Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

Origin and evolution of assortative mating in actively speciating mole rats

The origin and evolution of positive assortative mating in the actively speciating subterranean mole rats of the Spalax ehrenbergi superspecies in Israel, may be deciphered by comparing female mate preference in the laboratory between ancestral and derivative species. Estrous females of the recent derivative of speciation (chromosomal species 2n = 60) showed trimodal mate preference distribution significantly differing from a normal curve. Females consisted of three phenotypes, comprising negative, low positive, and high positive preference for homospecific males. By contrast, mate preference in encounters of ancestral species (2n = 52, 54, and 58) showed a prevalence of a positive homospecific mate preference. It is suggested that the three modal distribution is explicable even on the basis of one major gene with three genotypes. The evolution of ethological reproductive isolation proceeded presumably from a high polymorphism in the most recent derivative of speciation towards increasing monomorphism of positive assortative mating among ancestral species. If an assortative mating locus combines with sexual selection of the frequent male adapted optimally to the local environment, then speciation and adaptation will be tightly linked in the evolution of mole rats.     

Reinforcement of mate preference among hybridizing Heliconius butterflies

Recent models of mate preference evolution suggest that direct selection on alleles at preference loci and correlated evolution of preference with locally adapted mating cues are more likely to drive the evolution of assortative mate preference than reinforcement. Mate preference evolution in mimetic Heliconius butterflies has been attributed to all three forms of selection, but here we show that reinforcement has been critical. By examining geographical variation in assortative mating and male mate preference among seven populations of three hybridizing Heliconius species from Costa Rica, we found pronounced character displacement of preference such that sexual isolation was enhanced in areas of interspecific contact. Of the different explanations for the evolution of assortative mate preference, only reinforcement is dependent on interspecific contact in this system. Thus, the observed pattern of reproductive character displacement of mate preference is best explained as a product of indirect selection generated by natural selection against nonmimetic hybrids.     

Pairing dynamics and the origin of species

Whether sexual selection alone can drive the evolution of assortative mating in the presence of gene flow is a long-standing question in evolutionary biology. Here, we report a role for pairing dynamics of individuals when mate choice is mutual, which is sufficient for the evolution of assortative mating by sexual selection alone in the presence of gene flow. Through behavioural observation, individual-based simulation and population genetic analysis, we evaluate the pairing dynamics of coral reef fish in the genus Hypoplectrus (Serranidae), and the role these dynamics can play for the evolution of assortative mating. When mate choice is mutual and the stability of mating pairs is critical for reproductive success, the evolution of assortative mating in the presence of gene flow is not only possible, but is also a robust evolutionary outcome.     

Assortative mating and the evolution of desirability covariation

Mate choice lies close to differential reproduction, the engine of evolution. Patterns of mate choice consequently have power to direct the course of evolution. Here we provide evidence suggesting one pattern of human mate choice—the tendency for mates to be similar in overall desirability—caused the evolution of a structure of correlations that we call the d factor. We use agent-based models to demonstrate that assortative mating causes the evolution of a positive manifold of desirability, d, such that an individual who is desirable as a mate along any one dimension tends to be desirable across all other dimensions. Further, we use a large cross-cultural sample with n = 14,478 from 45 countries around the world to show that this d-factor emerges in human samples, is a cross-cultural universal, and is patterned in a way consistent with an evolutionary history of assortative mating. Our results suggest that assortative mating can explain the evolution of a broad structure of human trait covariation.     

Genetics and demography: Notes on the third Princeton conference (Princeton,N.J., October 20–22, 1966)

Abstract

A method is presented for the analysis of deviations from random mating. Kinship, demographic, social, and spatial characteristics observed among married couples have been compared with the distributions expected if mates were chosen at random from all possible pairs of mates. This procedure has been used to investigate both failure to mate and patterns of assortative mating for cohorts born on Sanday, Orkney Islands, between 1885 and 1924. Differences in mating opportunity were observed. The 315 males who eventually married on the island differed from the 446 never‐married males in birth order and sibship size as well as geographic and kinship “distances” measured between ego and all females available for marriage. Comparison of wives with the potential mates of married males indicated that mating was assortative with respect to kinship, demographic, social, and geographic characteristics. Further implications of this nonrandom pattern of mate choice are discussed and application of this method to other populations suggested.     

On the Adaptive Value of Some Mate Selection Strategies

Results of an agent-based computer simulation of the evolution of diploid sexual organisms showed that several mate selection strategies confer much higher average fitness to the simulated populations, and higher evolutionary stability to the alleles coding for these strategies, than random mating. Strategies which select for 'good genes' were very successful, and so were strategies based on assortative mating. The results support the hypothesis that mating is not likely to be random in nature and that the most successful mate selection strategies are those based on assortative mating or on advantageous genes.     

