Microbial biomarkers as indicators of sperm viability in an insect.

Our understanding of microbial variation in male reproductive tissues is poorly understood, both regarding how it varies spatially across different tissues and its ability to affect male sperm and semen quality. To redress this gap, we explored the relationship between male sperm viability and male gut and reproductive tract microbiomes in the Pacific field cricket, Teleogryllus oceanicus. We selected cohorts of males within our populations with the highest and lowest natural sperm viability and characterized the bacterial microbiota present in the gut, testes, seminal vesicle, accessory glands and the spermatophore (ejaculate) using 16S ribosomal RNA gene metabarcoding. We identified bacterial taxa corresponding to sperm viability, highlighting for the first time an association between the host's microbial communities and male competitive fertilization success. We also found significant spatial variation in bacterial community structure of reproductive tissue types. Our data demonstrate the importance of considering the microbial diversity of both the host gut and reproductive tract when investigating male fertility in wildlife and potentially human clinical settings.

No evidence for an up-regulation of female immune function in response to elevated risk of sexual conflict.

Sexual conflict is widespread among sexually reproducing organisms. Phenotypic plasticity in female resistance traits has the potential to moderate the harm imposed by males during mating, yet female plasticity has rarely been explored. In this experiment, we investigated whether female seed beetles invest more in immunocompetence, measured as phenoloxidase (PO) capacity, when exposed to cues signalling a greater risk of sexual conflict. Risk perception was manipulated by housing focal individuals alone or with a companion as developing larvae, followed by exposure to a mating-free male- or female-biased social environment when adults. We predicted that females exposed to cues of increased sexual conflict would have increased PO capacity. However, PO capacity did not differ between either larval or adult social treatments. Our results suggest that females may not perceive a risk to their fitness on the basis of increased male presence or are unable to adjust this aspect of their phenotype in response to that risk.

Interacting phenotypic plasticities: Do male and female responses to the sociosexual environment interact to determine fitness?

Socially induced plasticity in reproductive effort is a widely documented phenomenon. However, few empirical studies have examined how male and female plastic responses to the social environment might interact in determining fitness outcomes. In field crickets, Teleogryllus oceanicus, males respond to rival song by increasing expenditure on seminal fluid proteins that enhance competitive fertilization success at the cost of reduced embryo survival. It remains unknown whether plastic responses in females could moderate the effects of male competitiveness on offspring performance. Here we used a fully factorial design to explore the interacting effects on fitness of male and female plasticity to the sociosexual environment. We found that female crickets exposed to male song increased the number of eggs produced during early life reproduction, which came at a cost of reduced offspring size. There was evidence, albeit weak, that interacting effects of male and female sociosexual environment contributed to variation in the hatching success of eggs laid by females. Lifetime offspring production was unaffected by the sociosexual environments to which upstream male and female plastic responses were made. Our data offer a rare test of the theoretical expectation that male and female plasticities should interact in their effects on female fitness.

Aggressive interactions influence cognitive performance in Western Australian magpies.

Extensive research has investigated the relationship between the social environment and cognition, suggesting that social complexity may drive cognitive evolution and development. However, evidence for this relationship remains equivocal. Group size is often used as a measure of social complexity, but this may not capture intraspecific variation in social interactions. Social network analysis can provide insight into the cognitively demanding challenges associated with group living at the individual level. Here, we use social networks to investigate whether the cognitive performance of wild Western Australian magpies (Gymnorhina tibicen dorsalis) is related to group size and individual social connectedness. We quantified social connectedness using four interaction types: proximity, affiliative, agonistic and vocal. Consistent with previous research on this species, individuals in larger groups performed better on an associative learning task. However, social network position was also related to cognitive performance. Individuals receiving aggressive interactions performed better, while those involved in aggressive interactions with more group members performed worse. Overall, this suggests that cognitive performance is related to specific types of social interaction. The findings from this study highlight the value of considering fine-grained metrics of sociality that capture the challenges associated with social life when testing the relationship between the social environment and cognition.

Extreme range in adult body size reveals hidden trade-offs among sexually selected traits.

Sexually selected weapons used to monopolize mating opportunities are predicted to trade-off with traits used in competition for fertilization. Yet, the limited size range typically found among adults of a species often precludes clear comparisons between population-level and individual-level relative trait investment. The jousting weevil, Brentus anchorago (Coleoptera: Brentidae), varies more than 26-fold in body mass, which is among the most extreme adult body size ranges of any solitary terrestrial species. We reveal a trade-off at a population level: hypermetric scaling in male weapons (slope = 1.59) and a closely mirrored reversal in allocation to postcopulatory traits (slope = 0.54). Yet, at the individual level, we find the opposite pattern; males that invest relatively more in weapons for their size class also invest more in postcopulatory traits. Across 36 dung beetle and 41 brentine weevil species, we find the allometric slope explains more trait variation at larger body size ranges; in brentines, population-level scaling patterns become more detectable in species with a larger range in adult body size. Our findings reveal that population-level allometries and individual-level trade-offs can both be important in shaping relative trait allocation; we highlight that the adult body size range is rarely examined but may be integral to gaining a deeper understanding of trade-offs in reproductive allocation.

Meta-analyses reveal support for the Social Intelligence Hypothesis.

