Sexual selection and mating patterns in a mammal with female-biased sexual size dimorphism

In mammals, species with highly male-biased sexual size dimorphismtend to have high variance in male reproductive success. However,little information is available on patterns of sexual selection,variation in male and female reproductive success, and bodysize and mating success in species with female-biased size dimorphism.We used parentage data from microsatellite DNA loci to examinethese issues in the yellow-pine chipmunk (Tamias amoenus), asmall ground squirrel with female-biased sexual size dimorphism.Chipmunks were monitored over 3 years in the Kananaskis Valley,Alberta, Canada. We found evidence of high levels of multiplepaternity within litters. Variation in male and female reproductivesuccess was equal, and the opportunity for sexual selectionwas only marginally higher in males than females. Male and femalereproductive success both depended on mating success. We foundno evidence that the number of genetic mates a male had dependedon body size. Our results are consistent with a promiscuousmating system in which males and female mate with multiple partners.Low variation in male reproductive success may be a generalfeature of mammalian species in which females are larger thanmales.     

Assortative mating through a mechanism of sexual selection

We propose that assortative mating can arise through a mechanism of sexual selection by active female choice of partners based on a 'self-seeking like' decision rule. Using a mathematical model, we show that a gene can be selected that make females to choose mates that are similar to themselves with respect to an arbitrary tag, even if two independent and unlinked genes determine the preference and the tag. The necessary requisite for this process to apply is an asymmetry between partners, such that the female can choose the male but this one must always accept to mate. The fitness advantage is due to linkage disequilibrium built up between both genes. Simulations have been run to check the algebraic results and to analyse the influence of several factors on the evolution of the system. Any factor that favors linkage disequilibrium also favors the evolution of the preference allele. Moreover, in a large population subdivided in small subpopulations connected by migration, the assortative mating homogenizes the population genotypic structure for the tags in contrast to random mating that maintains most of the variation.     

JMATING: a software for the analysis of sexual selection and sexual isolation effects from mating frequency data

Background  

Many different sexual isolation and sexual selection statistics have been proposed in the past. However, there is no available software that implements all these statistical estimators and their corresponding tests for the study of mating behaviour.     

Polyandry as a mediator of sexual selection before and after mating

The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male''s ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.     

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.     

Mating portfolios: bet-hedging,sexual selection and female multiple mating

Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here, we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most ‘model’ species. In this study, we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.     

Loading constraints sexual selection and assortative mating in peracarid Crustacea

In precopula pairs of amphipod and isopod Crustacea in which males carry females, the males are larger than their mates and mating is size-assortative. Mate-guarding is a product of sexual selection. Size dimorphism and assortative mating have also been attributed to sexual selection but the supporting evidence for amphipods is equivocal. We describe a series of experiments confirming that relatively large male Gammarus pulex L. have an advantage because they can swim against stronger currents when carrying a mate. At higher current speeds, the male/female size ratio which forms is significantly greater, and in field collections size ratios of pairs are higher in streams than in lakes for a number of species. In a simulation we show that a size-assortative pattern inevitably develops if the observed size restriction is used as a rule for pairing. The results are discussed with respect to size-assortative mating, which has been attributed to male selectivity and male-male competition for access to large, fecund females.     

Assortative mating in fallow deer reduces the strength of sexual selection

Background

Assortative mating can help explain how genetic variation for male quality is maintained even in highly polygynous species. Here, we present a longitudinal study examining how female and male ages, as well as male social dominance, affect assortative mating in fallow deer (Dama dama) over 10 years. Assortative mating could help explain the substantial proportion of females that do not mate with prime-aged, high ranking males, despite very high mating skew. We investigated the temporal pattern of female and male matings, and the relationship between female age and the age and dominance of their mates.

Results

The peak of yearling female matings was four days later than the peak for older females. Younger females, and especially yearlings, mated with younger and lower-ranking males than older females. Similarly, young males and lower-ranking males mated with younger females than older males and higher-ranking males. Furthermore, the timing of matings by young males coincided with the peak of yearling female matings, whereas the timing of older male matings (irrespective of rank) coincided with the peak of older female matings.

Conclusions

Assortative mating, through a combination of indirect and/or direct female mate choice, can help explain the persistence of genetic variation for male traits associated with reproductive success.     

