Preferential mating in symmetric multilocus systems: stability conditions of the central equilibrium

Several multilocus models that incorporate both preferential mating and viability selection are studied. Specifically, a class of symmetric heterozygosity models are considered that assign individuals to phenotypic classes according to which loci are in heterozygous state regardless of the actual allelic content. Otherwise, an arbitrary number of loci, number of alleles per locus, and arbitrary recombination scheme, viability parameters and preferential mating pattern based on phenotypes are allowed. The conditions for the stability of a central polymorphism are indicated and interpreted. The effects of viability and preference selection may be summarized in a single quantity for each phenotypic class, a generalized fitness. Preferential assortative mating alone can produce stability for a central polymorphism as in the case of viability selection when sexual attractiveness or general fitness increases with higher levels of heterozygosity. The situation is more complex with sexual selection.     

Large-scale fungal strain sequencing unravels the molecular diversity in mating loci maintained by long-term balancing selection

Balancing selection, an evolutionary force that retains genetic diversity, has been detected in multiple genes and organisms, such as the sexual mating loci in fungi. However, to quantify the strength of balancing selection and define the mating-related genes require a large number of strains. In tetrapolar basidiomycete fungi, sexual type is determined by two unlinked loci, MATA and MATB. Genes in both loci define mating type identity, control successful mating and completion of the life cycle. These loci are usually highly diverse. Previous studies have speculated, based on culture crosses, that species of the non-model genus Trichaptum (Hymenochaetales, Basidiomycota) possess a tetrapolar mating system, with multiple alleles. Here, we sequenced a hundred and eighty strains of three Trichaptum species. We characterized the chromosomal location of MATA and MATB, the molecular structure of MAT regions and their allelic richness. The sequencing effort was sufficient to molecularly characterize multiple MAT alleles segregating before the speciation event of Trichaptum species. Analyses suggested that long-term balancing selection has generated trans-species polymorphisms. Mating sequences were classified in different allelic classes based on an amino acid identity (AAI) threshold supported by phylogenetics. 17,550 mating types were predicted based on the allelic classes. In vitro crosses allowed us to support the degree of allelic divergence needed for successful mating. Even with the high amount of divergence, key amino acids in functional domains are conserved. We conclude that the genetic diversity of mating loci in Trichaptum is due to long-term balancing selection, with limited recombination and duplication activity. The large number of sequenced strains highlighted the importance of sequencing multiple individuals from different species to detect the mating-related genes, the mechanisms generating diversity and the evolutionary forces maintaining them.     

A Symmetric Two-Locus Fertility Model

A model in which selection is mediated by differential fertilities among the genotypes at two diallelic loci is proposed. Fertility depends only on the number of heterozygous loci participating in the mating. Classes analogous to symmetric equilibria in symmetric viability models are determined explicitly and shown to exhibit stability behavior very different from the viability results. Linkage equilibrium is shown to occur in a relatively asymmetric fashion and to overlap in stability with linkage disequilibrium. In many cases single-locus or two-locus polymorphism is shown to be stable simultaneously with chromosome fixation even under very tight linkage. It is suggested that historical effects may be of great significance in the evolution of systems in which fertility is the primary agent of natural selection.     

Quantitative measures of sexual selection reveal no evidence for sex-role reversal in a sea spider with prolonged paternal care

Taxa in which males alone invest in postzygotic care of offspring are often considered good models for investigating the proffered relationships between sexual selection and mating systems. In the pycnogonid sea spider Pycnogonum stearnsi, males carry large egg masses on their bodies for several weeks, so this species is a plausible candidate for sex-role reversal (greater intensity of sexual selection on females than on males). Here, we couple a microsatellite-based assessment of the mating system in a natural population with formal quantitative measures of genetic fitness to investigate the direction of sexual selection in P. stearnsi. Both sexes proved to be highly polygamous and showed similar standardized variances in reproductive and mating successes. Moreover, the fertility (number of progeny) of males and females appeared to be equally and highly dependent on mate access, as shown by similar Bateman gradients for the two sexes. The absence of sex-role reversal in this population of P. stearnsi is probably attributable to the fact that males are not limited by brooding space but have evolved an ability to carry large numbers of progeny. Body length was not a good predictor of male mating or reproductive success, so the aim of future studies should be to determine what traits are the targets of sexual selection in this species.     