The Social Intelligence Hypothesis (SIH) is one of the leading explanations for the evolution of cognition. Since its inception a vast body of literature investigating the predictions of the SIH has accumulated, using a variety of methodologies and species. However, the generalisability of the hypothesis remains unclear. To gain an understanding of the robustness of the SIH as an explanation for the evolution of cognition, we systematically searched the literature for studies investigating the predictions of the SIH. Accordingly, we compiled 103 studies with 584 effect sizes from 17 taxonomic orders. We present the results of four meta-analyses which reveal support for the SIH across interspecific, intraspecific and developmental studies. However, effect sizes did not differ significantly between the cognitive or sociality metrics used, taxonomy or testing conditions. Thus, support for the SIH is similar across studies using neuroanatomy and cognitive performance, those using broad categories of sociality, group size and social interactions, across taxonomic groups, and for tests conducted in captivity or the wild. Overall, our meta-analyses support the SIH as an evolutionary and developmental explanation for cognitive variation.

Mating competition among females: testing the distinction between natural and sexual selection in an insect.

In species where females compete for mates, the male often provides the female with resources in addition to gametes. A recently suggested definition of sexual selection proposed that if females only benefit from additional resources that come with each mating and not additional gametes, female intrasexual competition for mating opportunities would result in natural selection rather than sexual selection. The nuptial gift-giving bushcricket Kawanaphila nartee has dynamic sex roles and has been a textbook example of sexual selection acting on females via mating competition. We investigated whether females of this species gain fitness benefits from nuptial gifts, additional ejaculates or both by controlling the number of matings and whether the female was allowed to consume the nutritious gift (spermatophylax) at mating. We found that egg production per day of life increased with the number of additional matings, both with and without spermatophylax consumption, but consuming the spermatophylax had an additional positive effect on the number of eggs. These effects were particularly strong in females with shorter lifespans. We discuss how the recently suggested definition of sexual selection applies to nuptial-feeding insects and conclude that both natural and sexual selections influence mating competition in K. nartee females.

Dung beetles increase plant growth: a meta-analysis.

The ecosystem services provided by dung beetles are well known and valued. Dung beetles bury dung for feeding and breeding, and it is generally thought that the process of burying dung increases nutrient uptake by plant roots, which promotes plant growth. Many studies have tested the effects of dung beetles on plant growth, but there has been no quantitative synthesis of these studies. Here we use a multi-level meta-analysis to estimate the average effect of dung beetles on plant growth and investigate factors that moderate this effect. We identified 28 publications that investigated dung beetle effects on plant growth. Of these, 24 contained the minimum quantitative data necessary to include in a meta-analysis. Overall, we found that dung beetles increased plant growth by 17%; the 95% CI for possible values for the true increase in plant growth that were most compatible with our data, given our statistical model, ranged from 1% to 35%. We found evidence that the dung beetle-plant growth relationship is influenced by the plant measurement type and the number of beetles accessing the dung. However, beetles did not increase plant growth in all quantitative trials, as individual effect sizes ranged from -72% to 806%, suggesting important context-dependence in the provision of ecosystem services.

Heritability of cognitive performance in wild Western Australian magpies.

Individual differences in cognitive performance can have genetic, social and environmental components. Most research on the heritability of cognitive traits comes from humans or captive non-human animals, while less attention has been given to wild populations. Western Australian magpies (Gymnorhina tibicen dorsalis, hereafter magpies) show phenotypic variation in cognitive performance, which affects reproductive success. Despite high levels of individual repeatability, we do not know whether cognitive performance is heritable in this species. Here, we quantify the broad-sense heritability of associative learning ability in a wild population of Western Australian magpies. Specifically, we explore whether offspring associative learning performance is predicted by maternal associative learning performance or by the social environment (group size) when tested at three time points during the first year of life. We found little evidence that offspring associative learning performance is heritable, with an estimated broad-sense heritability of just -0.046 ± 0.084 (confidence interval: -0.234/0.140). However, complementing previous findings, we find that at 300 days post-fledging, individuals raised in larger groups passed the test in fewer trials compared with individuals from small groups. Our results highlight the pivotal influence of the social environment on cognitive development.

Rapid divergent evolution of internal female genitalia and the coevolution of male genital morphology revealed by micro-computed tomography.

Animal genitalia are thought to evolve rapidly and divergently in response to sexual selection. Studies of genital evolution have focused largely on male genitalia. The paucity of work on female genital morphology is probably due to problems faced in quantifying shape variation, due to their composition and accessibility. Here we use a combination of micro-computed tomography, landmark free shape quantification and phylogenetic analysis to quantify the rate of female genital shape evolution among 29 species of Antichiropus millipedes, and their coevolution with male genitalia. We found significant variation in female and male genital shape among species. Male genital shape showed a stronger phylogenetic signal than female genital shape, although the phylogenetic signal effect sizes did not differ significantly. Male genital shape was found to be evolving 1.2 times faster than female genital shape. Female and male genital shape exhibited strong correlated evolution, indicating that genital shape changes in one sex are associated with corresponding changes in the genital shape of the other sex. This study adds novel insight into our growing understanding of how female genitalia can evolve rapidly and divergently, and highlights the advantages of three-dimensional techniques and multivariate analyses in studies of female genital evolution.