Inbreeding alters intersexual fitness correlations in Drosophila simulans.

Intralocus sexual conflict results from sexually antagonistic selection on traits shared by the sexes. This can displace males and females from their respective fitness optima, and negative intersexual correlations (r_mf) for fitness are the unequivocal indicator of this evolutionary conflict. It has recently been suggested that intersexual fitness correlations can vary depending on the segregating genetic variation present in a population, and one way to alter genetic variation and test this idea is via inbreeding. Here, we test whether intersexual correlations for fitness vary with inbreeding in Drosophila simulans isolines reared under homogenous conditions. We measured male and female fitness at different times following the establishment of isofemale lines and found that the sign of the association between the two measures varied with time after initial inbreeding. Our results are consistent with suggestions that the type of genetic variation segregating within a population can determine the extent of intralocus sexual conflict and also support the idea that sexually antagonistic alleles segregate for longer in populations than alleles with sexually concordant effects.     

Possible Balancing Selection in Human Female Homosexuality

A growing number of researchers suggest that female homosexuality is at least in part influenced by genetic factors. Unlike for male homosexuality, few familial studies have attempted to explore maintenance of this apparently fitness-detrimental trait in the population. Using multiple recruitment methods, we explored fecundity and sexual orientation within the pedigrees of 1,458 adult female respondents. We compared 487 homosexual and 163 bisexual with 808 heterosexual females and 30,203 of their relatives. Our data suggest that the direct fitness of homosexual females is four times lower than the direct fitness of heterosexual females of corresponding ages. The prevalence of nonheterosexuality within the homosexual female respondents’ families (2.83%) appear to be more than four times higher than the basal prevalence in the Italian population (0.63%). Pedigree size and relative fecundity in both the paternal and maternal sides of the homosexual women’s families were significantly higher than in the heterosexuals’ families. If confirmed, the relative average fecundity increase within the family seems to offset the loss in fitness due to the low direct fitness of homosexual females. Therefore, the balanced fecundity in the homosexual females’ families may allow the trait to be maintained at a low-frequency equilibrium in the population.     

Genetic variation in a female genital trait evolved by sexual coevolution

Understanding the patterns of genetic variation of traits subject to sexual selection is fundamental for explaining its evolutionary dynamics and potential for sexual coevolution. The signa of female Lepidoptera are sclerotized structures located on the inner surface of the genital receptacle that receives the spermatophore during copulation (the corpus bursae), whose main function is tearing the spermatophore envelope. Comparative data indicate that the evolution of signa has been influenced by sexually antagonistic coevolution with spermatophore envelopes. We looked for additive genetic variation in the size and shape of signa in females of the butterfly Callophrys xami (Lycaenidae) from two localities (BG and FC) in Mexico City. We also looked for genetic variation in female body size and in the size of corpus bursae. There were significant between-population differences in female body size, signa width and three signa shape traits. We found significant extranuclear maternal effects in one component of signa shape in the BG population, and in body weight, signa length and in one uniform component of signa shape in the FC population. Extranuclear maternal contributions could permit the evolution of female adaptations even if these reduce male fitness. We found additive genetic variation in signa length and width only in one population (BG); heritability estimates were high: 0.96 and 0.8, respectively. The existence of additive genetic variation in signa size could be, at least in part, a result of relaxed sexually antagonistic selection pressures due to the low level of polyandry exhibited by this species. Our results imply that there is currently potential for further sexual coevolution in this trait.     

