The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication.

Kirill Borziak,Steve Dorus,Aitor Álvarez-Fernández,Tommaso Pizzari,Timothy L Karr

doi:10.1038/srep35864

Abstract

Seminal fluid proteins (SFPs) are emerging as fundamental contributors to sexual selection given their role in post-mating reproductive events, particularly in polyandrous species where the ejaculates of different males compete for fertilisation. SFP identification however remains taxonomically limited and little is known about avian SFPs, despite extensive work on sexual selection in birds. We characterize the SF proteome of the polyandrous Red junglefowl, Gallus gallus, the wild species that gave rise to the domestic chicken. We identify 1,141 SFPs, including proteins involved in immunity and antimicrobial defences, sperm maturation, and fertilisation, revealing a functionally complex SF proteome. This includes a predominant contribution of blood plasma proteins that is conserved with human SF. By comparing the proteome of young and old males with fast or slow sperm velocity in a balanced design, we identify proteins associated with ageing and sperm velocity, and show that old males that retain high sperm velocity have distinct proteome characteristics. SFP comparisons with domestic chickens revealed both qualitative and quantitative differences likely associated with domestication and artificial selection. Collectively, these results shed light onto the functional complexity of avian SF, and provide a platform for molecular studies of fertility, reproductive ageing, and domestication.

Highlights

Seminal fluid proteins (SFPs) are emerging as fundamental contributors to sexual selection given their role in post-mating reproductive events, in polyandrous species where the ejaculates of different males compete for fertilisation
Tandem mass spectrometry analyses were conducted on SF from 12 male Red junglefowl (RJF), where each sample was the product of 3 pooled SF samples from the same male
This revealed that 52.1% (137 out of 263) of identified blood plasma proteins were present in RJF SF (Table S1, Supporting Information)

Summary

Introduction

Seminal fluid proteins (SFPs) are emerging as fundamental contributors to sexual selection given their role in post-mating reproductive events, in polyandrous species where the ejaculates of different males compete for fertilisation. A growing body of empirical work has demonstrated the involvement of several such molecules in different stages of reproduction, including sperm fertilising efficiency and longevity, antimicrobial defences, female sperm utilisation, the coordination of ovulation and oviposition in females, maternal allocation, and female remating propensity[2] Given their modulation of postcopulatory reproductive events, much research has focused on the role of seminal fluid proteins (SFPs) in polyandrous species, where females obtain ejaculates from multiple partners, prolonging sexual selection on males after copulation via sperm competition and cryptic female choice[1]. Amongst D. melanogaster SFPs, Sex Peptide (Acp70A) delays female remating[8], while ovulin (Acp26Aa) enhances short term egg production by the female[9] These functionalities, while adaptive to males within the context of postcopulatory sexual selection, can have detrimental repercussions on the fitness of females, and have been put forth as potential examples of sexual conflict[10]. Polyandry can drive the rapid evolution of SFPs and this, in turn, can contribute to the establishment of reproductive barriers and, eventually, to speciation[14,15]

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