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paco.garcia[at]ebd.csic.es

Male-by-female interactions

Publications filtered by: Male-by-female interactions

Lifetime changes in phenotypic expression and evolutionary potential of female mating traits in Drosophila melanogaster
Travers, L. M., Simmons, L. W. & Garcia-Gonzalez, F. 2016 Lifetime changes in phenotypic expression and evolutionary potential of female mating traits in Drosophila melanogaster Animal Behaviour, 121: 147-155
Abstract

Recognition of the ubiquity of female multiple mating has evoked an important shift in sexual selection research, emphasising the adaptive nature of female mating strategies. While phenotypic changes in female mating traits have been previously studied, little is known about the genetic basis of female mating behaviour and its potential to respond to selection at different stages throughout an individual’s life. Using a large quantitative genetic breeding design, we observed lifetime female mating behaviour in Drosophila melanogaster to examine the effect of female age and mating history on three key mating traits: courtship latency, mating latency and copula duration. Courtship latency (time until males initiate courtship) decreased with the cumulative number of females’ previous matings. Mating latency (defined here as the time between the beginning of courtship and the start of copulation) increased with female age, and copula duration was found to decrease as females aged. We calculated quantitative genetic estimates for mating traits in virgin females and at the females’ third mating to examine changes in the evolutionary potential of mating traits. We found considerable additive genetic variation in courtship latency and mating latency measured in virgin females. Copula duration displayed no heritable variation among females across sire families, but male effects were consistent with the idea that this trait is under male control. Heritability estimates differed significantly from zero in virgin females for courtship latency and mating latency. Heritability estimates did not differ significantly from zero when females were mating for the third time. However, overlapping 84% confidence intervals between heritability estimates obtained from virgin and mated females suggest that female mating strategies may have the potential to respond to selection at these different life stages.

Additive genetic variance in polyandry enables its evolution but polyandry is unlikely to evolve through sexy or good sperm processes
Travers, L. M., Simmons, L. W. & Garcia-Gonzalez, F. 2016 Additive genetic variance in polyandry enables its evolution but polyandry is unlikely to evolve through sexy or good sperm processes Journal of Evolutionary Biology, 29: 916-928.
Abstract

Polyandry is widespread despite its costs. The sexually selected sperm hypotheses (‘sexy’ and ‘good’ sperm) posit that sperm competition plays a role in the evolution of polyandry. Two poorly studied assumptions of these hypotheses are the presence of additive genetic variance in polyandry and sperm competitiveness. Using a quantitative genetic breeding design in a natural population of Drosophila melanogaster, we first established the potential for polyandry to respond to selection. We then investigated whether polyandry can evolve through sexually selected sperm processes. We measured lifetime polyandry and offensive sperm competitiveness (P2) while controlling for sampling variance due to male x male x female interactions. We also measured additive genetic variance in egg-to-adult viability and controlled for its effect on P2 estimates. Female lifetime polyandry showed significant and substantial additive genetic variance and evolvability. In contrast, we found little genetic variance or evolvability in P2 or egg-to-adult viability. Additive genetic variance in polyandry highlights its potential to respond to selection. However, the low levels of genetic variance in sperm competitiveness suggest the evolution of polyandry may not be driven by sexy sperm or good sperm processes.

Bet-hedging as a mechanism for the evolution of polyandry, revisited
Yasui, Y. & Garcia-Gonzalez, F. 2016 Bet-hedging as a mechanism for the evolution of polyandry, revisited Evolution, 70: 385-397
Abstract

Females that mate with multiple males (polyandry) may reduce the risk that their eggs are fertilized by a single unsuitable male. About 25 years ago it was hypothesized that bet-hedging could function as a mechanism favoring the evolution of polyandry, but this idea is controversial because theory indicates that bet-hedging via polyandry can compensate the costs of mating only in small populations. Nevertheless, populations are often spatially structured, and even in the absence of spatial structure, mate choice opportunity can be limited to a few potential partners. We examined the effectiveness of bet-hedging in such situations with simulations carried out under two scenarios; (1) intrinsic male quality, with offspring survival determined by male phenotype (male’s ability to generate viable offspring), and (2) genetic incompatibility (offspring fitness determined non-additively by parental genotypes). We find higher fixation probabilities for a polyandrous strategy compared to a monandrous strategy if complete reproductive failure due to male effects or parental incompatibility is pervasive in the population. Our results also indicate that bet-hedging polyandry can delay the extinction of small demes. Our results underscore the potential for bet-hedging to provide benefits to polyandrous females and have valuable implications for conservation biology.

