On the resolution of sexual conflict over shared traits.

Anisogamy, different-sized male and female gametes, sits at the heart of sexual selection and conflict between the sexes. Sperm producers (males) and egg producers (females) of the same species generally share most, if not all, of the same genome, but selection frequently favours different trait values in each sex for traits common to both. The extent to which this conflict might be resolved, and the potential mechanisms by which this can occur, have been widely debated. Here, we summarize recent findings and emphasize that once the sexes evolve, sexual selection is ongoing, and therefore new conflict is always possible. In addition, sexual conflict is largely a multivariate problem, involving trait combinations underpinned by networks of interconnected genes. Although these complexities can hinder conflict resolution, they also provide multiple possible routes to decouple male and female phenotypes and permit sex-specific evolution. Finally, we highlight difficulty in the study of sexual conflict over shared traits and promising directions for future research.

Nutrition affects larval survival and the development of morphological traits in male and female flour beetles, but genital size and shape remains canalised.

The caloric content and macronutrient ratio of diet consumed is a major source of phenotypic variation in most animal populations. While these nutritional effects have been well-documented for a variety of life-history and morphological traits, the effects of nutrition on male genitals are poorly understood but genitals are thought to be more canalised than general morphology and hence less susceptible to variation in nutrition. Even less is known about the effects of nutrition on female genital form, which to our knowledge, have never been investigated. Here we tested for effects of juvenile dietary macronutrients (protein and carbohydrate) on larval survival, adult morphology, including genital size and shape in male and female flour beetles (Tribolium castaneum). We found there was nutritionally induced plasticity in larval survival and morphology, although the latter effect was variable, with body size being most responsive to dietary macronutrients and genital size and shape being least responsive. Functionally equivalent morphological traits in the sexes responded similarly to nutrition. Previously, we showed that the genitalia of male and female T. castaneum are subject to strong stabilising sexual selection, and our current findings suggest that developmental mechanisms reduce the nutritional sensitivity of male and female genitals, possibly to ensure matching during mating.

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.

Mapping sex differences in the effects of protein and carbohydrates on lifespan and reproduction in Drosophila melanogaster: is measuring nutrient intake essential?

Understanding how diet affects reproduction and survival is a central aim in evolutionary biology. Although this relationship is likely to differ between the sexes, we lack data relating diet to male reproductive traits. One exception to this general pattern is Drosophila melanogaster, where male dietary intake was quantified using the CApillary FEeder (CAFE) method. However, CAFE feeding reduces D. melanogaster survival and reproduction, so may distort diet-fitness outcomes. Here, we use the Geometric Framework of Nutrition to create nutrient landscapes that map sex-specific relationships between protein, carbohydrate, lifespan and reproduction in D. melanogaster. Rather than creating landscapes with consumption data, we map traits onto the nutrient composition of forty agar-based diets, generating broad coverage of nutrient space. We find that male and female lifespan was maximised on low protein, high carbohydrate blends (~ 1P:15.9C). This nutrient ratio also maximised male reproductive rates, but females required more protein to maximise daily fecundity (1P:1.22C). These results are consistent with CAFE assay outcomes. However, the approach employed here improved female fitness relative to CAFE assays, while effects of agar versus CAFE feeding on male fitness traits depended on the nutrient composition of experimental diets. We suggest that informative nutrient landscapes can be made without measuring individual nutrient intake and that in many cases, this may be preferable to using the CAFE approach. The most appropriate method will depend on the question and species being studied, but the approach adopted here has the advantage of creating nutritional landscapes when dietary intake is hard to quantify.

Kin-mediated plasticity in alternative reproductive tactics.

Conditional strategies occur when the relative fitness pay-off from expressing a given phenotype is contingent upon environmental circumstances. This conditional strategy model underlies cases of alternative reproductive tactics, in which individuals of one sex employ different means to obtain reproduction. How kin structure affects the expression of alternative reproductive tactics remains unexplored. We address this using the mite Rhizoglyphus echinopus, in which large males develop into aggressive 'fighters' and small males develop into non-aggressive 'scramblers.' Because only fighters kill their rivals, they should incur a greater indirect fitness cost when competing with their relatives, and thus fighter expression could be reduced in the presence of relatives. We raised mites in full-sibling or mixed-sibship groups and found that fighters were more common at higher body weights in full-sibling groups, not less common as we predicted (small individuals were almost exclusively scramblers in both treatments). This result could be explained if relatedness and cue variability are interpreted signals of population density, since fighters are more common at low densities in this species. Alternatively, our results may indicate that males compete more intensely with relatives in this species. We provide the first evidence of kin-mediated plasticity in the expression of alternative reproductive tactics.

