Investigating the interaction between inter-locus and intra-locus sexual conflict using hemiclonal analysis in Drosophila melanogaster

Divergence in the evolutionary interests of males and females leads to sexual conflict. Traditionally, sexual conflict has been classified into two types: inter-locus sexual conflict (IeSC) and intra-locus sexual conflict (IaSC). IeSC is modeled as a conflict over outcomes of intersexual reproductive interactions mediated by loci that are sex-limited in their effects. IaSC is thought to be a product of selection acting in opposite directions in males and females on traits with a common underlying genetic basis. While in their canonical formalisms IaSC and IeSC are mutually exclusive, there is growing support for the idea that the two may interact. Empirical evidence for such interactions, however, is limited. Here, we investigated the interaction between IeSC and IaSC in Drosophila melanogaster. Using hemiclonal analysis, we sampled 39 hemigenomes from a laboratory-adapted population of D. melanogaster. We measured the contribution of each hemigenome to adult male and female fitness at three different intensities of IeSC, obtained by varying the operational sex-ratio. Subsequently, we estimated the intensity of IaSC at each sex-ratio by calculating the intersexual genetic correlation for fitness and the proportion of sexually antagonistic fitness-variation. Our results indicate a statistically non-significant trend suggesting that increasing the strength of IeSC ameliorates IaSC in the population.

Male diet affects female fitness and sperm competition in human- and bat-associated lineages of the common bedbug, Cimex lectularius

Sperm performance can vary in ecologically divergent populations, but it is often not clear whether the environment per se or genomic differences arising from divergent selection cause the difference. One powerful and easily manipulated environmental effect is diet. Populations of bedbugs (Cimex lectularius) naturally feed either on bat or human blood. These are diverging genetically into a bat-associated and a human-associated lineage. To measure how male diet affects sperm performance, we kept males of two HL and BL populations each on either their own or the foreign diet. Then we investigated male reproductive success in a single mating and sperm competition context. We found that male diet affected female fecundity and changed the outcome of sperm competition, at least in the human lineage. However, this influence of diet on sperm performance was moulded by an interaction. Bat blood generally had a beneficial effect on sperm competitiveness and seemed to be a better food source in both lineages. Few studies have examined the effects of male diet on sperm performance generally, and sperm competition specifically. Our results reinforce the importance to consider the environment in which sperm are produced. In the absence of gene flow, such differences may increase reproductive isolation. In the presence of gene flow, however, the generally better sperm performance after consuming bat blood suggests that the diet is likely to homogenise rather than isolate populations.

Twisting to freedom: The evolution of copulation termination techniques across 48 species of sepsids (Diptera, Sepsidae)

Studies of insect mating behaviour usually focus on what happens before and during copulation. Few pay close attention to the actions needed to end copulation. However, genital separation after copulation is likely to be an important cause of mechanical stress and injuries because it often involves the withdrawal of heavily armoured male intromittent organs from membranous female reproductive tracts. Difficult and/or slow separations can also reduce male and female fitness by increasing their exposure to predation. We here report the results of a comparative study of separation behaviour in 48 species of Sepsidae (Diptera) and one outgroup. We find a surprising amount of qualitative and quantitative behavioural variability within and between species. We characterize and reconstruct three types of behaviours: 1) The sepsid ancestor likely used `back-off; a gentle separation technique that does not involve any pulling or twisting (https://youtu.be/EbkJvOaubZ0). 2) This potentially gave rise to the most common `pull' technique where the male turns 180 degrees and pulls in an opposite direction from the female (https://youtu.be/oLf4xGpkk1s). This separation can be quick and straightforward, but in some species the `pull' is slow and protracted and we routinely find dead males and/or females attached to their living partners in the latter (difficult: https://youtu.be/MbYPbXN6jr0; failure: https://youtu.be/leTiXefFzCc). 3) Finally, several species use `twist', a new technique where the male rotates >360 degrees from the initial mounting position (https://youtu.be/WMUXbIPyLbk). We document that species capable of using `twist' have shorter and less variable separation times than those using "pull". However, many species capable of `twist' also retain the ability to use `pull' (`back-off'/'pull'= 8%; `pull' only= 41%; `twist'/ `pull'= 24%; `twist' only = 27%). Overall, our study suggests that separation behaviour can vary among closely related species and highlights the significance of studying variable behavioural traits in a phylogenetic context.

Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait

Theory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.

Traumatic mating increases anchorage of mating male and reduces female remating duration and fecundity in a scorpionfly species

Traumatic mating is the male wounding his mate during mating using specialized anatomy. However, why males have evolved to injure their mates during mating remains poorly understood. We studied traumatic mating in Dicerapanorpa magna to determine its effects on male and female fitness. The sharp teeth on male gonostyli penetrate the female genitalia and cause copulatory wounds, and the number of scars on the female genitals is positively related to the number of times females mated. When the injurious teeth were encased with low-temperature wax, preventing their penetration of the female's genitalia during mating, male mating success and copulation duration were reduced significantly, indicating the importance of the teeth in allowing the male to secure copulation, remain in copula and effectively inseminate his mate. The remating experiments showed that traumatic mating had little effect on the female mating refractory period, but significantly reduced female remating duration with subsequent males, probably benefiting the first-mating male with longer copulation duration and transferring more sperm into the female's spermatheca. The copulatory wounds reduced female fecundity, but did not accelerate the timing of egg deposition. This is probably the first report that traumatic mating reduces female remating duration through successive remating experiments in animals. Overall, our results provide evidence that traumatic mating in the scorpionfly helps increase the male's anchoring control during mating and provides him advantage in sperm competition, but at the expense of lowering female fecundity.

Florivory by the occupants of phytotelmata in flower parts can decrease host plant fecundity

Some types of plant accumulate liquid in their inflorescences creating phytotelmata. These environments protect the flowers against florivory, although they may be colonized by aquatic or semi-aquatic florivorous insect larvae, whose effects on the fitness of the plants remain unclear. We tested the hypothesis of floral antagonism by the occupants of phytotelmata, which predicts that florivory by the occupants of the phytotelmata represents a cost to the female fitness of the plant, reducing its fecundity. We manipulated experimentally the infestation by three florivores larvae species occupants of phytotelmata in inflorescences of Heliconia spathocircinata (Heliconiaceae) to test for negative direct trophic effects on the fecundity of the flowering and fruiting bracts. We found that the foraging of the hoverfly (Syrphidae) and moth (Lepidoptera) larvae in the inflorescences contributed to a decline in the fecundity of the plant. While the lepidopteran impacted fecundity when foraging in both flowering and fruiting bracts, the syrphid only affected the fruiting bracts, which indicates that the nectar and floral tissue are the principal resource exploited by the hoverfly. By contrast, soldier fly (Stratiomyidae) had a neutral effect on fecundity, while foraging in flowering or fruiting bracts. These findings corroborate our hypothesis, that herbivory by the larval occupants represents cost to the host plant having phytotelmata. The negative influence of this foraging on plant fecundity will nevertheless depend on the consequences of the exploitation of resources, which vary considerably in ephemeral habitats such as the phytotalmanta of flower parts.

Male coercion and female injury in a sexually cannibalistic mantis

Sexual conflict can generate coercive traits in males that enhance mating success at the expense of female fitness. Pre-copulatory sexual cannibalism—where females consume males without mating—typically favours cautious rather than coercive mating tactics, and few examples of the latter are known. Here, we show that males of the highly cannibalistic springbok mantis, Miomantis caffra , wrestle females during pre-mating interactions. We find that most initial contacts between males and females involve a violent struggle whereby each sex tries be the first to grasp hold of the other with their raptorial forelegs. When females win the struggle, they always cannibalize males. However, when males grasp females first, they dramatically increase the chance of mating. We also find striking evidence that, on some occasions, males wound females with their fore-tibial claws during struggles, resulting in haemolymph loss and scar tissue formation. Taken together, our results show how males can overcome the threat of cannibalism by coercively wrestling females. We argue that pre-copulatory injury in this species is likely to be a negative pleiotropic side-effect of coercive mating behaviour and foraging morphology.