Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild.

Females often mate with several males before producing offspring. Field studies of vertebrates suggest, and laboratory experiments on invertebrates confirm, that even when males provide no material benefits, polyandry can enhance offspring survival. This enhancement is widely attributed to genetic benefits that arise whenever paternity is biased towards males that sire more viable offspring. Field studies suggest that post-mating sexual selection biases fertilization towards genetically more compatible males and one controlled experiment has shown that, when females mate with close kin, polyandry reduces the relative number of inbred offspring. Another potential genetic benefit of polyandry is that it increases offspring survival because males with more competitive ejaculates sire more viable offspring. Surprisingly, however, there is no unequivocal evidence for this process. Here, by experimentally assigning mates to females, we show that polyandry greatly increases offspring survival in the Australian marsupial Antechinus stuartii. DNA profiling shows that males that gain high paternity under sperm competition sire offspring that are more viable. This beneficial effect occurs in both the laboratory and the wild. Crucially, there are no confounding non-genetic maternal effects that could arise if polyandry increases female investment in a particular reproductive event because A. stuartii is effectively semelparous. Our results therefore show that polyandry improves female lifetime fitness in nature. The threefold increase in offspring survival is not negated by a decline in maternal lifespan and is too large to be offset by an equivalent decline in the reproductive performance of surviving offspring.

Fisher DO ，Double MC ，Blomberg SP ，Jennions MD ，Cockburn A ... -  《-》

Do female black field crickets Teleogryllus commodus benefit from polyandry?

Female insects that mate multiply tend to have increased lifetime fitness, apparently because of greater access to male-derived resources (e.g. sperm, nuptial gifts) that elevate fertility/fecundity. Experiments that standardize the number of matings per female also show that polyandry can improve aspects of offspring performance, most notably early embryo survival (egg hatching success). This improvement is widely attributed to genetic benefits which would arise if polyandrous females skew paternity to produce fitter offspring. In two separate experiments with field crickets (Teleogryllus commodus) polyandrous females (two, three or four mates) did not have higher egg hatching success than monandrous females (effect sizes: r = 0.03 and 0.08 for the respective experiments), which is consistent with our finding of no sire effect on hatching success. Polyandry also had no effect on post-hatching offspring survival. Polyandrous females' offspring took significantly longer to mature but their sons were not heavier and their daughters were actually significantly smaller than those of monandrous females. Finally, after controlling for relative male size, monandrous females' sons were more successful when directly competing for a mate.

Jennions MD ，Drayton JM ，Brooks R ，Hunt J ... -  《JOURNAL OF EVOLUTIONARY BIOLOGY》

Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii.

Mating in the marsupial genus Antechinus is a synchronous annual event that is characterized by monoestry in females and abrupt postmating mortality in males. Male semelparity (multiple copulations during a single breeding season per lifetime) is often assumed to occur as a consequence of the intense mating effort expended by males in the rut, but the forces selecting for this remain elusive. Here, we investigate selection in male brown antechinus, Antechinus stuartii, and test two hypotheses for the evolution of semelparity: intermale competition and sperm competition. If intermale competition drives semelparity, we predicted that males would be under strong selection for large body size. If sperm competition is important, we predicted that selection would be strongest on scrotal size, a surrogate for testes volume. Using microsatellite markers, we found that 92% of females in free-living conditions mated with multiple males, producing litters of eight that had up to four fathers. These observations confirm the potential for sperm competition. Using selection analysis, we then found paternity success in 119 males to be related most strongly to body mass and scrotal size, thus providing support for both hypotheses. Large males presumably experience increased paternity success by gaining more matings or prolonged copulations via mate guarding, while large testes may allow increased sperm investment per copulation. Increased levels of free corticosteroid hormones in males facilitate the extreme mating effort during the short period of rut, but lead to immune suppression and consequently to the phenomenon of postmating mortality.

Holleley CE ，Dickman CR ，Crowther MS ，Oldroyd BP ... -  《MOLECULAR ECOLOGY》

An integrative view of sexual selection in Tribolium flour beetles.

Sexual selection is a major force driving the evolution of diverse reproductive traits. This evolutionary process is based on individual reproductive advantages that arise either through intrasexual competition or through intersexual choice and conflict. While classical studies of sexual selection focused mainly on differences in male mating success, more recent work has focused on the differences in paternity share that may arise through sperm competition or cryptic female choice whenever females mate with multiple males. Thus, an integrative view of sexual selection needs to encompass processes that occur not only before copulation (pre-mating), but also during copulation (peri-mating), as well as after copulation (post-mating), all of which can generate differences in reproductive success. By encompassing mechanisms of sexual selection across all of these sequential reproductive stages this review takes an integrative approach to sexual selection in Tribolium flour beetles (Coleoptera: Tenebrionidae), a particularly well-studied and economically important model organism. Tribolium flour beetles colonize patchily distributed grain stores, and juvenile and adult stages share the same food resources. Adults are highly promiscuous and female reproduction is distributed across an adult lifespan lasting approximately 1 year. While Tribolium males produce an aggregation pheromone that attracts both sexes, there appears to be little pre-mating discrimination among potential mates by either sex. However, recent work has revealed several peri-mating and post-mating mechanisms that determine how offspring paternity is apportioned among a female's mates. During mating, Tribolium females reject spermatophore transfer and limit sperm numbers transferred by males with low phenotypic quality. Although there is some conflicting evidence, male copulatory leg-rubbing appears to be associated with overcoming female resistance to insemination and does not influence a male's subsequent paternity share. Evidence suggests that Tribolium beetles have several possible post-mating mechanisms that they may use to bias paternity. Male sperm precedence has been extensively studied in Tribolium spp. and the related Tenebrio molitor, and several factors influencing male paternity share among a female's progeny have been identified. These include oviposition time, inter-mating interval, male strain/genotype, the mating regimen of a male's mother, male starvation, and tapeworm infection. Females exert muscular control over sperm storage, although there is no evidence to date that females use this to differentiate among mates. Females could also influence offspring paternity by re-mating with additional males, and T. castaneum females more readily accept spermatophores when they are re-mating with more attractive males. Additional work is needed to examine the possible roles played by both male and female accessory gland products in determining male paternity share. Sexual selection during pre-mating episodes may be reinforced or counteracted by peri- and post-copulatory selection, and antagonistic coevolution between the sexes may be played out across reproductive stages. In Tribolium, males' olfactory attractiveness is positively correlated with both insemination success and paternity share, suggesting consistent selection across different reproductive stages. Similar studies across sequential reproductive stages are needed in other taxa to provide a more integrative view of sexual selection.

Fedina TY ，Lewis SM 《-》

Postmating sexual selection favors males that sire offspring with low fitness.

Despite the costs of mating, females of most taxa mate with multiple males. Polyandrous females are hypothesized to gain genetic benefits for their offspring, but this assumes paternity bias favoring male genotypes that enhance offspring viability. We determined net male genetic effects on female and offspring fitness in a seed beetle and then tested whether fertilization success was biased in favor of high-quality male genotypes in double mating experiments. Contrary to expectations, high-quality male genotypes consistently had a lower postmating fertilization success in two independent assays. Our results imply that sexually antagonistic adaptations have a major and unappreciated influence on male postmating fertilization success. Such genetic variation renders indirect genetic benefits an unlikely driver of the evolution of polyandry.

Bilde T ，Foged A ，Schilling N ，Arnqvist G ... -  《-》