Susan N. Gershman

Lovesick: immunological costs of mating to male sagebrush crickets.

A growing body of evidence suggests that resources invested in reproduction often come at the expense of the ability to mount an immune response. During mating, female sagebrush crickets, Cyphoderris strepitans, consume the ends of the male’s hind wings and ingest his haemolymph. Previous research has shown that this behaviour impairs the ability of males to secure additional matings. One hypothesis to account for this effect is that wing wounding triggers an energetically costly immune response, such that nonvirgin males are unable to sustain the costly acoustical signalling needed to attract additional females. To test this hypothesis, we injected virgin males with lipopolysaccharides (LPS) to provoke an immune response, and monitored their mating success in the field. LPS‐injected virgin males took significantly longer to mate than sham‐injected virgin males, and spent significantly less time calling. We also compared virgin, nonvirgin and experimentally wing‐wounded virgin males with respect to: (1) their ability to encapsulate a foreign invader via the accumulation of haemocytes and deposition of melanin and (2) baseline levels of phenoloxidase (PO), a key enzyme in the biochemical cascade leading to the production of melanin. Although encapsulation ability did not differ with reproductive experience, virgin males had significantly higher levels of PO than either nonvirgin or experimentally wing‐wounded virgin males. These results suggest that wing‐wounding alone is sufficient to impair male immunity, and that males trade‐off investment in reproduction and immunity.

Give 'til it hurts: trade-offs between immunity and male reproductive effort in the decorated cricket, Gryllodes sigillatus

Trade‐offs between life‐history variables can be manifested at either the phenotypic or genetic level, with vastly different evolutionary consequences. Here, we examined whether male decorated crickets (Gryllodes sigillatus) from eight inbred lines and the outbred founder population from which they were derived, trade‐off immune effort [lytic activity, phenoloxidase (PO) activity or encapsulation] to produce spermatophylaxes: costly nuptial food gifts essential for successful sperm transfer. Canonical correlation analysis of the outbred population revealed a trade‐off between spermatophylax mass and lytic activity. Analysis of our inbred lines, however, revealed that although PO activity, encapsulation, body mass, spermatophylax mass and ampulla (sperm capsule) mass were all highly heritable, lytic activity was not, and there was, therefore, no negative genetic correlation between lytic activity and spermatophylax mass. Thus, males showed a phenotypic but not a genetic trade‐off between spermatophylax mass and lytic activity, suggesting that this trade‐off is mediated largely by environmental factors.

Inbred decorated crickets exhibit higher measures of macroparasitic immunity than outbred individuals

Inbreeding is assumed to have negative effects on fitness, including the reduced ability to withstand immune challenges. We examined the immunological consequences of inbreeding in decorated crickets, Gryllodes sigillatus, by comparing lytic activity, phenoloxidase (PO) activity, and encapsulation ability of crickets from eight inbred lines with that of crickets from the outbred founder population. Surprisingly, crickets from inbred lines had a greater encapsulation ability compared with crickets from the outbred population. We suggest that because inbred crickets have reduced reproductive effort, they may, therefore, have the option of devoting more resources to this form of immunity than outbred individuals. We also found that both inbred and outbred females had higher immunity than males in PO activity and implant darkness. This result supports the hypothesis that females should devote more effort to somatic maintenance and immunity than males. PO activity and implant darkness were heritable in both males and females, but lytic activity was only heritable in females. Males and females differed in the heritability of, and genetic correlations among, immune traits, suggesting that differences in selective pressures on males and females may have resulted in a sexual conflict over optimal immune trait values.

Postcopulatory female choice increases the fertilization success of novel males in the field cricket, Gryllus vocalis.

Although recent studies have demonstrated that female crickets prefer novel males to previous mates, the relative contribution of pre- and postcopulatory behaviors to this advantage remain unknown, as do the reproductive consequences to males. I paired females either with previous or novel mates, and recorded the latency to mating and the time after mating at which the female removed the males spermatophore, terminating sperm transfer. Females that mated with familiar males removed their spermatophores sooner than females that mated with novel males. Females paired with novel males also mated more quickly than females paired with familiar males, but this difference was not statistically significant. A molecular-based paternity analysis was used to determine whether the postcopulatory preference of females for novel males influences a males fertilization success. Females were assigned to either mate three times with the same male and then once with a novel male, or four times with four different males. The paternity of the last male was higher when the female previously had mated repeatedly with the same male than when she had mated previously with different males. These results suggest that female spermatophore removal behavior influences male paternity such that novel males receive a fertility benefit.

