It is well known that sexual selection can target reproductive traits during successive pre‐ and post‐mating episodes of selection. A key focus of recent studies has been to understand and quantify ...how these episodes of sexual selection interact to determine overall variance in reproductive success. In this article, we review empirical developments in this field but also highlight the considerable variability in patterns of pre‐ and post‐mating sexual selection, attributable to variation in patterns of resource acquisition and allocation, ecological and social factors, genotype‐by‐environment interaction and possible methodological factors that might obscure such patterns. Our aim is to highlight how (co)variances in pre‐ and post‐mating sexually selected traits can be sensitive to changes in a range of ecological and environmental variables. We argue that failure to capture this variation when quantifying the opportunity for sexual selection may lead to erroneous conclusions about the strength, direction or form of sexual selection operating on pre‐ and post‐mating traits. Overall, we advocate for approaches that combine measures of pre‐ and post‐mating selection across contrasting environmental or ecological gradients to better understand the dynamics of sexual selection in polyandrous species. We also discuss some directions for future research in this area.
ABSTRACT
Mammalian sperm must spend a minimum period of time within a female reproductive tract to achieve the capacity to fertilize oocytes. This phenomenon, termed sperm ‘capacitation’, was ...discovered nearly seven decades ago and opened a window into the complexities of sperm–female interaction. Capacitation is most commonly used to refer to a specific combination of processes that are believed to be widespread in mammals and includes modifications to the sperm plasma membrane, elevation of intracellular cyclic AMP levels, induction of protein tyrosine phosphorylation, increased intracellular Ca2+ levels, hyperactivation of motility, and, eventually, the acrosome reaction. Capacitation is only one example of post‐ejaculatory modifications to sperm (PEMS) that are widespread throughout the animal kingdom. Although PEMS are less well studied in non‐mammalian taxa, they likely represent the rule rather than the exception in species with internal fertilization. These PEMS are diverse in form and collectively represent the outcome of selection fashioning complex maturational trajectories of sperm that include multiple, sequential phenotypes that are specialized for stage‐specific functionality within the female. In many cases, PEMS are critical for sperm to migrate successfully through the female reproductive tract, survive a protracted period of storage, reach the site of fertilization and/or achieve the capacity to fertilize eggs. We predict that PEMS will exhibit widespread phenotypic plasticity mediated by sperm–female interactions. The successful execution of PEMS thus has important implications for variation in fitness and the operation of post‐copulatory sexual selection. Furthermore, it may provide a widespread mechanism of reproductive isolation and the maintenance of species boundaries. Despite their possible ubiquity and importance, the investigation of PEMS has been largely descriptive, lacking any phylogenetic consideration with regard to divergence, and there have been no theoretical or empirical investigations of their evolutionary significance. Here, we (i) clarify PEMS‐related nomenclature; (ii) address the evolutionary origin, maintenance and divergence in PEMS in the context of the protracted life history of sperm and the complex, selective environment of the female reproductive tract; (iii) describe taxonomically widespread types of PEMS: sperm activation, chemotaxis and the dissociation of sperm conjugates; (iv) review the occurence of PEMS throughout the animal kingdom; (v) consider alternative hypotheses for the adaptive value of PEMS; (vi) speculate on the evolutionary implications of PEMS for genomic architecture, sexual selection, and reproductive isolation; and (vii) suggest fruitful directions for future functional and evolutionary analyses of PEMS.
Sexual selection shapes the adaptive landscape in complex ways that lead to trait integration. Much of our understanding of selection comes from studies of morphological traits. However, few studies ...attempt to quantify the form and direction of selection on performance even though it is predicted to be a more direct target of selection in nature. We measured sexual selection on performance traits (bite force, sprint speed and endurance) in an Australian lizard, the Eastern water skink (Eulamprus quoyii). We first staged 123 contests between size‐matched males to investigate whether performance traits were important in determining contest outcome. In a second experiment, we established six breeding populations in large replicate semi‐natural enclosures to estimate whether performance traits predicted reproductive success. Our results show that none of the performance measures were important in predicting contest outcome and were not generally strong predictors of reproductive success. However, our analyses suggest a complex fitness landscape driven by males adopting different alternative reproductive tactics (ARTs). We provide a rare test of the role performance plays in sexual selection and highlight the need to test common assumptions regarding the link between maximal performance and fitness. Our results suggest that performance traits may not necessarily be direct targets of sexual selection, but rather indirect targets through their integration with morphological and/or behavioural traits, highlighting a need for more explicit tests of the predicted links between performance and fitness.
