefit from being manipulated or ‘seduced’, if the manipulative or seductive ability of males is heritable. Here I build a model where male dominance (or coerciveness) improves his mating success, and this relationship can be modified by female behaviour. This clarifies the definitions of resistance and preference: resisting females diminish the benefit a male gains from being dominant, while preferences enhance this pre-existing benefit enjoyed by dominant males. In keeping with earlier theory, females may evolve to resist costly mating attempts as a counterstrategy to male traits, particularly if male dominance is environmentally rather than genetically determined. Contrary to earlier results, however, indirect benefits are also predicted to influence female mating behaviour, and if sufficiently strong, they may produce female preferences for males that harm them.     

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.     

A sex-specific trade-off between mating preferences for genetic compatibility and body size in a cichlid fish with mutual mate choice

Mating preferences for genetic compatibility strictly depend on the interplay of the genotypes of potential partners and are therein fundamentally different from directional preferences for ornamental secondary sexual traits. Thus, the most compatible partner is on average not the one with most pronounced ornaments and vice versa. Hence, mating preferences may often conflict. Here, we present a solution to this problem while investigating the interplay of mating preferences for relatedness (a compatibility criterion) and large body size (an ornamental or quality trait). In previous experiments, both sexes of Pelvicachromis taeniatus, a cichlid fish with mutual mate choice, showed preferences for kin and large partners when these criteria were tested separately. In the present study, test fish were given a conflicting choice between two potential mating partners differing in relatedness as well as in body size in such a way that preferences for both criteria could not simultaneously be satisfied. We show that a sex-specific trade-off occurs between mating preferences for body size and relatedness. For females, relatedness gained greater importance than body size, whereas the opposite was true for males. We discuss the potential role of the interplay between mating preferences for relatedness and body size for the evolution of inbreeding preference.     

The lek mating system of the worm pipefish (Nerophis lumbriciformis): a molecular maternity analysis and test of the phenotype‐linked fertility hypothesis

The origin and maintenance of mating preferences continues to be an important and controversial topic in sexual selection research. Leks and lek‐like mating systems, where individuals gather in particular spots for the sole purpose of mate choice, are particularly puzzling, because the strong directional selection imposed by mate choice should erode genetic variation among competing individuals and negate any benefit for the choosing sex. Here, we take advantage of the lek‐like mating system of the worm pipefish (Nerophis lumbriciformis) to test the phenotype‐linked fertility hypothesis for the maintenance of mating preferences. We use microsatellite markers to perform a parentage analysis, along with a mark–recapture study, to confirm that the worm pipefish has an unusual mating system that strongly resembles a female lek, where females display and males visit the lek to choose mates. Our results show that the most highly ornamented females occupy positions near the centre of the breeding area, and males mating with these females receive fuller broods with larger eggs compared to males mating with less‐ornamented females. We also conduct a laboratory experiment to show that female ornaments are condition‐dependent and honestly signal reproductive potential. Overall, these results are consistent with the predictions of a sex‐independent version of the phenotype‐linked fertility hypothesis, as male preference for female ornaments correlates with fertility benefits.     

‘Do you remember the first time?’ Host plant preference in a moth is modulated by experiences during larval feeding and adult mating

In insects, like in other animals, experience‐based modulation of preference, a form of phenotypic plasticity, is common in heterogeneous environments. However, the role of multiple fitness‐relevant experiences on insect preference remains largely unexplored. For the multivoltine polyphagous moth Spodoptera littoralis we investigated effects of larval and adult experiences on subsequent reproductive behaviours. We demonstrate, for the first time in male and female insects, that mating experience on a plant modulates plant preference in subsequent reproductive behaviours, whereas exposure to the plant alone or plant together with sex pheromone does not affect this preference. When including larval feeding experiences, we found that both larval rearing and adult mating experiences modulate host plant preference. These findings represent the first evidence that host plant preferences in polyphagous insects are determined by a combination of innate preferences modulated by sensory feedback triggered by multiple rewarding experiences throughout their lifetime.