Mate selection in man: Evidence,theory, and outcome

Abstract

This review presents a comprehensive survey of the literature on mate selection and non‐random mating in man. The topics discussed include: (1) genetic aspects of non‐random mating for complex traits; (2) evidence on resemblance between spouses on a large variety of traits such as intelligence, personality, physical characteristics, and sociocultural traits; (3) a critical review of sociological and psychological theories offered to account for assortative mating, and (4) implications of assortative mating for marital satisfaction. It is suggested that the factors leading to choice of marriage partners need to be studied from the point of view of multivariate profiles rather than single traits. Such studies will require sophisticated methodologies of research design and data analysis.     

HOST-PLANT-INDUCED ASSORTATIVE MATING IN ENCHENOPA TREEHOPPERS

The hypothesis tested here is whether extrinsic host-plant-induced life-history timing and mating biology promote assortative mating along host-plant lines. In the arboreal, univoltine Enchenopa treehopper system, host plants mediate the timing and synchronization of egg hatch. The result is a uniform age structure with a restricted mating window during which females mate once. Enchenopa on host plants that differ in phenology have asynchronous life histories and mating windows, suggesting that temporal differences may promote assortative mating. To test this hypothesis, egg hatch of Enchenopa from the same host-plant species was manipulated to produce continuous adult age-classes. Under experimental conditions with no spatial barriers, mating occurred between individuals similar in age. The mechanism promoting this assortative mating is differential mortality in males and females, such that few males are still alive when females in successive age-classes mate. Such host-plant-induced assortative mating is viewed as an effective mechanism to protect the integrity of gene pools from migrants, permitting selection for host-plant-adapted genotypes and speciation.     

Experimental evolution of mating discrimination in budding yeast

Assortative mating, when individuals of similar phenotypes mate, likely plays a key role in preventing gene flow during speciation. Reinforcement occurs when two previously geographically separated (allopatric) groups meet after having evolved partial postzygotic isolation; they are selected to evolve or enhance assortative mating to prevent costly intergroup matings that produce only maladaptive or sterile hybrids. Studies in Drosophila have shown that the genetic architectures of mating discrimination could differ significantly with or without reinforcement, suggesting that the evolution of assortative mating may be more complicated than expected. To study the evolution of assortative mating, we evolved mating discrimination in populations of the budding yeast, Saccharomyces cerevisiae. After 36 cycles of selection, these cells are five times more likely to mate with each other than to their ancestors, despite detectable one-way gene flow between the selected and reference populations. Several individual cultures evolved mating discrimination by changing their mating kinetics, with some mating more rapidly and others more slowly than the ancestral population. Genetic analysis indicates that multiple mutations have accumulated to produce the altered mating preference. Our results show that subtle details of mating behavior can play an important role in the evolution of reproductive isolation.     

Temporal variation of heterozygosity‐based assortative mating and related benefits in a lesser kestrel population

Heterozygosity as a target of mate choice has received much attention in recent years and there is growing evidence supporting its role in the evolution of mate preferences. In this study we analyse mating patterns in relation to heterozygosity in a lesser kestrel (Falco naumanni) population intensively monitored over six study years (2002–2007). The magnitude of heterozygosity‐based assortative mating varied over time, being particularly patent in the last study years (2006, 2007). We have found evidence that this mating pattern entails both direct and indirect‐genetic benefits. Clutch size increased with female heterozygosity and more heterozygous males raised a higher number of fledglings particularly in those years when the strength of the heterozygosity‐based assortative mating was markedly higher. In the last study year, parent–offspring correlation of heterozygosity was stronger and higher than the expected if individuals would have randomly mated with respect to heterozygosity. Overall, our results offer empirical support to the heterozygous mate hypothesis of sexual selection but suggest that genetic diversity may act as a temporally variable target for mate choice.     

Frequency-dependent selection and the evolution of assortative mating

A long-standing goal in evolutionary biology is to identify the conditions that promote the evolution of reproductive isolation and speciation. The factors promoting sympatric speciation have been of particular interest, both because it is notoriously difficult to prove empirically and because theoretical models have generated conflicting results, depending on the assumptions made. Here, we analyze the conditions under which selection favors the evolution of assortative mating, thereby reducing gene flow between sympatric groups, using a general model of selection, which allows fitness to be frequency dependent. Our analytical results are based on a two-locus diploid model, with one locus altering the trait under selection and the other locus controlling the strength of assortment (a "one-allele" model). Examining both equilibrium and nonequilibrium scenarios, we demonstrate that whenever heterozygotes are less fit, on average, than homozygotes at the trait locus, indirect selection for assortative mating is generated. While costs of assortative mating hinder the evolution of reproductive isolation, they do not prevent it unless they are sufficiently great. Assortative mating that arises because individuals mate within groups (formed in time or space) is most conducive to the evolution of complete assortative mating from random mating. Assortative mating based on female preferences is more restrictive, because the resulting sexual selection can lead to loss of the trait polymorphism and cause the relative fitness of heterozygotes to rise above homozygotes, eliminating the force favoring assortment. When assortative mating is already prevalent, however, sexual selection can itself cause low heterozygous fitness, promoting the evolution of complete reproductive isolation (akin to "reinforcement") regardless of the form of natural selection.     

