Evolution of female choice under intralocus sexual conflict and genotype-by-environment interactions.
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ABSTRACT:
SUBMITTER: Li XY
PROVIDER: S-EPMC6125721 | biostudies-literature | 2018 Oct
REPOSITORIES: biostudies-literature
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Project description:At any given age, men are more likely to die than women, but women have poorer health at older ages. This is referred to as the "male-female, health-survival paradox", which is not fully understood. Here, we provide a general solution to the paradox that relies on intralocus sexual conflict, where alleles segregating in the population have late-acting positive effects on male fitness, but negative effects on female health. Using an evolutionary modelling framework, we show that male-benefit, female-detriment alleles can spread if they are expressed after female reproduction stops. We provide support for our conflict based solution using experimental Drosophila data. Our results show that selecting for increased late-life male reproductive effort can increase male fitness but have a detrimental effect on female fitness. Furthermore, we show that late-life male fertility is negatively genetically correlated with female health. Our study suggests that intralocus sexual conflict could resolve the health-survival paradox.
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Project description:The loss of sexual ornaments is observed across taxa, and pleiotropic effects of such losses provide an opportunity to gain insight into underlying dynamics of sex-biased gene expression and intralocus sexual conflict (IASC). We investigated this in a Hawaiian field cricket, Teleogryllus oceanicus, in which an X-linked genotype ( flatwing) feminizes males' wings and eliminates their ability to produce sexually selected songs. We profiled adult gene expression across somatic and reproductive tissues of both sexes. Despite the feminizing effect of flatwing on male wings, we found no evidence of feminized gene expression in males. Instead, female transcriptomes were more strongly affected by flatwing than males', and exhibited demasculinized gene expression. These findings are consistent with a relaxation of IASC constraining female gene expression through loss of a male sexual ornament. In a follow-up experiment, we found reduced testes mass in flatwing males, whereas female carriers showed no reduction in egg production. By contrast, female carriers exhibited greater measures of body condition. Our results suggest sex-limited phenotypic expression offers only partial resolution to IASC, owing to pleiotropic effects of the loci involved. Benefits conferred by release from intralocus conflict could help explain widespread loss of sexual ornaments across taxa.
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Project description:Sexual selection theory models evolution of sexual signals and preferences using simple life histories. However, life-history models predict that males benefit from increasing sexual investment approaching old age, producing age-dependent sexual traits. Age-dependent traits require time and energy to grow, and will not fully mature before individuals enter mating competition. Early evolutionary stages pose several problems for these traits. Age-dependent traits suffer from strong viability selection and gain little benefit from mate choice when rare. Few males will grow large traits, and they will rarely encounter choosy females. The evolutionary origins of age-dependent traits therefore remain unclear. I used numerical simulations to analyze evolution of preferences, condition (viability) and traits in an age-structured population. Traits in the model depended on age and condition ("good genes") in a population with no genetic drift. I asked (1) if age-dependent indicator traits and their preferences can originate depending on the strength of selection and the size of the trait; (2) which mode of development (age-dependent versus age-independent) eventually predominates when both modes occur in the population; and (3) if age-independent traits can invade a population with age-dependent traits. Age-dependent traits evolve under weaker selection and at smaller sizes than age-independent traits. This result held in isolation and when the types co-occur. Evolution of age-independent traits depends only on trait size, whereas evolution of age-dependent traits depends on both strength of selection and growth rate. Invasion of age-independence into populations with established traits followed a similar pattern with age-dependence predominating at small trait sizes. I suggest that reduced adult mortality facilitates sexual selection by favoring the evolution of age-dependent sexual signals under weak selection.
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Project description:Evolutionary conflict between the sexes can induce arms races in which males evolve traits that are detrimental to the fitness of their female partners, and vice versa. This interlocus sexual conflict (IRSC) has been proposed as a cause of perpetual intersexual antagonistic coevolution with wide-ranging evolutionary consequences. However, theory suggests that the scope for perpetual coevolution is limited, if traits involved in IRSC are subject to pleiotropic constraints. Here, we consider a biologically plausible form of pleiotropy that has hitherto been ignored in treatments of IRSC and arrive at drastically different conclusions. Our analysis is based on a quantitative genetic model of sexual conflict, in which genes controlling IRSC traits have side effects in the other sex, due to incompletely sex-limited gene expression. As a result, the genes are exposed to intralocus sexual conflict (IASC), a tug-of-war between opposing male- and female-specific selection pressures. We find that the interaction between the two forms of sexual conflict has contrasting effects on antagonistic coevolution: Pleiotropic constraints stabilize the dynamics of arms races if the mating traits are close to evolutionary equilibrium but can prevent populations from ever reaching such a state. Instead, the sexes are drawn into a continuous cycle of arms races, causing the buildup of IASC, alternated by phases of IASC resolution that trigger the next arms race. These results encourage an integrative perspective on the biology of sexual conflict and generally caution against relying exclusively on equilibrium stability analysis.