SELECTION FOR ALTERNATIVE MALE REPRODUCTIVE TACTICS ALTERS INTRALOCUS SEXUAL CONFLICT

Intralocus sexual conflict (IASC) arises when fitness optima for a shared trait differ between the sexes; such conflict may help maintain genetic variation within populations. Sex‐limited expression of sexually antagonistic traits may help resolve the conflict, but the extent of this resolution remains a subject of debate. In species with alternative male reproductive tactics, unresolved conflict should manifest more in a more sexually dimorphic male phenotype. We tested this prediction in the bulb mite (Rhizoglyphus robini), a species in which aggressive fighters coexist with benign scramblers. To do this, we established replicated lines in which we increased the proportion of each of the alternative male morphs using artificial selection. After approximately 40 generations, the proportion of fighters and scramblers stabilized at >0.9 in fighter‐ and scrambler‐selected lines, respectively. We then measured several female fitness components. As predicted by IASC theory, female fecundity and longevity were lower in lines selected for fighters and higher in lines selected for scramblers. This finding indicates that sexually selected phenotypes are associated with an ontogenetic conflict that is not easily resolved. Furthermore, we suggest that IASC may be an important mechanism contributing to the maintenance of genetic variation in the expression of alternative reproductive tactics.     

Androgenesis is a maternal trait in the invasive ant Wasmannia auropunctata

Androgenesis is the production of an offspring containing exclusively the nuclear genome of the fathering male via the maternal eggs. This unusual mating system is generally considered a male trait, giving to androgenetic males a substantial fitness advantage over their sexually reproducing relatives. We here provide the first empirical study of the evolutionary outcomes of androgenesis in a haplo-diploid organism: the invasive ant Wasmannia auropunctata. Some of the populations of this species have a classical haplo-diploid sexual mating system. In other populations, females and males are produced through parthenogenesis and androgenesis, respectively, whereas workers are produced sexually. We conducted laboratory reciprocal-cross experiments with reproductive individuals from both types of populations and analysed their progenies with genetic markers, to determine the respective contribution of males and females to the production of androgenetic males. We found that androgenesis was a parthenogenetic female trait. A population genetic study conducted in natura confirmed the parthenogenetic female origin of androgenesis, with the identification of introgression events of sexual male genotypes into androgenetic/parthenogenetic lineages. We argue that by producing males via androgenesis, parthenogenetic queen lineages may increase and/or maintain their adaptive potential, while maintaining the integrity of their own genome, by occasionally acquiring new male genetic material and avoiding inbreeding depression within the sexually produced worker cast.     

A test of genetic models for the evolutionary maintenance of same-sex sexual behaviour

The evolutionary maintenance of same-sex sexual behaviour (SSB) has received increasing attention because it is perceived to be an evolutionary paradox. The genetic basis of SSB is almost wholly unknown in non-human animals, though this is key to understanding its persistence. Recent theoretical work has yielded broadly applicable predictions centred on two genetic models for SSB: overdominance and sexual antagonism. Using Drosophila melanogaster, we assayed natural genetic variation for male SSB and empirically tested predictions about the mode of inheritance and fitness consequences of alleles influencing its expression. We screened 50 inbred lines derived from a wild population for male–male courtship and copulation behaviour, and examined crosses between the lines for evidence of overdominance and antagonistic fecundity selection. Consistent variation among lines revealed heritable genetic variation for SSB, but the nature of the genetic variation was complex. Phenotypic and fitness variation was consistent with expectations under overdominance, although predictions of the sexual antagonism model were also supported. We found an unexpected and strong paternal effect on the expression of SSB, suggesting possible Y-linkage of the trait. Our results inform evolutionary genetic mechanisms that might maintain low but persistently observed levels of male SSB in D. melanogaster, but highlight a need for broader taxonomic representation in studies of its evolutionary causes.     

The role of maternal and paternal effects in the evolution of parental quality by sexual selection

