Female novelty and male status dynamically modulate ejaculate expenditure and seminal fluid proteome over successive matings in red junglefowl

Aitor Alvarez-Fernandez,Tommaso Pizzari,Kirill Borziak,Grant C Mcdonald,Steve Dorus

doi:10.1038/s41598-019-41336-5

Aitor Alvarez-Fernandez, Tommaso Pizzari + Show 3 more

Open Access

https://doi.org/10.1038/s41598-019-41336-5

Copy DOI

Journal: Scientific Reports	Publication Date: Apr 10, 2019
Citations: 10	License type: open-access

Affiliation: University of Oxford, Syracuse University

Abstract

Theory predicts that males will strategically invest in ejaculates according to the value of mating opportunities. While strategic sperm allocation has been studied extensively, little is known about concomitant changes in seminal fluid (SF) and its molecular composition, despite increasing evidence that SF proteins (SFPs) are fundamental in fertility and sperm competition. Here, we show that in male red junglefowl, Gallus gallus, along with changes in sperm numbers and SF investment, SF composition changed dynamically over successive matings with a first female, immediately followed by mating with a second, sexually novel female. The SF proteome exhibited a pattern of both protein depletion and enrichment over successive matings, including progressive increases in immunity and plasma proteins. Ejaculates allocated to the second female had distinct proteomic profiles, where depletion of many SFPs was compensated by increased investment in others. This response was partly modulated by male social status: when mating with the second, novel female, subdominants (but not dominants) preferentially invested in SFPs associated with sperm composition, which may reflect status-specific differences in mating rates, sperm maturation and sperm competition. Global proteomic SF analysis thus reveals that successive matings trigger rapid, dynamic SFP changes driven by a combination of depletion and strategic allocation.

Highlights

Sperm competition, arising from polyandry, favours the production of competitive ejaculates[1,2,3]
Ejaculates delivered to sexually novel females on average contained a higher number of sperm than one would predict based on the overall pattern of sperm depletion, indicating that males progressively reduce ejaculate expenditure with increasing sexual familiarity and bias sperm allocation in favour of sexually novel females[6]
A male will encounter mating opportunities sequentially, and strategies of ejaculate expenditure should seek to optimise investment in a current female given a certain probability of encountering a new female in the near future

Summary

Introduction

Sperm competition, arising from polyandry, favours the production of competitive ejaculates[1,2,3]. Theoretical work has shown that explicit consideration of potential SF effects can drastically change predictions of evolutionarily stable strategies of male ejaculate expenditure, calling for empirical research to elucidate patterns of male SF allocation[25,26,27] Consistent with this expectation, empirical evidence is beginning to emerge suggesting that patterns of SFP allocation might vary with the level of sperm competition[28,29,30,31,32,33] and access to new mating opportunities as determined by male social status[34]. The recent characterisation of the red junglefowl seminal fluid proteome identified more than 1,100 SFPs including some potentially involved in immunity and antimicrobial defences, sperm maturation, and fertilisation, revealing that this is a functionally complex medium with potentially important effects in sperm competition and postcopulatory events[40]

Methods

Results

Conclusion