EXPERIMENTAL CONFIRMATION THAT BODY SIZE DETERMINES MATE PREFERENCE VIA PHENOTYPE MATCHING IN A STICKLEBACK SPECIES PAIR

Mate choice by phenotype matching, whereby individuals prefer a mate whose phenotype is similar to their own, should facilitate speciation with gene flow. This is because the genes that control mate signal (the phenotype being matched) also determine the preferred mate signal (“mate preference”). Speciation is made even easier if phenotype matching is based on a trait under divergent natural selection. In this case, assortative mating should readily evolve as a byproduct of divergent selection on the trait. Previous observational studies of assortative mating between sympatric, hybridizing threespine stickleback species (Gasterosteus aculeatus complex) suggested that phenotype matching might occur by body size, a trait under divergent natural selection. To test this, we used experimental manipulation of body size to rule out the effects of confounding variables. We found that size‐manipulated benthic and limnetic stickleback females prefer mates whose body size more closely matches their own. It is thus likely that assortative mating by phenotype matching has facilitated the origin and persistence of benthic and limnetic threespine sticklebacks in the face of gene flow.     

COLOR PATTERN EVOLUTION,ASSORTATIVE MATING,AND GENETIC DIFFERENTIATION IN BRIGHTLY COLORED BUTTERFLYFISHES (CHAETODONTIDAE)

In butterflyfishes (Chaetodontidae), color pattern evolves rapidly and is often the only morphological trait separating closely related species. Vivid coloration is frequently assumed to provide critical signals for mate recognition and mate choice, but few direct experimental tests are available. Here we analyze the relationship between color pattern change, mate choice, and genetic differentiation in a group of three very closely related allopatric butterflyfishes. We found that in only one member of this group, Chaetodon multicinctus, is color pattern evolution associated with mate preference and genetic divergence. For its two sister species, C. punctatofasciatus and C. pelewensis, color pattern change has not resulted in assortative mating (based on laboratory pairing experiments and field observations) or in significant mtDNA or allozyme differentiation. In a contact zone on reefs in the Solomon Islands and Papua New Guinea, hybridization between the two forms has nearly homogenized color pattern differences. Outside these areas, however, color pattern remains distinct. Genetic variation is homogeneous over a much larger geographic scale. Sequence variation in the tRNA-proline end of the mitochondrial control region and allozyme variation was distributed widely within C. punctatofasciatus and C. pelewensis, which suggests few constraints to mitochondrial or nuclear gene flow across the color pattern boundary. These contrasting patterns strongly suggest that selection is maintaining color pattern differences in allopatry in the face of potentially homogenizing levels of gene flow. The mating pattern data show that this selection is not operating on mate recognition in the strictest sense, but probably on some other aspect of the social system of these territorial fish. In this case, divergence in mating preference can follow color pattern evolution, but is not contemporaneous with it.     

Effects of female preference intensity on the permissiveness of sexual trait polymorphisms

Recent developments in sexual selection theory suggest that on their own, mate preferences can promote the maintenance of sexual trait diversity. However, how mate preferences constrain the permissiveness of sexual trait diversity in different environmental regimes remains an open question. Here, we examine how a range of mate choice parameters affect the permissiveness of sexual trait polymorphism under several selection regimes. We use the null model of sexual selection and show that environments with strong assortative mating significantly increase the permissiveness of sexual trait polymorphism. We show that for a given change in mate choice parameters, the permissiveness of polymorphism changes more in environments with strong natural selection on sexual traits than in environments with weak selection. Sets of nearly stable polymorphic populations with weak assortative mating are more likely to show accidental divergence in sexual traits than sets of populations with strong assortative mating. The permissiveness of sexual trait polymorphism critically depends upon particular combinations of natural selection and mate choice parameters.     

