Juvenile Experience with Male Cues Triggers Cryptic Choice Mechanisms in Adult Female Redback Spiders

SIMPLE SUMMARY: Females of many species vary in their receptivity to male mating attempts. When many males are present in the habitat, the theory predicts that females should be choosy and discriminate among potential mates. When few males are available, females should mate readily with the first male who courts, and thus avoid the risk of remaining unmated. We predicted that cues perceived as juveniles that indicate male availability would affect the mating behaviour of adult females. In our first experiment, juvenile females were exposed to airborne chemicals produced by males at high or low densities. In our second experiment, we mimicked a natural situation where males or other juveniles live on the webs of females shortly before they become sexually mature, and compared this to females developing in isolation. As was consistent with our predictions, we found that the adult females changed their behaviour after exposure to cues of high male availability during development. When the females perceived many males nearby (high density airborne cues or living with males) they more often interrupted copulation, or cannibalized the males before the mating was complete as adults. In comparison, when the cues indicated low male availability, the adult females were more likely to allow the males to complete mating, and cannibalism was less common. ABSTRACT: Female choice may be linked to population density if the expected encounter rates with potential mates affects choosiness (the energy and risk engaged to express mate preferences). Choosiness should covary with male availability, which could be assessed using the social cues available during development. We tested whether the exposure of juvenile females to cues of male density affected the mechanisms of choosiness of adult Latrodectus hasselti spiders in two experiments simulating natural contexts. The juvenile females were exposed to (1) volatile chemicals from two densities of adult males (airborne cues), and (2) tactile, vibrational and chemical cues from adult males or other females (cohabitation cues). As adults, the females mated readily, regardless of the treatment, but there was strong evidence for post-copulatory mechanisms of choosiness in females exposed to cues of high male availability. These included abbreviated matings (in both experiments), cannibalism of the males before the mating was complete (cohabitation), and, remarkably, a reduction in the successful placement of internal sperm plugs (cohabitation). These shifts decrease the likelihood that the first mate would monopolize paternity if the female chose to mate again. We conclude that female choosiness may impose a strong selection on males despite the high mating rates, and these effects can hinge on the cues of male availability detected by juveniles.