Offspring sex ratios are stable across the life course in Drosophila simulans.

Within populations, adult sex ratios influence population growth and extinction risk, mating behaviours and parental care. Sex ratio adjustment can also have pronounced effects on individual fitness. Accordingly, it is important that we understand how often, and why, offspring sex ratios deviate from parity. In Drosophila melanogaster, females appear to improve their fitness by producing fewer sons when paired with older males. However, facultative sex ratio adjustment in D. melanogaster is controversial, and our understanding of how sex ratio skew affects fitness is hampered by pronounced sexual conflict in this species. Additionally, it is unclear whether maternal age or quality interacts with paternal age to influence offspring sex ratios. Here, we test whether offspring sex ratios vary as a function of maternal quality, and maternal and paternal age in Drosophila simulans, a sister species of D. melanogaster that lacks overt sexual conflict. We find that offspring sex ratios are slightly male-biased overall, but constant across the female life course, and independent of female quality, or paternal age. To really understand if, how and when females skew offspring sex ratios, we need studies linking offspring sex ratios to paternal and maternal phenotypes that are predicted to shift optimal investment in sons and daughters.

Loser-effect duration evolves independently of fighting ability.

Winning or losing contests can impact subsequent competitive behaviour and the duration of these effects can be prolonged. While it is clear effects depend on social and developmental environments, the extent to which they are heritable, and hence evolvable, is less clear and remains untested. Furthermore, theory predicts that winner and loser effects should evolve independently of actual fighting ability, but again tests of this prediction are limited. Here we used artificial selection on replicated beetle populations to show that the duration of loser effects can evolve, with a realized heritability of about 17%. We also find that naive fighting ability does not co-evolve with reductions in the duration of the loser effect. We discuss the implications of these findings and how they corroborate theoretical predictions.

Climate change and pollution speed declines in zebrafish populations.

Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28 °C (current ambient mean spawning temperature) and 33 °C (projected for the year 2100). The EDC selected was clotrimazole (at 2 µg/L and 10 µg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced male-skewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.

Pleiotropic Effects of DDT Resistance on Male Size and Behaviour.

Understanding the evolution and spread of insecticide resistance requires knowing the relative fitness of resistant organisms. In the absence of insecticides, resistance is predicted to be costly. The Drosophila melanogaster DDT resistance allele (DDT-R) is associated with a male mating cost. This could be because resistant males are generally smaller, but DDT-R may also alter courtship behaviours. Here we tested for body size and courtship effects of DDT-R on mating success in competitive and non-competitive mating trials respectively. We also assessed relative aggression in resistant and susceptible males because aggression can also influence mating success. While the effect of DDT-R on male size partly contributed to reduced mating success, resistant males also had lower rates of courtship and were less aggressive than susceptible males. These differences contribute to the observed DDT-R mating costs. Additionally, these pleiotropic effects of DDT-R are consistent with the history and spread of resistance alleles in nature.

Experimental evolution under hyper-promiscuity in Drosophila melanogaster.

