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.     

Reinforcement and divergence under assortative mating

Traits that cause assortative mating such as the flowering time in plants and body size in animals can produce reproductive isolation between hybridizing populations. Can selection against unfit hybrids cause two populations to diverge in their mean values for these kinds of traits? Here I present a haploid analytical model of one population that receives gene flow from another. The partial pre-zygotic isolation between the two populations is caused by assortative mating for a trait that is influenced by any number of genes with additive effects. The post-zygotic isolation is caused by selection against genetic incompatibilities that can involve any form of selection on individual genes and gene combinations (epistasis). The analysis assumes that the introgression rate and selection coefficients are small. The results show that the assortment trait mean will not diverge from the immigrants unless there is direct selection on the trait favouring it to do so or there are genes of very large effect. The amount of divergence at equilibrium is determined by a balance between direct selection on the assortment trait and introgression from the other population. Additional selection against hybrid genetic incompatibilities reduces the effective migration rate and allows greater divergence. The role of assortment in speciation is discussed in the light of these results.     

The meaning of assortative mating

Patterns of positive assortative mating are commonly inferred to result from homotypic preferences (preferences for self's type). This paper demonstrates that such preferences can result from heterotypic and type preferences as well. Because several kinds of preferences can lead to the same pattern, experimentation to measure preferences is necessary to determine the process responsible. The apparent weight of evidence for homotypic preferences may result from the kinds of preferences experimenters have selected to examine.     

Transfer systems and covariance under assortative mating

Summary This paper introduces the concept of a transfer system of random variables and uses it ot study various types of assortative mating. The standard correlation structure between relatives under phenotypic and genetic assortative mating are obtained easily and these results are then extended to multiple characters by means of multivariate transfer systems. Equilibrium values for the parameters are found and index assortative mating is considered with specific applications.     

Studies on assortative mating. III. The effects of incomplete penetrance in assortative mating systems

Four models of positive and negative assortative mating systems, exclusive or partial, in relation to phenotypes determined by a pair of autosomal alleles with dominance but with incomplete penetrance of the dominant allele in heterozygous state, are presented. By introducing the parameter of incomplete penetrance in the models of assortative matings, matings between individuals with identical genotypes will occur within the negative systems, as well as matings between individuals with different genotypes within the positive assortative mating systems. Thus, incomplete penetrance has the effect of retarding equilibrium on an assortative mating system, making this equilibrium equivalent to a system with a lower degree of assortative mating, where the penetrance equals 1 or 0. Another conclusion of biological interest drawn from the mathematical analysis presented in this paper is that for any value of the penetrance, the frequency of 0.5 for recessive individuals is also typical of exclusive or partial negative assortative mating systems at equilibrium.     

Ancestry-related assortative mating in Latino populations

Background

While spouse correlations have been documented for numerous traits, no prior studies have assessed assortative mating for genetic ancestry in admixed populations.

Results

Using 104 ancestry informative markers, we examined spouse correlations in genetic ancestry for Mexican spouse pairs recruited from Mexico City and the San Francisco Bay Area, and Puerto Rican spouse pairs recruited from Puerto Rico and New York City. In the Mexican pairs, we found strong spouse correlations for European and Native American ancestry, but no correlation in African ancestry. In the Puerto Rican pairs, we found significant spouse correlations for African ancestry and European ancestry but not Native American ancestry. Correlations were not attributable to variation in socioeconomic status or geographic heterogeneity. Past evidence of spouse correlation was also seen in the strong evidence of linkage disequilibrium between unlinked markers, which was accounted for in regression analysis by ancestral allele frequency difference at the pair of markers (European versus Native American for Mexicans, European versus African for Puerto Ricans). We also observed an excess of homozygosity at individual markers within the spouses, but this provided weaker evidence, as expected, of spouse correlation. Ancestry variance is predicted to decline in each generation, but less so under assortative mating. We used the current observed variances of ancestry to infer even stronger patterns of spouse ancestry correlation in previous generations.

Conclusions

Assortative mating related to genetic ancestry persists in Latino populations to the current day, and has impacted on the genomic structure in these populations.     