Genetic models of maternal effects and models of mate choice have focused on the evolutionary effects of variation in parental quality. There have been, however, few attempts to combine these into a single model for the evolution of sexually selected traits. We present a quantitative genetic model that considers how male and female parental quality (together or separately) affect the expression of a sexually selected offspring trait. We allow female choice of males based on this parentally affected trait and examine the evolution of mate choice, parental quality and the indicator trait. Our model reveals a number of consequences of maternal and paternal effects. (1) The force of sexual selection owing to adaptive mate choice can displace parental quality from its natural selection optimum. (2) The force of sexual selection can displace female parental quality from its natural selection optimum even when nonadaptive mate choice occurs (e.g. runaway sexual selection), because females of higher parental quality produce more attractive sons and these sons counterbalance the loss in fitness owing to over-investment in each offspring. (3) Maternal and paternal effects can provide a source of genetic variation for offspring traits, allowing evolution by sexual selection even when those traits do not show direct genetic variation (i.e. are not heritable). (4) The correlation between paternal investment and the offspring trait influenced by the parental effects can result in adaptive mate choice and lead to the elaboration of both female preference and the male sexually selected trait. When parental effects exist, sexual selection can drive the evolution of parental quality when investment increases the attractiveness of offspring, leading to the elaboration of indicator traits and higher than expected levels of parental investment.     

The contribution of the mitochondrial genome to sex‐specific fitness variance

Maternal inheritance of mitochondrial DNA (mtDNA) facilitates the evolutionary accumulation of mutations with sex‐biased fitness effects. Whereas maternal inheritance closely aligns mtDNA evolution with natural selection in females, it makes it indifferent to evolutionary changes that exclusively benefit males. The constrained response of mtDNA to selection in males can lead to asymmetries in the relative contributions of mitochondrial genes to female versus male fitness variation. Here, we examine the impact of genetic drift and the distribution of fitness effects (DFE) among mutations—including the correlation of mutant fitness effects between the sexes—on mitochondrial genetic variation for fitness. We show how drift, genetic correlations, and skewness of the DFE determine the relative contributions of mitochondrial genes to male versus female fitness variance. When mutant fitness effects are weakly correlated between the sexes, and the effective population size is large, mitochondrial genes should contribute much more to male than to female fitness variance. In contrast, high fitness correlations and small population sizes tend to equalize the contributions of mitochondrial genes to female versus male variance. We discuss implications of these results for the evolution of mitochondrial genome diversity and the genetic architecture of female and male fitness.     

Evidence for maternally inherited factors favouring male homosexuality and promoting female fecundity

The Darwinian paradox of male homosexuality in humans is examined, i.e. if male homosexuality has a genetic component and homosexuals reproduce less than heterosexuals, then why is this trait maintained in the population? In a sample of 98 homosexual and 100 heterosexual men and their relatives (a total of over 4600 individuals), we found that female maternal relatives of homosexuals have higher fecundity than female maternal relatives of heterosexuals and that this difference is not found in female paternal relatives. The study confirms previous reports, in particular that homosexuals have more maternal than paternal male homosexual relatives, that homosexual males are more often later-born than first-born and that they have more older brothers than older sisters. We discuss the findings and their implications for current research on male homosexuality.     

Early determinants of lifetime reproductive success differ between the sexes in red deer.

In polygynous, sexually dimorphic species, sexual selection should be stronger in males than in females. Although this prediction extends to the effects of early development on fitness, few studies have documented early determinants of lifetime reproductive success in a natural mammal population. In this paper, we describe factors affecting the reproductive success of male and female red deer (Cervus elaphus) on the island of Rum, Scotland. Birthweight was a significant determinant of total lifetime reproductive success in males, with heavier-born males being more successful than lighter ones. In contrast, birthweight did not affect female reproductive success. High population density and cold spring temperatures in the year of birth decreased several components of fitness in females, but did not affect the breeding success of males. The results confirm the prediction that selection on a sexually dimorphic trait should be greater in males than in females, and explain the differential maternal expenditure between sons and daughters observed in red deer. Differences between the sexes in the effects of environmental and phenotypic variation on fitness may generate differences in the amount of heritable genetic variation underlying traits such as birthweight.     

