Does sexual cannibalism secure genetic benefits of polyandry in a size-dimorphic spider?

Abstract

Abstract Females mate multiply despite numerous costs. It is well established that polyandry can result in sexual conflict, favoring male adaptations that prevent sperm competition often to the disadvantage of the female. Such adaptations are extreme in spiders with one-shot genitalia of which parts break off and act as mating plugs, rendering them dysfunctional. In the spider Argiope bruennichi, mating plugs effectively prevent further males from inseminating and males that inseminate and plug both genital openings of a female secure exclusive paternity. However, females frequently prevent monopolization by attacking and cannibalizing males during their first copulation, leaving their second spermatheca free for another male. Here, we test whether the high frequency of sexual cannibalism evolved as a female adaptation to resist monopolization and secure indirect benefits of polyandry. To standardize conditions, we double-mated females either with the same or two different males and prevented male consumption. Using a split-brood design, we raised offspring to maturity under poor and rich food conditions and measured their survival, duration of juvenile phase, and adult body mass. Under low food, daughters of polyandrous mothers matured later but slightly heavier than daughters of monandrous females. Since the adaptive value of this combination is unclear, these findings lend no conclusive support to our hypothesis. We discuss the stereotypic nature of the female attack in the context of antagonistic co-evolution considering previous studies that found modest direct benefits of cannibalism as well as a potential for non-additive benefits. Significance statement Sexual conflict is extreme in spiders where sexual cannibalism impairs male mating rates. Males of the spider Argiope bruennichi possess one-shot genitalia which they break off to plug female genital openings. They gain exclusive paternity with a female if two copulations are achieved and both genital openings plugged. Females, however, stereotypically attack every male at the onset of copulation, limiting most males to single copulation but retaining the option to secure potential benefits of polyandry. Previous studies revealed weak direct and non-additive indirect benefits of multiple mating. In this study, we tested for the presence of additive genetic benefits but again found only inconclusive evidence for adaptive differences in offspring quality between monandrous and polyandrous females. All results combined, we here speculate that the stereotypic female attack might be a ghost of a past antagonistic co-evolution.