Quantitative genetic models of sexual selection by male choice

There are many examples of male mate choice for female traits that tend to be associated with high fertility. I develop quantitative genetic models of a female trait and a male preference to show when such a male preference can evolve. I find that a disagreement between the fertility maximum and the viability maximum of the female trait is necessary for directional male preference (preference for extreme female trait values) to evolve. Moreover, when there is a shortage of available male partners or variance in male nongenetic quality, strong male preference can evolve. Furthermore, I also show that males evolve to exhibit a stronger preference for females that are more feminine (less resemblance to males) than the average female when there is a sexual dimorphism caused by fertility selection which acts only on females.     

Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics

Female remating rate dictates the level of sperm competition in a population, and extensive research has focused on how sperm competition generates selection on male ejaculate allocation. Yet the way ejaculate allocation strategies in turn generate selection on female remating rates, which ultimately influence levels of sperm competition, has received much less consideration despite increasing evidence that both mating itself and ejaculate traits affect multiple components of female fitness. Here, we develop theory to examine how the effects of mating on female fertility, fecundity and mortality interact to generate selection on female remating rate. When males produce more fertile ejaculates, females are selected to mate less frequently, thus decreasing levels of sperm competition. This could in turn favour decreased male ejaculate allocation, which could subsequently lead to higher female remating. When remating simultaneously increases female fecundity and mortality, females are selected to mate more frequently, thus exacerbating sperm competition and favouring male traits that convey a competitive advantage even when harmful to female survival. While intuitive when considered separately, these predictions demonstrate the potential for complex coevolutionary dynamics between male ejaculate expenditure and female remating rate, and the correlated evolution of multiple male and female reproductive traits affecting mating, fertility and fecundity.     

Fertility and viability at the Sod locus in Drosophila melanogaster: non-additive and asymmetric selection

Experiments were designed to test in Drosophila melanogaster the effect of mating type at the Sod locus on fertility and viability. The experiments show that fertility is neither additive (or multiplicative) nor symmetric, i.e. that the fertility of a mating type cannot be predicted from the average fertility of the two genotypes involved in the mating. There is no significant male x female interaction with respect or progeny viability; but the interaction is significant for productivity, i.e. when fertility and viability are jointly taken into account. There is overdominance with respect to female fertility, but not with respect to male fertility or to viability. There also is alloprocoptic selection with respect to fertility and with respect to productivity, i.e. mating between like homozygotes are less fertile and productive than matings between dissimilar homozygotes. Selection at the Sod locus yields stable polymorphic equilibria, with the frequency of the F allele predicted at P = 0.641 or 0.695, respectively for low and high larval density.     

Gynodioecy to dioecy: are we there yet?

Background

The ‘gynodioecy–dioecy pathway’ is considered to be one of the most important evolutionary routes from hermaphroditism to separate sexes (dioecy). Despite a large accumulation of evidence for female seed fertility advantages in gynodioecious species (females and hermaphrodites coexist) in support of the first step in the gynodioecy–dioecy pathway, we still have very little evidence for the second step, i.e. the transition from gynodioecy to dioecy.

Scope

We review the literature to evaluate whether basic predictions by theory are supported. To establish whether females'' seed fertility advantage and frequencies are sufficient to favour the invasion of males, we review these for species along the gynodioecy–dioecy pathway published in the last 5 years. We then review the empirical evidence for predictions deriving from the second step, i.e. hermaphrodites'' male fertility increases with female frequency, selection favours greater male fertility in hermaphrodites in gynodioecious species, and, where males and hermaphrodites coexist with females (subdioecy), males have greater male fertility than hermaphrodites. We review how genetic control and certain ecological features (pollen limitation, selfing, plasticity in sex expression and antagonists) influence the trajectory of a population along the gynodioecy–dioecy pathway.