The evolution of sexually selected traits and antagonistic androgen expression in actinopterygiian fishes

Many sexually selected traits in male fishes are controlled by testosterone. Directional selection for male ornaments could theoretically increase male testosterone levels over evolutionary timescales, and when genetically correlated, female testosterone levels as well. Because of the negative fitness consequences of high testosterone, it is plausible that female choice for sexually selected traits in males results in decreased female reproductive fitness. I used comparative analysis to examine the association between male peak testosterone expression and sexually selected ornaments. I also tested for genetic correlation between male and female androgen levels. The presence of sexually selected traits in males was significantly correlated with increased peak androgen levels in males as well as females, and female testosterone levels were significantly correlated with male peak testosterone titers, although the slope was only marginally <1. This suggests that selection to decouple high male and female testosterone levels is either weak or otherwise ineffective.     

Very low levels of direct additive genetic variance in fitness and fitness components in a red squirrel population

A trait must genetically correlate with fitness in order to evolve in response to natural selection, but theory suggests that strong directional selection should erode additive genetic variance in fitness and limit future evolutionary potential. Balancing selection has been proposed as a mechanism that could maintain genetic variance if fitness components trade off with one another and has been invoked to account for empirical observations of higher levels of additive genetic variance in fitness components than would be expected from mutation–selection balance. Here, we used a long‐term study of an individually marked population of North American red squirrels (Tamiasciurus hudsonicus) to look for evidence of (1) additive genetic variance in lifetime reproductive success and (2) fitness trade‐offs between fitness components, such as male and female fitness or fitness in high‐ and low‐resource environments. “Animal model” analyses of a multigenerational pedigree revealed modest maternal effects on fitness, but very low levels of additive genetic variance in lifetime reproductive success overall as well as fitness measures within each sex and environment. It therefore appears that there are very low levels of direct genetic variance in fitness and fitness components in red squirrels to facilitate contemporary adaptation in this population.     

Sexually selected male weapon is associated with lower inbreeding load but higher sex load in the bulb mite

Elaborate sexually selected ornaments and armaments are costly but increase the reproductive success of their bearers (usually males). It has been postulated that high-quality males can invest disproportionately more in such traits, making those traits honest signals of genetic quality. However, genes associated with such traits may have sexually antagonistic effects on fitness. Here, using a bulb mite Rhizoglyphus robini, a species in which a distinct dimorphism exists between males in the expression of a sexually selected weapon, we compare inbreeding and gender load between lines derived from armed fighters and unarmed scramblers. After four generations of sib-mating, inbreeding depression for female fitness was significantly lower in fighter-derived lines compared to scrambler-derived lines, suggesting that fighter males had significantly higher genetic quality. However, outbred females from fighter-derived lines had significantly lower fitness compared to outbred females from scrambler-derived lines, demonstrating significant gender load associated with the presence of a sexually selected male weapon. Our results imply that under outbreeding, genetic benefits of mating with bearers of elaborate sexually selected traits might be swamped by the costs of decreased fitness of female progeny due to sexually antagonistic effects.     

The resolution of sexual antagonism by gene duplication

Disruptive selection between males and females can generate sexual antagonism, where alleles improving fitness in one sex reduce fitness in the other. This type of genetic conflict arises because males and females carry nearly identical sets of genes: opposing selection, followed by genetic mixing during reproduction, generates a population genetic "tug-of-war" that constrains adaptation in either sex. Recent verbal models suggest that gene duplication and sex-specific cooption of paralogs might resolve sexual antagonism and facilitate evolutionary divergence between the sexes. However, this intuitive proximal solution for sexual dimorphism potentially belies a complex interaction between mutation, genetic drift, and positive selection during duplicate fixation and sex-specific paralog differentiation. The interaction of these processes--within the explicit context of duplication and sexual antagonism--has yet to be formally described by population genetics theory. Here, we develop and analyze models of gene duplication and sex-specific differentiation between paralogs. We show that sexual antagonism can favor the fixation and maintenance of gene duplicates, eventually leading to the evolution of sexually dimorphic genetic architectures for male and female traits. The timescale for these evolutionary transitions is sensitive to a suite of genetic and demographic variables, including allelic dominance, recombination, sex linkage, and population size. Interestingly, we find that female-beneficial duplicates preferentially accumulate on the X chromosome, whereas male-beneficial duplicates are biased toward autosomes, independent of the dominance parameters of sexually antagonistic alleles. Although this result differs from previous models of sexual antagonism, it is consistent with several findings from the empirical genomics literature.     