BACKGROUND: The number of partners that individuals mate with over their lifetime is a defining feature of mating systems, and variation in mate number is thought to be a major driver of sexual evolution. Although previous research has investigated the evolutionary consequences of reductions in the number of mates, we know little about the costs and benefits of increased numbers of mates. Here, we use a genetic manipulation of mating frequency in Drosophila melanogaster to create a novel, highly promiscuous mating system. We generated D. melanogaster populations in which flies were deficient for the sex peptide receptor (SPR) gene - resulting in SPR- females that mated more frequently - and genetically-matched control populations, and allowed them to evolve for 55 generations. At several time-points during this experimental evolution, we assayed behavioural, morphological and transcriptional reproductive phenotypes expected to evolve in response to increased population mating frequencies. RESULTS: We found that males from the high mating frequency SPR- populations evolved decreased ability to inhibit the receptivity of their mates and decreased copulation duration, in line with predictions of decreased per-mating investment with increased sperm competition. Unexpectedly, SPR- population males also evolved weakly increased sex peptide (SP) gene expression. Males from SPR- populations initially (i.e., before experimental evolution) exhibited more frequent courtship and faster time until mating relative to controls, but over evolutionary time these differences diminished or reversed. CONCLUSIONS: In response to experimentally increased mating frequency, SPR- males evolved behavioural responses consistent with decreased male post-copulatory investment at each mating and decreased overall pre-copulatory performance. The trend towards increased SP gene expression might plausibly relate to functional differences in the two domains of the SP protein. Our study highlights the utility of genetic manipulations of animal social and sexual environments coupled with experimental evolution.

Sexual conflict maintains variation at an insecticide resistance locus.

BACKGROUND: The maintenance of genetic variation through sexually antagonistic selection is controversial, partly because specific sexually-antagonistic alleles have not been identified. The Drosophila DDT resistance allele (DDT-R) is an exception. This allele increases female fitness, but simultaneously decreases male fitness, and it has been suggested that this sexual antagonism could explain why polymorphism was maintained at the locus prior to DDT use. We tested this possibility using a genetic model and then used evolving fly populations to test model predictions. RESULTS: Theory predicted that sexual antagonism is able to maintain genetic variation at this locus, hence explaining why DDT-R did not fix prior to DDT use despite increasing female fitness, and experimentally evolving fly populations verified theoretical predictions. CONCLUSIONS: This demonstrates that sexually antagonistic selection can maintain genetic variation and explains the DDT-R frequencies observed in nature.

Sexual conflict over mating in Gnatocerus cornutus? Females prefer lovers not fighters.

Female mate choice and male-male competition are the typical mechanisms of sexual selection. However, these two mechanisms do not always favour the same males. Furthermore, it has recently become clear that female choice can sometimes benefit males that reduce female fitness. So whether male-male competition and female choice favour the same or different males, and whether or not females benefit from mate choice, remain open questions. In the horned beetle, Gnatocerus cornutus, males have enlarged mandibles used to fight rivals, and larger mandibles provide a mating advantage when there is direct male-male competition for mates. However, it is not clear whether females prefer these highly competitive males. Here, we show that female choice targets male courtship rather than mandible size, and these two characters are not phenotypically or genetically correlated. Mating with attractive, highly courting males provided indirect benefits to females but only via the heritability of male attractiveness. However, mating with attractive males avoids the indirect costs to daughters that are generated by mating with competitive males. Our results suggest that male-male competition may constrain female mate choice, possibly reducing female fitness and generating sexual conflict over mating.

The condition-dependence of male genital size and shape.

The male genitals of internal fertilisers evolve rapidly and divergently, and sexual selection is generally responsible for this. Many sexually selected traits are condition-dependent-with their expression dependent upon the resources available to be allocated to them-as revealed by genetic or environmental manipulations of condition. However, it is not clear whether male genitals are also condition-dependent. Here we manipulate condition in two ways (via inbreeding and diet) to test the condition-dependence of the genital arch of Drosophila simulans. We found that genital size but not genital shape suffered from inbreeding depression, whereas genital size and shape were affected by dietary manipulation of condition. The differential effects of these treatments likely reflect underlying genetic architecture that has been shaped by past selection: inbreeding depression is only expected when traits have a history of directional selection, while diet impacts traits regardless of historical selection. Nonetheless, our results suggest genitals can be condition-dependent like other sexually selected traits.

The evolutionary ecology of ethanol.

The consumption of ethanol has frequently been seen as largely restricted to humans. Here, we take a broad eco-evolutionary approach to understanding ethanol's potential impact on the natural world. There is growing evidence that ethanol is present in many wild fruits, saps, and nectars and that ethanol ingestion offers benefits that favour adaptations for its use in multiple taxa. Explanations for ethanol consumption span both the nutritional and non-nutritional, with potential medicinal value or cognitive effects (with social-behavioural benefits) explored. We conclude that ethanol is ecologically relevant and that it has shaped the evolution of many species and structured symbiotic relationships among organisms, including plants, yeast, bacteria, insects, and mammals.