Sensory drive speciation and patterns of variation at selectively neutral genes

Speciation by sensory drive can occur if divergent adaptation of sensory systems causes rapid evolution of mating traits and the resulting development of assortative mating. Previous theoretical studies have shown that sensory drive can cause rapid divergent adaptive evolution from one to two phenotypes. In this study, we examined two topics: the possibility of adaptive radiation by sensory drive from one to more than two phenotypes and the relationships of patterns of variation at selectively neutral genes to levels of viability selection, habitat and mating preferences and migration. We conducted individual-based simulations assuming a sensory trait and a mating trait controlled by a small number of loci. We found that adaptive radiation is possible when the number of loci controlling the sensory trait is small; the levels of viability selection, habitat and mating preferences are intermediate; and the emigration rate is high. We also found that emigration rates as well as the levels of habitat and mating preferences are related to F _ST values at neutral loci, but F _ST proved to be insensitive to a small change in the number of loci controlling the mating trait. This suggests that an estimation of the past population history is possible without an accurate genetic model.     

Variation in mate-recognition pheromones of the fungal genus Microbotryum

Mate recognition is an essential life-cycle stage that exhibits strong conservation in function, whereas diversification of mating signals can contribute directly to the integrity of species boundaries through assortative mating. Fungi are simple models, where compatibility is based on the recognition of pheromone peptides by corresponding receptor proteins, but clear patterns of diversification have not emerged from the species examined, which are few compared with mate signaling studies in plant and animal systems. In this study, candidate loci from Microbotryum species were used to characterize putative pheromones that were synthesized and found to be functional across multiple species in triggering a mating response in vitro. There is no significant correlation between the strength of a species'' response and its genetic distance from the pheromone sequence source genome. Instead, evidence suggests that species may be strong or weak responders, influenced by environmental conditions or developmental differences. Gene sequence comparisons reveals very strong purifying selection on the a₁ pheromone peptide and corresponding receptor, but significantly less purifying selection on the a₂ pheromone peptide that corresponds with more variation across species in the receptor. This represents an exceptional case of a reciprocally interacting mate-recognition system in which the two mating types are under different levels of purifying selection.     

Bateman's principle is reversed in a cooperatively breeding bird

Bateman''s principle is not only used to explain sex differences in mating behaviour, but also to determine which sex has the greater opportunity for sexual selection. It predicts that the relationship between the number of mates and the number of offspring produced should be stronger for males than for females. Yet, it is unclear whether Bateman''s principle holds in cooperatively breeding systems where the strength of selection on traits used in intrasexual competition is high in both sexes. We tested Bateman''s principle in the cooperatively breeding superb starling (Lamprotornis superbus), finding that only females showed a significant, positive Bateman gradient. We also found that the opportunity for selection was on average higher in females, but that its strength and direction oscillated through time. These data are consistent with the hypothesis that sexual selection underlies the female trait elaboration observed in superb starlings and other cooperative breeders. Even though the Bateman gradient was steeper for females than for males, the year-to-year oscillation in the strength and direction of the opportunity for selection likely explains why cooperative breeders do not exhibit sexual role reversal. Thus, Bateman''s principle may not hold in cooperative breeders where both sexes appear to be under mutually strong sexual selection.     

