Males of a sexually cannibalistic spider chemically assess relative female quality

Mate choice is a taxonomically wide-spread phenomenon, mostly exerted by females although male mate choice occurs as well. While costs and benefits of choosiness have been well studied, the underlying mechanisms are largely unclear. Different models exist, namely best-of-n or threshold rules, based on sequential or simultaneous sampling, which differ in the required cognitive demands. We applied an experimental approach to shed light on the underlying mechanisms of male mate choice in the sexually cannibalistic spider Argiope bruennichi. Males are limited to two copulations and preferentially monopolise large females, while they may leave smaller females after a single copulation and resume mate search. Here, we utilised significant size-differences between females from Northern and Southern populations and presented males with three different-sized females that were matched for origin: all three females originated either from the same Northern European population as the males or from Southern populations where the smallest female was about the same size as the largest Northern female. This allowed testing the hypothesis that males base their mating tactic on a fixed local size threshold. We predicted Northern males to be choosy among Northern females, but to accept all Southern females since they would all be above that threshold.

Males copulated with the first female they encountered, which was independent of her body size. Regardless of the females' origins, males chose a monogynous tactic with the largest female in the trio, while they left the smallest female after one copulation. The same pattern applied to Southern females even though the smallest females in the trio were of a similar size as monopolised Northern females. Since males have poor eyesight and did not actively sample all females, they likely have gained information about relative size differences between females based on volatile chemical cues only.

Our findings suggest that male A. bruennichi can assess relative differences in mate quality and adjust their mating tactic to the prevailing conditions (Northern vs. Southern). We reject the presence of a locally-adapted fixed threshold and argue that our results are best explained by an adjustable threshold that was raised under Southern conditions.