Drosophila seminal sex peptide associates with rival as well as own sperm, providing SP function in polyandrous females

Abstract

When females mate with more than one male, the males' paternity share is affected by biases in sperm use. These competitive interactions occur while female and male molecules and cells work interdependently to optimize fertility, including modifying the female’s physiology through interactions with male seminal fluid proteins (SFPs). Some modifications last long-term, indirectly benefiting later males. Indeed, rival males tailor their ejaculates accordingly. Here we show that SFPs from one male can directly benefit a rival's sperm. We report that Sex Peptide (SP) that a female Drosophila receives from a male can bind sperm that she had stored from a previous male, and rescue the sperm utilization and fertility defects of an SP-deficient first-male. Other seminal proteins received in the first mating 'primed' the sperm (or the female) for this binding. Thus, SP from one male can directly benefit another, making SP a key molecule in inter-ejaculate interaction.

Identification of a micropeptide and multiple secondary cell genes that modulate Drosophila male reproductive success

“…Thus, there are more of them left to compete with the second male’s sperm when second mating occurs. In light of these and recent data ( 64 ), we propose that while overretention of sperm (such as those from ΔMSAmiP males) in storage organ may enhance success in sperm-competition assays, the failure to properly release those sperm in the first place may be detrimental to the male’s production of offspring over time, and hence the genes are not lost during evolution.…”

TheDrosophilaseminal proteome and its role in postcopulatory sexual selection

“…Consistent with the idea that one male's Sfps can help another, seminal fluid can boost the offspring production of rivals [106]. For example, the female receipt of Acp36DE from a subsequent male can improve the offspring production of an Acp36DEdeficient male [67], and SP can bind to a previous rival male's sperm and provide SP function to those sperm [107].…”

“…In social insects, there is evidence that sperm survival suffers in the seminal fluid of non-self males, suggesting that in those species Sfps might directly bias against rival sperm [130]: but there is no compelling evidence to date for the same in D. melanogaster. By contrast, SP can associate with rival sperm and restore its function, potentially benefitting the rival male [107]. There is also evidence that seminal fluid can promote the survival of self or rival sperm equally [131] (but see also [132]).…”

Research gaps and new insights in the intriguing evolution of Drosophila seminal proteins

“…These proteins, likely adapted to sperm competition and fertilization, have been highly studied in Drosophila melanogaster (e.g., Civetta & Ranz 2019;Hopkins, Sepil, Bonham et al 2019;Hopkins, Sepil, Thézénas et al 2019;Misra & Wolfner 2020;Ravi Ram et al 2005;Ravi Ram & Ramesh 2003;Ravi Ram & Wolfner 2007;Wigby et al 2020;Wolfner 2007). Once inside the female, some of these proteins will remain bound to spermatozoa, contributing to sperm functions, and some may even interact with the already stored sperm from previous mates (e.g., Avila et al 2011;Holman 2009;Misra & Wolfner 2020;Ravi Ram & Wolfner 2007;Singh et al 2018;Wolfner 2007). Many others instead will interact intimately with female biomolecules in the reproductive tract and other organs, and are capable of changing drastically her physiology and behavior (e.g., Avila et al 2011;Avila et al 2016;Avila & Wolfner 2017;Lung & Wolfner 1999;Ravi Ram et al 2005;Ravi Ram & Wolfner 2007).…”

“…During mating, spermatozoa expelled from the testes travel throughout the ejaculatory duct into the female reproductive tract accompanied by a rich repertoire of proteins and peptides known as Seminal Fluid Proteins (SFPs) (reviewed in, e.g., Avila et al 2011; Avila et al 2016; Chapman 2008; Ramm 2020). These proteins, likely adapted to sperm competition and fertilization, have been highly studied in Drosophila melanogaster (e.g., Civetta & Ranz 2019; Hopkins, Sepil, Bonham et al 2019; Hopkins, Sepil, Thézénas et al 2019; Misra & Wolfner 2020; Ravi Ram et al 2005; Ravi Ram & Ramesh 2003; Ravi Ram & Wolfner 2007; Wigby et al 2020; Wolfner 2007). Once inside the female, some of these proteins will remain bound to spermatozoa, contributing to sperm functions, and some may even interact with the already stored sperm from previous mates (e.g., Avila et al 2011; Holman 2009; Misra & Wolfner 2020; Ravi Ram & Wolfner 2007; Singh et al 2018; Wolfner 2007).…”