Reproductive Success and Sexual Selection in Wild Eastern Tiger Salamanders (<Emphasis Type="Italic">Ambystoma t. tigrinum</Emphasis>)

Variation in reproductive success is most pronounced in species with strongly biased operational sex ratios, prominent sexual dimorphisms, and where mate competition and choice are likely. We studied sexual selection in eastern tiger salamanders (Ambystoma t. tigrinum) and examined the role of body size on reproductive success. We genotyped 155 adults and 1,341 larvae from 90 egg masses at six microsatellite loci. Parentage analyses revealed both sexes engaged in multiple matings, but was more common among females (64%) than males (27%). However, the standardized variance in mating and reproductive success was higher in males. Bateman gradients were significant and nearly identical in both sexes, suggesting that sexual selection was roughly equal between sexes. Body size was not correlated with mating or reproductive success in either sex. The apparent lack of sexual selection on body size may be a result of sperm storage, sperm competition, alternative mating tactics, and/or random induction of spermatophores.     

The distribution of the proportion of the genome which is homozygous by descent in inbred individuals.

The expected proportion of loci which are homozygous by descent in an inbred individual is the inbreeding coefficient of that individual. Confidence limits on this proportion depend on the number of loci controlling the trait under investigation and the linkage relationships among the loci. Such information is generally not available. If it is assumed that the number of loci is large, the variance of the proportion of homozygous loci is approximated by the variance of the total map length which is homozygous by descent; this is calculated for several regular mating systems, including selfing, sib mating, and parent-off-spring mating. In particular, the confidence interval on the proportion of homozygous loci in Drosophila is likely to be large, and this has a number of implications to the interpretation and analysis of experimental data.     

Natural and Sexual Selection on Many Loci

A method is developed that describes the effects on an arbitrary number of autosomal loci of selection on haploid and diploid stages, of nonrandom mating between haploid individuals, and of recombination. We provide exact recursions for the dynamics of allele frequencies and linkage disequilibria (nonrandom associations of alleles across loci). When selection is weak relative to recombination, our recursions provide simple approximations for the linkage disequilibria among arbitrary combinations of loci. We show how previous models of sex-independent natural selection on diploids, assortative mating between haploids, and sexual selection on haploids can be analyzed in this framework. Using our weak-selection approximations, we derive new results concerning the coevolution of male traits and female preferences under natural and sexual selection. In particular, we provide general expressions for the intensity of linkage-disequilibrium induced selection experienced by loci that contribute to female preferences for specific male traits. Our general results support the previous observation that these indirect selection forces are so weak that they are unlikely to dominate the evolution of preference-producing loci.     

How multiple mating by females affects sexual selection

Multiple mating by females is widely thought to encourage post-mating sexual selection and enhance female fitness. We show that whether polyandrous mating has these effects depends on two conditions. Condition 1 is the pattern of sperm utilization by females; specifically, whether, among females, male mating number, m (i.e. the number of times a male mates with one or more females) covaries with male offspring number, o. Polyandrous mating enhances sexual selection only when males who are successful at multiple mating also sire most or all of each of their mates'' offspring, i.e. only when Cov_♂(m,o), is positive. Condition 2 is the pattern of female reproductive life-history; specifically, whether female mating number, m, covaries with female offspring number, o. Only semelparity does not erode sexual selection, whereas iteroparity (i.e. when Cov_♀(m,o), is positive) always increases the variance in offspring numbers among females, which always decreases the intensity of sexual selection on males. To document the covariance between mating number and offspring number for each sex, it is necessary to assign progeny to all parents, as well as identify mating and non-mating individuals. To document significant fitness gains by females through iteroparity, it is necessary to determine the relative magnitudes of male as well as female contributions to the total variance in relative fitness. We show how such data can be collected, how often they are collected, and we explain the circumstances in which selection favouring multiple mating by females can be strong or weak.     