Conclusions

Females tend to have greater seed fertility advantages over hermaphrodites where the two coexist, and this advantage is positively correlated with female frequency across species, as predicted by theory. A limited number of studies in subdioecious species have demonstrated that males have an advantage over hermaphrodites, as also predicted by theory. However, less evidence exists for phenotypic selection to increase male traits of hermaphrodites or for increasing male function of hermaphrodites in populations with high female frequency. A few key case studies underline the importance of examining multiple components of male fertility and the roles of pollen limitation, selfing and plasticity, when evaluating advantages. We conclude that we do not yet have a full understanding of the transition from gynodioecy to dioecy.     

IDENTIFICATION OF GENETICALLY LINKED FEMALE PREFERENCE AND MALE TRAIT

Genetic variation in male traits and the female preferences for those traits allows for the evolution of sexual behavior. Trait–preference combinations are thought to improve the effectiveness of runaway sexual selection within a species, and are considered necessary for the induction of divergence between species. Novel traits, or variants of existing traits, and their associated preferences in the opposite sex are more likely to be maintained if they are genetically linked in proximity on a chromosome (the genetic coupling hypothesis), yet there is little empirical evidence that this genetic linkage occurs. Here we show for the first time that natural genetic variation at a single‐linked region can induce both species‐specific female choosiness and the male trait they are discriminating against. We found this effect in two separate regions of the genome, demonstrating that this linkage may be common. In contrast, female choosiness and male unattractiveness could not be alleviated by a single region. The close linkage of these loci and the strength of their effect provide an evolutionary means by which this preference–trait combination could arise and be maintained, thus enabling a more rapid route for runaway sexual selection, and providing empirical evidence supporting the genetic coupling hypothesis.     

A review of some factors affecting the expression of libido in beef cattle, and individual bull and herd fertility

This paper examines some of the factors that affect the expression of libido in beef cattle, focusing on the male and the free-ranging situation. The ways in which bull libido is assessed and the relationship between libido test results and fertility are discussed. Genetics play a role in determining libido, but there are many environmental factors affecting its expression, and a number of these factors influence sexual activity in both tests of libido and paddock mating. Herd fertility is multi-factorial and, consequently, it is difficult to draw definitive conclusions about the relationship between libido and fertility. Multiple males increase the expression of libido, but it is uncertain whether this translates into improvements in herd fertility. However, there are consequences for individual bull fertility, as there is ample evidence of inherent differences between bulls. Male:female ratios appear to have minor effects on libido and fertility. Anecdotal evidence indicates that multiple matings with the same or different bulls may reduce the duration of oestrus. Social relationships between bulls can affect the expression of libido, with subordinate bulls being inhibited by the presence of dominant bulls. There is evidence that dominant bulls may achieve more matings at pasture, but this is not necessarily shown in their fertility. Older bulls show greater expression of libido in tests and appear more efficient in serving, although these changes may reflect greater sexual experience. Provided bulls are sexually mature and physically able to mate, age per se appears not to affect fertility, but age interacts with dominance, which can influence fertility. There is evidence of breed differences in expression of libido, but this appears not to be demonstrated in fertility. There is anecdotal evidence that bulls and females prefer to mate with similar genotypes/phenotypes with implications for fertility. Limited research on thermal and nutritional effects indicate some adverse consequences for libido of climatic extremes for unadapted bulls and of over-feeding, but not under-feeding. Limited research has investigated the effects on libido and fertility of multiple stressors associated with relocation; relocation to dramatically different environments has long-lasting detrimental consequences for fertility. Too few studies have been conducted to draw conclusions about the effects of topography and herd dispersion on libido and fertility. Temperament is likely to affect the expression of libido when animals are put into new situations, but this has not been critically researched. In the light of this review, the implications for managing cattle to optimise fertility are discussed and suggestions made as to areas where further research is needed.     

