Silk-borne chemicals of spider nuptial gifts elicit female gift acceptance

Chemical communication is important in a reproductive context for conveying information used for mate recognition and/or assessment during courtship and mating. Spider silk is a common vehicle for chemical communication between the sexes. However, despite being well described in females, male silk-borne chemicals remain largely unexplored. Males of the spider Pisaura mirabilis silk-wrap prey (i.e. nuptial gifts) that is offered to females during courtship and eaten by the female during mating. Interestingly, rejected males often add more silk to their gift which leads to successful mating, suggesting the presence of silk-borne chemicals that facilitate female gift acceptance. To test this hypothesis, we offered females standardized gifts covered with male silk that was either washed in solvents or unwashed, respectively, to remove or not any chemically active components. We scored female gift acceptance, and as expected in the case chemicals that mediate female mating behaviour are present in male silk, females were more likely to accept gifts covered with unwashed silk. Our findings suggest that silk-borne chemicals of nuptial gifts prime female responses, potentially signalling male quality or manipulating females into mating beyond their interests given the occurrence of male cheating behaviour via nutritionally worthless gifts in this system.

Maintenance of deceptive gifts in a natural spider population: ecological and demographic factors

Alternative mating tactics are expected to occur predominantly when mate competition is intense, resources are in short supply, or as a result of asymmetric power relationships between individuals. Males of the nuptial gift-giving spider Pisaura mirabilis use a prevailing tactic of offering a nutritive gift (insect prey) and a deceptive tactic of offering a worthless gift (consumed prey) to prospective mates. If the male’s tactic depends on precopulatory male–male competition, worthless gifts should occur primarily late in the season, when the operational sex ratio (OSR) becomes male-biased. If it depends on resource availability and/or postcopulatory sexual selection (sperm competition), worthless gifts should occur mostly early in the mating season, when prey availability is low and most females are unmated (i.e., postcopulatory sexual selection is weak). Nuptial gift construction correlated positively with prey availability and negatively with OSR, suggesting that males increase reproductive effort when resource and mate availability increase. We did not find evidence for body condition affecting male tactic use. Male size had a marked effect on the reproductive tactic employed. Males that matured early in the season were very small and employed mostly the nutritive gift tactic during their short life. Among the males that matured later and persisted through the season, relatively small males employed the worthless gift tactic whereas large males employed the nutritive gift tactic. We suggest that the existence of 2 distinct life-history strategies among males (early small and late large size) interacts with environmental and demographic conditions to maintain the deceptive tactic.

The shield effect: nuptial gifts protect males against pre-copulatory sexual cannibalism

Several not mutually exclusive functions have been ascribed to nuptial gifts across different taxa. Although the idea that a nuptial prey gift may protect the male from pre-copulatory sexual cannibalism is attractive, it has previously been considered of no importance based on indirect evidence and rejected by experimental tests. We reinvestigated whether nuptial gifts may function as a shield against female attacks during mating encounters in the spider Pisaura mirabilis and whether female hunger influences the likelihood of cannibalistic attacks. The results showed that pre-copulatory sexual cannibalism was enhanced when males courted without a gift and this was independent of female hunger. We propose that the nuptial gift trait has evolved partly as a counteradaptation to female aggression in this spider species.

Sperm storage mediated by cryptic female choice for nuptial gifts

Polyandrous females are expected to discriminate among males through postcopulatory cryptic mate choice. Yet, there is surprisingly little unequivocal evidence for female-mediated cryptic sperm choice. In species in which nuptial gifts facilitate mating, females may gain indirect benefits through preferential storage of sperm from gift-giving males if the gift signals male quality. We tested this hypothesis in the spider Pisaura mirabilis by quantifying the number of sperm stored in response to copulation with males with or without a nuptial gift, while experimentally controlling copulation duration. We further assessed the effect of gift presence and copulation duration on egg-hatching success in matings with uninterrupted copulations with gift-giving males. We show that females mated to gift-giving males stored more sperm and experienced 17% higher egg-hatching success, compared with those mated to no-gift males, despite matched copulation durations. Uninterrupted copulations resulted in both increased sperm storage and egg-hatching success. Our study confirms the prediction that the nuptial gift as a male signal is under positive sexual selection by females through cryptic sperm storage. In addition, the gift facilitates longer copulations and increased sperm transfer providing two different types of advantage to gift-giving in males.