Social variables and divergent selection for mating behaviour of male chickens (Gallus domesticus)

Heterosexual or unisexual contact of juvenile males from two lines divergently selected for male mating frequency, and a control line had little, if any influence on their subsequent mating behaviour. The interaction of lines x social environments for mating behaviour was not significant, showing that lines responded in a similar manner to the environments. It is hypothetized that selection for low cumulative number of completed matings (CNCM) was primarily for higher neural thresholds, whereas selection for high CNCM affected loci operative after neural thresholds are attained. The magnitude of the sexual component of a court was found to be dependent on the genetic background of the population, being less in the low mating than in the high mating line.     

A multilocus-multiallele analysis of frequency-dependent selection induced by intraspecific competition

The study of the mechanisms that maintain genetic variation has a long history in population genetics. We analyze a multilocus-multiallele model of frequency- and density-dependent selection in a large randomly mating population. The number of loci and the number of alleles per locus are arbitrary. The n loci are assumed to contribute additively to a quantitative character under stabilizing or directional selection as well as under frequency-dependent selection caused by intraspecific competition. We assume the strength of stabilizing selection to be weak, whereas the strength of frequency dependence may be arbitrary. Density-dependence is induced by population regulation. Our main result is a characterization of the equilibrium structure and its stability properties in terms of all parameters. It turns out that no equilibrium exists with more than two alleles segregating per locus. We give necessary and sufficient conditions on the strength of frequency dependence to ensure the maintenance of multilocus polymorphism. We also give explicit formulas on the number of polymorphic loci maintained at equilibrium. These results are based on the assumption that selection is sufficiently weak compared with recombination, so that linkage equilibrium can be assumed. If additionally the population size is assumed to be constant, we prove that the dynamics of the model form a generalized gradient system. For the model in its general form we are able to derive necessary and sufficient conditions for the stability of the monomorphic equilibria. Furthermore, we briefly analyze a special symmetric two-locus two-allele model for a constant population size but allowing for linkage disequilibrium. Finally, we analyze a single diallelic locus with dominance to illustrate the complications that can occur if the assumption of additivity is relaxed.     

The conditions for speciation through intraspecific competition

Abstract It has been shown theoretically that sympatric speciation can occur if intraspecific competition is strong enough to induce disruptive selection. However, the plausibility of the involved processes is under debate, and many questions on the conditions for speciation remain unresolved. For instance, is strong disruptive selection sufficient for speciation? Which roles do genetic architecture and initial composition of the population play? How strong must assortative mating be before a population can split in two? These are some of the issues we address here. We investigate a diploid multilocus model of a quantitative trait that is under frequency‐dependent selection caused by a balance of intraspecific competition and frequency‐independent stabilizing selection. This trait also acts as mating character for assortment. It has been established previously that speciation can occur only if competition is strong enough to induce disruptive selection. We find that speciation becomes more difficult for very strong competition, because then extremely strong assortment is required. Thus, speciation is most likely for intermediate strengths of competition, where it requires strong, but not extremely strong, assortment. For this range of parameters, however, it is not obvious how assortment can evolve from low to high levels, because with moderately strong assortment less genetic variation is maintained than under weak or strong assortment sometimes none at all. In addition to the strength of frequency‐dependent competition and assortative mating, the roles of the number of loci, the distribution of allelic effects, the initial conditions, costs to being choosy, the strength of stabilizing selection, and the particular choice of the fitness function are explored. A multitude of possible evolutionary outcomes is observed, including loss of all genetic variation, splitting in two to five species, as well as very short and extremely long stable limit cycles. On the methodological side, we propose quantitative measures for deciding whether a given distribution reflects two (or more) reproductively isolated clusters.     

