Intra-specific correlations between ejaculate traits and competitive fertilization success: a meta-analysis across species and fertilization modes.

Understanding of how selection can act on traits that improve competitiveness and subsequent paternity has advanced, including the idea that internal and external fertilization presents different environments that may select differentially on ejaculate traits. However, no studies have quantitatively synthesized the intra-specific relationships between these traits and paternity. Therefore, we conducted a meta-analysis across 52 papers to determine which ejaculate traits positively correlate with paternity share and how these correlations vary with fertilization mode. Overall, most ejaculate traits were positively associated with paternity, with the notable exception of sperm length. Sub-analyses on sperm number, sperm length, and sperm velocity revealed no statistical differences between fertilization modes in the relationship between traits and paternity when all effect sizes across species were combined. However, in a sub-analysis on fish species only, we found evidence that sperm velocity may be more important in external fertilizers. We also observed differences in the importance of phylogenetic relatedness and some species-specific differences. Our results suggest that while most ejaculate traits should be under positive directional selection in both internal and external fertilizers, sperm length may be subject to more nuanced selection pressures. Overall, we highlight important patterns of intra-specific relationships between ejaculate traits and competitive fertilization success.

The impact of rising temperatures on the prevalence of coral diseases and its predictability: A global meta-analysis.

Coral reefs are under threat from disease as climate change alters environmental conditions. Rising temperatures exacerbate coral disease, but this relationship is likely complex as other factors also influence coral disease prevalence. To better understand this relationship, we meta-analytically examined 108 studies for changes in global coral disease over time alongside temperature, expressed using average summer sea surface temperature (SST) and cumulative heat stress as weekly sea surface temperature anomalies (WSSTAs). We found that both rising average summer SST and WSSTA were associated with global increases in the mean and variability in coral disease prevalence. Global coral disease prevalence tripled, reaching 9.92% in the 25 years examined, and the effect of 'year' became more stable (i.e. prevalence has lower variance over time), contrasting the effects of the two temperature stressors. Regional patterns diverged over time and differed in response to average summer SST. Our model predicted that, under the same trajectory, 76.8% of corals would be diseased globally by 2100, even assuming moderate average summer SST and WSSTA. These results highlight the need for urgent action to mitigate coral disease. Mitigating the impact of rising ocean temperatures on coral disease is a complex challenge requiring global discussion and further study.

The relative benefits of environmental enrichment on learning and memory are greater when stressed: A meta-analysis of interactions in rodents.

Environmental enrichment ("EE") is expected to alleviate the negative effects of stress on cognitive performance. However, there are complexities associated with interpreting interactions that obscure determining the benefit EE may play in mitigating the negative effects of stress. To clarify these complexities, we conducted a systematic review with meta-analysis on the main and interactive effects of EE and stress on learning and memory in rodents. We show that EE and stress interact 'synergetically' where EE provides a greater relative benefit to stressed individuals compared to those reared in conventional housing. Importantly, EE can fully-compensate for the negative effects of stress where stressed individuals with EE performed equally to enriched individuals without a stress manipulation. Additionally, we show the importance of other mediating factors, including the order of treatment exposure, duration and type of stress, type of EE, and type of cognitive assays used. This study not only quantifies the interactions between EE and stress, but also provides a clear example for how to conduct and interpret a meta-analysis of interactions.

Does female resistance to mating select for live-fast-die-young strategies in males? A comparative analysis in the genus Drosophila.

Female promiscuity is a pervasive selective force on male reproductive traits, and the strength of sexual selection is predicted to influence the trade-off between lifespan and reproduction. In species where sexual selection is intense, males are predicted to invest in sexual strategies that shorten their lifespan, potentially resulting in female-biased sexual dimorphism in longevity. However, comparative analyses have provided contrasting results, potentially due to the use of broad mating system categories or sexual size dimorphism as a proxy for sexual selection. Here, we used female remating rate (i.e. female promiscuity) as a more direct measure of sexual selection strength and conducted a phylogenetic comparative analysis of the relationship between female remating rate and sexual dimorphism in lifespan in 29 species of Drosophila. We did not find strong evidence that female remating rate was correlated with sexual dimorphism in lifespan. However, we found that male and female lifespans are positively correlated among species and that phylogeny and residual variance (i.e. variation in non-phylogenetic factors) are important in determining female remating rate, male and female lifespans separately, and the correlation between male and female lifespan. We suggest that variation in the nature of sexual competition and variation between studies could account for some of the unexplained variation among species in the relation between female remating rate and sexual dimorphism in lifespan.