A model of sexual selection and female use of refuge in a coercive mating system

In many non-monogamous systems, males invest less in progeny than do females. This leaves males with higher potential rates of reproduction, and a likelihood of sexual conflict, including, in some systems, coercive matings. If coercive matings are costly, the best female strategy may be to avoid male interaction. We present a model that demonstrates female movement in response to male harassment as a mechanism to lower the costs associated with male coercion, and the effect that female movement has on selection in males for male harassment. We found that, when females can move from a habitat patch to a refuge to which males do not have access, there may be a selection for either high, or low harassment male phenotype, or both, depending on the relationship between the harassment level of male types in the population and a threshold level of male harassment. This threshold harassment level depends on the relative number of males and females in the population, and the relative resource values of the habitat; the threshold increases as the sex ratio favours females, and decreases with the value of the refuge patch or total population. Our model predicts that selection will favour the harassment level that lies closest to this threshold level of harassment, and differing harassment levels will coexist within the population only if they lie on the opposite sides of the threshold harassment. Our model is consistent with empirical results suggesting that an intermediate harassment level provides maximum reproductive fitness to males when females are mobile.     

Cytogenetic and genetic evidence of male sexual inversion by heat treatment in the newt Pleurodeles poireti

Larvae of Pleurodeles poireti were maintained during their development at a high temperature (31° C). In several species of amphibians, such a treatment is known to change the sex ratio through the inversion of genotypic females into phenotypic males. Pleurodeles poireti is an exception. It is the first reported amphibian in which heat induces an inversion of genotypic males into functional phenotypic females. The sexual genotype of standard and experimental phenotypic females was determined through heterochromosomes in lampbrush stage. In the present study, we have utilised another technique for identification of sexual genotype, applicable to both phenotypic males and females. It is based on the differential expression of a sexlinked gene, the peptidase 1.     

Polyploidy influences sexual system and mating patterns in the moss Atrichum undulatum sensu lato

Background and Aims

Evolutionary transitions between separate and combined sexes have frequently occurred across various plant lineages. In mosses, which are haploid-dominant, evolutionary transitions from separate to combined sexes are often associated with genome doubling. Polyploidy and hermaphroditism have strong effects on the inbreeding depression of a population, and are subsequently predicted to affect the mating system.

Methods

We tested the association between ploidy (haploid, diploid or triploid gametophytes) and mating system in 21 populations of Atrichum undulatum sensu lato, where sex ratios vary widely. For each population, we measured the sex ratio, estimated selfing rates using allozyme markers and determined the level of ploidy through flow cytometry.

Key Results

Hermaphrodites in A. undulatum were either diploid or triploid. However, many diploid populations were strictly separate-sexed, suggesting that hermaphroditism is not a necessary result of genome doubling. Levels of selfing were strongly supported as being greater than zero in one population with strictly separate-sexed individuals, and one-third of populations with hermaphrodites.

Conclusions

Although hermaphrodites are associated with triploidy, hermaphroditism is not a necessary outcome of genome duplication. Hermaphroditism, but not genome duplication alone, increased estimated selfing rates, probably due to the occurrence of selfing within a gametophyte. Thus, genome duplication can influence the mating system and the associated evolution and maintenance of reproductive traits.     

Age-specific patterns of infection with haemosporidians and trypanosomes in a warbler: implications for sexual selection

Although the selective loss of individuals susceptible to disease can favor the evolution of female preference for older males, the interrelationship between age, infection, longevity, and mating success remains poorly characterized in natural populations. In a longitudinal study of 61 male common yellowthroats (Geothlypis trichas), we found that the probability of infection with hematozoa increased as males aged from 1 to 5 years. Despite a significant, negative association between infection and longevity that partially masked age-effects, the odds that a male was infected with Trypanosoma, Plasmodium, or Leucocytozoon increased 71–212% per year. Nearly 75% of males in their first breeding season were either uninfected or infected with only a single parasite, while 50% of older males were infected with at least two parasites and 16% were infected with all three. No males escaped infection after their second breeding season. Older males were also more likely to sire extra-pair young (EPY) and, as a consequence, infection with multiple parasites was associated with a fourfold increase in the odds of producing EPY. Unlike younger males, 80% of the oldest males had a history of either surviving chronic infection or recovering. Combined with previous work showing higher diversity at the major histocompatibility complex among older males, our results suggest that the song and plumage traits that signal male age in common yellowthroats also, perforce, signal resistance to parasites. By preferring older males, females may obtain good genes for disease resistance even in the absence of any effect of infection on male ornamentation.     

