Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

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.     

Sexual conflict in a changing environment

Sexual conflict has extremely important consequences for various evolutionary processes including its effect on local adaptation and extinction probability during environmental change. The awareness that the intensity and dynamics of sexual conflict is highly dependent on the ecological setting of a population has grown in recent years, but much work is yet to be done. Here, we review progress in our understanding of the ecology of sexual conflict and how the environmental sensitivity of such conflict feeds back into population adaptivity and demography, which, in turn, determine a population's chances of surviving a sudden environmental change. We link two possible forms of sexual conflict – intralocus and interlocus sexual conflict – in an environmental context and identify major gaps in our knowledge. These include sexual conflict responses to fluctuating and oscillating environmental changes and its influence on the interplay between interlocus and intralocus sexual conflict, among others. We also highlight the need to move our investigations into more natural settings and to investigate sexual conflict dynamics in wild populations.     

Antagonistic pleiotropy in species with separate sexes,and the maintenance of genetic variation in life‐history traits and fitness

Antagonistic pleiotropy (AP)—where alleles of a gene increase some components of fitness at a cost to others—can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex‐specific phenotypic selection estimates—many of which are based on single fitness components.     

Mate choice in the predaceous mite Phytoseiulus persimilis: evidence of self‐referent phenotype matching?

Close inbreeding may have negative fitness effects. Consequently, organisms have evolved various mechanisms, which enable them to avoid close inbreeding. In no‐choice and choice experiments we assessed whether the predaceous mite Phytoseiulus persimilis Athias‐Henriot (Acari: Phytoseiidae) avoids close inbreeding by kin recognition. No‐choice experiments demonstrated that virgin females more readily accept unrelated males than they accept related ones, which suggests a female preference for unrelated mates. Because each female had been reared in isolation prior to experiments, females most likely imprinted on themselves, and later used self‐referent phenotype matching to assess potential mating partners. In contrast, neither female nor male choice experiments indicated a preference. Analyses of female and male behavior revealed that in choice experiments, female preference for unrelated males was probably confounded by male competition and/or altered by the different ecological context posed by choice experiments.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

Polyandry: the history of a revolution

We give a historic overview and critical perspective of polyandry in the context of sexual selection. Early approaches tended to obfuscate the fact that the total matings (copulations) by the two sexes is equal, neglecting female interests and that females often mate with (or receive ejaculates from) more than one male (polyandry). In recent years, we have gained much more insight into adaptive reasons for polyandry, particularly from the female perspective. However, costs and benefits of multiple mating are unlikely to be equal for males and females. These must be assessed for each partner at each potential mating between male i and female j, and will often be highly asymmetric. Interests of i and j may be in conflict, with (typically, ultimately because of primordial sex differences) i benefitting and j losing from mating, although theoretically the reverse can also obtain. Polyandry reduces the sex difference in Bateman gradients, and the probability of sexual conflict over mating by: (i) reducing the potential expected value of each mating to males in inverse proportion to the number of mates per female per clutch, and also often by (ii) increasing ejaculate costs through increased sperm allocation. It can nevertheless create conflict over fertilization and increase conflict over parental investment. The observed mean mating frequency for the population (and hence the degree of polyandry) is likely, at least in part, to reflect a resolution of sexual conflict. Immense diversity exists across and within taxa in the extent of polyandry, and views on its significance have changed radically, as we illustrate using avian polyandry as a case study. Despite recent criticisms, the contribution of the early pioneers of sexual selection, Darwin and Bateman, remains generally valid, and should not, therefore, be negated; as with much in science, pioneering advances are more often amplified and refined, rather than replaced with entirely new paradigms.     

Old‐male paternity advantage is a function of accumulating sperm and last‐male precedence in a butterfly

Old‐male mating advantage has been convincingly demonstrated in Bicyclus anynana butterflies. This intriguing pattern may be explained by two alternative hypotheses: (i) an increased aggressiveness and persistence of older males during courtship, being caused by the older males' low residual reproductive value; and (ii) an active preference of females towards older males what reflects a good genes hypothesis. Against this background, we here investigate postcopulatory sexual selection by double‐mating Bicyclus anynana females to older and younger males, thus allowing for sperm competition and cryptic mate choice, and by genotyping the resulting offspring. Virgin females were mated with a younger virgin (2–3 days old) and afterwards an older virgin male (12–13 days old) or vice versa. Older males had a higher paternity success than younger ones, but only when being the second (=last) mating partner, while paternity success was equal among older and younger males when older males were the first mating partner. Older males produced larger spermatophores with much higher numbers of fertile sperm than younger males. Thus, we found no evidence for cryptic female mate choice. Rather, the findings reported here seem to result from a combination of last‐male precedence and the number of sperm transferred upon mating, both increasing paternity success.     