Parental dietary protein effects on offspring viability in insects and other oviparous invertebrates: a meta-analysis.

Dietary protein is a key regulator of reproductive effort in animals, but protein consumption also tends to accelerate senescence and reduce longevity. Given this protein-mediated trade-off between reproduction and survival, how does protein consumption by parents affect the viability of their offspring? In insects, protein consumption by females enhances fecundity, but trade-offs between offspring quantity and quality could result in negative effects of protein consumption on offspring viability. Likewise, protein consumption by males tends to enhance the expression of sexual traits but could have negative effects on offspring viability, mediated by epigenetic factors transmitted via the ejaculate. It remains unclear whether dietary protein has consistent effects on offspring viability across species, and whether these effects are sex-specific. To address this, we conducted a meta-analysis of experimental studies that examined the effects of protein content in the maternal and/or paternal diet in insects and other oviparous invertebrates. We did not find consistent effects of paternal or maternal protein consumption on offspring viability. Rather, effects of dietary protein on offspring vary in both magnitude and sign across taxonomic groups. Further studies are needed to determine how the effects of dietary protein on offspring relate to variation in reproductive biology across species. Our findings also highlight important gaps in the literature and limitations in experiment design.

Sperm depletion in relation to developmental nutrition and genotype in Drosophila melanogaster.

Nutrient limitation during development can restrict the ability of adults to invest in costly fitness traits, and genotypes can vary in their sensitivity to developmental nutrition. However, little is known about how genotype and nutrition affect male ability to maintain ejaculate allocation and achieve fertilization across successive matings. Using 17 isogenic lines of Drosophila melanogaster, we investigated how variation in developmental nutrition affects males' abilities to mate, transfer sperm, and sire offspring when presented with successive virgin females. We found that, with each successive mating, males required longer to initiate copulation, transferred fewer sperm, and sired fewer offspring. Males reared on a low-nutrient diet transferred fewer sperm than those reared on nutritionally superior diets, but the rate at which males depleted their sperm, as well as their reproductive performance, was largely independent of diet. Genotype and the genotype × diet interaction explained little of the variation in these male reproductive traits. Our results show that sperm depletion can occur rapidly and impose substantial fitness costs for D. melanogaster males across multiple genotypes and developmental environments.

Effects of nutrient limitation on sperm and seminal fluid: a systematic review and meta-analysis.

Theory predicts that costly sexual traits should be reduced when individuals are in poor condition (i.e. traits should exhibit condition-dependent expression). It is therefore widely expected that male ejaculate traits, such as sperm and seminal fluid, will exhibit reduced quantity and quality when dietary nutrients are limited. However, reported patterns of ejaculate condition dependence are highly variable, and there has been no comprehensive synthesis of underlying sources of such variation in condition-dependent responses. In particular, it remains unclear whether all ejaculate traits are equally sensitive to nutrient intake, and whether such traits are particularly sensitive to certain dietary nutrients, respond more strongly to nutrients during specific life stages, or respond more strongly in some taxonomic groups. We systematically reviewed these potential sources of variation through a meta-analysis across 50 species of arthropods and vertebrates (from 71 papers and 348 effect sizes). We found that overall, ejaculate traits are moderately reduced when dietary nutrients are limited, but we also detected substantial variation in responses. Seminal fluid quantity was strongly and consistently condition dependent, while sperm quantity was moderately condition dependent. By contrast, aspects of sperm quality (particularly sperm viability and morphology) were less consistently reduced under nutrient limitation. Ejaculate traits tended to respond in a condition-dependent manner to a wide range of dietary manipulations, especially to caloric and protein restriction. Finally, while all major taxa for which sufficient data exist (i.e. arthropods, mammals, fish) showed condition dependence of ejaculate traits, we detected some taxonomic differences in the life stage that is most sensitive to nutrient limitation, and in the degree of condition dependence of specific ejaculate traits. Together, these biologically relevant factors accounted for nearly 20% of the total variance in ejaculate responses to nutrient limitation. Interestingly, body size showed considerably stronger condition-dependent responses compared to ejaculate traits, suggesting that ejaculate trait expression may be strongly canalised to protect important reproductive functions, or that the cost of producing an ejaculate is relatively low. Taken together, our findings show that condition-dependence of ejaculate traits is taxonomically widespread, but there are also many interesting, biologically relevant sources of variation that require further investigation. In particular, further research is needed to understand the differences in selective pressures that result in differential patterns of ejaculate condition dependence across taxa and ejaculate traits.

