Molecular social interactions: Drosophila melanogaster seminal fluid proteins as a case study

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.

Figure 1

Female Drosophila melanogaster reproductive tract. During mating, the ejaculate is transferred into the uterus. From there, different components of the ejaculate move to different locations within the female reproductive tract. Some seminal fluid proteins also move out of the reproductive tract and into circulation. SR: seminal receptacle; ST: spermatheca. Drawing by J. Sitnik; for clarity, some parts have been simplified in the figure.

Figure 2

Mating attempt by male and (insets) position of female abdomen when she is receptive (A) and unreceptive (B; ovipositor extruded) to the mating attempt. Drawing by J. Sitnik.

Figure 3

Ovulin processing. Western blot showing intact ovulin in the male and ovulin processing products over time after the start of mating (ASM) in the female reproductive tract. Schematic of ovulin processing is on right (schematic adapted from Park & Wolfner 1995; 37kDa is the size of intact ovulin; in some places on the blot, bands are broad due to glycosylation variants that are not shown in the schematic).

Figure 4

Male D. melanogaster transfer more sex peptide and ovulin when they are in the presence of another male before and during copulation than when they are alone. Data figure adapted from Wigby et al. 2009. Drawing by J. Sitnik; for clarity, some body parts have been simplified in the figure.

Figure 5

Male and female genotypes affect outcome of sperm competition experiments. The genotypes of the particular male and female involved in a mating affect the defensive component of sperm defense, P1. P1 measures the proportion of offspring sired by the first male after the female has remated. In this hypothetical example, male A has a much higher P1 than male B when either of them mates with a female of genotype 1. However, when these same males mate a female of genotype 2, male B now has the advantage. Here, the second male to mate in each competition experiment does not vary. These interactions become even more complex when the genotype of the second male to mate is taken into consideration.

Figure 6

Sexual conflict may maintain polymorphisms in the population. Competition among males for mates/fertilizations drives selection for new alleles that confer a competitive advantage to males for some reproductive trait. For example, males with this allele may induce a higher rate of ovulation in females by way of a particular Sfp. This higher ovulation rate may be harmful to females due to higher energy costs, driving selection for alleles that allow females to resist the effects of the harmful male allele. This cycle continues, with males developing new competitive strategies, each with a potential female cost associated with them. As a result of this process occurring simultaneously at many loci, polymorphisms are maintained in the population. Adapted from Arnqvist & Rowe 2005.