Polyandrous mating increases offspring production and lifespan in female Drosophila arizonae
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.
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.
KeywordsMonogamy Virginity Polyandry Sperm allocation Cost of mating Coolidge effect
We thank N.R. Schroeder and J.A. Gómez for their help in handling flies and media preparation. S. Pitnick provided helpful comments on an earlier draft. Materials and other support were provided by the Department of Biological Sciences and Office of Research and Graduate Studies at Florida Gulf Coast University.
- Caspers BA, Krause ET, Hendrix R, Kopp M, Rupp O, Rosentreter K, Steinfartz S (2014) The more the better—polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra). Mol Ecol 23:239–250CrossRefPubMedGoogle Scholar
- Markow TA (1982) Mating systems of cactophilic Drosophila. In: Barker JSF, Starmer WT (eds) Ecological genetics and evolution. The cactus-yeast-Drosophila model system. Academic Press Australia, Sydney, pp 273–287Google Scholar
- Markow TA (1996) Evolution of Drosophila mating systems. Evol Biol 29:73–106Google Scholar
- SAS Institute (2003) SAS system for Windows. Release 8.01 edition. SAS Institute, CaryGoogle Scholar
- Tan CKW, Lovlie H, Greenway E, Goodwin SF, Pizzari T, Wigby S (2013) Sex-specific responses to sexual familiarity, and the role of olfaction in Drosophila. Proc R Soc Lond B 280Google Scholar
- Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179Google Scholar