Sperm-limited males continue to mate, but females cannot detect the male state in a parasitoid wasp

Jun Abe

doi:10.1007/s00265-019-2653-4

Abstract

Female mating frequency and male ejaculate allocation are likely to interact. Females may adjust their propensity for remating based on the amount of provided sperm to ensure a sufficient sperm supply, and males may determine sperm allocation based on female availability and female mating frequency. In this study, I investigated male and female mating behaviors in the parasitoid wasp Anisopteromalus calandrae. The wasp exhibits the haplo-diploid sex determination, in which sperm-depleted females are constrained to produce only sons by laying unfertilized eggs. The first experiment showed that a rapid succession of male mating decreased the production of daughters (fertilized eggs) by the inseminated females, suggesting that sperm-limited males provided an insufficient amount of sperm to the females. Although the males appeared to replenish their sperm store after 6 h, they mated upon encountering females despite their sperm shortage. The second experiment showed that copulation reduced the subsequent mating receptivity of the inseminated females irrespective of whether the females received a sufficient amount of sperm. Moreover, although approximately 26% of females accepted a second mating and recovered a certain degree of daughter production, remating was independent of the mating status of their first mating partner or the social environment. These results suggest that sperm-limited males may benefit from continuing to mate because their copulation prevents competing males from reproducing with their mates. Females incur a cost from not remating depending on the amount of sperm provided, which may result from weak environmental selection pressure or manipulation by the initial mate.Significance statementMale and female mating strategies are likely to evolve interdependently. Specifically, in species that produce limited numbers of sperm, the mating behavior of males and females is likely to be influenced by sperm transfer. The results of the present study suggest that males of the parasitoid wasp Anisopteromalus calandrae can replenish their sperm stores over time. However, sperm-limited males that encounter a potential mating partner mate rather than wait for sperm recovery. Females do not discriminate the male state before copulation, and those that mate with sperm-limited males suffer from sperm shortage. Although females can augment their sperm supply by remating, only a portion of females do so, regardless of sperm supply. The lack of a female facultative response suggests weak environmental selection on the species or the existence of sexual conflict over sperm transfer.

Highlights

The ubiquity of polyandry in nature implies that multiple mating yields benefits that can offset the costs imposed on females (Arnqvist and Nilsson 2000; Pizzari and Wedell 2013; Parker and Birkhead 2013)
Females are predicted to favor multiple matings to acquire sufficient male reproductive budgets to prevent reproductive constraint (Abe and Kamimura 2015). While this and other theoretical works have incorporated coevolutionary feedbacks, the sperm economy theory emphasizes the importance of simultaneously examining both male ejaculate allocation and female mating frequency to reveal the balance of sperm supply in empirical investigations
The present study revealed that sperm limitation could be a restricting factor that regulates the reproduction of male and female A. calandrae

Summary

Introduction

The ubiquity of polyandry in nature implies that multiple mating yields benefits that can offset the costs imposed on females (Arnqvist and Nilsson 2000; Pizzari and Wedell 2013; Parker and Birkhead 2013). To examine the interaction between male and female reproductive strategies, Abe and Kamimura (2015) proposed a novel framework called the Bsperm economy^ theory and developed a model that investigated the coevolutionary dynamics between male ejaculate allocation and female remating frequency (see Bocedi and Reid 2016) The interaction between these strategies is likely to be influenced by factors that determine the level of sperm limitation in the population, such as operational sex ratios. Females are predicted to favor multiple matings to acquire sufficient male reproductive budgets to prevent reproductive constraint (Abe and Kamimura 2015) While this and other theoretical works have incorporated coevolutionary feedbacks, the sperm economy theory emphasizes the importance of simultaneously examining both male ejaculate allocation and female mating frequency to reveal the balance of sperm supply in empirical investigations

Methods

Results

Conclusion