No fitness effects of same-sex copulations in male red flour beetles.

Same-sex sexual behavior occurs in diverse animal taxa, yet its evolutionary maintenance is poorly understood as such behavior seems to be costly and does not directly increase reproductive success. We used male Tribolium castaneum beetles, which frequently engage in same-sex copulations, to test if same-sex sexual behavior influences future male mating behavior and reproductive success of males. Furthermore, we tested whether same-sex sexual behavior has benefits via indirect sperm translocation. We conducted a series of mating trials demonstrating that males exposed to same-sex behavior did not sire less offspring compared to control males that did not engage in same-sex behavior. This suggests that same-sex copulations did not lead to fitness costs in subsequent mating interactions. In addition, we found no evidence that indirect sperm translocation via an intermediate male occurs in T. castaneum. Taken together, these results imply that same-sex sexual behavior in males is associated with no costs in terms of lower mating rate and reduced siring success and does not seem to entail benefits. Moreover, our data conform to the hypothesis that sexual indiscrimination is prevalent in this species, which may explain the relatively high frequency of same-sex sexual behavior in T. castaneum.

Sexual selection in females and the evolution of polyandry.

Over the last decades, the field of sexual selection underwent a paradigm shift from sexual-stereotype thinking of "eager" males and "coy" females towards a more nuanced perspective acknowledging that not only males but also females can benefit from multiple mating and compete for mating partners. Yet, sexual selection in females is still considered a peculiarity, and the evolution of polyandry is often viewed to result from a higher mating interest of males. Here, we present meta-analytic evidence from 77 species across a broad range of animal taxa to demonstrate that female reproductive success is overall positively correlated with mating success, suggesting that females typically benefit from multiple mating. Importantly, we found that these fitness gains likely promote the evolution of polyandry. Our findings offer support for the idea that sexual selection is widespread in females and to play a key role for the evolution of animal mating systems. Thereby, our results extend our understanding of the evolutionary consequences of sexual reproduction and contribute to a more balanced view of how sexual selection operates in males and females.

Diet quality impairs male and female reproductive performance and affects the opportunity for selection in an insect model.

Environmental factors can have profound effects on the strength and direction of selection and recent studies suggest that such environment-dependent selection can be sex-specific. Sexual selection theory predicts that male fitness is more condition dependent compared to female fitness, suggesting that male fitness is more sensitive to environmental stress. However, our knowledge about the effect of environmental factors on sex-specific reproductive performance and on sex differences in the opportunity for selection is still very limited. In the present study, we investigated the sex-specific effects of diet quality (yeast deprivation and flour type) in the red flour beetle Tribolium castaneum. Specifically, we manipulated yeast supplementation in wheat and whole-wheat flour in competition assays allowing us to test for sex-specific effects of food quality (i) on reproductive success and (ii) on the opportunity for selection. Our data show that yeast deprivation in wheat flour had significantly negative effects on body mass and reproductive success of both sexes, while high-quality flour (whole-wheat flour) was able to buffer the negative impact to a large extent. Importantly, our data suggest no sex-specific effect of dietary stress on reproductive success because the magnitude of the negative effect of yeast deprivation was similar for males and females. Moreover, our study demonstrates that low food quality inflated the opportunity for selection and did not differ between sexes neither under benign nor stressful dietary conditions. We discuss the implications of our findings for the adaptation to stressful environments.

A meiotic driver alters sperm form and function in house mice: a possible example of spite.

The ability to subvert independent assortment of chromosomes is found in many meiotic drivers, such as the t haplotype in house mice Mus musculus, in which the t-bearing chromosomal homolog is preferentially transmitted to offspring. This is explained by a poison-antidote system, in which developing + and t sperm in testes of + /t males are exposed to 'poison' coded by t loci, from which t sperm are protected, allowing t sperm an overwhelming fertilisation advantage in monogamous matings. This system is thought to result in poorly and normally motile sperm subpopulations within + /t sperm, leaving t sperm unharmed. Conversely, we found that the fastest quartile of sperm from + /t males swam more slowly, both forwards and along their travel path, and had reduced straightness and linearity, compared to the fastest quartile of + / + sperm. Moreover, sperm from + /t males had shorter tails and narrower heads than + / + sperm, and these morphological differences covaried with motility differences. Finally, + /t traits did not show evidence of bimodal distributions. We conclude that the t haplotype drive results in lasting damage to the motility of both + and t developing sperm, although previous studies indicate that + must be more harmed than t sperm. This damage to all sperm may explain the low success of + /t males in sperm competition with + / + males, seen in earlier studies. We propose that the harm the t causes to itself could be termed 'spiteful', which may also be common to other gamete-harming meiotic drive systems.

Sexual selection moderates heat stress response in males and females.

A widespread effect of climate change is the displacement of organisms from their thermal optima. The associated thermal stress imposed by climate change has been argued to have a particularly strong impact on male reproduction but evidence for this postulated sex-specific stress response is equivocal.One important factor that may explain intra- and interspecific variation in stress responses is sexual selection, which is predicted to magnify negative effects of stress. Nevertheless, empirical studies exploring the interplay of sexual selection and heat stress are still scarce.We tested experimentally for an interaction between sexual selection and thermal stress in the red flour beetle Tribolium castaneum by contrasting heat responses in male and female reproductive success between enforced monogamy and polygamy.We found that polygamy magnifies detrimental effects of heat stress in males but relaxes the observed negative effects in females. Our results suggest that sexual selection can reverse sex differences in thermal sensitivity, and may therefore alter sex-specific selection on alleles associated with heat tolerance.Assuming that sexual selection and natural selection are aligned to favour the same genetic variants under environmental stress, our findings support the idea that sexual selection on males may promote the adaptation to current global warming. Read the free Plain Language Summary for this article on the Journal blog.