Eastern Water Skinks, Eulamprus quoyii, exhibit complex patterns of selection on performance as a result of alternative reproductive tactics in this species.
Abstract
Postcopulatory sexual selection (PCSS), namely sperm competition and cryptic female choice, is typically investigated in benign environments, with a fixed number of partners, which mate at ...the same time intervals; all conditions that are rarely met in natural populations.
Although there is increasing evidence that environmental fluctuations affect sexual selection before mating, whether and to which extent they influence postcopulatory trajectories is still little explored.
PCSS was investigated in replicate populations of guppies (
Poecilia reticulata
) in which males and females mated after maintained for 2 weeks on either restricted (RE) or ad libitum (AL) diet and the paternity of the offspring produced by multiply mated females was assigned using microsatellite markers.
Compared to AL fish, RE females (i) had fewer mating partners, but the time interval between the first and the last mating was not affected; (ii) produced broods with a lower variance in male fertilization success (a measure of the opportunity for PCSS); and (iii) produced broods with a paternity bias towards the first mate (reversing the last sperm precedence observed in AL populations), and associated more towards males with higher courtship rate.
Our results demonstrate that short‐term limitation in food availability significantly influence PCSS by modifying both fertilization success variance and sperm precedence pattern. Environmental variation should therefore become part of the research paradigm to improve our understanding of postcopulatory evolutionary dynamics.
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Plain Language Summary
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Abstract
La selezione sessuale postcopulatoria, ossia la competizione spermatica maschile e la scelta criptica femminile, è solitamente studiata in un ambiente florido, dove il numero dei partner e l'intervallo tra accoppiamenti sono costanti, tutte condizioni che raramente si verificano in natura.
Nonostante ci siano sempre maggiori evidenze che le fluttuazioni ambientali influenzino la selezione sessuale prima dell'accoppiamento, se e quanto queste influenzino le traiettorie postcopulatorie resta ancora poco esplorato.
Abbiamo indagato la selezione sessuale postcopulatoria in repliche sperimentali di popolazioni di guppies (
Poecilia reticulata
) in cui i maschi e le femmine sono stati mantenuti per due settimane o a dieta ristretta o a dieta abbondante e abbiamo assegnato la paternità della prole attraverso marcatura con miscrosatelliti.
Rispetto alla popolazione soggetta a dieta abbondante, le femmine a dieta ristretta hanno: (i) un numero minore di partners, ma un uguale intervallo temporale tra il primo e l'ultimo accoppiamento; (ii) una prole la cui varianza del successo di fertilizzazione maschile è minore (una misura di opportunità per la selezione sessuale postcopulatoria); e (iii) la paternità della prole è sbilanciata verso il primo maschio con cui si sono accoppiate (rovesciando la precedenza dell'ultimo maschio osservata nelle popolazioni a dieta abbondante), e associata ai maschi con il più alto tasso di corteggiamento.
I nostri risultati dimostrano che la limitazione di cibo per un arco temporale breve influenza significativamente la selezione sessuale postcopulatoria modificando sia la varianza sia l'ordine di successo di fertilizzazione. Pertanto, le variazioni ambientali dovrebbero diventare parte del paradigma sperimentale allo scopo di incrementare la nostra comprensione delle dinamiche evolutive postcopulatorie.
Classical sexual selection theory provides a well-supported conceptual framework for understanding the evolution and signalling function of male ornaments. It predicts that males obtain greater ...fitness benefits than females through multiple mating because sperm are cheaper to produce than eggs. Sexual selection should therefore lead to the evolution of male-biased secondary sexual characters. However, females of many species are also highly ornamented. The view that this is due to a correlated genetic response to selection on males was widely accepted as an explanation for female ornamentation for over 100 years and current theoretical and empirical evidence suggests that genetic constraints can limit sex-specific trait evolution. Alternatively, female ornamentation can be the outcome of direct selection for signalling needs. Since few studies have explored interspecific patterns of both male and female elaboration, our understanding of the evolution of animal ornamentation remains incomplete, especially over broad taxonomic scales. Here we use a new method to quantify plumage colour of all ~6,000 species of passerine birds to determine the main evolutionary drivers of ornamental colouration in both sexes. We found that conspecific male and female colour elaboration are strongly correlated, suggesting that evolutionary changes in one sex are constrained by changes in the other sex. Both sexes are more ornamented in larger species and in species living in tropical environments. Ornamentation in females (but not males) is increased in cooperative breeders--species in which female-female competition for reproductive opportunities and other resources related to breeding may be high. Finally, strong sexual selection on males has antagonistic effects, causing an increase in male colouration but a considerably more pronounced reduction in female ornamentation. Our results indicate that although there may be genetic constraints to sexually independent colour evolution, both female and male ornamentation are strongly and often differentially related to morphological, social and life-history variables.