Environmental and genetic variation factors of artificial insemination success in French dairy sheep

Artificial inseminations (n = 678 168) recorded during 5 years in five French artificial insemination (AI) centres (2 'Lacaune', 1 'Manech tête rousse', 1 'Manech tête noire' and 1 'Basco béarnaise') were analysed to determine environmental and genetic factors affecting the insemination results. Analyses within centre-breed were performed using a linear model, which jointly estimates male and female fertility. This model combined four categories of data: the environmental effects related to the female, those related to the male, the non-sex-specific effects and finally the pedigree data of these males and females. After selection, the environmental female effects considered were age, synchronisation (0/1) on the previous year, total number of synchronisations during the female reproductive life, time interval between previous lambing and insemination, already dry or still lactating (0/1) when inseminated, and milk quantity produced during the previous year expressed as quartiles intra herd * year. The environmental male effects were motility and concentration of the semen. The non-sex-specific effects were the inseminator, the interaction herd * year nested within the inseminator, considered as random effects and the interaction year * season considered as a fixed effect. The main variation factors of AI success were relative to non-sex-specific effects and to female effects. Heritability estimates varied from 0.001 to 0.005 for male fertility and from 0.040 to 0.078 for female fertility. Repeatability estimates varied from 0.007 to 0.015 for male fertility and from 0.104 to 0.136 for female fertility. These parameters indicate that genetic improvement of AI results through a classical polygenic selection would be difficult. Moreover, in spite of the large quantity of variation factors fitted by the joint model, a very large residual variance remained unexplained.     

Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly

Inbreeding depression is most pronounced for traits closely associated with fitness. The traditional explanation is that natural selection eliminates deleterious mutations with additive or dominant effects more effectively than recessive mutations, leading to directional dominance for traits subject to strong directional selection. Here we report the unexpected finding that, in the butterfly Bicyclus anynana, male sterility contributes disproportionately to inbreeding depression for fitness (complete sterility in about half the sons from brother-sister matings), while female fertility is insensitive to inbreeding. The contrast between the sexes for functionally equivalent traits is inconsistent with standard selection arguments, and suggests that trait-specific developmental properties and cryptic selection play crucial roles in shaping genetic architecture. There is evidence that spermatogenesis is less developmentally stable than oogenesis, though the unusually high male fertility load in B. anynana additionally suggests the operation of complex selection maintaining male sterility recessives. Analysis of the precise causes of inbreeding depression will be needed to generate a model that reliably explains variation in directional dominance and reconciles the gap between observed and expected genetic loads carried by populations. This challenging evolutionary puzzle should stimulate work on the occurrence and causes of sex differences in fertility load.     

Factors affecting captive whooping crane egg fertility: A retrospective analysis

The whooping crane (Grus americana) has been managed in captivity since the 1960s following a substantial genetic bottleneck in the wild population. Through major ex situ conservation efforts, there are 158 whooping cranes managed in North American institutions and chicks are released annually into the wild. Current reintroduction goals for the whooping crane however, are impeded by poor reproduction within the ex situ population, in part because of low egg fertility. Development of improved management techniques to overcome low egg fertility requires a better understanding of factors that influence egg fertility. We collected data for eggs laid at Patuxent Wildlife Research Center from 2005–2014 (n = 438 eggs; n = 23 pairs). We constructed 5 sets of generalized linear mixed-models, with a Bernoulli-distributed response variable (fertile or infertile), to address the effects of egg-specific variables (month laid, sequence, and clutch order of the egg), life-history events of the male and female (age, rearing method, wing condition, age at first pairing, age at current pairing, and female age at first laying), pair-specific characteristics (kinship, years paired, chick-rearing experience, and previous pairings), and captive management decisions (inclusion in the artificial insemination program and pair experience chick-rearing) on the probability of egg fertility. Our results indicate that female-specific factors (especially age, age at current pairing, and wing status) and pair-specific factors of kinship, chick-rearing experience, copulation, and inclusion in the artificial insemination program influenced fertile egg production. Specifically, the younger a female is when paired with her current social mate, the higher probability that her eggs will be fertile. Furthermore, high kinship reduced fertility, whereas chick-rearing experience and artificial insemination of females with a donor male other than her social mate increased fertility. Further research on mate selection and reproductive mechanisms is needed to better understand egg laying and egg fertility in the whooping crane. © 2019 The Wildlife Society.     