Behavioural Consistency in Female Resistance to Male Harassment in a Water Strider Species

Sexual conflict over mating rate often implies that males persist at frequently harassing females to gain matings while females resist mating attempts. In water striders, females can resist by engaging in vigorous pre‐copulatory struggles to dislodge males, but alternative means of resistance have seldom been investigated. Contrary to males, female resistance has not been investigated as a repeatable behaviour. We used Gerris buenoi to investigate the capacity to abbreviate struggles and the tendency to hide off the water as two potential female resistance traits. Specifically, we asked whether these behaviours are repeatable and whether they vary according to sexual conflict intensity and past mating experience. Also, we studied the possible connections between these behaviours and traits linked to fitness, namely endured harassment and mating activity. The capacity to abbreviate struggles was poorly repeatable and decreased with sexual conflict intensity and endured harassment. It seems to be mainly determined by the social environment and by recent events related to sexual conflict. The tendency to hide off the water was significantly repeatable across sexual conflict intensities and can be considered as a repeatable behaviour. Hiding frequently off the water allowed females to decrease the harassment endured by females and may enhance female fitness. In nature, hiding is more readily and more frequently observed than pre‐copulatory struggles. Directly associating hiding off water with female fitness would confirm that this consistent phenotype contributes to sexually antagonistic female resistance.     

Operational sex ratio predicts the opportunity and direction of sexual selection across animals

The operational sex ratio (OSR) has long been assumed to be a key ecological factor determining the opportunity and direction of sexual selection. However, recent theoretical work has challenged this view, arguing that a biased OSR does not necessarily result in greater monopolisation of mates and therefore stronger sexual selection in the mate‐limited sex. Hence, the role of the OSR for shaping animal mating systems remains a conundrum in sexual selection research. Here we took a meta‐analytic approach to test whether OSR explains interspecific variation in sexual selection metrics across a broad range of animal taxa. Our results demonstrate that the OSR predicts the opportunity for sexual selection in males and the direction of sexual selection in terms of sex differences in both the opportunity for sexual selection and the Bateman gradient (i.e. the selection differential of mating success), as predicted by classic theory.     

Proximate mechanisms of the differences in reproductive success of males bearing different alleles of Pgdh – a gene involved in a sexual conflict in bulb mite

Enzyme polymorphism in phosphogluconate dehydrogenase (Pgdh) is a striking example of single gene polymorphism involved in sexual conflict in bulb mite Rhizoglyphus robini. Males homozygous for the S Pgdh allele were shown to achieve higher reproductive success than FF homozygous males, while negatively influencing fecundity of their female partners. Here, we investigate proximate mechanisms responsible for the increased reproductive success of SS males and find that the S allele is associated with shorter time until copulation, higher copulation frequency and increased sperm production. We also show that Pgdh alleles are probably codominant, with SS males gaining the highest reproductive success, FF males – the lowest – and FS‐heterozygous males taking an intermediate position in all fitness parameters differentiating males of different genotypes. Additionally, we confirm the negative effect that S‐bearing males impose on the fecundity of females they mate with, showing a clear pattern of interlocus sexual conflict. We discuss that this effect is probably associated with increased copulation frequency. Whereas, contrary to what we have predicted, the S allele does not cause increased general male mobility, we speculate that the S allele‐bearing males are more efficient in forcing copulation and/or detecting females.     

Sex ratio schedules in a dynamic game: the effect of competitive asymmetry by male emergence order

Studies of sex allocation have provided some of the most successfultests of theory in behavioral and evolutionary ecology. Forinstance, local mate competition (LMC) theory has explainedvariation in sex allocation across numerous species. However,some patterns of sex ratio variation remain unexplained by existingtheory. Most existing models have ignored variation in malecompetitive ability and assumed all males have equal opportunitiesto mate within a patch. However, in some species experiencingLMC, males often fight fiercely for mates, such that male matingsuccess varies with male fighting ability. Here, we examinethe effect of competitive ability on optimal sex allocationschedules using a dynamic programming approach. This model assumesan asymmetric competitive ability derived from different mortalitiesaccording to the timing of male emergence. If the mortalityof newly emerging males is larger than that of already emergedmales, our model predicts a more female-biased sex ratio thanexpected under traditional LMC models. In addition, femalesare predicted to produce new males constantly at a low rateover the offspring emergence period. We show that our modelsuccessfully predicts the sex ratios produced by females ofthe parasitoid wasp Melittobia, a genus renowned for its vigorouslyfighting males and lower than expected sex ratios.     

Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids

Disruptive sexual selection on colour patterns has been suggested as a major cause of diversification in the cichlid species flock of Lake Victoria. In Neochromis omnicaeruleus, a colour and sex determination polymorphism is associated with a polymorphism in male and female mating preferences. Theoretical work on this incipient species complex found conditions for rapid sympatric speciation by selection on sex determination and sexual selection on male and female colour patterns, under restrictive assumptions. Here we test the biological plausibility of a key assumption of such models, namely, the existence of a male preference against a novel female colour morph before its appearance in the population. We show that most males in a population that lacks the colour polymorphism exhibit a strong mating preference against the novel female colour morph and that reinforcement is not a likely explanation for the origin of such male preferences. Our results show that a specific condition required for the combined action of selection on sex determination and sexual selection to drive sympatric speciation is biologically justified. Finally, we suggest that Lake Victoria cichlids might share an ancestral female recognition scheme, predisposing colour monomorphic populations/species to similar evolutionary pathways leading to divergence of colour morphs in sympatry.     