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.     

Two-trait selection response with marker-based assortative mating

 Marker-based assortative mating (MAM) – the mating of individuals that have similar genotypes at random marker loci – can increase selection response for a single trait by 3–8% over random mating (RM). Genetic gain is usually desired for multiple traits rather than for a single trait. My objectives in this study were to (1) compare MAM, phenotypic assortative mating (PAM), and RM of selected individuals for improving two traits and (2) determine when MAM will be most useful for improving two traits. I simulated 20 generations of selecting 32 out of 200 individuals in an F₂ population. The individuals were selected based on an index (SI) of two traits and were intermated by MAM, PAM, or RM. I studied eight genetic models that differed in three contrasts: (1) weight, number of quantitative trait loci (QTL), and heritability (h ²) for each trait; (2) linkage of QTL for each trait; and (3) trait means of the inbred parents of the F₂. For SI and the two component traits, MAM increased short-term selection response by 5–8% in six out of the eight genetic models. The MAM procedure was least effective in two genetic models, wherein the QTL for one trait were unlinked to the QTL for the other trait and the parents of the F₂ had divergent means for each trait. The loss of QTL heterozygosity was much greater with MAM than with PAM or RM. Consequently, the advantage of MAM over RM dissipated after 5–7 generations. Differences were small between selection responses with PAM and RM. The MAM procedure can enhance short-term selection response for two traits when selection is not stringent, h ² is low, and the means of the parents of the F₂ are equal for each trait. Received: 10 June 1998 / Accepted: 5 August 1998     

Intraspecific competitive divergence and convergence under assortative mating

Ecologically driven sympatric speciation has received much attention recently. We investigate a multilocus model of a quantitative trait that is under frequency-dependent selection caused by intraspecific competition and acts as mating character for assortment. We identify the conditions that lead to the establishment of reproductively isolated clusters. This may be interpreted as evolutionary splitting or sympatric speciation. In our model, there are parameters that independently determine the strength of assortment, the costs for being choosy, and the strength of frequency-dependent natural selection. Sufficiently strong frequency dependence leads to disruptive selection on the phenotypes. The population consists of (sexual) haploid individuals. If frequency dependence is strong enough to induce disruptive selection and costs are absent or low, the result of evolution depends in a distinctive nonlinear way on the strength of assortment: under moderately strong assortment, less genetic variation is maintained than under weak or strong assortment, and sometimes there is none at all. Evolutionary splitting occurs only if frequency dependence and assortment are both strong enough and costs are low. Even then, the evolutionary outcome depends on the genetics and the initial conditions. The roles of the number of loci, of linkage, and of asymmetric selection are also explored.     

Phenotypic assortative mating among the Peruvian Cashinahua

The persistence of behaviorally deleterious genes in the human population poses an interesting question for population genetics: If certain alleles at these loci are deleterious, why have they survived in the population? We consider evidence for phenotypic capacitance and/or frequency-dependent selection for an allele that has been putatively shown to have negative associations with human behaviors (the “short” 5-HTT promoter region allele) yet has persisted in human and nonhuman primate populations. Using data from the National Longitudinal Study of Adolescent Health, we compare sibling and twin variation in depression by 5-HTT genotype (specified in several ways) and investigate sibship-level cross-person gene-gene interactions. In support of the “orchid/dandelion” hypothesis, we find evidence that the short allele increases variation in phenotypes in response to environmental (or genetic) differences (i.e., acts as a perturbation of a phenotypic capacitor). Further, we also find some evidence that the effects of allelic variation at this locus are moderated by the genetic environment of the sibship unit (i.e., effects may be susceptible to frequency-dependent selection). We discuss implications of these findings for genetic models in general, specifically with respect to stable unit treatment value assumption violations (i.e., nonindependence of units of analysis).     

