Amanda Bretman

Seminal fluid protein allocation and male reproductive success.

Postcopulatory sexual selection can select for sperm allocation strategies in males [1, 2], but males should also strategically allocate nonsperm components of the ejaculate [3, 4], such as seminal fluid proteins (Sfps). Sfps can influence the extent of postcopulatory sexual selection [5-7], but little is known of the causes or consequences of quantitative variation in Sfp production and transfer. Using Drosophila melanogaster, we demonstrate that Sfps are strategically allocated to females in response to the potential level of sperm competition. We also show that males who can produce and transfer larger quantities of specific Sfps have a significant competitive advantage. When males were exposed to a competitor male, matings were longer and more of two key Sfps, sex peptide [8] and ovulin [9], were transferred, indicating strategic allocation of Sfps. Males selected for large accessory glands (a major site of Sfp synthesis) produced and transferred significantly more sex peptide, but not more ovulin. Males with large accessory glands also had significantly increased competitive reproductive success. Our results show that quantitative variation in specific Sfps is likely to play an important role in postcopulatory sexual selection and that investment in Sfp production is essential for male fitness in a competitive environment.

Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness

Evolutionary and plastic responses by males to the level of sperm competition (SC) are reported across widespread taxa, but direct tests of the consequences for male reproductive success in a competitive context are lacking. We varied male perception of SC to examine the effect on male competitive reproductive success and to test whether the outcomes were as predicted by theory. Exposure to rival males prior to mating increased a males ejaculate investment (measured as mating duration); by contrast, exposure to rival males in the mating arena decreased mating duration. The results therefore suggested that SC intensity is important in shaping male responses to SC in this system, although the patterns were not strictly in accord with existing theory. We then tested whether males that responded to the level of SC had higher reproductive fitness in a competitive context. We found that males kept with rivals prior to mating again mated for longer; furthermore, they achieved significantly higher paternity share regardless of whether they were the first or second males to mate with a female. The plastic strategies employed by males therefore resulted in significantly increased reproductive success in a competitive context, even following subsequent rematings in which the majority of sperm were displaced.

Natural and Sexual Selection in a Wild Insect Population

Insects in the Wild Insects are of fundamental importance to terrestrial ecosystems and provide laboratory model systems for the study of physiology and genetics. Studies examining how natural and sexual selection operate to drive evolution in wild populations have often neglected invertebrates, resulting in a chasm between our understandings of how things work in the lab versus the natural environment. Rodríguez-Muñoz et al. (p. 1269; see the Perspective by Zuk) bridge this gap by comprehensively monitoring the life histories, behavior, and reproductive success of an entire population of field crickets. Adding genetic data allowed evaluation of how behavior impacts reproductive success and confirmed that male reproductive success varies more than that of females. Monitoring reproduction in wild crickets confirms that male success varies more than female success. The understanding of natural and sexual selection requires both field and laboratory studies to exploit the advantages and avoid the disadvantages of each approach. However, studies have tended to be polarized among the types of organisms studied, with vertebrates studied in the field and invertebrates in the lab. We used video monitoring combined with DNA profiling of all of the members of a wild population of field crickets across two generations to capture the factors predicting the reproductive success of males and females. The factors that predict a male’s success in gaining mates differ from those that predict how many offspring he has. We confirm the fundamental prediction that males vary more in their reproductive success than females, and we find that females as well as males leave more offspring when they mate with more partners.

Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus.

Female promiscuity has broad implications for individual behaviour, population genetics and even speciation. In the field cricket Gryllus bimaculatus, females will mate with almost any male presented to them, despite receiving no recorded direct benefits. Previous studies have shown that female crickets can benefit from polyandry through increased hatching success of their eggs. There is evidence that this effect is driven by the potential of polyandrous females to avoid fertilizing eggs with sperm from genetically incompatible males. We provide direct evidence supporting the hypothesis that polyandry is a mechanism to avoid genetic incompatibilities resulting from inbreeding. Using microsatellite markers we examined patterns of paternity in an experiment where each female mated with both a related and an unrelated male in either order. Overall, unrelated males were more successful in gaining paternity than were related males, but this effect was driven by a much greater success of unrelated males when they were the first to mate.

Measuring polyandry in wild populations: a case study using promiscuous crickets

Mating rate has important implications for patterns of sexual selection and sexual conflict and hence for issues such as speciation and the maintenance of genetic diversity. Knowledge of natural mating rates can provide insights into the factors driving female mating behaviour. We investigated the level of polyandry in a Spanish population of the field cricket Gryllus bimaculatus using microsatellite markers. Two approaches were employed: (i) genotyping the offspring of wild‐caught gravid females to determine the number of males siring the brood and (ii) genotyping sperm stored in the spermathecae of females mated in the wild to estimate the number of mating partners. We compared existing methods for inferring the minimum and probable number of fathers and described a novel probabilistic technique estimating the number of mates by genotyping stored sperm. Using the most conservative allele‐counting method, 71% of females produced offspring sired by at least two males (a minimum mean of 2.4 fathers per clutch), and all females had mated to at least two males with minimum mean estimates of 2.7–5.1 mates per female. Our study reveals high levels of polyandry in the wild and suggests that females mate with more males than sire their offspring.