Parental age has profound consequences for offspring’s phenotype. However, whether patrilineal age affects offspring sperm production remains unknown, despite the importance of sperm production for ...male reproductive success in species facing post‐copulatory sexual selection. Using a longitudinal dataset on ejaculate attributes of the houbara bustard, we showed that offspring sired by old fathers had different age‐dependent trajectories of sperm production compared to offspring sired by young fathers. Specifically, they produced less sperm (−48%) in their first year of life, and 14% less during their lifetime. Paternal age had the strongest effect, with weak evidence for grandpaternal or great grandpaternal age effects. These results show that paternal age can affect offspring reproductive success by reducing sperm production, establishing an intergenerational link between ageing and sexual selection.
Parental age has profound consequences for offspring’s phenotype. Number of gametes transferred during the mating is an important driver of siring success and especially so in species where females mate with several males and ejaculates compete for egg fertilization. We investigated if maternal and paternal age affect sperm production in a bird species with post‐copulatory sexual selection. We found that offspring sired by old fathers had different age‐dependent trajectories of sperm production compared to offspring sired by young fathers, producing less sperm (‐48%) in their first year of life, and 14% less during their lifetime. These results show that paternal age can affect offspring reproductive success by reducing sperm production, establishing an intergenerational link between aging and sexual selection.
Exaggerated sexual traits, such as ornaments and courtship displays, are crucial for mate acquisition in many species and are often subject to directional runaway selection. However, in the face of ...high predation risk, natural selection can result in a reduction of conspicuous precopulatory displays to avoid detection by potential predators. Sexual selection may then favour increased investment in inconspicuous postcopulatory traits. Here, we investigated the transgenerational effects of predation on precopulatory male courtship and postcopulatory sexual traits (testes size, sperm length) in a dung fly, Sepsis punctum (Sepsidae). Behavioural assays prior to selection document a marked decrease in male courtship displays in the presence of a predator, the Asian Ant Mantis (Odontomantis planiceps). However, after ten generations of experimental evolution, flies exhibited a marked increase in courtship, both in the absence and presence of a predator. Additionally, under sustained predation pressure, male and female body size decreased but male postcopulatory traits were not significantly affected. These results suggest that precopulatory courtship can be under strong sexual selection even in the face of predation pressure. Larger flies were more susceptible to predation, and there could be canalisation of postcopulatory traits that are crucial for fertilisation.
•Male courtship activity increased over generations regardless of predation risk•Adult body size decreased over generations of sustained predation pressure•Male postcopulatory traits (testes volume, sperm length) were not significantly affected•Crucial postcopulatory traits may be under strong stabilising selection due to their role in fertilisation
Male genital traits exhibit extraordinary interspecific phenotypic variation. This remarkable and general evolutionary trend is widely considered to be the result of sexual selection. However, we ...still do not have a good understanding of whether or how individual genital traits function in different competitive arenas (episodes of sexual selection), or how different genital traits may interact to influence competitive outcomes. Here, we use an experimental approach based on high‐precision laser phenotypic engineering to address these outstanding questions, focusing on three distinct sets of micron‐scale external (nonintromittent) genital spines in male Drosophila kikkawai Burla (Diptera: Drosophilidae). Elimination of the large pair of spines on the male secondary claspers sharply reduced male ability to copulate, yet elimination of the other sets of spines on the primary and secondary claspers had no significant effects on copulation probability. Intriguingly, both the large spines on the secondary claspers and the cluster of spines on the primary claspers were found to independently promote male competitive fertilization success. Moreover, when large and small secondary clasper spines were simultaneously shortened in individual males, these males suffered greater reductions in fertilization success relative to males whose traits were altered individually, providing evidence for synergistic effects of external genital traits on fertilization success. Overall, the results are significant in demonstrating that a given genital trait (the large spines on the secondary claspers) can function in different episodes of sexual selection, and distinct genital traits may interact in sexual selection. The results offer an important contribution to evolutionary biology by demonstrating an understudied selective mechanism, operating via subtle trait interactions in a post‐insemination context, by which genital traits may be co‐evolving.
The sickle‐shaped large and small genital spines of Drosophila kikkawai exert synergistic effects in post‐mating sexual selection. Such joint effects on reproductive fitness, demonstrated here using ultra‐precise laser surgery, may fuel co‐evolutionary diversification of genital morphology.
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