Developmental diet irreversibly shapes male post-copulatory traits in the neriid fly Telostylinus angusticollis.

Nutrient availability has been shown to influence investment in many fitness-related traits, including male reproductive success. Many studies have demonstrated that a reduction in nutrient availability alters male post-copulatory trait expression, with some studies demonstrating an effect of developmental nutrients and others, an effect of adult nutrients. However, few studies have manipulated both developmental and adult nutrients in the same experiment. Therefore, it is not clear what life-stage has the greatest effect on post-copulatory trait expression, and if the effects of developmental and adult nutrients can interact. Here, we investigate effects of developmental and adult nutrition on male testes and accessory gland size, sperm movement within the female reproductive tract and sperm length in the neriid fly, Telostylinus angusticollis. We found that males fed a nutrient-poor developmental diet produced sperm with a reduced tail beat frequency and had smaller testes and accessory glands compared to males fed a nutrient-rich developmental diet. In contrast, we found no effects of adult nutrition on any traits measured, although sperm length was correlated with body size and male age but unaffected by nutrition at any stage. Therefore, investment in adult post-copulatory traits is determined early on by developmental nutrients in male neriid flies, and this effect is not altered by adult nutrient availability.

Epigenetic paternal effects as costly, condition-dependent traits.

It is now recognized that post-copulatory traits, such as sperm and ejaculate production can impose metabolic costs, and such traits are therefore expected to exhibit condition-dependent expression, whereby, low condition individuals experience a greater marginal cost of investment compared to high condition individuals. Ejaculates are especially costly in species where males invest in offspring quality through nutrient-rich spermatophores or other seminal nuptial gifts. However, recent evidence shows that, in species where males do not provision females or offspring, males can still influence offspring development through paternal effects mediated by epigenetic factors, such as non-coding RNAs, DNA methylation and chromatin structure. Because such epigenetic paternal effects do not involve the transfer of substantial quantities of resources, such as nutrients, the costs of conferring such effects have not been considered. Here we argue that if selection favours paternal investment in offspring quality through epigenetic factors, then the epigenetic machinery required to bring about such effects may also be expected to evolve strongly condition-dependent expression. We outline indirect evidence suggesting that epigenetic paternal effects could impose substantial metabolic costs, consider the conditions under which selection may act on such effects, and suggest ways to test for differential costs and condition-dependence of these effects. Incorporating epigenetic paternal effects into condition-dependent life history theory will further our understanding of the heritability of fitness and the evolution of paternal investment strategies.

Measuring sperm movement within the female reproductive tract using Fourier analysis.

The adaptive significance of variation in sperm phenotype is still largely unknown, in part due to the difficulties of observing and measuring sperm movement in its natural, selective environment (i.e., within the female reproductive tract). Computer-assisted sperm analysis systems allow objective and accurate measurement of sperm velocity, but rely on being able to track individual sperm, and are therefore unable to measure sperm movement in species where sperm move in trains or bundles. Here we describe a newly developed computational method for measuring sperm movement using Fourier analysis to estimate sperm tail beat frequency. High-speed time-lapse videos of sperm movement within the female tract of the neriid fly Telostylinus angusticollis were recorded, and a map of beat frequencies generated by converting the periodic signal of an intensity versus time trace at each pixel to the frequency domain using the Fourier transform. We were able to detect small decreases in sperm tail beat frequency over time, indicating the method is sensitive enough to identify consistent differences in sperm movement. Fourier analysis can be applied to a wide range of species and contexts, and should therefore facilitate novel exploration of the causes and consequences of variation in sperm movement.