Flexible polyandry in female flies is an adaptive response to infertile males

Abstract

Infertility is common in nature despite its obvious cost to individual fitness. Rising global temperatures are predicted to decrease fertility, and male sterility is frequently used in attempts to regulate pest or disease vector populations. When males are infertile, females may mate with multiple males to ensure fertilization, and changes in female mating behavior in turn could intensify selection on male fertility. Fertility assurance is a potentially wide-spread explanation for polyandry, but whether and how it actually contributes to the evolution of polyandry is not clear. Moreover, whether a drop in male fertility would lead to a genetic increase in polyandry depends on whether females respond genetically or through behavioral plasticity to male infertility. Here, we experimentally manipulate male fertility through heat-exposure in Drosophila pseudoobscura, and test female discrimination against infertile males before and after mating. Using isogenic lines, we compare the roles of behaviorally plastic versus genetically fixed polyandry. We find that heat-exposed males are less active and attractive, and that females are more likely to remate after mating with these males. Remating rate increases with reduced reproductive output, indicating that females use current sperm storage threshold to make dynamic remating decisions. After remating with fertile males, females restore normal fecundity levels. Our results suggest that male infertility could explain the evolution of adaptively flexible polyandry, but is less likely to cause an increase in genetic polyandry.

Age‐specific sensitivity of sperm length and testes size to developmental temperature in the bruchid beetle

“…Females that mate with males better able to buffer their development against thermal stress will have enhanced fertility themselves. This process could be further augmented by the fact that males experiencing thermal stress during development are less likely to mate with females (Vasudeva et al ., 2018; Iossa et al ., 2019; Sutter et al ., 2019) and, if they do, are more likely to lose out in terms of sperm competition (Vasudeva et al ., 2014). However, this scenario ignores the impact of thermal stress on female reproductive form and function (Iossa, 2019).…”

Female fruit flies cannot protect stored sperm from high temperature damage

“…Sterilisation of mated females could be particularly devastating to species with low remating rates. However, females can use facultative polyandry to improve offspring production when mating with sub-fertile males (Sutter et al, 2019; Vasudeva et al, 2021). For example, heat-shocked males of the flour beetle Tribolium castaneum have low numbers of viable sperm after heat-stress (Vasudeva et al, 2021).…”

Fluctuating heat stress during development exposes reproductive costs and putative benefits

“…In addition, developmental heat stress may have negative or positive carry over effects on adult reproductive fitness during high temperatures (Porcelli et al, 2017) or trans-generational effects (Walzer et al, 2020). Finally, remating of both males and females could mitigate such impacts (Sutter et al, 2019;Vasudeva et al, 2021).…”