Zofia M. Prokop

META-ANALYSIS SUGGESTS CHOOSY FEMALES GET SEXY SONS MORE THAN “GOOD GENES”

Female preferences for specific male phenotypes have been documented across a wide range of animal taxa, including numerous species where males contribute only gametes to offspring production. Yet, selective pressures maintaining such preferences are among the major unknowns of evolutionary biology. Theoretical studies suggest that preferences can evolve if they confer genetic benefits in terms of increased attractiveness of sons (“Fisherian” models) or overall fitness of offspring (“good genes” models). These two types of models predict, respectively, that male attractiveness is heritable and genetically correlated with fitness. In this meta‐analysis, we draw general conclusions from over two decades worth of empirical studies testing these predictions (90 studies on 55 species in total). We found evidence for heritability of male attractiveness. However, attractiveness showed no association with traits directly associated with fitness (life‐history traits). Interestingly, it did show a positive correlation with physiological traits, which include immunocompetence and condition. In conclusion, our results support “Fisherian” models of preference evolution, while providing equivocal evidence for “good genes.” We pinpoint research directions that should stimulate progress in our understanding of the evolution of female choice.

Age dependence of male mating ability and sperm competition success in the bulb mite

In many species, the genetic quality of gametes is likely to decline with age of the male. Some form of discrimination against mating with old males, or against fertilization by their sperm, can be expected to evolve. We investigated the effect of male age on the probability of mating and on sperm competitiveness in the bulb mite, Rhizoglyphus robini. There was no significant difference between male age classes in the probability of mating with virgin females, but young males were more likely to mate with already mated females. Furthermore, young males won sperm competition against older males. This implies that polyandry may be an effective way of avoiding fertilization by the sperm of older males. It has also been suggested that polyandry insures females against the infertility of old males. Our results do not support this hypothesis: matings with older males did not result in female infertility significantly more often than matings with young males.

Mating system affects population performance and extinction risk under environmental challenge

Failure of organisms to adapt to sudden environmental changes may lead to extinction. The type of mating system, by affecting fertility and the strength of sexual selection, may have a major impact on a populations chances to adapt and survive. Here, we use experimental evolution in bulb mites (Rhizoglyphus robini) to examine the effects of the mating system on population performance under environmental change. We demonstrate that populations in which monogamy was enforced suffered a dramatic fitness decline when evolving at an increased temperature, whereas the negative effects of change in a thermal environment were alleviated in polygamous populations. Strikingly, within 17 generations, all monogamous populations experiencing higher temperature went extinct, whereas all polygamous populations survived. Our results show that the mating system may have dramatic effects on the risk of extinction under environmental change.

Low inbreeding depression in a sexual trait in the stalk-eyed fly Teleopsis dalmanni

The genic capture hypothesis implies that the expression of sexual ornaments largely depends on genes affecting resource acquisition and use. The ornaments should thus show high degree of directional dominance typical of life-history traits, and consequently, they should be severely affected by inbreeding. Here we investigated the effect of inbreeding on a sexual ornament (male eyespan) in stalk-eyed fly, Teleopsis dalmanni. For comparison, we also measured inbreeding depression in non-sexual morphological traits: female eyespan as well as wing and thorax lengths in both sexes. Both eyespan, and other morphological traits we measured, showed significant inbreeding depression. In accord with predictions of genic capture hypothesis, male eyespan did decrease under inbreeding significantly more than female eyespan. However, the decline in male eyespan was fully explained by overall decline in body length. Moreover, the magnitude of inbreeding depression in male eyespan was considerably lower than that typically observed for life-histories; in fact, it fitted within the range typically characterizing morphological traits. We therefore conclude that our results provide weak support for genic capture hypothesis.

Genetic variation in male attractiveness: It is time to see the forest for the trees.

Female choice based on multiple male traits, rather than on any single one, has been reported in many species and may well be a rule rather than an exception. However, the implications this has for selection acting on choosiness itself remain underappreciated. We argue that this constitutes one of the important impediments to our understanding of the evolution of mate choice. We discuss this issue primarily in the context of the Fisherian model of sexual selection. We review theory and empirical data, showing how the crucial parameter of the model—genetic variation in male attractiveness—can be estimated when attractiveness is a function of multiple traits. Based on the reviewed theory, we show how relying on individual male traits, instead of overall attractiveness, can produce biased estimates of Fisherian benefits of female choice. This bias can be substantial, especially when many traits contribute to male attractiveness. We discuss a number of methodological issues that, we hope, will stimulate future studies and help resolving the long‐standing mystery of mate choice.