Effects of diet restriction on life history in a sexually cannibalistic spider

Diet restriction increases longevity while reducing fecundity in a broad range of organisms. However, there are exceptions to this rule, and the causes of these exceptions remain unclear. One hypothesis is that short‐lived, semelparous organisms gain no benefit from increased longevity regardless of nutritional resources. Another hypothesis is that organisms may alter their behaviour to compensate for nutrient deficiencies. We examined these hypotheses in the colonial orb‐weaving spider Cyrtophora citricola. Sexual cannibalism is frequent in this species so that females are long lived and interoparous while males are semelparous. Because of these differing sexual strategies, we predicted that the common pattern of increased longevity under diet restriction would hold for females but not for males. We also investigated in a semi‐natural setting whether spiders could compensate for diet restriction by altering their feeding behaviour. Diet‐restricted females produced fewer offspring but lived longer than well‐fed females, while diet had no effect on male longevity. Despite being semelparous, virgin males were quite long‐lived, suggesting that potential lifespan is relatively unimportant in determining the effects of diet restriction. Contrary to our predictions, females were unable to compensate for their restricted diet by altering their foraging behaviour. Instead, semi‐natural conditions increased the differences between spiders on high and low diets, suggesting that the effects of diet restriction can be pervasive under natural conditions.     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

Food affects the potential reproductive rates of sand goby females but not of males

The interspawning interval of female sand gobies, Pomatoschistusminutus, a batch-spawning fish with paternal care, was significantlyshorter when the fish were fed daily than when they were fedevery fourth day. The incubation time of males was not affectedby feeding, nor was the interbrood interval Males have an equalor higher potential reproductive rate than females. As femalesreproduce more slowly when food is scarce than when it is abundant,and males do not, the difference between the sexes in potentialreproductive rate increases when there is food shortage. Becauseof this difference, both male bias in operational sex ratioand intensity in male-male competition for mates are predictedto increase as food availability decreases. Furthermore, a tradeoffbetween current and future reproduction is demonstrated to operateonly when resources are limited, because the correlation betweenegg number of the first and second clutch was positive amonghigh-food females but negative among low-food females. The numberof eggs per female clutch did, however, not differ between treatmentsin first or second dutch. I conclude that operational sex ratioand sexual selection are expected to vary within and betweensand goby populations in accordance with prey availability     

Variation in the post‐mating fitness landscape in fruit flies

Sperm competition is pervasive and fundamental to determining a male's overall fitness. Sperm traits and seminal fluid proteins (Sfps) are key factors. However, studies of sperm competition may often exclude females that fail to remate during a defined period. Hence, the resulting data sets contain fewer data from the potentially fittest males that have most success in preventing female remating. It is also important to consider a male's reproductive success before entering sperm competition, which is a major contributor to fitness. The exclusion of these data can both hinder our understanding of the complete fitness landscapes of competing males and lessen our ability to assess the contribution of different determinants of reproductive success to male fitness. We addressed this here, using the Drosophila melanogaster model system, by (i) capturing a comprehensive range of intermating intervals that define the fitness of interacting wild‐type males and (ii) analysing outcomes of sperm competition using selection analyses. We conducted additional tests using males lacking the sex peptide (SP) ejaculate component vs. genetically matched (SP⁺) controls. This allowed us to assess the comprehensive fitness effects of this important Sfp on sperm competition. The results showed a signature of positive, linear selection in wild‐type and SP⁺ control males on the length of the intermating interval and on male sperm competition defence. However, the fitness surface for males lacking SP was distinct, with local fitness peaks depending on contrasting combinations of remating intervals and offspring numbers. The results suggest that there are alternative routes to success in sperm competition and provide an explanation for the maintenance of variation in sperm competition traits.     

Maintenance of polygenic sex determination in a fluctuating environment: an individual‐based model

R. A. Fisher predicted that individuals should invest equally in offspring of both sexes, and that the proportion of males and females produced (the primary sex ratio) should evolve towards 1:1 when unconstrained. For many species, sex determination is dependent on sex chromosomes, creating a strong tendency for balanced sex ratios, but in other cases, multiple autosomal genes interact to determine sex. In such cases, the maintenance of multiple sex‐determining alleles at multiple loci and the consequent among‐family variability in sex ratios presents a puzzle, as theory predicts that such systems should be unstable. Theory also predicts that environmental influences on sex can complicate outcomes of genetic sex determination, and that population structure may play a role. Tigriopus californicus, a copepod that lives in splash‐pool metapopulations and exhibits polygenic and environment‐dependent sex determination, presents a test case for relevant theory. We use this species as a model for parameterizing an individual‐based simulation to investigate conditions that could maintain polygenic sex determination. We find that metapopulation structure can delay the degradation of polygenic sex determination and that periods of alternating frequency‐dependent selection, imposed by seasonal fluctuations in environmental conditions, can maintain polygenic sex determination indefinitely.