The evolution of sexual imprinting through reinforcement*

Reinforcement is the process whereby assortative mating evolves due to selection against costly hybridization. Sexual imprinting could evolve as a mechanism of reinforcement, decreasing hybridization, or it could potentially increase hybridization in genetically purebred offspring of heterospecific social pairs. We use deterministic population genetic simulations to explore conditions under which sexual imprinting can evolve through reinforcement. We demonstrate that a sexual imprinting component of female preference can evolve as a one‐allele assortative mating mechanism by reducing the risk of hybridization, and is generally effective at causing trait divergence. However, imprinting often evolves to be a component rather than the sole determinant of female preference. The evolution of imprinting has the unexpected side effect of homogenizing existing innate preference, because the imprinted preference neutralizes any innate preference. We also find that the weight of the imprinting component may evolve to a lower value when migration and divergent selection are strong and the cost of hybridization is low; these conditions render hybridization adaptive for immigrant females because they can acquire locally adaptive genes by mating with local males. Together, these results suggest that sexual imprinting can itself evolve as part of the speciation process, and in doing so has the capacity to promote or retard divergence through complex interactions.     

Mate choice, sexual imprinting, and speciation: a test of a one-allele isolating mechanism in sympatric sticklebacks

One-allele isolating mechanisms should make the evolution of reproductive isolation between potentially hybridizing taxa easier than two-allele mechanisms, but the generality of one-allele mechanisms in nature has yet to be established. A potentially important one-allele mechanism is sexual imprinting, where the mate preferences of individuals are based on the phenotype of their parents. Here I test the possibility that sexual imprinting promotes reproductive isolation using sympatric species of threespine sticklebacks (Gasterosteus aculeatus). Sympatric species of sticklebacks consist of large benthic species and small limnetic species that are reproductively isolated and adapted to feeding in different environments. I fostered families of F1 hybrids between the species to males of both species. Preferences of these fostered females for males of either type revealed little or no effect of sexual imprinting on assortative mating. However, F1 females showed preferences for males that were similar to themselves in length, suggesting that size-assortative mating may be more important than sexual imprinting for promoting reproductive isolation between species pairs of threespine sticklebacks.     

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.     

Comparisons of positive assortative mating and sexual selection models

A series of theoretical models of positive assortative mating and sexual selection are contrasted. It is established that for a dominant trait partial positive assortative mating generally implies some fixation, whereas sexual selection exhibits a unique globally stable polymorphism exhibiting Hardy-Weinberg proportions. The effects of monogamy against polygamy do not qualitatively alter the equilibrium outcomes, although the rate of evolutionary change is generally slowed with monogamy vis-à-vis polygamy. For sexual selection the influence of timing of random mating as against preferential mating causes no change in the equilibrium states, although the rates of convergence can be slowed if sexual selection occurs late in the breeding season. Under assortative mating the timing can alter the equilibrium outcomes. The amount of heterozygosity is always deficient in cases of assortative mating, but always exhibits Hardy-Weinberg ratios under a sexual selection mechanism. This suggests that observations consistent with Hardy-Weinberg equilibrium states cannot preclude ipso facto certain forms of selection forces, including mating patterns and some natural selection structures.     

Limits to the evolution of assortative mating by female choice under restricted gene flow

The evolution of assortative mating is a key component of the process of speciation with gene flow. Several recent theoretical studies have pointed out, however, that sexual selection which can result from assortative mating may cause it to plateau at an intermediate level; this is primarily owing to search costs of individuals with extreme phenotypes and to assortative preferences developed by individuals with intermediate phenotypes. I explore the limitations of assortative mating further by analysing a simple model in which these factors have been removed. Specifically, I use a haploid two-population model to ask whether the existence of assortative mating is sufficient to drive the further evolution of assortative mating. I find that a weakening in the effective strength of sexual selection with strong assortment leads to the existence of both a peak level of trait differentiation and the evolution of an intermediate level of assortative mating that will cause that peak. This result is robust to the inclusion of local adaptation and different genetic architecture of the trait. The results imply the existence of fundamental limits to the evolution of assortment via sexual selection in this situation, with which other factors, such as search costs, may interact.     

ASSORTATIVE MATING PREFERENCES AMONG HYBRIDS OFFERS A ROUTE TO HYBRID SPECIATION

Homoploid speciation generates species without a change in chromosome number via introgressive hybridization and has been considered rare in animals. Heliconius butterflies exhibit bright aposematic color patterns that also act as cues in assortative mating. Heliconius heurippa has a color pattern that can be recreated by introgression of the H. melpomene red band into an H. cydno genetic background. Wild H. heurippa males show assortative mating based on color pattern and we here investigate the origin of this preference by studying first-generation backcross hybrids between H. melpomene and H. cydno that resemble H. heurippa . These hybrids show assortative mating preferences, showing a strong preference for their own color pattern over that of either parental species. This is consistent with a genetic basis to wing pattern preference and implies, first, that assortative mating preferences would facilitate the initial establishment of a homozygous hybrid color pattern by increasing the likelihood that early generation hybrids mate among themselves. Second, once established such a lineage would inherit assortative mating preferences that would lead to partial reproductive isolation from parental lineages.     

Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks

During sexual imprinting, offspring learn parental phenotypes and then select mates who are similar to their parents. Imprinting has been thought to contribute to the process of speciation in only a few rare cases; this is despite imprinting's potential to generate assortative mating and solve the problem of recombination in ecological speciation. If offspring imprint on parental traits under divergent selection, these traits will then be involved in both adaptation and mate preference. Such 'magic traits' easily generate sexual isolation and facilitate speciation. In this study, we show that imprinting occurs in two ecologically divergent stickleback species (benthics and limnetics: Gasterosteus spp.). Cross-fostered females preferred mates of their foster father's species. Furthermore, imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers. Daughters imprinted on father odour and colour during a critical period early in development. These traits have diverged between the species owing to differences in ecology. Therefore, we provide the first evidence that imprinting links ecological adaptation to sexual isolation between species. Our results suggest that imprinting may facilitate the evolution of sexual isolation during ecological speciation, may be especially important in cases of rapid diversification, and thus play an integral role in the generation of biodiversity.     

Sexual size dimorphism and assortative mating for morphological traits in Passer domesticus

In this study, assortative mating for different morphological traits was studied in a captive population of house sparrows (Passer domesticus). Males were larger than females. Assortative mating was found for tail length, wing length and general body size. Males with larger badge size mated with females with longer tails. The strongest assortative mating occurred for tail length (r=0.77), and this assortative mating remained significant after controlling for wing length, mass and tarsus length, suggesting that it was not an artefact of assortative mating for body size. The possibility of sexual selection for tail length in the house sparrow is discussed.     

ON THE EVOLUTIONARY CONSEQUENCES OF SEXUAL IMPRINTING

The idea that sexual imprinting may generate sexual selection and possibly lead to speciation has been much discussed in the ethological literature. Here the feasibility of three such hypotheses is investigated using mathematical models of sexual selection in which mating preferences are acquired through imprinting and hence dependent upon the parental phenotypes. The principal findings are the following. (1) Sexual imprinting reduces the likelihood of novel adaptive traits spreading through a population, except in some circumstances in which there is heterozygote advantage. (2) Asymmetrical mating preferences, acquired through imprinting, can generate sexual selection for traits that impair survival. (3) The conditions under which sexual imprinting will maintain a genetic polymorphism in a population are fairly restricted. (4) Sexual imprinting can act as a barrier to gene flow minimizing the impact of migration and preserving and accentuating genetic differences between populations. The findings suggest that sexual imprinting may be of considerable evolutionary significance.     

Sexual selection and assortative mating by size and their roles in the maintenance of a polymorphism in Swedish Littorina saxatilis populations

Two independent components of mating behaviour, sexual selection and assortative mating, were studied in two allopatric morphs, one sheltered boulder shore form (S-morph) and one exposed cliff shore form (E-morph), of Littorina saxatilis from the west coast of Sweden. Sexual selection was studied by comparing the sizes of copulating and non-copulating snails in the field. Size assortative mating was studied by collecting copulating pairs in the field, while assortative mating between morphs was investigated by bringing the pure morphs together in intermediary habitats and then noting the matings. The S-morph mated randomly in relation to size in two of the studied populations and exhibited a trend towards size assortative mating in a third, while the E-morph showed size assortative mating in both studied populations. The microdistribution of sizes of snails on the shores could not explain all the size assortative mating found, and instead it is argued that a size-based mate rejection behaviour also contributes to the assortative mating in at least some of these populations. There was sexual selection on size in both males and females in the S-morph, with large individuals being favoured as mates. In contrast, copulating snails of the E-morph were smaller than non-copulating ones. The significantly different sexual selection intensities between the two morphs may help to explain the size differences between them. There was random mating between the E- and the S-morphs of L. saxatilis, which suggests no incipient reproductive isolation between morphs on Swedish rocky shores. This is in agreement with earlier studies of Swedish populations, but is in contrast to the situation found in other geographical areas.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.     

