Costs of multiple mates: an experimental study in horseshoe crabs

Abstract

Why do females mate with multiple males? Since females often acquire all the sperm they need in one mating and since mating is usually costly, the evolution of polyandry is puzzling. Females may gain from mating multiply by ensuring fertilization, increasing offspring diversity, improving mate quality (‘good genes’) or increasing genetic compatibility. Alternatively, multiple mating may result in a net cost to females as a by-product of male–male competition. We report on field experiments in which we evaluated whether spawning with multiple males is costly or beneficial for female horseshoe crabs, Limulus polyphemus . Unpaired male horseshoe crabs crowd around some spawning pairs (polyandrous) as satellites while ignoring others (monandrous). We conducted three field experiments in which we compared the success of (1) unmanipulated polyandrous and monandrous females, (2) polyandrous females with and without satellites (satellites removed) and (3) monandrous females without and with satellites (forced to be polyandrous by adding satellites). When polyandrous females lost their satellite males, they laid more eggs than did polyandrous females that retained their satellites. When a satellite male arrives at a monandrous pair, some females are tolerant and will nest as a polyandrous female, but many females are intolerant of satellite males and leave immediately, thus laying fewer eggs. These results indicate that spawning with multiple males is costly in terms of nesting success for female horseshoe crabs. Yet, natural monandrous and polyandrous females did equally well, suggesting that there are compensating benefits from multiple males for polyandrous females. We suggest that monandry and polyandry may be alternative reproductive tactics for female horseshoe crabs.