Ineffective nuptial gifts suggest female emancipation from sensory exploitation

Abstract

Male sensory exploitation of female gustatory pre-existing bias has been proposed for the origin of nuptial gifts in insects and spiders. This sexual trait may have been beneficial to both sexes, giving mating and survival advantages to males and providing nutritional resources for females. However, the evolution of deceptive worthless gifts is against females’ interests and may trigger a co-evolutionary change in females’ preferences. We evaluated females’ preferences for nuptial gifts and the adaptive function of the gift in the spider Trechaleoides keyserlingi. The genus belongs to the understudied Neotropical family Trechaleidae in which nuptial gifts are widespread. The family is composed of only two species, and the gift seems to be absent in the sister species, creating a relevant scenario for understanding co-evolutionary processes. In the laboratory, we found that although males invested more in nuptial gifts when encountering mated females compared to unmated, they had similar mating access and duration than males lacking a gift. We also found an absence of female choice between males offering nutritive and worthless gifts. Few females were aggressive and cannibalized males, and we did not find evidence that the gift protected males from cannibalism. In the field, 50% of the gifts were worthless items. This is congruent with the laboratory findings where males offering worthless gifts seem to better attract females, which we discuss in the context of exploitation of female gustatory bias. We therefore propose that females may have evolved indifference for the gift and that gift-giving in this species represents a currently non-functional remnant of a behaviour.

Significance statement

Nutritive nuptial gifts can exploit female gustatory preferences, with mutual benefits for both sexes: males can increase mating success and survival, while females increase their fecundity. But males can offer worthless gifts leading females to suboptimal matings, and in turn females can evolve indifference for the trait. The spider genus Trechaleoides is ideal to examine this process because gift-giving behaviour is present in one species and absent in the other. We examined females’ preferences for nuptial gifts and its function for males in the gift-giving species T. keyserlingi. We found that males invest in a gift but gain no reproductive advantage, as females were equally likely to mate with them regardless of whether they offered a gift or whether the gift was nutritive or worthless. We propose that females may have changed their preferences and that the gift is a remnant non-functional trait.