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Project description:Males and females share most of their genome and develop many of the same traits. However, each sex frequently has different optimal values for these shared traits, creating intralocus sexual conflict. This conflict has been observed in wild and laboratory populations of insects and affects important evolutionary processes such as sexual selection, the maintenance of genetic variation, and possibly even speciation. Given the broad impacts of intralocus conflict, accurately detecting and measuring it is important. A common way to detect intralocus sexual conflict is to calculate the intersexual genetic correlation for fitness, with negative values suggesting conflict. Here, we highlight a potential confounder of this measure-cytoplasmic incompatibility caused by the intracellular parasite Wolbachia. Infection with Wolbachia can generate negative intersexual genetic correlations for fitness in insects, suggestive of intralocus sexual conflict. This is because cytoplasmic incompatibility reduces the fitness of uninfected females mated to infected males, while uninfected males will not suffer reductions in fitness if they mate with infected females and may even be fitter than infected males. This can lead to strong negative intersexual genetic correlations for fitness, mimicking intralocus conflict. We illustrate this issue using simulations and then present Drosophila simulans data that show how reproductive incompatibilities caused by Wolbachia infection can generate signals of intralocus sexual conflict. Given that Wolbachia infection in insect populations is pervasive, but populations usually contain both infected and uninfected individuals providing scope for cytoplasmic incompatibility, this is an important consideration for sexual conflict research but one which, to date, has been largely underappreciated.
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Project description:Sexual conflict can promote the evolution of dramatic reproductive adaptations as well as resistance to its potentially costly effects. Theory predicts that responses to sexual conflict will vary significantly with resource levels-when scant, responses should be constrained by trade-offs, when abundant, they should not. However, this can be difficult to test because the evolutionary interests of the sexes align upon short-term exposure to novel environments, swamping any selection due to sexual conflict. What is needed are investigations of populations that are well adapted to both differing levels of sexual conflict and resources. Here, we used this approach in a long-term experimental evolution study to track the evolution of female resistance to sexual conflict in the fruit fly Drosophila melanogaster. In resource-rich regimes, high-conflict females evolved resistance to continual exposure to males. There was no difference in baseline survival, consistent with the idea that responses evolving under nutritional abundance experienced no trade-offs with resistance. In the poor resource regimes, the ability of high-conflict females to evolve resistance to males was severely compromised and they also showed lower baseline survival than low-conflict females. This suggested high-conflict females traded off somatic maintenance against any limited resistance they had evolved in response to sexual conflict. Overall, these findings provide experimental support for the hypothesis that evolutionary responses to sexual conflict are critically dependent upon resource levels.
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Project description:Existing models explaining the evolution of sexual dimorphism in the timing of emergence (SDT) in Lepidoptera assume equal mortality rates for males and females. The limiting assumption of equal mortality rates has the consequence that these models are only able to explain the evolution of emergence of males before females, i.e. protandry-the more common temporal sequence of emergence in Lepidoptera. The models fail, however, in providing adaptive explanations for the evolution of protogyny, where females emerge before males, but protogyny is not rare in insects. The assumption of equal mortality rates seems too restrictive for many insects, such as butterflies. To investigate the influence of unequal mortality rates on the evolution of SDT, we present a generalised version of a previously published model where we relax this assumption. We find that longer life-expectancy of females compared to males can indeed favour the evolution of protogyny as a fitness enhancing strategy. Moreover, the encounter rate between females and males and the sex-ratio are two important factors that also influence the evolution of optimal SDT. If considered independently for females and males the predicted strategies can be shown to be evolutionarily stable (ESS). Under the assumption of equal mortality rates the difference between the females' and males' ESS remains typically very small. However, female and male ESS may be quite dissimilar if mortality rates are different. This creates the potential for an 'evolutionary conflict' between females and males. Bagworm moths (Lepidoptera: Psychidae) provide an exemplary case where life-history attributes are such that protogyny should indeed be the optimal emergence strategy from the males' and females' perspectives: (i) Female longevity is considerably larger than that of males, (ii) encounter rates between females and males are presumably low, and (iii) females mate only once. Protogyny is indeed the general mating strategy found in the bagworm family.
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Project description:BackgroundCrossover localization during meiotic recombination is mediated by the fast-evolving zinc-finger (ZnF) domain of gene PRDM9. To study its impact on dairy cattle performance, we compared its genetic variation between the relatively small Israeli (IL) Holsteins and the North American (US) Holsteins that count millions.ResultsInitially, we analyzed the major BTA1 haplotypes present in IL Holsteins based on the 10 most telomeric SNPs of the BovineSNP50 BeadChip. Sequencing of representative haplotype carriers indicated that for all frequent haplotypes (> 6%), the variable PRDM9 ZnF array consisted of seven tandem ZnF repeats. Two rare haplotypes (frequency < 4%) carried an indicine PRDM9, whereas all others were variants of the taurine type. These two haplotypes included the minor SNP allele, which was perfectly linked with a previously described PRDM9 allele known to induce unique localization of recombination hotspots. One of them had a significant (p = 0.03) negative effect on IL sire fertility. This haplotype combined the rare minor alleles of the only SNPs with significant (p < 0.05) negative substitution effects on US sire fertility (SCR). Analysis of telomeric SNPs indicated general agreement of allele frequencies (R = 0.95) and of the substitution effects on sire fertility (SCR, R = 0.6) between the US and IL samples. Surprisingly, the alleles that had a negative impact on male fertility had the most positive substitution effects on female fertility traits (DPR, CCR and HCR).ConclusionsA negative genetic correlation between male and female fertility is encoded within the BTA1 telomere. Cloning the taurine PRDM9 gene, which is the common form carried by Holsteins, we encountered the infiltration of an indicine PRDM9 variant into this population. During meiosis, in heterozygous males, the indicine PRDM9 variant may induce incompatibility of recombination hotspots and male infertility. However, this variant is associated with favorable female fertility, which would explain its survival and the general negative correlation (R = - 0.3) observed between male and female fertility in US Holsteins. Further research is needed to explain the mechanism underlying this positive effect and to devise a methodology to unlink it from the negative effect on male fertility during breeding.
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Project description: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.
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