Travers, L. M., Garcia-Gonzalez, F. & Simmons, L. W. 2015 Live fast die young life history in females: evolutionary trade-off between early life mating and lifespan in female Drosophila melanogaster Scientific Reports, 5: 15469
Abstract

The trade-off between survival and reproduction is fundamental to life history theory. Sexual selection is expected to favour a live fast die young life history pattern in males due to increased risk of extrinsic mortality associated with obtaining mates. Sexual conflict may also drive a genetic trade-off between reproduction and lifespan in females. We found significant additive genetic variance in longevity independent of lifetime mating frequency, and in early life mating frequency. There was significant negative genetic covariance between these traits indicating that females from families characterized by high levels of multiple mating early in life die sooner than females that engage in less intense early life mating.  Thus, despite heritable variation in both traits, their independent evolution is constrained by an evolutionary trade-off. Our findings indicate that, in addition to the well-known male-driven direct costs of mating on female lifespan (mediated by male harassment and the harmful effects of male seminal fluids), females with a genetic propensity to mate multiply live shorter lives. We discuss the potential role of sexual conflict in driving the evolutionary trade-off between reproduction and lifespan in Drosophila. More generally, our data show that, like males, females can exhibit a live fast die young life history strategy.

Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation
Garcia-Gonzalez, F. and Dowling, D. K. 2015 Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation Biology Letters, 11:20150067
Abstract

The consequences of sexual interactions extend beyond the simple production of offspring. These interactions typically entail direct effects on female fitness, but may also impact the life histories of later generations. Evaluating the cross-generational effects of sexual interactions provides insights into the dynamics of sexual selection and conflict. Such studies can elucidate whether offspring fitness optima diverge across sexes upon heightened levels of sexual interaction among parents. Here, we found that, in Drosophila melanogaster, components of reproductive success in females, but not males, were contingent on the nature of sexual interactions experienced by their mothers. In particular, maternal sexual interactions with non-sires enhanced female fecundity in the following generation. This highlights the importance of non-sire influences of sexual interactions on the expression of offspring life histories.The consequences of sexual interactions extend beyond the simple production of offspring. These interactions typically entail direct effects on female fitness, but may also impact the life histories of later generations. Evaluating the cross-generational effects of sexual interactions provides insights into the dynamics of sexual selection and conflict. Such studies can elucidate whether offspring fitness optima diverge across sexes upon heightened levels of sexual interaction among parents. Here, we found that, in Drosophila melanogaster, components of reproductive success in females, but not males, were contingent on the nature of sexual interactions experienced by their mothers. In particular, maternal sexual interactions with non-sires enhanced female fecundity in the following generation. This highlights the importance of non-sire influences of sexual interactions on the expression of offspring life histories.

Mating portfolios: bet-hedging, sexual selection and female multiple mating
Garcia-Gonzalez, F., Yasui, Y. and Evans, J. P. 2015 Mating portfolios: bet-hedging, sexual selection and female multiple mating Proceedings of the Royal Society of London B, 282: 20141525
Abstract

