Sexually antagonistic co-evolution can explain female display signals and male sensory adaptations.

The prevalence and diversity of female ornaments poses a challenge to evolutionary theory because males should prefer mates that spend resources on offspring rather than ornaments. Among dance flies, there is extraordinary variation in sexual dimorphism. Females of many species have conspicuous ornaments (leg scales and inflatable abdominal sacs). Meanwhile males of some species have exaggerated regions of their eyes with larger ommatidial facets that allow for regionally elevated photosensitivity and/or acuity. Here, we conduct a comparative study of these traits using both species descriptions available from the literature, as well as quantitative measures of eyes and ornaments from wild-caught flies. We show a conspicuous covariance across species between exaggerated male dorsal eye regions and the extent of female ornaments: species with highly ornamented females have males with more exaggerated eyes. We discuss this pattern in the context of competing hypotheses for the evolution of these traits and propose a plausible role for sexually antagonistic coevolution.

Pre-natal exposure to glucocorticoids causes changes in developmental circadian clock gene expression and post-natal behaviour in the Japanese quail.

The embryonic environment is critical in shaping developmental trajectories and consequently post-natal phenotypes. Exposure to elevated stress hormones during this developmental stage is known to alter a variety of post-natal phenotypic traits, and it has been suggested that pre-natal stress can have long term effects on the circadian rhythm of glucocorticoid hormone production. Despite the importance of the circadian system, the potential impact of developmental glucocorticoid exposure on circadian clock genes, has not yet been fully explored. Here, we showed that pre-natal exposure to corticosterone (CORT, a key glucocorticoid) resulted in a significant upregulation of two key hypothalamic circadian clock genes during the embryonic period in the Japanese quail (Coturnix japonica). Altered expression was still present 10 days into post-natal life for both genes, but then disappeared by post-natal day 28. At post-natal day 28, however, diel rhythms of eating and resting were influenced by exposure to pre-natal CORT. Males exposed to pre-natal CORT featured an earlier acrophase, alongside spending a higher proportion of time feeding. Females exposed to pre-natal CORT featured a less pronounced shift in acrophase and spent less time eating. Both males and females exposed to pre-natal CORT spent less time inactive during the day. Pre-natal CORT males appeared to feature a delay in peak activity levels. Our novel data suggest that these circadian clock genes and aspects of diurnal behaviours are highly susceptible to glucocorticoid disruption during embryonic development, and these effects are persistent across developmental stages, at least into early post-natal life.

resevol: An R package for spatially explicit models of pesticide resistance given evolving pest genomes.

The evolution of pesticide resistance is a widespread problem with potentially severe consequences for global food security. We introduce the resevol R package, which simulates individual-based models of pests with evolving genomes that produce complex, polygenic, and covarying traits affecting pest life history and pesticide resistance. Simulations are modelled on a spatially-explicit and highly customisable landscape in which crop and pesticide application and rotation can vary, making the package a highly flexible tool for both general and tactical models of pest management and resistance evolution. We present the key features of the resevol package and demonstrate its use for a simple example simulating pests with two covarying traits. The resevol R package is open source under GNU Public License. All source code and documentation are available on GitHub.

Increasing ecological heterogeneity can constrain biopesticide resistance evolution.

Microbial biopesticides containing living parasites are valuable emerging crop protection technologies against insect pests, but they are vulnerable to resistance evolution. Fortunately, the fitness of alleles that provide resistance, including to parasites used in biopesticides, frequently depends on parasite identity and environmental conditions. This context-specificity suggests a sustainable approach to biopesticide resistance management through landscape diversification. To mitigate resistance risks, we advocate increasing the range of biopesticides available to farmers, whilst simultaneously encouraging other aspects of landscape-wide crop heterogeneity that can generate variable selection on resistance alleles. This approach requires agricultural stakeholders to prioritize diversity as well as efficiency, both within agricultural landscapes and the biocontrol marketplace.

The timings of host diapause and epidemic progression mediate host genetic diversity and future epidemic size in Daphnia-parasite populations.

Epidemics commonly exert parasite-mediated selection and cause declines in host population genetic diversity. This can lead to evolution of resistance in the long term and smaller subsequent epidemics. Alternatively, the loss of genetic diversity can increase host vulnerability to future disease spread and larger future epidemics. Matters are made more complex by the fact that a great many host organisms produce diapausing life stages in response to environmental change (often as a result of sexual reproduction; e.g. plant seeds and invertebrate resting eggs). These diapausing stages can disrupt the relationship between past epidemics, host genetic diversity and future epidemics because they allow host dispersal through time. Specifically, temporally dispersing hosts avoid infection and thus selection from contemporary parasites, and also archive genetic variation for the future. We studied 80 epidemics in 20 semi-natural populations of the temporally dispersing crustacean Daphnia magna and its sterilizing bacterial parasite Pasteuria ramosa, and half of these populations experienced a simulated environmental disturbance treatment. We found that early initiation of diapause relative to the timing of the epidemic led to greater host genetic diversity and reduced epidemic size in the subsequent year, but this was unaffected by environmental disturbance.