SEX CHROMOSOME LINKAGE OF MATE PREFERENCE AND COLOR SIGNAL MAINTAINS ASSORTATIVE MATING BETWEEN INTERBREEDING FINCH MORPHS

Assortative mating is a key aspect in the speciation process because it is important for both initial divergence and maintenance of distinct species. However, it remains a challenge to explain how assortative mating evolves when diverging populations are undergoing gene flow (e.g., during hybridization). Here I experimentally test how assortative mating is maintained with frequent gene flow between diverged head‐color morphs of the Gouldian finch (Erythrura gouldiae). Contrary to the predominant view on the development of sexual preferences in birds, cross‐fostered offspring did not imprint on the phenotype of their conspecific (red or black morphs) or heterospecific (Bengalese finch) foster parents. Instead, the mating preferences of F₁ and F₂ intermorph‐hybrids are consistent with inheritance on the Z chromosomes, which are also the location for genes controlling color expression and the genes causing low fitness of intermorph‐hybrids. Genetic associations between color signal and preference loci on the sex chromosomes may prevent recombination from breaking down these associations when the morphs interbreed, helping to maintain assortative mating in the face of gene flow. Although sex linkage of reproductively isolating traits is theoretically expected to promote speciation, social and ecological constraints may enforce frequent interbreeding between the morphs, thus preventing complete reproductive isolation.     

Analysis of partial assortative mating and sexual selection models for a polygamous species involving a trait based on levels of heterozygosity

The consequences of preferential mating in the presence of partial assortative and sexual selection mechanisms are ascertained for a two-allele one-locus trait involving two phenotype classes C₁ = {all homozygotes} and C₂ = {heterozygotes}. Relevant biological cases may include Burley (1977, Proc. Nat. Acad. Sci. USA74, 3476–3479), Wilbur et al. (1978, Evolution32, 264–270), and Singh and Zouros (1978, Evolution32, 342–353). When the preference rate for the heterozygote exceeds that for homozygotes, it is established that the unique stable state is the central Hardy-Weinberg equilibrium. The rate of approach is faster with sexual selection than for the corresponding model of assortative mating. When the preference rates favor the homozygotes then in this symmetric model of sexual selection two asymmetric Hardy-Weinberg polymorphisms can evolve, and which succeeds depends on initial conditions. The models are also analyzed with natural selection acting on phenotypes superimposed on assortative mating. In this case we can have up to three coexisting stable states involving both fixation alternatives and a central polymorphism. The corresponding model with sexual selection maintains either the central equilibrium as in assortative mating or two asymmetric polymorphic equilibria.     

Does runaway sexual selection work in finite populations?

Fisher's runaway process is an explanation for the origin of conspicuous features which make one sex more attractive to the other. It has been suggested that it could lead to the evolution of sexual characters that significantly impair viability. Runaway selection requires a genetic correlation between alleles affecting the sexual character and alleles affecting the preference. Correlations may be expected because of assortative mating when there is variation in both the sexual character and sexual preferences. We contend that such genetic correlations are unlikely to persist in finite populations. We present simulations which confirm our expectations. They suggest that assortative mating is inefficient at generating correlations, especially if sexual selection maintains characters away from their viability optimum. In finite populations, such weak correlations will be overwhelmed by drift.     

Introgressive hybridization as a mechanism for species rescue

Rapid evolution on ecological time scales can play a key role in species responses to environmental change. One dynamic that has the potential to generate the diversity necessary for evolution rapid enough to allow response to sudden environmental shifts is introgressive hybridization. However, if distinct sub-species exist before an environmental shift, mechanisms that impede hybridization, such as assortative mating and hybrid inferiority, are likely to be present. Here we explore the theoretical potential for introgressive hybridization to play a role in response to environmental change. In particular, we incorporate assortative mating, hybrid inferiority, and demographic stochasticity into a two-locus, two-allele population genetic model of two interacting species where one locus identifies the species and the other determines how fitness depends on the changing environment. Simulation results indicate that moderately high values for the strength of assortative mating will allow enough hybridization events to outweigh demographic stochasticity but not so many that continued hybridization outweighs backcrossing and introgression. Successful introgressive hybridization also requires intermediate relative fitness at the allele negatively affected by environmental change such that hybrid survivorship outweighs demographic stochasticity but selection remains strong enough to affect the genetic dynamics. The potential for successful introgression instead of extinction with greater environmental change is larger with monogamous rather than promiscuous mating due to lower stochasticity in mating events. These results suggest species characteristics (e.g., intermediate assortative mating and mating systems with low variation in mating likelihood) which indicate a potential for rapid evolution in response to environmental change via introgressive hybridization.     