Reversal of female mate choice by copying in the guppy (Poecilia reticulata).

Ever since Fisher (1958) formalized models of sexual selection, female mate choice has been assumed to be a genetically determined trait. Females, however, may also use social cues to select mates. One such cue might be the mate choice of conspecifics. Here we report the first direct evidence that a female's preference for a particular male can in fact be reversed by social cues. In our experiments using the Trinidadian guppy (Poecilia reticulata), this reversal was mediated by mate-copying opportunities, such that a female (the 'focal' female) is given the opportunity to choose between two males, followed by a period in which she observes a second female (the 'model' female) displaying a preference for the male she herself did not prefer initially. When allowed to choose between the same males a second time, compared with control tests, a significant proportion of focal females reversed their mate choice and copied the preference of the model female. These results provide strong evidence for the role of non-genetic factors in sexual selection and underlie the need for new models of sexual selection that explicitly incorporate both genetic and cultural aspects of mate choice.     

Mate Choice and the Origin of Menopause

Human menopause is an unsolved evolutionary puzzle, and relationships among the factors that produced it remain understood poorly. Classic theory, involving a one-sex (female) model of human demography, suggests that genes imparting deleterious effects on post-reproductive survival will accumulate. Thus, a ‘death barrier’ should emerge beyond the maximum age for female reproduction. Under this scenario, few women would experience menopause (decreased fertility with continued survival) because few would survive much longer than they reproduced. However, no death barrier is observed in human populations. Subsequent theoretical research has shown that two-sex models, including male fertility at older ages, avoid the death barrier. Here we use a stochastic, two-sex computational model implemented by computer simulation to show how male mating preference for younger females could lead to the accumulation of mutations deleterious to female fertility and thus produce a menopausal period. Our model requires neither the initial assumption of a decline in older female fertility nor the effects of inclusive fitness through which older, non-reproducing women assist in the reproductive efforts of younger women. Our model helps to explain why such effects, observed in many societies, may be insufficient factors in elucidating the origin of menopause.     

Socially transmitted mate preferences in a monogamous bird: a non-genetic mechanism of sexual selection

There is increasing evidence that animals can acquire mate preferences through the use of public information, notably by observing (and copying) the mate preferences of others in the population. If females acquire preferences through social mechanisms, sexual selection could act very rapidly to spread the preference and drive elaboration of the preferred trait(s). Although there are reports of 'mate-choice copying' in polygynous species, there is no clear evidence for this process in monogamous species. Here, we investigated whether adult female zebra finches Taeniopygia guttata can socially acquire sexual preferences for individual males and, in a separate study, for a generalized trait (coloured leg bands) of males. In both studies, test females observed males in two simultaneous conditions: a ('chosen') mixed-sex situation in which a male was paired with a (model) female, and a ('unchosen') same-sex situation in which a male was paired with another male. In the first experiment, after two weeks of females observing males, test females significantly preferred individual males who had been paired with another female (i.e. chosen males). In the second experiment, test females significantly preferred novel males that were wearing the same leg band colour as the apparently chosen males. Our findings are consistent with the conclusion that female zebra finches' mate preferences are altered by public information. Our study implies that mate preferences can spread rapidly through populations by social mechanisms, affecting the strength of sexual selection in a monogamous species.     

LIFETIME REPRODUCTIVE SUCCESS AND THE OPPORTUNITY FOR SELECTION IN A NONTERRITORIAL DAMSELFLY (ODONATA: COENAGRIONIDAE)

Major components of male and female lifetime reproductive success (LRS) were quantified for a damselfly that exhibits “scramble competition” for mates. The opportunity for selection on male reproduction was potentially 2.9 times that for females. Differential fertility/clutch and survivorship each accounted for about half of the total variation in female reproductive success. Variation in fertilization efficiency accounted for 7% of the total opportunity for selection on males. Although differences in survivorship and mating efficiency each contributed to about a third of the total opportunity for selection on male reproduction, both components appeared to be influenced by random factors. Survivorship was age-independent, and the mating distributions among males with equal mating opportunities were indistinguishable from those expected if matings were random with respect to male phenotype. Because the proportion of the standarized variance (I) in LRS that was attributed to sexual selection depended on the way the selective episodes were defined, the sample of individuals included in the partitioning analysis, and the degree of sexual selection on mated males that could be detected, my results caution against drawing conclusions about the dynamics of sexual selection on populations based on a superficial comparison of I values.     