Male courtship song and female preference variation between phylogeographically distinct populations of Drosophila montana

Understanding the variation within and between populations in important male mating traits and female preferences is crucial to theories concerning the origin of sexual isolation by coevolution or other processes. There have been surprisingly few studies on the extent of variation and covariation within and between populations, especially where the evolutionary relationships between populations are understood. Here we examine variation in female preferences and a sexually selected male song trait, the carrier frequency of the song, within and between populations from different phylogeographic clusters of Drosophila montana. Song is obligatory for successful mating in this species, and both playback and field studies implicate song carrier frequency as the most important parameter in male song. Carrier frequency varied among three recently collected populations from Oulanka (Finland), Vancouver (Canada), and Colorado (central United States), which represent the main phylogeographic groups in D. montana. Males from Colorado had the most distinct song frequency, which did not follow patterns of genetic differentiation. There was considerable variation in preference functions within, and some variation between, populations. Surprisingly, females from three lines from Colorado seem to have preferences disfavoring the extreme male trait found in this population. We discuss sources of selection on male song and female preference.     

Heterosis for viability,fecundity, and male fertility in Drosophila melanogaster: comparison of mutational and standing variation.

If genetic variation for fitness traits in natural populations ("standing" variation) is maintained by recurrent mutation, then quantitative-genetic properties of standing variation should resemble those of newly arisen mutations. One well-known property of standing variation for fitness traits is inbreeding depression, with its converse of heterosis or hybrid vigor. We measured heterosis for three fitness traits, pre-adult viability, female fecundity, and male fertility, among a set of inbred Drosophilia melanogaster lines recently derived from the wild, and also among a set of lines that had been allowed to accumulate spontaneous mutations for over 200 generations. The inbred lines but not the mutation-accumulation (MA) lines showed heterosis for pre-adult viability. Both sets of lines showed heterosis for female fecundity, but heterosis for male fertility was weak or absent. Crosses among a subset of the MA lines showed that they were strongly differentiated for male fertility, with the differences inherited in autosomal fashion; the absence of heterosis for male fertility among the MA lines was therefore not caused by an absence of mutations affecting this trait. Crosses among the inbred lines also gave some, albeit equivocal, evidence for male fertility variation. The contrast between the results for female fecundity and those for male fertility suggests that mutations affecting different fitness traits may differ in their average dominance properties, and that such differences may be reflected in properties of standing variation. The strong differentiation among the MA lines in male fertility further suggests that mutations affecting this trait occur at a high rate.     

Experimental evolution of a novel sexually antagonistic allele

Evolutionary conflict permeates biological systems. In sexually reproducing organisms, sex-specific optima mean that the same allele can have sexually antagonistic expression, i.e. beneficial in one sex and detrimental in the other, a phenomenon known as intralocus sexual conflict. Intralocus sexual conflict is emerging as a potentially fundamental factor for the genetic architecture of fitness, with important consequences for evolutionary processes. However, no study to date has directly experimentally tested the evolutionary fate of a sexually antagonistic allele. Using genetic constructs to manipulate female fecundity and male mating success, we engineered a novel sexually antagonistic allele (SAA) in Drosophila melanogaster. The SAA is nearly twice as costly to females as it is beneficial to males, but the harmful effects to females are recessive and X-linked, and thus are rarely expressed when SAA occurs at low frequency. We experimentally show how the evolutionary dynamics of the novel SAA are qualitatively consistent with the predictions of population genetic models: SAA frequency decreases when common, but increases when rare, converging toward an equilibrium frequency of ～8%. Furthermore, we show that persistence of the SAA requires the mating advantage it provides to males: the SAA frequency declines towards extinction when the male advantage is experimentally abolished. Our results empirically demonstrate the dynamics underlying the evolutionary fate of a sexually antagonistic allele, validating a central assumption of intralocus sexual conflict theory: that variation in fitness-related traits within populations can be maintained via sex-linked sexually antagonistic loci.     