Some population genetic models combining artificial and natural selection pressures in the presence of assortative mating

Summary We have attempted quantitatively through a series of assortative mating models to gain insight into the interaction between the usually antagonistic tendencies of artificial and natural selection pressures. We summarize some of the robust conclusions. In cases where natural selection is expressed only through the phenotype and acts in the opposite direction to the culling incline, then fixation of the dominant or recessive type can be achieved and which occurs depends critically on the initial composition of the population and the magnitude of the degree of culling compared to the selection coefficients.With traits determined at two loci in the case that the double heterozygote is the desired kind, the effect of selfing can only be overcome by very strong artificial selection pressures (high culling order). The degree of culling to achieve its objective can be relaxed with weakening of linkage. The relevant comparison is r ₂ + (1 – r)₂ < (1 – c)indicating the precise extent of culling needed, to prevent fixation. The relationships are more complex when natural selection forces are also involved (see Model IV).Supported in part by NIH Grant USPHS 10452-09.     

Emergence and loss of assortative mating in sympatric speciation

We have studied an agent model which presents the emergence of sexual barriers through the onset of assortative mating, a condition that might lead to sympatric speciation. In the model, individuals are characterized by two traits, each determined by a single locus A or B. Heterozygotes on A are penalized by introducing an adaptive difference from homozygotes. Two niches are available. Each A homozygote is adapted to one of the niches. The second trait, called the marker trait has no bearing on the fitness. The model includes mating preferences, which are inherited from the mother and subject to random variations. A parameter controlling recombination probabilities of the two loci is also introduced. We study the phase diagram by means of simulations, in the space of parameters (adaptive difference, carrying capacity, recombination probability). Three phases are found, characterized by (i) assortative mating, (ii) extinction of one of the A alleles and (iii) Hardy-Weinberg like equilibrium. We also make perturbations of these phases to see how robust they are. Assortative mating can be gained or lost with changes that present hysteresis loops, showing the resulting equilibrium to have partial memory of the initial state and that the process of going from a polymorphic panmictic phase to a phase where assortative mating acts as sexual barrier can be described as a first-order transition.     

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.     

Stress-induced assortative mating and the evolution of stress resistance

We show with a model that variation in environmental stress between generations facilitates the evolution of stress resistance through assortative mating. Stress induces delayed maturation of susceptible phenotypes, segregating their fertile period from resistant phenotypes. Assortment of mates enhances the responsiveness of populations to natural selection by inflating genetic variance. Thus, positive selection and inflated genetic variance in stressful environments can cause a strong evolutionary increase in resistance. By contrast, benign environments do not segregate phenotypes, and the random mating among phenotypes deflates genetic variance, leading to a weaker response to selection against resistance, assuming that resistance is costly. When environments vary randomly from benign to stressful, populations respond asymmetrically to negative and positive selection. This asymmetry (1) accelerates fixation of a resistance allele if resistance is generally favoured (stressful generations more frequent) but delays the loss of the allele if it is generally disfavoured (benign generations more frequent), and (2) it can push a resistance allele to fixation even when long‐term costs modestly exceed benefits. When resistance alleles pleiotropically delay mating, stress‐induced random mating has complementary effects. Serial autocorrelation in the stressor amplifies these effects. These results suggest a novel mechanism for the persistence of resistance polymorphisms.     

Sexual size dimorphism and assortative mating in Carolina Wrens

ABSTRACT.   Sexual size dimorphism (SSD) may be due to sexual and natural selection, but identifying specific mechanisms that generate such dimorphism in a species is difficult. I examined SSD in Carolina Wrens ( Thryothorus ludovicianus ) by examining (1) the degree of SSD in the population and between pairs using five morphometrics, (2) assortative mating patterns based on size and age, and (3) relationships between size and longevity. Analysis revealed that males were significantly larger than females in all body measurements. For example, mass, bill, and wing measurements yielded a canonical variable that permitted separation of the sexes and linear classification functions correctly determined the sex of 95% (238/250) of all wrens measured. No evidence was found to suggest that SSD was related to resource partitioning. However, assortative mating trends based on morphometrics (e.g., wing length), positive associations between longevity and morphometrics (e.g., wing length in females and body size in males), and intense male-male contests for territorial resources year-round provide evidence that sexual selection may contribute to SSD in Carolina Wrens.