Selection on floral characters in natural Spanish populations of Silene latifolia

In insect-pollinated plants, floral characters are expected to play an important role in paternal and maternal reproductive success. Bateman's principle states that male reproductive success increases with more mating opportunities, while female reproductive success is limited by the amount of resources available to produce progeny, thus there should be greater selection on male floral characters than on female. In the case of the dioecious plant Silene latifolia, floral characters are likely to be influenced by its association within its native European range with moths of the genus Hadena, which serve as both pollinators and seed predators. The present study addresses relationships between male and female reproductive success, spatial location and floral characters (corolla, calyx and claw) over a 2-year period in two Spanish populations of S. latifolia in the presence of Hadena moths. A maximum likelihood paternity analysis using genetic variation at six allozyme markers showed heterogeneity in male reproductive success. There was much less variation in female reproductive success. When this analysis was extended to include interplant distance as a causal factor underlying variation in male success, we found that successful pollination tended to be limited to nearby females, in accordance with exponential decay of pollen dispersal with increasing distance. When the paternity analysis included floral characters as a causal factor underlying variation in male success, our data showed little evidence for directional selection, but there was stabilizing selection in one of the two years for calyx diameter. Selection on female characters varied widely between sites and years, in most of the site/year combinations there was little selection on female floral characters; however, in one site/year there was evidence for selection on all three floral characters. We conclude that pollinators visit flowers that are close together, and that while floral characters are important for the attraction of pollinators, larger flowers do not necessarily attract more pollinators at all sites and that variation among sites and years makes difficult any conclusions about the long-term importance of the predictions suggested by Bateman's principle.     

Evolution at HLA: possible explanations for the deficiency of homozygotes in two populations

There is substantial evidence that some form of balancing selection is important for loci in the HLA region. Two classic studies found a large deficiency of homozygotes for these loci. Four possible proposed selective explanations were proposed: (1) heterozygous advantage; (2) linked lethal; (3) maternal-fetal interaction, and (4) resistance to infectious disease. These hypotheses as well as another explanation, different male and female gametic frequencies, have been examined here to try and evaluate their potential impact on genotypic frequencies. For any of these selective mechanisms to alone account for the observed homozygous deficiency, selection and/or others factors would have to be extremely strong. The linked lethal selection model and the hypothesis based on different male and female gametic frequencies appear to be unlikely explanations for these observations. Other factors that may influence genotypic frequencies are also discussed.     

Antlers honestly advertise sperm production and quality

Evolutionary theory proposes that exaggerated male traits have evolved via sexual selection, either through female mate choice or male-male competition. While female preferences for ornamented males have been amply demonstrated in other taxa, among mammals sexual characters are commonly regarded as weapons whose main function is to enhance male competitiveness in agonistic encounters. One particularly controversial hypothesis to explain the function of male sexual characters proposes that they advertise male fertility. We test this hypothesis in red deer (Cervus elaphus), a species where sexual characters (antlers) reach an extreme degree of elaboration. We find that a global measure of relative antler size and complexity is associated with relative testes size and sperm velocity. Our results exclude the possibility that condition dependence, age or time of culling, drive these associations. Red deer antlers could signal male fertility to females, the ability to avoid sperm depletion throughout the reproductive season and/or the competitive ability of ejaculates. By contrast, male antlers could also signal to other males not only their competitive ability at the behavioural level (fighting ability) but also at the physiological level (sperm competition).     

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.     

