The evolution of multiple mating

Abstract

Polyandry is a paradox: why do females mate multiple times when a single ejaculate often provides enough sperm for lifetime egg production? Gowaty et al. addressed explanations for polyandry in Drosophila pseudoobscura from the perspective of hypotheses based on sex differences in costs of reproduction (CoR). Contrary to CoR, Gowaty et al. showed that (1) a single ejaculate was inadequate for lifetime egg production; (2) polyandry provided fitness benefits to females beyond provision of adequate sperm and (3) fitness benefits of polyandry were not offset by costs. Here, I discuss predictions of the ad hoc hypotheses of CoR and three alternative hypotheses to CoR to facilitate a discussion and further development of a strong inference approach to experiments on the adaptive significance of polyandry for females. Each of the hypotheses makes testable predictions; simultaneous tests of the predictions will provide a strong inference approach to understanding the adaptive significance of multiple mating. I describe a sex-symmetric experiment meant to evaluate variation in fitness among lifelong virgins (V); monogamous females and males with one copulation (MOC); monogamous females and males with multiple copulations (MMC); PAND, polyandrous females; and PGYN, polygynous males. Last, I recommend the study of many different species, while taking care in choice of study species and attention to the assumptions of specific hypotheses. I particularly urge the study of many more Drosophila species both in laboratory and the wild to understand the “nature of flies in nature,” where opportunities and constraints mold evolutionary responses.

Polyandry enhances offspring viability with survival costs to mothers only when mating exclusively with virgin males inDrosophila melanogaster

“…Table 2 summarizes predictions and results of a priori planned tests of hypotheses (Gowaty, 2012, 2013; Gowaty et al., 2010). Exploratory analyzes were of: (1) comparative lifespan variation among females (Figure 5a) and among males (Figure 5b); (2) mean changes over female lifespan in components of RS (Figure 6); and (3) variances in female RS and survival (Table 3).…”

“…We report variation in components of fitness of female subjects in two by two matched sets of treatments testing a priori predictions (Leek & Peng, 2015) of hypotheses (Gowaty, 2012, 2013; Gowaty et al., 2010) about the fitness costs/benefits of mating opportunities available to female subjects. Predictions include the following:

Females may gain direct fitness benefits from exposure to males in which case virgins may die faster than mated females.

Limits to the number of, or the viability of sperm in a single ejaculate, probably occasionally occur in most organisms, especially those without sperm‐storing tissues or organs, but flies do have “sperm management” organs (Markow & O'Grady, 2005) suggesting that one copulation for many organisms is enough to fertilize a females’ lifelong production of eggs.

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“…Classical ideas (Bateman, 1948) say females are "passive" and choosy with limited reproductive capacities predicting few benefits for polyandrous females. Yet, polyandry is common (Anderson, 1974;Gowaty, 2006Gowaty, , 2012Gowaty, , 2013Gowaty & Hubbell, 2013;Taylor, Price, & Wedell, 2014), despite potential fitness costs to females (Otti, 2015). Given classical assumptions, several functional hypotheses may explain why females multiply mate including that female multiple mating may be a result of male-male competitive drive (Trivers, 1972), occurring when males coerce females to mate.…”

“…Given the diversity of the hypotheses explaining multiple mating and recently reviewed in Gowaty (2012;, we used an experimental design (Table 1) allowing simultaneous tests of alternative predictions of multiple hypotheses, while reducing opportunities for male behavioral coercion of females. Using captive Drosophila melanogaster free of Wolbachia and Spiroplasma endosymbionts, we controlled females' exposure to conspecific males so that no female in any treatment was with more than one male in a single day, providing some leveling of the ecological playing field of subjects in a way that seldom occurs in captive studies (Billeter, Jagadeesh, Stepek, Azanchi, & Levine, 2012;Maklakov, Immler, Løvlie, Flis, & Friberg, 2013).…”

“…We report variation in components of fitness of female subjects in two by two matched sets of treatments testing a priori predictions (Leek & Peng, 2015) of hypotheses (Gowaty, 2012(Gowaty, , 2013Gowaty et al, 2010) about the fitness costs/benefits of mating opportunities available to female subjects. Predictions include the following:…”