Perceived Sperm Competition Intensity Influences Seminal Fluid Protein Production Prior to Courtship and Mating

Abstract

Sperm competition is a potent postcopulatory selective force where sperm from rival males compete to fertilize a limited set of ova. Considering that sperm production is costly, we expect males to strategically allocate sperm in accordance with the level of competition. Accordingly, previous work has examined a male's strategic allocation in terms of sperm number. However, the seminal fluid proteins (Sfps) transferred along with sperm may also play a crucial role in competition. Surprisingly, the strategic allocation of Sfps has remained largely unexplored. Using Drosophila melanogaster, we examined the expression of three seminal fluid and four spermatogenesis genes in response to perceived sperm competition intensity by manipulating male density in a pre-mating and courtship environment. In the pre-mating environment, we found that males modified Sfp ratios by reducing the production of two spfs when potential rivals were present, while one Sfp and all spermatogenesis genes remained unaltered. In the courtship environment, males did not modify spermatogenesis or Sfp production in response to either rival males or female presence. Our data suggest that perceived competition in the pre-mating environment places a significant influence on Sfp allocation, which may be a general trend in promiscuous animal systems with internal fertilization.K E Y W O R D S : Acps, Drosophila melanogaster, ejaculate, gene expression, spermatogenesis.

Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster

“…One plausible mechanism is through differential gene expression. Expression levels of specific Sfps vary with the perceived level of sperm competition (31). Furthermore, SP and ovulin expression varies among cell type within the male Sfp-producing accessory glands (32,33).…”

Exposure to sperm competition risk improves survival of virgin males

“…We predicted exposure to sperm competition risk would reduce males' survival as a result of costs arising from previously documented adjustments to behaviour and physiology [6,[8][9][10]. Investment in reproductive tissues and fluids is expensive: insects exposed to long-term nutritional stress restrict investment in ejaculates [12] and produce smaller testes [21].…”

“…Theory and empirical data suggest that males exposed to a fluctuating sperm competition environment may also benefit by plastically adjusting their investment in sperm according to the perceived risk [4,5]. Male Drosophila melanogaster exhibit a number of additional plastic responses: males perceiving a high risk of sperm competition mate for longer [6][7][8], downregulate genes for the production of seminal fluid proteins (Sfps) [9] and increase transfer of some Sfps [10]. However, mating is energetically costly: ejaculate quality suffers under nutritional stress in insects [11][12][13], and mating reduces longevity among male D. melanogaster [14].…”

Perception of male–male competition influences Drosophila copulation behaviour even in species where females rarely remate

“…Males use olfactory, visual, auditory and touch cues prior to encountering females to assess the presence of competitor males [5], and respond by prolonging copulation and increasing transfer of accessory gland peptides [3,6]. This behaviour enhances male fitness through increasing his success in sperm competition, and by decreasing his mate's receptiveness to rival males [4].…”