Do males pay for sex? : sex-specific selection coefficients suggest not

Selection acting on males can reduce mutation load of sexual relative to asexual populations, thus mitigating the twofold cost of sex, provided that it seeks and destroys the same mutations as selection acting on females, but with higher efficiency. This could happen due to sexual selection—a potent evolutionary force that in most systems predominantly affects males. We used replicate populations of red flour beetles (Tribolium castaneum) to study sex‐specific selection against deleterious mutations introduced with ionizing radiation. We found no evidence for selection being stronger in males than in females; in fact, we observed a nonsignificant trend in the opposite direction. This suggests that selection on males does not reduce mutation load below the level expected under the (hypothetical) scenario of asexual reproduction. Additionally, we employed a novel approach, based on a simple model, to quantify the relative contributions of sexual and offspring viability selection to the overall selection observed in males. We found them to be similar in magnitude; however, only the offspring viability component was statistically significant. In summary, we found no support for the hypothesis that selection on males in general, and sexual selection in particular, contributes to the evolutionary maintenance of sex.

No evidence for reproductive isolation through sexual conflict in the bulb mite Rhizoglyphus robini.

Sexual conflict leading to sexual antagonistic coevolution has been hypothesized to drive reproductive isolation in allopatric populations and hence lead to speciation. However, the generality of this speciation mechanism is under debate. We used experimental evolution in the bulb mite Rhizoglyphusrobini to investigate whether sexual conflict promotes reproductive isolation measured comprehensively to include all possible pre- and post-zygotic mechanisms. We established replicate populations in which we either enforced monogamy, and hence removed sexual conflict by making male and female evolutionary interests congruent, or allowed promiscuity. After 35 and 45 generations of experimental evolution, we found no evidence of reproductive isolation between the populations in any of the mating systems. Our results indicate that sexual conflict does not necessarily drive fast reproductive isolation and it may not be a ubiquitous mechanism leading to speciation.

Sexual dimorphism in immunity across animals: a meta‐analysis

In animals, sex differences in immunity are proposed to shape variation in infection prevalence and intensity among individuals in a population, with females typically expected to exhibit superior immunity due to life-history trade-offs. We performed a systematic meta-analysis to investigate the magnitude and direction of sex differences in immunity and to identify factors that shape sex-biased immunocompetence. In addition to considering taxonomic and methodological effects as moderators, we assessed age-related effects, which are predicted to occur if sex differences in immunity are due to sex-specific resource allocation trade-offs with reproduction. In a meta-analysis of 584 effects from 124 studies, we found that females exhibit a significantly stronger immune response than do males, but the effect size is relatively small, and became non-significant after controlling for phylogeny. Female-biased immunity was more pronounced in adult than immature animals. More recently published studies did not report significantly smaller effect sizes. Among taxonomic and methodological subsets of the data, some of the largest effect sizes were in insects, further supporting previous suggestions that testosterone is not the only potential driver of sex differences in immunity. Our findings challenge the notion of pervasive biases towards female-biased immunity and the role of testosterone in driving these differences.

Fitness Effects of Thermal Stress Differ Between Outcrossing and Selfing Populations in Caenorhabditis elegans

The maintenance of males and outcrossing is widespread, despite considerable costs of males. By enabling recombination between distinct genotypes, outcrossing may be advantageous during adaptation to novel environments and if so, it should be selected for under environmental challenge. However, a given environmental change may influence fitness of male, female, and hermaphrodite or asexual individuals differently, and hence the relationship between reproductive system and dynamics of adaptation to novel conditions may not be driven solely by the level of outcrossing and recombination. This has important implications for studies investigating the evolution of reproductive modes in the context of environmental changes, and for the extent to which their findings can be generalized. Here, we use Caenorhabditis elegans—a free-living nematode species in which hermaphrodites (capable of selfing but not cross-fertilizing each other) coexist with males (capable of fertilizing hermaphrodites)—to investigate the response of wild type as well as obligatorily outcrossing and obligatorily selfing lines to stressfully increased ambient temperature. We found that thermal stress affects fitness of outcrossers much more drastically than that of selfers. This shows that apart from the potential for recombination, the selective pressures imposed by the same environmental change can differ between populations expressing different reproductive systems and affect their adaptive potential.

Assessing sex-specific selection against deleterious alleles: males don't pay for sex.

Selection acting on males can reduce mutation load of sexual relative to asexual populations, thus mitigating the two-fold cost of sex. This requires that it seeks and destroys the same mutations as selection acting on females, but with higher efficiency, which could happen due to sexual selection-a potent evolutionary force that in most systems predominantly affects males. We used replicate populations of red flour beetles (Tribolium castaneum) to study sex-specific selection against deleterious mutations introduced with ionizing radiation. Additionally, we employed a novel approach to quantify the relative contribution of sexual selection to the overall selection observed in males. The induced mutations were selected against in both sexes, with decreased sexual competitiveness contributing, on average, over 40% of the total decline in male fitness. However, we found no evidence for selection being stronger in males than in females; in fact, we observed a non-significant trend in the opposite direction. These results suggest that selection on males does not reduce mutation load below the level expected under the (hypothetical) scenario of asexual reproduction. Thus, we found no support for the hypothesis that sexual selection contributes to the evolutionary maintenance of sex.