Can diet niche partitioning enhance sexual dimorphism?

Classic evolutionary theory suggests that sexual dimorphism evolves primarily via sexual and fecundity selection. However, theory and evidence are beginning to accumulate suggesting that resource competition can drive the evolution of sexual dimorphism, via ecological character displacement between sexes. A key prediction of this hypothesis is that the extent of ecological divergence between sexes will be associated with the extent of sexual dimorphism. As the stable isotope ratios of animal tissues provide a quantitative measure of various aspects of ecology, we carried out a meta-analysis examining associations between the extent of isotopic divergence between sexes and the extent of body size dimorphism. Our models demonstrate that large amounts of between-study variation in isotopic (ecological) divergence between sexes is nonrandom and may be associated with the traits of study subjects. We, therefore, completed meta-regressions to examine whether the extent of isotopic divergence between sexes is associated with the extent of sexual size dimorphism. We found modest but significantly positive associations across species between size dimorphism and ecological differences between sexes, that increased in strength when the ecological opportunity for dietary divergence between sexes was greatest. Our results, therefore, provide further evidence that ecologically mediated selection, not directly related to reproduction, can contribute to the evolution of sexual dimorphism.

Mating and Sexual Selection in Empidine Dance Flies (Empididae).

Species whose behaviour or morphology diverges from typical patterns can provide unique insights on the evolutionary forces that promote diversity. Darwin recognised that while elaborate sexually selected traits mostly occurred among males, in a few species females possess such traits. Some species from the subfamily Empidinae (Diptera: Empididae) are among the animals that are often invoked to illustrate female ornaments. Empidines include taxa that exhibit varying levels of female ornament expression; some species possess multiple, elaborate female-specific ornaments while others have fewer and more modest adornments, and many species are altogether lacking discernible sexual ornamentation. This continuous variation in display traits in the Empidinae provides unique opportunities to explore the causes and consequences of sexually selected ornament expression. Here, we review the literature on sexual selection and mating systems in these flies and synthesise the evidence for various evolutionary forces that could conceivably create this impressive morphological and behavioural diversity, despite evolutionary constraints on female ornament exaggeration that help to explain its general rarity among animals. We also suggest some aspects of diversity that remain relatively unexplored or poorly understood, and close by offering suggestions for future research progress in the evolutionary ecology of mating behaviour among empidine flies.

Sperm competition in yellow dung flies: No consistent effect of sperm size.

The male competition for fertilization that results from female multiple mating promotes the evolution of increased sperm numbers and can impact sperm morphology, with theory predicting that longer sperm can at times be advantageous during sperm competition. If so, males with longer sperm should sire more offspring than competitors with shorter sperm. Few studies have directly tested this prediction, and findings are inconsistent. Here we assessed whether longer sperm provide a competitive advantage in the yellow dung fly (Scathophaga stercoraria; Diptera: Scathophagidae). Initially, we let brothers with different temperature-mediated mean sperm lengths compete - thus minimizing confounding effects of genetic background - and found no clear advantage of longer sperm. We then used flies from lines subjected to bidirectional selection on phenoloxidase activity that had shown correlated evolutionary responses in sperm and female spermathecal duct lengths. This experiment also yielded no main effect of sperm size on siring success. Instead, there was a trend for a shorter-sperm advantage, but only when competing in females with longer spermathecal ducts. Our data corroborated many previously reported findings (last-male precedence, effects of copula duration and body size), suggesting our failure to find sperm size effects is not inherently due to our experimental protocols. We conclude that longer sperm are not competitively superior in yellow dung flies under most circumstances, and that, consistent with previous work, in this species competitive fertilization success is primarily determined by the relative numbers of sperm competing.

Growth rate mediates hidden developmental plasticity of female yellow dung fly reproductive morphology in response to environmental stressors.