Revealing the mechanisms of sexual isolation in a case of sympatric and parallel ecological divergence

Two ecotypes of a marine intertidal snail (Littorina saxatilis), living at different microhabitats and shore levels, have evolved in sympatry and in parallel across the Galician rocky shore. These ecotypes differ in many traits (including size) due to differential adaptation. They meet, mate assortatively, and partially hybridize at the mid shore where the two microhabitats overlap. The partial sexual isolation observed is claimed to be a side‐effect of the size differences between ecotypes combined with a size assortative mating found in most populations of this species. We investigated this hypothesis using three complementary experimental approaches. First, we investigated which of the different shell variables contributed most to the variation in individual sexual isolation in the field by using two new statistics developed for that purpose: (1) pair sexual isolation and (2) r_i, which is based on the Pearson correlation coefficient. We found that size is the most important trait explaining the sexual isolation and, in particular, the males appear to be the key sex contributing to sexual isolation. Second, we compared the size assortative mating between regions: exposed rocky shore populations from north‐westwern Spain (showing incomplete reproductive isolation due to size assortative mating) and protected Spanish and Swedish populations (showing size assortative mating but not reproductive isolation between ecomorphs). Most of the variation in size assortative mating between localities was significantly explained by the within‐population level of variation on size. Third, we performed a laboratory male choice experiment, which further suggested that the choice is made predominantly on the basis of size. These results confirm the mechanism proposed to explain the sexual isolation in the Galician hybrid zone and thus support this case as a putative example of parallel incipient speciation. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 513–526.     

Random size‐assortative mating despite size‐dependent fecundity in a Neotropical amphibian with explosive reproduction

Sexual selection theory predicts that, when body size is correlated with fecundity, there should be fitness advantages for mate choice of the largest females. Moreover, because larger males are expected to monopolise the largest females, this should result in an assortative mating based on body size. Although such patterns could be expected in both explosive and prolonged breeders, non‐assortative mating should be more widespread in species under time constraints. However, patterns of sexual selection are largely unexplored in explosive breeding species, and contrasting patterns have been found previously. We expect that the active choice of partners may be particularly risky when the time period during which sexual partners are available is severely limited. Therefore, to avoid missing an entire reproductive act, males and females should pair irrespective of traits, such as body size. We tested this hypothesis by investigating the mating patterns of the Pacific horned toad, Ceratophrys stolzmanni, a short‐lived fossorial species inhabiting Neotropical dry forests. This species is particularly adequate to test our prediction because it reproduces explosively over the course of a single night per year. Although the number of eggs laid was proportional to the size of females, and individuals of both sexes showed variation in body size, there was no assortative mating based either on size, body condition or age of mates. Egg size was not influenced by either female size or clutch size. The larger body size of females compared to males is likely due to fecundity selection, that is, the selective pressure that enhances reproductive output. Although we cannot dismiss the possibility that individuals could select their partners based on other criteria than those related to size or age, the results fit well our prediction, showing that the explosive breeding makes improbable an active choice of partners in both sexes and therefore favours a random mating pattern.     

Substrate selection and assortative mating in Gammarus pulex L.

We reject the published proposition that assortative mating for size in Gammarus is brought about purely as a result of spatial heterogeneity in substrate particle size. We confirm that, in general, large Gammarus prefer substrates with larger particle size than small Gammarus. However, in artificial streams in the laboratory, in choice experiments Gammarus males and females showed positive assortative mating for size in each of three substrates differing in mean particle size. We propose an explanation for assortative mating based on sexual selection.     

Early learning influences species assortative mating preferences in Lake Victoria cichlid fish

The Lake Victoria 'species flock' of cichlids is puzzling because reproductive isolation often occurs in the absence of substantial ecological differences among species. Theory predicts that this cannot evolve with most genetic mechanisms for mate choice. We provide the first evidence that learning, in the form of sexual imprinting, helps maintain reproductive isolation among closely related cichlid species. Using a cross-fostering experiment, we show that young females develop a sexual preference for males of their foster mothers' species, even reversing species assortative mating preferences. We suggest that learning creates favourable conditions for reproductive isolation to evolve.     

Variation in human mate choice: simultaneously investigating heritability, parental influence, sexual imprinting, and assortative mating

Human mate choice is central to individuals' lives and to the evolution of the species, but the basis of variation in mate choice is not well understood. Here we looked at a large community-based sample of twins and their partners and parents ([Formula: see text] individuals) to test for genetic and family environmental influences on mate choice, while controlling for and not controlling for the effects of assortative mating. Key traits were analyzed, including height, body mass index, age, education, income, personality, social attitudes, and religiosity. This revealed near-zero genetic influences on male and female mate choice over all traits and no significant genetic influences on mate choice for any specific trait. A significant family environmental influence was found for the age and income of females' mate choices, possibly reflecting parental influence over mating decisions. We also tested for evidence of sexual imprinting, where individuals acquire mate-choice criteria during development by using their opposite-sex parent as the template of a desirable mate; there was no such effect for any trait. The main discernible pattern of mate choice was assortative mating; we found that partner similarity was due to initial choice rather than convergence and also at least in part to phenotypic matching.