Polyandrous mating increases offspring production and lifespan in female Drosophila arizonae

Abstract

Multiple mating by females is a widespread but often costly behavior. However, according to the Bateman principle, mating with multiple males may not increase the number of offspring produced by females. Despite the Bateman paradigm, many studies have shown advantages to polyandry. We investigated the fitness consequences of different mating regimes (virginity, once-mated, serial monogamy, and polyandry) in Drosophila arizonae, a species in which females remate frequently, experience a possible cost of mating in the form of an insemination reaction, and receive nutritive seminal contributions from males. Although monogamous and polyandrous females mated at similar rates, polyandry caused females to produce significantly more offspring for a longer period of their lives. Females with greater access to males laid significantly more eggs than those mated just once, and polyandrous females had a longer oviposition period than once mated females. Polyandrous females lived significantly longer than both virgin and serially monogamous females, suggesting that costs of mating are either low or offset by other benefits. A statistically significant interaction between the number of matings and mating treatment showed that additional matings allowed fitness increases for polyandrous, but not serially monogamous, flies. A direct fitness benefit for females by sperm replenishment is the most likely explanation for these results. Males may have partitioned their sperm and/or seminal fluid protein contributions to provide less for females they previously mated (i.e., the Coolidge effect), but male ejaculate exploitation and female effects are also possible. The high benefits and low costs of polyandry in our study contrast with other Drosophila papers and therefore highlight the extreme mating system diversity across the genus.

Significance statement

In most mating systems, it is unclear why females mate with more than one male. Fruit fly females generally are expected to experience severe costs of mating. We used a highly promiscuous fruit fly species to test for costs and benefits to females of remaining virgins, mating once, remating many times with the same male (monogamy), and remating several times with a different male (polyandry). Polyandry was advantageous for females over monogamy because it allowed them to produce more adult offspring for a longer period of their lives. Additional copulations resulted in strong fitness increases for polyandrous, but not monogamous, female flies. Both polyandry and monogamy were better than mating just once because they allowed increases in egg and offspring production. Polyandry also conferred increases in lifespan over both virginity and monogamy. Therefore, we show benefits to mating with multiple males and failed to observe substantial costs of mating. The most likely explanation for our findings is a male effect by which they transfer fewer sperm and/or other ejaculate components to females they have previously mated (the Coolidge effect), though other mechanisms are possible.