Polyandry (female multiple mating) has profound evolutionary and ecological implications. Despite considerable work devoted to understanding why females mate multiply, we currently lack convincing empirical evidence to explain the adaptive value of polyandry. Here we provide a direct test of the controversial idea that bet-hedging functions as a risk-spreading strategy that yields multi-generational fitness benefits to polyandrous females. Unfortunately, testing this hypothesis is far from trivial, and the empirical comparison of the across-generations fitness payoffs of a polyandrous (bet hedger) versus a monandrous (non-bet hedger) strategy has never been accomplished because of numerous experimental constraints presented by most ‘model’ species. In the present study we take advantage of the extraordinary tractability and versatility of a marine broadcast spawning invertebrate to overcome these challenges. We are able to simulate multi-generational (geometric mean) fitness among individual females assigned simultaneously to a polyandrous and monandrous mating strategy. Our approaches, which separate and account for the effects of sexual selection and pure bet-hedging scenarios, reveal that bet-hedging, in addition to sexual selection, can enhance evolutionary fitness in multiply-mated females. In addition to offering a tractable experimental approach for addressing bet-hedging theory, our study provides key insights into the evolutionary ecology of sexual interactions.

Shorter sperm confer higher competitive fertilization success
Garcia-Gonzalez, F. & Simmons, L. W. 2007 Shorter sperm confer higher competitive fertilization success Evolution, 61: 816-824
Abstract

Spermatozoa exhibit taxonomically widespread patterns of divergent morphological evolution. However, the adaptive significance of variation in sperm morphology remains unclear. In this study we examine the role of natural variation in sperm length on fertilization success in the dung beetle Onthophagus taurus. We conducted sperm competition trials between males that differed in the length of their sperm and determined the paternity of resulting offspring using amplified fragment length polymorphism (AFLP) markers. We also quantified variation in the size and shape of the female’s sperm storage organ to determine whether female morphology influenced the competitiveness of different sperm morphologies. We found that fertilization success was biased toward males with relatively shorter sperm, but that selection on sperm length was dependent on female tract morphology; selection was directional for reduced sperm length across most of the spermathecal size range, but stabilizing in females with the smallest spermathecae. Our data provide empirical support for the theory that sperm competition should favor the evolution of numerous tiny sperm. Moreover, because sperm length is both heritable and genetically correlated with condition, our results are consistent with a process by which females can accrue genetic benefits for their offspring from the incitement of sperm competition and/or cryptic female choice, as proposed by the “sexy sperm” and “good sperm” models for the evolution of polyandry.

Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate
Evans, J. P., F. Garcia-Gonzalez, M. Almbro, O. Robinson, & J. L. Fitzpatrick. 2012 Assessing the potential for egg chemoattractants to mediate sexual selection in a broadcast spawning marine invertebrate Proceedings of the Royal Society of London B, 279:2855-2861
Abstract

In numerous species, egg chemoattractants play a critical role in guiding sperm towards unfertilized eggs (sperm chemotaxis). Until now the known functions of sperm chemotaxis include increasing the effective target size of eggs, thereby promoting sperm-egg encounters, and facilitating species recognition. Here we report that in the broadcast spawning mussel Mytilus galloprovincialis egg chemoattractants may play an unforeseen role in sexual selection by enabling sperm to effectively ‘choose’ between the eggs of different conspecific females. In an initial experiment we confirmed that sperm chemotaxis occurs in M. galloprovincialis by showing that sperm are attracted towards unfertilized eggs when given the choice of eggs or no eggs in a dichotomous chamber. We then conducted two cross-classified mating experiments, each comprising the same individual males and females crossed in identical male x female combinations but under experimental conditions that offered sperm ‘no-choice’ (each fertilization trial took place in a petri dish and involved a single male and female) or a ‘choice’ of a female’s eggs (sperm were placed in the centre of a dichotomous choice chamber and allowed to choose eggs from different females). We show that male-by-female interactions characterized fertilization rates in both experiments, and that there was remarkable consistency between patterns of sperm migration in the egg choice experiment and fertilization rates in the no-choice experiment. These results reveal that sperm differentially select eggs on the basis of chemical cues, thus exposing the potential for egg chemoattractants to mediate mate choice for genetically compatible partners. Given the prevalence of sperm chemotaxis across diverse taxa, our findings may have broad implications for sexual selection in other mating systems.