Molecular Social Interactions

Abstract

Studies of social behavior generally focus on interactions between two or more individual animals. However, these interactions are not simply between whole animals, but also occur between molecules that were produced by the interacting individuals. Such “molecular social interactions” can both influence and be influenced by the organismal-level social interactions. We illustrate this by reviewing the roles played by seminal fluid proteins (Sfps) in molecular social interactions between males and females of the fruit fly Drosophila melanogaster. Sfps, which are produced by males and transferred to females during mating, are involved in inherently social interactions with female-derived molecules, and they influence social interactions between males and females and between a female’s past and potential future mates. Here, we explore four examples of molecular social interactions involving D. melanogaster Sfps: processes that influence mating, sperm storage, ovulation, and ejaculate transfer. We consider the molecular and organismal players involved in each interaction and the consequences of their interplay for the reproductive success of both sexes. We conclude with a discussion of the ways in which Sfps can both shape and be shaped by (in an evolutionary sense) the molecular social interactions in which they are involved.

Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions

“…The proteins that accompany sperm into the female—once dismissed as simply a supportive medium for sperm—are now known to be potent modulators of female reproductive biology; in some cases, they even have effects on offspring (reviewed in Martan and Shepherd 1976; Chapman 2001; Gillott 2003; Kubli 2003; Poiani 2006; Sirot et al 2009; Avila et al 2011; Rodríguez-Martínez et al 2011; Ratto et al 2012; Bromfield et al 2014). Most SFPs are the products of secretory glands in the male reproductive tract; these include the prostate glands, epididymi, and seminal vesicles of mammals (Poiani 2006; Rodríguez-Martínez et al 2011) and the male accessory glands and ejaculatory ducts/bulb of arthropods (Gillott 2003).…”

“…Females of many insect species show dramatic changes in postmating behavior (reviewed in Gillott 2003; Sirot et al 2009; Avila et al 2011). In some species, mated females do not remate, or they remate at very low levels.…”

“…In several insect species, receipt of SFPs decreases the probability of female remating (reviewed in Gillott 2003; Sirot et al 2009; Avila et al 2011). Initial decreases in remating may not involve SFPs and can result from processes such as transfer of cuticular pheromones (e.g., in Drosophila [Zawistowski and Richmond 1986]) or from physical mate guarding.…”

“…Here, we explore the roles, evolution, and significance of these male-derived players in sexual conflict. We refer the reader to previous reviews for much of the detailed functional information on SFPs (e.g., Chapman 2001; Gillott 2003; Kubli 2003; Arnqvist and Rowe 2005; Poiani 2006; Sirot et al 2009; Avila et al 2011; Rodríguez-Martínez et al 2011) and focus here instead on selected examples, drawn largely from the study of insects.…”

Oh, the places they’ll go

“…Moreover, direct examination of sperm localization in the female reproductive tract has revealed that a component of the mating stimulus that is neither sperm nor male accessory gland product is sufficient to cause physical displacement of sperm 21 , 36 . Finally, SFPs influence levels of sperm competition through their effects on sperm recruitment, retention and distribution among SSOs (described below, and reviewed in refs 8 , 9 , 130 …”