Reproductive and Mating Success in the Small-Mouthed Salamander (Ambystoma texanum) Estimated via Microsatellite Parentage Analysis

Bateman’s principles of sexual selection predict that the sex with “cheaper” gametes may maximize reproductive efforts by mating multiply and so display greater positive covariance between reproductive and mating success. We conducted a semi-controlled breeding experiment to genetically quantify sexual selection in adult Ambystoma texanum, a sexually monomorphic salamander with simple courtship behaviors. We used four polymorphic microsatellite loci to genotype 57 adults enclosed in a breeding wetland and compared their multilocus profiles to that of 862 embryos collected from the enclosure. The molecular data were used to assign parentage, investigate the mating system, and measure sexual selection intensity. Parentage analyses indicated 36% of dams and 93% of sires were genetically sampled via their gametes but physically unsampled, suggesting that a large number of breeders over-wintered within the enclosure and/or some females released into the enclosure were already inseminated. We used the genetic data to generate estimates of individual reproductive and mating success and we interpret these in light of salamander behavior and sexual selection theory. The incidence of multiple mating in females (86%) was considerably higher than in males (32%) and the standardized variance in mating success was significantly greater in females. The correlations between reproductive and mating success were significant and of similar magnitude between the sexes, indicating that both sexes increased reproductive success through increased mating success. This pattern may be a function of differential opportunities for mating success between the sexes. Electronic Supplementary Material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Genetics of decayed sexual traits in a parasitoid wasp with endosymbiont-induced asexuality

Trait decay may occur when selective pressures shift, owing to changes in environment or life style, rendering formerly adaptive traits non-functional or even maladaptive. It remains largely unknown if such decay would stem from multiple mutations with small effects or rather involve few loci with major phenotypic effects. Here, we investigate the decay of female sexual traits, and the genetic causes thereof, in a transition from haplodiploid sexual reproduction to endosymbiont-induced asexual reproduction in the parasitoid wasp Asobara japonica. We take advantage of the fact that asexual females cured of their endosymbionts produce sons instead of daughters, and that these sons can be crossed with sexual females. By combining behavioral experiments with crosses designed to introgress alleles from the asexual into the sexual genome, we found that sexual attractiveness, mating, egg fertilization and plastic adjustment of offspring sex ratio (in response to variation in local mate competition) are decayed in asexual A. japonica females. Furthermore, introgression experiments revealed that the propensity for cured asexual females to produce only sons (because of decayed sexual attractiveness, mating behavior and/or egg fertilization) is likely caused by recessive genetic effects at a single locus. Recessive effects were also found to cause decay of plastic sex-ratio adjustment under variable levels of local mate competition. Our results suggest that few recessive mutations drive decay of female sexual traits, at least in asexual species deriving from haplodiploid sexual ancestors.     

Assortative mating,sexual selection,and their consequences for gene flow in Littorina

When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple-effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis, occur in North Atlantic rocky-shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size-assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment.     

Body size, age and paternity in common brushtail possums (Trichosurus vulpecula)

Sexual selection should produce sexual size dimorphism in species where larger members of one sex obtain disproportionately more matings. Recent theory suggests that the degree of sexual size dimorphism depends on physical and temporal constraints involving the operational sex ratio, the potential reproductive rate and the trade-off between current reproductive effort and residual reproductive value. As part of a large-scale experiment on dispersal, we investigated the mating system of common brushtail possums inhabiting old-growth Eucalyptus forest in Australia. Paternity was assigned to 20 of 28 pouch-young (maternity known) genotyped at six microsatellite loci. Male mating success was strongly related to body size and age; male body weight and age being highly correlated. Despite disproportionate mating success favouring larger males, sexual size dimorphism was only apparent among older animals. Trapping and telemetry indicated that the operational sex ratio was effectively 1 : 1 and the potential reproductive rate of males was at most four times that of females. Being larger appeared to entail significant survival costs because males 'died-off' at the age at which sexual size dimorphism became apparent (8-9 years). Male and female home ranges were the same size and males appeared to be as sedentary as females. Moreover, longevity appears to be only slightly less important to male reproductive success than it is to females. It is suggested that a sedentary lifestyle and longevity are the key elements constraining selection for greater sexual size dimorphism in this 'model' medium-sized Australian marsupial herbivore.