Stronger net selection on males across animals.

Sexual selection is considered the major driver for the evolution of sex differences. However, the eco-evolutionary dynamics of sexual selection and their role for a population's adaptive potential to respond to environmental change have only recently been explored. Theory predicts that sexual selection promotes adaptation at a low demographic cost only if sexual selection is aligned with natural selection and if net selection is stronger on males compared to females. We used a comparative approach to show that net selection is indeed stronger in males and provide preliminary support that this sex bias is associated with sexual selection. Given that both sexes share the vast majority of their genes, our findings corroborate the notion that the genome is often confronted with a more stressful environment when expressed in males. Collectively, our study supports one of the long-standing key assumptions required for sexual selection to bolster adaptation, and sexual selection may therefore enable some species to track environmental change more efficiently.

The baculum affects paternity success of first but not second males in house mouse sperm competition.

The vast variation observed in genital morphology is a longstanding puzzle in evolutionary biology. Studies showing that the morphology of the mammalian baculum (penis bone) can covary with a male's paternity success indicate a potential impact of baculum morphology on male fitness, likely through influencing sperm competition outcomes. We therefore measured the size (measurements of length and width) and shape (geometric morphometric measurements) of the bacula of male house mice used in previously published sperm competition experiments, in which two males mated successively with the same female in staged matings. This enabled us to correlate baculum morphology with sperm competition success, incorporating potential explanatory variables related to copulatory plugs, male mating behavior and a selfish genetic element that influences sperm motility. We found that a wider baculum shaft increased a male's paternity share when mating first, but not when mating second with a multiply-mating female. Geometric morphometric shape measurements were not clearly associated with fertilization success for either male. We found limited evidence that the effect of baculum morphology on male fertilization success was altered by experimental removal of the copulatory plug. Furthermore, neither genetic differences in sperm motility, nor covariation with male mating behavior mediated the effect of baculum morphology on male fertilization success. Taken together with previous findings, the mating-order effects we found here suggest that baculum-mediated stimulation by the first male might be particularly important for fertilization.

Steroid hormones in hair reveal sexual maturity and competition in wild house mice (Mus musculus domesticus).

Endocrine data from wild populations provide important insight into social systems. However, obtaining samples for traditional methods involves capture and restraint of animals, and/or pain, which can influence the animal's stress level, and thereby undesirable release of hormones. Here, we measured corticosterone, testosterone and progesterone in the hair of 482 wild-derived house mice that experienced sexual competition while living under semi-natural conditions. We tested whether sex, age, weight and indicators of sexual maturity, reproduction and social conflicts predict hormone concentrations measured in hair (sampling at endpoint). We show that body weight, sex and age significantly predict cumulative testosterone and progesterone levels, allowing the differentiation between subadults and adults in both sexes. Corticosterone was only slightly elevated in older males compared to older females and increased with the level of visible injuries or scars. Testosterone in males positively correlated with body weight, age, testes size, and sperm number. Progesterone in females significantly increased with age, body weight, and the number of embryos implanted throughout life, but not with the number of litters when controlled for age and weight. Our results highlight the biological validity of hair steroid measurements and provide important insight into reproductive competition in wild house mice.

Impact of low sperm competition on male reproductive trait allometries in a bush-cricket.

BACKGROUND: Studying reproductive trait allometries can help to understand optimal male investment strategies under sexual selection. In promiscuous mating systems, studies across several taxa suggest that testes allometry is usually positive, presumably due to strong selection on sperm numbers through intense sperm competition. Here, we investigated testes allometry in a bush-cricket species, Metaplastes ornatus, in which females mate promiscuously, but where sperm removal behaviour by males likely drastically reduces realised sperm competition level. RESULTS: As hypothesised, we found evidence for negative testes allometry and hence a fundamentally different male investment strategy compared to species under intense sperm competition. In addition, the mean relative testes size of M. ornatus was small compared to other species of bush-crickets. Surprisingly, the spermatophore gland, a potential alternative trait that males could invest in instead of testes, also did not show positive allometry, but was approximately isometric. We further observed the expected pattern of negative allometry for the male morphological structure responsible for sperm removal in this species, the subgenital plate, supporting the one-size-fits-all hypothesis for intromittent genitalia. CONCLUSION: Our findings suggest that the evolution of sperm removal behaviour in M. ornatus was a key adaptation for avoiding sperm competition, with important consequences for reproductive trait allometries. Nevertheless, they also imply that it does not pay for larger males to invest disproportionately in nuptial gift production in this species.

Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal.

Self-fertilization is widespread among simultaneously hermaphroditic animals and plants, but is often only facultatively deployed under circumstances that constrain outcrossing. A central prediction of sex allocation (SA) theory is that because exclusive selfing reduces sperm or pollen competition to zero, this should favour extreme economy in resources channelled to the male sex function. We can therefore expect that organisms switching from outcrossing to selfing should reduce their male allocation. However, to date this prediction has received relatively little support in animal taxa, especially compared to plants. Here we show that isolated individuals (under enforced selfing conditions) have a less male-biased SA than do grouped conspecifics (under outcrossing conditions) in the preferentially outcrossing flatworm Macrostomum hystrix This shift arises from a reduced male allocation (testis area) in isolated individuals, although we did not find any evidence for a re-allocation of these resources to the female sex function (i.e. ovary area was unaffected by selfing/outcrossing conditions). Our results provide some of the clearest experimental evidence to date for reduced male allocation under selfing in simultaneously hermaphroditic animals, extending previous findings comparing SA between populations differing in selfing rates to the level of individual plasticity in gametogenesis.