Quick-change artists: male plastic behavioural responses to rivals

Behavioural plasticity allows animals to attune their behaviour to rapid environmental changes. Here we focus on plasticity in male mating behaviour in response to socio-sexual conditions. We discuss existing theory, generate predictions to facilitate exploration of the benefits of plastic behaviour, and identify parameters with the highest leverage on fitness. Existing data are synthesised to assess whether plasticity occurs pre- and post-copulation, to determine the direction of changes in behaviour, and to examine if plastic behaviour is fully flexible. We find that plasticity in males is widespread and not dominated by responses that occur pre- or post-copulation. Our synthesis also highlights areas that are underexplored, such as the limited data on the ultimate fitness consequences of such plastic behaviour.

Promiscuous females avoid inbreeding by controlling sperm storage

Recent studies in a variety of species have shown that polyandrous females are somehow able to bias paternity against their relatives postcopulation, although how they do so remains unknown. Field crickets readily mate with their siblings, but when also mated to an unrelated male, they produce disproportionately fewer inbred offspring. We use a new competitive microsatellite polymerase chain reaction technique to determine the contribution of males to stored sperm and subsequent paternity of offspring. Paternity is almost completely predicted by how much sperm from a particular male is stored, and unrelated males contribute more sperm to storage and have a corresponding higher paternity success.

Adult Male Nutrition and Reproductive Success in Drosophila melanogaster

Abstract Explanations for the maintenance of variation in reproductive traits influenced by seminal fluid accessory gland proteins (Acps) in male Drosophila melanogaster include nontransitivity in the outcome of sperm competition and/or condition dependence of the traits involved. We investigated the effects of adult male nutrition (five diets) on the expression of Acp- and sperm- mediated traits. We found novel, nonlinear effects, with females showing lower levels of refractoriness to remating after mating with males held on the lowest and highest yeast diets. There were no significant effects of adult male nutrition on male paternity share, but there was a striking, nonlinear effect on second male progeny production, with males kept on intermediate yeast diets fathering the highest number of offspring. Such “bell shaped” responses of life-history traits to nutrition have only previously been reported for longevity. Consistent with previous reports, males maintained on low protein diets had lower premating success and gained fewer rematings with nonvirgins. We show novel and body size independent effects of adult male nutrition on traits influenced by Acps and sperm, which do not fit current condition-dependent handicap models and can affect the strength of sexual selection acting upon such fitness-related traits.

Males Use Multiple, Redundant Cues to Detect Mating Rivals

Across many species, males exhibit plastic responses when they encounter mating rivals. The ability to tailor responses to the presence of rivals allows males to increase investment in reproduction only when necessary. This is important given that reproduction imposes costs that limit male reproductive capacity, particularly when sperm competition occurs. Fruitfly (Drosophila melanogaster) males exposed to rivals subsequently mate for longer and thus accrue fitness benefits under increased competition, in line with theory. Here, we show that male D. melanogaster detect rivals by using a suite of cues and that the resulting responses lead directly to significant fitness benefits. We used multiple techniques to systematically remove auditory, olfactory, tactile, and visual cues, first singly and then in all possible combinations. No single cue alone was sufficient to allow males to detect rivals. However, the perception of any two cues from sound, smell, or touch permitted males to detect and respond adaptively to rivals through increased offspring production. Vision was only of marginal importance in this context. The findings indicate adaptive redundancy through the use of multiple, but interchangeable, cues. We reveal the robust mechanisms by which males assess their socio-sexual environment to precisely attune responses via the expression of plastic behavior.

Female nutritional status determines the magnitude and sign of responses to a male ejaculate signal in Drosophila melanogaster.

Ejaculate chemicals transferred from males to females during mating cause significant changes in female behaviour and physiology, but the causes of phenotypic variation in these responses is little understood. We tested here the effect of adult female nutrition on the response of female Drosophila melanogaster to a specific ejaculate component, the sex peptide (SP), which is of interest because of its effects on female egg laying, sexual receptivity, feeding rate, immune responses and potential role in mediating sexual conflict. We exposed adult females to five different diets and kept them continuously with males that did or did not transfer SP. Diet altered the presence, magnitude and sign of the effects of SP on different phenotypic traits (egg laying, receptivity and lifespan) and different traits responded in different ways. This showed that the set of responses to mating can be uncoupled and can vary independently in different environments. Importantly, diet also significantly affected whether exposure to SP transferring males was beneficial or costly to females, with beneficial effects occurring more often than expected. Hence, the food environment can also shape significantly the strength and direction of selection on mating responses.