Understanding how environmental variation influences even cryptic traits is important to clarify the roles of selection and developmental constraints in past evolutionary divergence and to predict future adaptation under environmental change. Female yellow dung flies (Scathophaga stercoraria) typically have three sperm storage compartments (3S), but occasionally four (4S). More spermathecae are thought to be a female adaptation facilitating sperm sorting after mating, but the phenotype is very rare in nature. We manipulated the flies' developmental environment by food restriction, pesticides, and hot temperatures to investigate the nature and extent of developmental plasticity of this trait, and whether spermatheca expression correlates with measures of performance and developmental stability, as would be expected if 4S expression is a developmental aberration. The spermathecal polymorphism of yellow dung fly females is heritable, but also highly developmentally plastic, varying strongly with rearing conditions. 4S expression is tightly linked to growth rate, and weakly positively correlated with fluctuating asymmetry of wings and legs, suggesting that the production of a fourth spermatheca could be a nonadaptive developmental aberration. However, spermathecal plasticity is opposite in the closely related and ecologically similar Scathophaga suilla, demonstrating that overexpression of spermathecae under developmental stress is not universal. At the same time, we found overall mortality costs as well as benefits of 4S pheno- and genotypes (also affecting male siblings), suggesting that a life history trade-off may potentially moderate 4S expression. We conclude that the release of cryptic genetic variation in spermatheca number in the face of strong environmental variation may expose hidden traits (here reproductive morphology) to natural selection (here under climate warming or food augmentation). Once exposed, hidden traits can potentially undergo rapid genetic assimilation, even in cases when trait changes are first triggered by random errors that destabilize developmental processes.

Competition for access to mates predicts female-specific ornamentation and male investment in relative testis size.

Sexually selected ornaments are highly variable and the factors that drive variation in ornament expression are not always clear. Rare instances of female-specific ornament evolution (such as in some dance fly species) are particularly puzzling. While some evidence suggests that such rare instances represent straightforward reversals of sexual selection intensity, the distinct nature of trade-offs between ornaments and offspring pose special constraints in females. To examine whether competition for access to mates generally favors heightened ornament expression, we built a phylogeny and conducted a comparative analysis of Empidinae dance fly taxa that display female-specific ornaments. We show that species with more female-biased operational sex ratios in lek-like mating swarms have greater female ornamentation, and in taxa with more ornate females, male relative testis investment is increased. These findings support the hypothesis that ornament diversity in dance flies depends on female receptivity to mates, which is associated with contests for nutritious nuptial gifts provided by males. Moreover, our results suggest that increases in female receptivity lead to higher levels of sperm competition among males. The incidence of both heightened premating sexual selection on females and postmating selection on males contradicts assertions that sex roles are straightforwardly reversed in dance flies.

The role of functional constraints in nonrandom mating patterns for a dance fly with female ornaments.

Most hypotheses to explain nonrandom mating patterns invoke mate choice, particularly in species that display elaborate ornaments. However, conflicting selection pressures on traits can result in functional constraints that can also cause nonrandom mating patterns. We tested for functional load-lifting constraints during aerial copulation in Rhamphomyia longicauda, a species of dance fly that displays multiple extravagant female-specific ornaments that are unusual among sexual traits because they are under stabilizing selection. R. longicauda males provide females with a nuptial gift before engaging in aerial mating, and the male bears the entire weight of the female and nuptial gift for the duration of copulation. In theory, a male's ability to carry females and nuptial gifts could constrain pairing opportunities for the heaviest females, as reported for nonornamented dance flies. In concert with directional preferences for large females with mature eggs, such a load-lifting constraint could produce the stabilizing selection on female size previously observed in this species. We therefore tested whether wild-caught male R. longicauda collected during copulation were experiencing load-lift limitations by comparing the mass carried by males during copulation with the male's wing loading traits. We also performed permutation tests to determine whether the loads carried by males during copulation were lighter than expected. We found that heavier males are more often found mating with heavier females suggesting that whereas R. longicauda males do not experience a load-lift constraint, there is a strong relationship of assortative mating by mass. We suggest that active male mate choice for intermediately adorned females is more likely to be causing the nonrandom mating patterns observed in R. longicauda.

Survival costs of reproduction are mediated by parasite infection in wild Soay sheep.

A trade-off between current and future fitness potentially explains variation in life-history strategies. A proposed mechanism behind this is parasite-mediated reproductive costs: individuals that allocate more resources to reproduction have fewer to allocate to defence against parasites, reducing future fitness. We examined how reproduction influenced faecal egg counts (FEC) of strongyle nematodes using data collected between 1989 and 2008 from a wild population of Soay sheep in the St. Kilda archipelago, Scotland (741 individuals). Increased reproduction was associated with increased FEC during the lambing season: females that gave birth, and particularly those that weaned a lamb, had higher FEC than females that failed to reproduce. Structural equation modelling revealed future reproductive costs: a positive effect of reproduction on spring FEC and a negative effect on summer body weight were negatively associated with overwinter survival. Overall, we provide evidence that parasite resistance and body weight are important mediators of survival costs of reproduction.