Large Numbers of Matings Give Female Field Crickets a Direct Benefit but not a Genetic Benefit

Female crickets can potentially gain both direct and indirect benefits from mating multiple times with different males. Most studies have only examined the effects of small numbers of matings, although female crickets are capable of mating many times. The goal of this paper is to examine the direct and indirect benefits of mating large numbers of times for female reproductive success. In a previous experiment, female Gryllus vocalis were found to gain diminishing direct benefits from mating large numbers of times. In this study I attempt to determine whether mating large numbers of times yields similar diminishing returns on female indirect benefits. Virgin female Gryllus vocalis crickets were assigned to mate five, ten or 15 times with either the same or different males. Females that mated more times gained direct benefits in terms of laying more eggs and more fertilized eggs. Females that mated with different males rather than mating repeatedly with the same male did not have higher offspring hatching success, a result that is contrary to other published results comparing female reproductive success with repeated versus different partners. These results suggest that females that mate large numbers of times fail to gain additional genetic benefits from doing so.

Food fight: sexual conflict over free amino acids in the nuptial gifts of male decorated crickets.

In decorated crickets, Gryllodes sigillatus, the spermatophore that a male transfers at mating includes a gelatinous spermatophylax that the female consumes, delaying her removal of the sperm‐filled ampulla. Male fertilization success increases with the length of time females spend feeding on the spermatophylax, while females may benefit by prematurely discarding the spermatophylaxes of undesirable males. This sexual conflict should favour males that produce increasingly appealing spermatophylaxes, and females that resist this manipulation. To determine the genetic basis of female spermatophylax feeding behaviour, we fed spermatophylaxes to females of nine inbred lines and found that female genotype had a major influence on spermatophylax feeding duration. The amino acid composition of the spermatophylax was also significantly heritable. There was a positive genetic correlation between spermatophylax feeding duration and the gustatory appeal of the spermatophylax. This correlation suggests that genes expressed in males that produce more manipulative spermatophylaxes are positively linked to genes expressed in females that make them more vulnerable to manipulation. Outbred females spent less time feeding on spermatophylaxes than inbred females, and thus showed greater resistance to male manipulation. Further, in a nonspermatophylax producing cricket (Acheta domesticus), females were significantly more prone to feeding on spermatophylaxes than outbred female Gryllodes. Collectively, these results suggest a history of sexually antagonistic coevolution over the consumption of nuptial food gifts.

TO PERSUADE OR BE PERSUADED: WHICH SEX CONTROLS MATING IN A PLETHODONTID SALAMANDER?

In the dynamic process of courtship, males often must perform behaviour patterns that function to persuade females that are initially unresponsive to mate. But, to what extent is the outcome of a sexual encounter determined by a males persuasiveness versus a females responsiveness? We addressed this question in three laboratory experiments using a plethodontid salamander, Desmognathus ocoee, for which persuasion by males appears to be obligatory. We found considerable variation in mating success among individuals of both sexes, indicating variation in both male persuasiveness and female responsiveness (Experiment 1). In addition, males of high persuasiveness mated more often than males of lower persuasiveness, regardless of the levels of responsiveness of the females that they encountered (Experiment 2). Finally, we found that males of high persuasiveness performed certain sexual behaviour patterns more frequently and more rapidly than males of lower persuasiveness (Experiment 3). Our results suggest that male D. ocoee of high persuasiveness can mate successfully even with unresponsive females, which may be especially choosy about which males they accept. Thus, those male behaviour patterns that increase female motivation to mate likely are targets of sexual selection by female choice. Whether females that mate with persuasive males enjoy increased fitness awaits further study.

Level up: the expression of male sexually selected cuticular hydrocarbons is mediated by sexual experience

The use of cuticular hydrocarbons (CHCs) in species recognition, sex identification and sexual selection is widespread in insects. However, few studies have studied plasticity in CHCs. Here we examine the effect of age and social environment on a suite of sexually selected CHCs in Drosophila serrata. We demonstrate that the combination of CHCs that is associated with increased male mating success (CHCβ) changes as males age, and this effect is mediated by social environment. When single males were housed with multiple females, their expression of CHCβ increased across the first few days of their adult life, after which expression declined with increasing age. In contrast, sexually selected CHCs of males housed with other males, males housed with other males and females, and males housed alone all decreased across days. To determine the long-term consequences of mating on CHC expression, we allowed males a single mating opportunity and subsequently found some indication of a brief spike in CHCβ. Finally, to determine whether visual and olfactory contact with females, copulation, or intromission causes males to express high values of CHCβ, we manipulated male access and physical contact with females. We found that although prolonged copulation causes a slight increase in male CHCβ, only a successful copulation with sperm transfer induced males to develop CHCs associated with high mating success. Taken as a whole, our results demonstrate that the expression of sexually selected CHCs in males varies with both age and social context, and suggest that the latter is mediated at least in part by successful matings with females. More generally, contextual plasticity in CHCs is likely to affect both the experimental design of CHC-based experiments and the evolution of CHC signals as naturally and sexually selected traits.