A QTL analysis of female variation contributing to refractoriness and sperm competition in Drosophila melanogaster

Sperm competition is an important fitness component in many animal groups. Drosophila melanogaster males exhibit substantial genetic variation for sperm competitive ability and females show considerable genetic variation for first versus second male sperm use. Currently, the forces responsible for maintaining genetic variation in sperm competition related phenotypes are receiving much attention. While several candidate genes contributing to the variation seen in male competitive ability are known, genes involved in female sperm use remain largely undiscovered. Without knowledge of the underlying genes, it will be difficult to distinguish between different models of sexual selection such as cryptic female choice and sexual conflict. We used quantitative trait locus (QTL) mapping to identify regions of the genome contributing to female propensity to use first or second male sperm, female refractoriness to re-mating, and early-life fertility. The most well supported markers influencing the phenotypes include 33F/34A (P2), 57B (refractoriness) and 23F/24A (fertility). Between 10% and 15% of the phenotypic variance observed in these recombinant inbred lines was explained by these individual QTLs. More detailed investigation of the regions detected in this experiment may lead to the identification of genes responsible for the QTLs identified here.     

Sex allocation in clonal plants: might clonal expansion enhance fitness gains through male function?

The returns on investment in sexual reproduction are described by fitness gain curves and the shapes of these curves affect, among other things, the evolutionary stability of reproductive systems. The available evidence indicates that gain curves for male function decelerate, corresponding to diminishing fitness returns on investment in pollen. In contrast, the gain curve for female function is thought to decelerate less strongly than it does for male function (e.g., if seed fertility is limited by more by resources than by mating opportunities). Here we suggest that when the shapes of the female and male gain curves differ, clonality alters the rates of return on investment via the two sex functions. In particular, we propose that clonal expansion might increase fitness gains through male function because the subdivision of reproductive effort among ramets allows each ramet to take advantage of the steepest parts of the male gain curve. We examined the interaction between clonal expansion and fitness gains using numerical analysis of a model of sex allocation in which we assumed that there is no mating interference among ramets. We found that clonal expansion led to substantial increases in fitness through male function, but to decreases in fitness through female function. Under intermediate investment in clonal growth, marginal fertility gains through the two sex functions did not intersect over a broad range of sex allocation patterns, suggesting that clonality could favor the evolution of separate sexes. Finally, we suggest an alternative explanation for the common observation of male-biased sex ratios in clonal dioecious plants. If male function fitness is maximized under higher rates of clonal expansion than for female function, greater frequencies of male ramets might reflect the outcome of fertility selection, rather than constraints on clonal expansion imposed by greater costs of reproduction for females.     

Do male secondary sexual characters signal ejaculate quality? A meta‐analysis

There are two reasons why researchers are interested in the phenotypic relationship between the expression of male secondary sexual characters (SSCs) and ‘ejaculate quality’ (defined as sperm/ejaculate traits that are widely assumed to increase female fertility and/or sperm competitiveness). First, if the relationship is positive then females could gain a direct benefit by choosing more attractive males for fertility assurance reasons (‘the phenotype‐linked fertility’ hypothesis). Second, there is much interest in the direction of the correlation between traits favoured by pre‐copulatory sexual selection (i.e. affecting mating success) and those favoured by post‐copulatory sexual selection (i.e. increasing sperm competitiveness). If the relationship is negative this could lead to the two forms of selection counteracting each other. Theory predicts that the direction of the relationship could be either positive or negative depending on the underlying genetic variance and covariance in each trait, the extent of variation among males in condition (resources available to allocate to reproductive traits), and variation among males in the cost or rate of mating. We conducted a meta‐analysis to determine the average relationship between the expression of behavioural and morphological male secondary sexual characters and four assays of ejaculate quality (sperm number, viability, swimming speed and size). Regardless of how the data were partitioned the mean relationship was consistently positive, but always statistically non‐significant. The only exception was that secondary sexual character expression was weakly but significantly positively correlated with sperm viability (r = 0.07, P < 0.05). There was no significant difference in the strength or direction of the relationship between behavioural and morphological SSCs, nor among relationships using the four ejaculate quality assays. The implications of our findings are discussed.