Contact pheromones mediate male preference in black widow spiders: avoidance of hungry sexual cannibals?

Abstract

Males often exercise mate choice when mating frequency is constrained, costs of choice are low and variation in female quality and/or expected paternity can be reliably detected. Across invertebrates, males use sex pheromones to discern female mating status, but there are few demonstrations that information about expected fecundity (‘quality’) is encoded in pheromones alone. Here we examine whether females' sex pheromones allow males to detect differences in female food intake and mass in two species of widow spiders (Latrodectus hesperus and Latrodectus hasselti) in which chemicals are deposited by females in silk. Recent work shows that male L. hesperus prefer well-fed females, and that these females produce more silk than hungry females. Thus, changes in diet could be mechanistically linked to changes in silk-bound pheromonal signals. We show that unmated females of both species lose more than half of their mass when food is withheld, and silk production is reduced by 48% (L. hesperus) to 67% (L. hasselti). Males had a significant sexual response to pheromones extracted from the females' silk in both species, although this response was not directly correlated with silk or female mass. In L. hesperus, but not in L. hasselti, males were less responsive to sex pheromones from food-deprived females compared to well-fed females. While females on good diets provide the benefit of higher fecundity in both species, the risk of being cannibalized by hungry females during courtship exists only in L. hesperus. We conclude that sex pheromones alone can provide information about recent female feeding history, possibly reducing the costs of males expressing choice in the field. The species difference in male response also suggests that male preferences in these spiders may depend less on the benefit of seeking a highly fecund female and more on avoiding the cost of risky mating attempts with a likely cannibal.