Sexual selection on multiple female ornaments in dance flies.

Sex-specific ornaments typically occur in males, but they can also develop in females. While there are several models concerning the evolution of male-specific ornaments, it is not clear how, or under what circumstances, those models apply to female-specific ornament evolution. Here, we present a manipulative field experiment that explores the theoretical 'trait space' of multiple female-specific ornaments to study how these unusual traits evolved. We measured the attractiveness of two female-specific ornaments (pinnate leg scales and inflatable abdominal sacs) in the dance fly Rhamphomyia longicauda in a wild mating swarm. We found significant directional preferences for larger ornaments of both types; however, variation in one of the ornaments (abdominal sacs) was almost three times more effective at improving attractiveness. The abdominal ornament was consistently effective in increasing attractiveness to males regardless of leg ornament expression, while leg ornament size was only effective if abdominal ornaments were very small. These results are consistent with predictions from a sexual conflict model of ornament expression in supporting the probable role of deception in the evolution of female-specific ornaments among dance flies. Sexual conflict can be an important force in generating elaborate sex-specific ornaments in females as well as males.

Are sex ratio distorting endosymbionts responsible for mating system variation among dance flies (Diptera: Empidinae)?

Maternally inherited bacterial endosymbionts are common in many arthropod species. Some endosymbionts cause female-biased sex ratio distortion in their hosts that can result in profound changes to a host's mating behaviour and reproductive biology. Dance flies (Diptera: Empidinae) are well known for their unusual reproductive biology, including species with female-specific ornamentation and female-biased lek-like swarming behaviour. The cause of the repeated evolution of female ornaments in these flies remains unknown, but is probably associated with female-biased sex ratios in individual species. In this study we assessed whether dance flies harbour sex ratio distorting endosymbionts that might have driven these mating system evolutionary changes. We measured the incidence and prevalence of infection by three endosymbionts that are known to cause female-biased sex ratios in other insect hosts (Wolbachia, Rickettsia and Spiroplasma) across 20 species of dance flies. We found evidence of widespread infection by all three symbionts and variation in sex-specific prevalence across the taxa sampled. However, there was no relationship between infection prevalence and adult sex ratio measures and no evidence that female ornaments are associated with high prevalences of sex-biased symbiont infections. We conclude that the current distribution of endosymbiont infections is unlikely to explain the diversity in mating systems among dance fly species.

Emerging issues in the evolution of animal nuptial gifts.

Uniquely positioned at the intersection of sexual selection, nutritional ecology and life-history theory, nuptial gifts are widespread and diverse. Despite extensive empirical study, we still have only a rudimentary understanding of gift evolution because we lack a unified conceptual framework for considering these traits. In this opinion piece, we tackle several issues that we believe have substantively hindered progress in this area. Here, we: (i) present a comprehensive definition and classification scheme for nuptial gifts (including those transferred by simultaneous hermaphrodites), (ii) outline evolutionary predictions for different gift types, and (iii) highlight some research directions to help facilitate progress in this field.

Enduring consequences of early experiences: 40 year effects on survival and success among African elephants (Loxodonta africana).

Growth from conception to reproductive onset in African elephants (Loxodonta africana) provides insights into phenotypic plasticity, individual adaptive plastic responses and facultative maternal investment. Using growth for 867 and life histories for 2652 elephants over 40 years, we demonstrate that maternal inexperience plus drought in early life result in reduced growth rates for sons and higher mortality for both sexes. Slow growth during early lactation was associated with smaller adult size, later age at first reproduction, reduced lifetime survival and consequently limited reproductive output. These enduring effects of trading slow early growth against immediate survival were apparent over the very long term; delayed downstream consequences were unexpected for a species with a maximum longevity of 70+ years and unpredictable environmental experiences.

Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers.