An introduction to genetic quality in the context of sexual selection

This special issue of Genetica brings together empirical researchers and theoreticians to present the latest on the evolutionary ecology of genetic quality in the context of sexual selection. The work comes from different fields of study including behavioral ecology, quantitative genetics and molecular genetics on a diversity of organisms using different approaches from comparative studies, mathematical modeling, field studies and laboratory experiments. The papers presented in this special issue primarily focus on genetic quality in relation to (1) sources of genetic variation, (2) polyandry, (3) new theoretical developments and (4) comprehensive reviews.     

Selfish genetic elements and sexual selection: their impact on male fertility

Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.     

Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection

Bumblebees and other eusocial bees offer a unique opportunity to analyze the evolution of body size differences between sexes. The workers, being sterile females, are not subject to selection for reproductive function and thus provide a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other natural selection. Using a phylogenetic comparative approach, we explored the allometric relationships among queens, males, and workers in 70 species of bumblebees (Bombus sp.). We found hyperallometry in thorax width for males relative to workers, indicating greater evolutionary divergence of body size in males than in sterile females. This is consistent with the hypothesis that selection for reproductive function, most probably sexual selection, has caused divergence in male size among species. The slope for males on workers was significantly steeper than that for queens on workers and the latter did not depart from isometry, providing further evidence of greater evolutionary divergence in male size than female size, and no evidence that reproductive selection has accelerated divergence of females. We did not detect significant hyperallometry when male size was regressed directly on queen size and our results thus add the genus Bombus to the increasing list of clades that have female-larger sexual size dimorphism and do not conform to Rensch's rule when analyzed according to standard methodology. Nevertheless, by using worker size as a common control, we were able to demonstrate that bumblee species do show the evolutionary pattern underlying Rensch's rule, that being correlated evolution of body size in males and females, but with greater evolutionary divergence in males.     

Mating preferences, sexual selection and patterns of cladogenesis in ray-finned fishes

Evolutionary theory predicts that sexual selection may increase taxonomic diversity when emergent mating preferences result in reproductive isolation and therefore speciation. This theory has been invoked to explain patterns of diversity in ray-finned fishes (most notably in the cichlids), but the theory has not been tested comparatively in fish. Additionally, several other unrelated factors have been identified as promoters of cladogenesis, so it is unclear how important sexual selection might be in diversification. Using sister-clade analysis, I tested the relationship between the presence of sexually selected traits and taxonomic diversification in actinopterygiian fishes, a large clade that shows substantial diversity in mating preferences and related sexually selected traits. In all identified sister-families that differed with regard to the proportion of species manifesting sexually selected traits, sexual selection was correlated with increased diversification, and this association was significant across all sister clades (P=0.02). This suggests that sexual selection, when present, is a substantial driver of diversification in the ray-finned fishes, and lends further empirical support to the theoretical link between mating preferences and accelerated cladogenesis.     

Spatial genetic patterns generated by two admixing genetic lineages: a simulation study

Two formerly geographically separated lineages of the zebra mussel Dreissena polymorpha had been given the opportunity to mix extensively across the newly built German Main–Danube canal. We had monitored this admixture of mussel lineages and had described spatial patterns in different genetic measures [Müller et al. 2001 (Heredity, 86: 103); 2002 (Proc. R. Soc. Lond., 269: 1139)]. Here, we present an individual-based model to assess the potential of spatial genetic patterns of detecting and quantifying admixture of mussel lineages. Genetic measures studied are (1) allele frequencies, (2) deviations from Hardy–Weinberg expectations of loci (deficit of heterozygotes, HWD) and (3) linkage disequilibria between unlinked loci (LD). For allele frequencies, we observed a cline over the zone of admixture in all simulations of mixing mussel lineages suggesting that these are appropriate for verification of their mixture. The point of the first contact between lineages was always detectable from their intermediate allele frequencies. LD and HWD were only spatially informative for diagnostic loci or loci with very strong differences in allele frequencies of lineages. For such loci, the probability of disequilibria was highest where lineages had met and decreased towards both sources of lineages Main and Danube. The overall probability of detecting any disequilibrium was higher for LD than for HWD and increased with an increasing rate of genetic interchange. Our simulation results are corroborated by our zebra mussel data and studies from literature. They are applicable to any case of two known linearly mixing genetic lineages.