Natural variation in male-induced ‘cost-of-mating’ and allele-specific association with male reproductive genes in Drosophila melanogaster

Abstract

One of the most sharply defined sexual conflicts arises when the act of mating is accompanied by an inflated risk of death. Several reports have documented an increased death rate of female Drosophila as a result of recurrent mating. Transgenic and mutation experiments have further identified components of seminal fluid that are at least in part responsible for this toxicity. Variation among males in their tendency for matings to be toxic to their partners has also been documented, but here for the first time we identify polymorphism within particular genes conferring differential postmating female mortality. Such polymorphism is important, as it raises the challenge of whether sexual conflict models can provide means for maintenance of polymorphism. Using a set of second chromosome extraction lines, we scored differences in post-mating female fecundity and longevity subsequent to mating, and identified significant among-line differences. Seventy polymorphisms in ten male reproductive genes were scored and permutation tests were used to identify significant associations between genotype and phenotype. One polymorphism upstream of PEBII and an amino acid substitution in CG17331 were both associated with male-induced female mortality. The same allele of CG17331 that is toxic to females also induces greater refractoriness to remating in the females, providing an example of an allele-specific sexual conflict. Postcopulatory sexual selection could lead to sexual conflict by favouring males that prevent their mates from mating, even when there is a viability cost to those females.

The evolutionary outcome of sexual conflict

“…The most renowned examples of this are the accessory gland proteins (Acps) in the seminal fluid of Drosophila species (Chapman 2001;Wolfner 2002;Kubli 2003;Fiumera et al 2006). There are over 80 different seminal peptides, some of which are known to modify female reproductive behaviour, in some cases by mimicking female hormones.…”

Introduction. Sexual conflict: a new paradigm?

“…The rapid evolution of male accessory gland proteins (Acps) and female reproductive proteins in Drosophila melanogaster remains the best-studied system to date in sexual conflict. New approaches, including large-scale screens to detect associations between different Acp variants and the performance of males bearing those variants in sperm competition assays (Fiumera et al 2006), are providing new insights into this system. Fiumera and colleagues' work reveals some significant, and sometimes antagonistic, associations between Acp alleles and performance as either the first or second mate of a female.…”

Genetic variation in male-induced harm in Drosophila melanogaster

“…The extent to which this trait is heritable will therefore have important consequences for the rate and/or trajectory of inter-sexual coevolution. Despite its importance, only a handful of attempts have been made to determine if there is additive genetic variance for male-induced harm [12][13][14]. Additionally, these studies have been limited in several ways.…”