Reinforcement and the genetics of nonrandom mating

Abstract.— The occurrence of reinforcement is compared when premating isolation is caused by the spread of a gene causing females to prefer to mate with males carrying a population-specific trait (a "preference" model) and by a gene that causes females to prefer to mate with males that share their own trait phenotype (an "assortative mating" model). Both two-island models, which have symmetric gene flow, and continent-island models, which have one-way gene flow, are explored. Reinforcement is found to occur much more easily in a two-island assortative mating model than in any of the other three models. This is due primarily to the fact that in this model the assortative mating allele will automatically become genetically associated in each population with the trait allele that is favored by natural selection on that island. In contrast, natural selection on the trait both favors and opposes the evolution of premating isolation in the two-island preference model, depending on the particular population. These results imply that species recognition in the context of mating may evolve particularly easily when it targets cues that are favored by natural selection in each population. In the continent-island models, reinforcement is found to occur more often under the preference model than the assortative mating model, thus reversing the trend from the two-island models. Patterns of population subdivision may therefore play a role in determining what types of premating isolation may evolve.     

‘Prudent habitat choice’: a novel mechanism of size‐assortative mating

Assortative mating, an ubiquitous form of nonrandom mating, strongly impacts Darwinian fitness and can drive biological diversification. Despite its ecological and evolutionary importance, the behavioural processes underlying assortative mating are often unknown, and in particular, mechanisms not involving mate choice have been largely ignored so far. Here, we propose that assortative mating can arise from ‘prudent habitat choice’, a general mechanism that acts under natural selection, and that it can occur despite a complete mixing of phenotypes. We show that in the cichlid Eretmodus cyanostictus size‐assortative mating ensues, because individuals of weaker competitive ability ignore high‐quality but strongly competed habitat patches. Previous studies showed that in E. cyanostictus, size‐based mate preferences are absent. By field and laboratory experiments, here we showed that (i) habitat quality and body size are correlated in this species; (ii) territories with more stone cover are preferred by both sexes in the absence of competition; and (iii) smaller fish prudently occupy vacant territories of worse quality than do larger fish. Prudent habitat choice is likely to be a widespread mechanism of assortative mating, as both preferences for and dominance‐based access to high‐quality habitats are generic phenomena in animals.     

You can't always get what you want: size assortative mating by mutual mate choice as a resolution of sexual conflict

Background  

Assortative mating patterns for mate quality traits like body size are often observed in nature. However, the underlying mechanisms that cause assortative mating patterns are less well known. Sexual selection is one important explanation for assortment, suggesting that i) one (usually the female) or both sexes could show preferences for mates of similar size or ii) mutual mate choice could resolve sexual conflict over quality traits into assortment. We tested these hypotheses experimentally in the socially monogamous cichlid fish Pelvicachromis taeniatus, in which mate choice is mutual.     

Color Assortative Mating in a Mainland Population of the Poison Frog Oophaga pumilio

Assortative mating is a reproductive strategy used by a diversity of animals, in which individuals choose a mate that shares similar characteristics. This mating strategy has the potential to promote the evolution of various sexual signals and has been a proposed mechanism driving and maintaining color variation in the anuran family Dendrobatidae. Most studies have examined this reproductive strategy in the polytypic poison frog, Oophaga pumilio, in the Bocas del Toro archipelago in Panama. Little attention, however, has been given to ancestral populations across this species’ mainland range, where dramatic color polytypism appears to lack. Additionally, most studies are exclusively experimental and investigate mate choice between allopatric populations, neglecting the behaviors of naturally occurring mates. This study observed natural mating pairs within a population of O. pumilio on mainland Costa Rica and tested the prediction that color phenotype of mating females and males would be correlated. Naturally occurring pairs were found to share similar coloration, suggesting that color assortative mating operates in nature, and in a mainland population. Our results indicate that coloration is an important trait in driving the natural mate choices of female O. pumilio, which provides valuable insight into realistic mate selection tactics of this dendrobatid frog.     

Testing alternative models for sexual isolation in natural populations of Littorina saxatilis: indirect support for by‐product ecological speciation?

Two ecotypes of the rough periwinkle Littorina saxatilis occur at different shore levels, showing assortative mating for size and partial reproductive isolation when they meet at the mid-shore. This system represents a putative case of incomplete speciation in sympatry. Two processes contribute to the assortative mating: morph-specific microhabitat aggregation and mate choice. The estimation of mate choice coefficients in nature and a simulation of the aggregation effects on sexual isolation were used to disentangle these processes as well as to test alternative mechanisms of mate choice. Mate choice significantly increased the frequency of within-morph pairs and significantly decreased the frequency of between-morph pairs, whereas those pairs including at least one hybrid morph mated randomly. These results allow us to reject a discriminant mate choice and support a model of evolution of sexual isolation as a side-effect of size-assortative mating in a context of divergent natural selection for size in the population. This mechanism is more compatible with a model of incomplete by-product ecological speciation, as suggested by previous evidence.