Intralocus sexual conflict and offspring sex ratio.

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.

The genetics of cuticular hydrocarbon profiles in the Fruit Fly Drosophila simulans.

Female mate choice is one mechanism of sexual selection and, provided there is adequate genetic variation in the male traits that are the target of this selection, they will evolve via female choice. Cuticular hydrocarbons (CHCs) are important in Drosophila mate choice, but relatively little is known about the underlying genetic architecture of CHC profiles in Drosophila simulans. Here, we used gas chromatography-mass spectrometry to investigate patterns of genetic variation in the CHC profiles of male and female D. simulans using isofemale lines. We found substantial genetic variation for CHC profiles and individual CHC components, and individual CHCs were frequently strongly genetically correlated, with a tendency for negative covariance between long- and short-chain CHCs in males. Intersexual genetic covariances were often weak and frequently differed in sign. These findings are novel and significant, highlighting the previously unexplored genetic architecture of CHCs in D. simulans and suggest that this architecture may facilitate sex-specific CHC evolution.

Digest: Brain or brawn: Trade-offs between brain size and flight mode in birds.

Brain size is extremely variable across species, and its evolution depends upon the calorific trade-offs between it and other organs and activities. Shiomi investigated potential brain size trade-offs with different flight modes in birds. Flight can be energetically expensive, and costs are especially high with powered flight. This comparative study indicated that migratory birds employing less energetic modes of flight had relatively larger brains than migratory birds using powered flight, suggesting that brain size is impacted by the energetic costs of flight.

The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg.

Recent studies of centrosome biogenesis, microtubule dynamics, and their management point to their role in mediating conditions such as aging and cancer. Centrosome dysfunction is also a hallmark of pathological polyspermy. Polyspermy occurs when the oocyte is penetrated by more than one sperm and can be pathological because an excess of centrosomes compromises development. However, in some taxa, multiple sperm enter the egg with no apparent adverse effect on zygote viability. Thus, some taxa can manage excess centrosomes and represent cases of non-pathological polyspermy. While these two forms of polyspermy have long been known, we argue that there is limited understanding of the proximate and ultimate processes that underlie this taxonomic variation in the outcome of polyspermy and that studying this variation could help uncover the control and role(s) of centrosomes during fertilization in particular, but also mitosis in general. To encourage such studies we: 1) describe taxonomic differences in the outcome of polyspermy, 2) discuss mechanistic aspects of reproductive biology that may contribute to the different consequences of polyspermy, and 3) outline the potential selective events that could lead to the evolution of variation in polyspermy outcomes. We suggest that novel insights into centrosome biology may occur by cooperative studies between reproductive and evolutionary biologists focusing on the mechanisms generating variation in the fitness consequences of polyspermy, and in the taxonomic distribution of all these events. The consequent discoveries of these studies may lead to informative insights into cancer and aging along with other centrosome-related diseases and syndromes.

Peaks in bat activity at turbines and the implications for mitigating the impact of wind energy developments on bats.

Wind turbines are a relatively new threat to bats, causing mortalities worldwide. Reducing these fatalities is essential to ensure that the global increase in wind-energy facilities can occur with minimal impact on bat populations. Although individual bats have been observed approaching wind turbines, and fatalities frequently reported, it is unclear whether bats are actively attracted to, indifferent to, or repelled by, the turbines at large wind-energy installations. In this study, we assessed bat activity at paired turbine and control locations at 23 British wind farms. The research focussed on Pipistrellus species, which were by far the most abundant bats recorded at these sites. P. pipistrellus activity was 37% higher at turbines than at control locations, whereas P. pygmaeus activity was consistent with no attraction or repulsion by turbines. Given that more than 50% of bat fatalities in Europe are P. pipistrellus, these findings help explain why Environmental Impact Assessments conducted before the installation of turbines are poor predictors of actual fatality rates. They also suggest that operational mitigation (minimising blade rotation in periods of high collision risk) is likely to be the most effective way to reduce collisions because the presence of turbines alters bat activity.