The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant

Pollen fate can strongly affect the genetic structure of populations with restricted gene flow and significant inbreeding risk. We established an experimental population of inbred and outbred Silene latifolia plants to evaluate the effects of (i) inbreeding depression, (ii) phenotypic variation and (iii) relatedness between mates on male fitness under natural pollination. Paternity analysis revealed that outbred males sired significantly more offspring than inbred males. Independently of the effects of inbreeding, male fitness depended on several male traits, including a sexually dimorphic (flower number) and a gametophytic trait (in vitro pollen germination rate). In addition, full-sib matings were less frequent than randomly expected. Thus, inbreeding, phenotype and genetic dissimilarity simultaneously affect male fitness in this animal-pollinated plant. While inbreeding depression might threaten population persistence, the deficiency of effective matings between sibs and the higher fitness of outbred males will reduce its occurrence and counter genetic erosion.     

Socially flexible female choice differs among populations of the Pacific field cricket: geographical variation in the interaction coefficient psi (Ψ)

Indirect genetic effects (IGEs) occur when genes expressed in one individual affect the phenotype of a conspecific. Theoretical models indicate that the evolutionary consequences of IGEs critically depend on the genetic architecture of interacting traits, and on the strength and direction of phenotypic effects arising from social interactions, which can be quantified by the interaction coefficient Ψ. In the context of sexually selected traits, strong positive Ψ tends to exaggerate evolutionary change, whereas negative Ψ impedes sexual trait elaboration. Despite its theoretical importance, whether and how Ψ varies among geographically distinct populations is unknown. Such information is necessary to evaluate the potential for IGEs to contribute to divergence among isolated or semi-isolated populations. Here, we report substantial variation in Ψ for a behavioural trait involved in sexual selection in the field cricket Teleogryllus oceanicus: female choosiness. Both the strength and direction of Ψ varied among geographically isolated populations. Ψ also changed over time. In a contemporary population of crickets from Kauai, experience of male song increased female choosiness. In contrast, experience of male song decreased choosiness in an ancestral population from the same location. This rapid change corroborates studies examining the evolvability of Ψ and demonstrates how interpopulation variation in the interaction coefficient might influence sexual selection and accelerate divergence of traits influenced by IGEs that contribute to reproductive isolation in nascent species or subspecies.     

Balancing in- and out-breeding by the predatory mite <Emphasis Type="Italic">Phytoseiulus persimilis</Emphasis>

In- and out-breeding depressions are commonly observed phenomena in sexually reproducing organisms with a patchy distribution pattern, and spatial segmentation and/or isolation of groups. At the genetic level, inbreeding depression is due to increased homozygosity, whereas outbreeding depression is due to inferior genetic compatibility of mates. Optimal outbreeding theory suggests that intermediate levels of mate relatedness should provide for the highest fitness gains. Here, we assessed the fitness consequences of genetic relatedness between mates in plant-inhabiting predatory mites Phytoseiulus persimilis, which are obligatory sexually reproducing but haplo-diploid. Both females and males arise from fertilized eggs but males lose the paternal chromosome set during embryogenesis, dubbed pseudo-arrhenotoky. Phytoseiulus persimilis are highly efficacious in reducing crop-damaging spider mite populations and widely used in biological control. Using iso-female lines of two populations, from Sicily and Greece, we assessed the fecundity of females, and sex ratio of their offspring, that mated with either a sibling, a male from the same population or a male from the other population. Additionally, we recorded mating latency and duration. Females mating with a male from the same population produced more eggs, with a lower female bias, over a longer time than females mating with a sibling or with a male from the other population. Mating latency was unaffected by mate relatedness; mating duration was disproportionally long in sibling couples, likely indicating female reluctance to mate and sub-optimal spermatophore transfer. Our study provides a rare example of in- and out-breeding depression in a haplo-diploid arthropod, supporting the optimal outbreeding theory.