Buzz-pollination is a plant strategy that promotes gamete transfer by requiring a pollinator, typically bees (Hymenoptera: Apoidea), to vibrate a flower's anthers in order to extract pollen. Although buzz-pollination is widespread in angiosperms with over 20,000 species using it, little is known about the functional connection between natural variation in buzzing vibrations and the amount of pollen that can be extracted from anthers. We characterized variability in the vibrations produced by Bombus terrestris bumblebees while collecting pollen from Solanum rostratum (Solanaceae), a buzz-pollinated plant. We found substantial variation in several buzzing properties both within and among workers from a single colony. As expected, some of this variation was predicted by the physical attributes of individual bumblebees: heavier workers produced buzzes of greater amplitude. We then constructed artificial "pollination buzzes" that varied in three parameters (peak frequency, peak amplitude, and duration), and stimulated S. rostratum flowers with these synthetic buzzes to quantify the relationship between buzz properties and pollen removal. We found that greater amplitude and longer duration buzzes ejected substantially more pollen, while frequency had no directional effect and only a weak quadratic effect on the amount of pollen removed. These findings suggest that foraging bumblebees may improve pollen collection by increasing the duration or amplitude of their buzzes. Moreover, given that amplitude is positively correlated with mass, preferential foraging by heavier workers is likely to result in the largest pollen yields per bee, and this could have significant consequences for the success of a colony foraging on buzz-pollinated flowers.

Senescence of the cellular immune response in Drosophila melanogaster.

Immune system effectiveness generally declines as animals age, compromising disease resistance. In Drosophila, expression of a variety of immune-related genes elevates during ageing; however how this is linked to increasing pathogen susceptibility in older flies has remained unclear. We investigated whether changes in the Drosophila cellular immune response might contribute to immunosenescence. Experiments studied fly cohorts of different ages and compared the numbers and activity of the circulating haemocytes involved in pathogen defence. In female wildtype Samarkand and Oregon R flies the haemocyte population fell by 31.8% and 10.2% respectively during the first four weeks of adulthood. Interestingly we detected no such decline in male flies. The impact of ageing on the phagocytic activity of haemocytes was investigated by injecting flies with fluorescently labelled microbes or latex beads and assessing the ability of haemocytes to engulf them. For all immune challenges the proportion of actively phagocytosing haemocytes decreased as flies aged. Whilst 24.3%±1.15% of haemocytes in one-week-old flies phagocytosed Escherichia coli bacteria or Beauveria bassiana fungal spores, this decreased to 16.7%±0.99% in four-week-old flies. This clear senescence of the Drosophila cellular immune response may underpin increased disease susceptibility in older flies.

Sperm competitive ability and indices of lifetime reproductive success.

Understanding the selection pressures shaping components of male reproductive success is essential for assessing the role of sexual selection on phenotypic evolution. A male's competitive reproductive success is often measured in sequential mating tests by recording P1 (first mating male) and P2 (second mating male) paternity scores. How each of these scores relates to a male's overall fitness, for example, lifetime reproductive success is, however, not known. This information is needed to determine whether males benefit from maximizing both P1 and P2 or by trading off P1 against P2 ability. We measured P1, P2, and an index of lifetime reproductive success (LRS(i) , a male's competitive reproductive success measured over 12 days) for individual male Drosophila melanogaster. We found no evidence for phenotypic correlations between P1 and P2. In addition, whereas both P1 and P2 were associated with relative LRS(i) , only P2 predicted absolute LRS(i) . The results suggest that P2 was most closely linked to LRS(i) in the wild-type population studied, a finding which may be common to species with strong second male sperm precedence. The study illustrates how P1 and P2 can have differing relationships with a male's overall reproductive success, and highlights the importance of understanding commonly used measures of sperm competition in the currency of fitness.

Competitive PCR reveals the complexity of postcopulatory sexual selection in Teleogryllus commodus.

The outcome of mate choice depends on complex interactions between males and females both before and after copulation. Although the competition between males for access to mates and premating choice by females are relatively well understood, the nature of interactions between cryptic female choice and male sperm competition within the female reproductive tract is less clear. Understanding the complexity of postcopulatory sexual selection requires an understanding of how anatomy, physiology and behaviour mediate sperm transfer and storage within multiply mated females. Here we use a newly developed molecular technique to directly quantify mixed sperm stores in multiple mating females of the black field cricket, Teleogryllus commodus. In this species, female postcopulatory choice is easily observed and manipulated as females delay the removal of the spermatophore in favour of preferred males. Using twice-mated females, we find that the proportion of sperm in the spermatheca attributed to the second male to mate with a female (S2) increases linearly with the time of spermatophore attachment. Moreover, we show that the insemination success of a male increases with its attractiveness and decreases with the size of the female. The effect of male attractiveness in this context suggests a previously unknown episode of mate choice in this species that reinforces the sexual selection imposed by premating choice and conflicts with the outcome of postmating male harassment. Our results provide some of the clearest evidence yet for how sperm transfer and displacement in multiply mated females can lead directly to cryptic female choice, and that three distinct periods of sexual selection operate in black field crickets.