Rival seminal fluid induces enhanced sperm motility in a polyandrous ant

Joanito Liberti,Boris Baer,Jacobus J Boomsma

doi:10.1186/s12862-018-1144-y

Joanito Liberti, Boris Baer + Show 1 more

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https://doi.org/10.1186/s12862-018-1144-y

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Abstract

BackgroundPromiscuous mating and sperm competition often induce arms races between the sexes with detrimental outcomes for females. However, ants with multiply-inseminated queens have only a single time-window for sperm competition and queens are predicted to gain control over the outcome of sperm storage quickly. The seminal fluid of Acromyrmex leaf-cutting ants reduces the viability of rival sperm, but how confrontations between unrelated ejaculates affect sperm storage remains unknown.ResultsWe investigated the effects of ejaculate admixture on sperm motility in A. echinatior and found that the proportion of motile spermatozoa, sperm swimming speed, and linearity of sperm movement increased when rival ejaculates were mixed in vitro. Major effects induced by the seminal fluid of rival males were of similar magnitude to those generated by queen reproductive tract secretions, whereas own seminal fluid induced lower sperm activation levels.ConclusionsOur results suggest that ant sperm respond via a self–non-self recognition mechanism to similar or shared molecules expressed in the reproductive secretions of both sexes. Lower sperm motility in the presence of own seminal fluid indicates that enhanced motility is costly and may trade-off with sperm viability during sperm storage, consistent with studies in vertebrates. Our results imply that ant spermatozoa have evolved to adjust their energetic expenditure during insemination depending on the perceived level of sperm competition.

Highlights

Promiscuous mating and sperm competition often induce arms races between the sexes with detrimental outcomes for females
This increase in motile sperm was correlated with a > 20% average increase in composite sperm velocity as captured by first principal component (PC1), similar to the separate variables that loaded PC1, and an increase in sperm linearity (LIN; fig. 2c) of 11.6% (F1,106 = 5.54, P = 0.0204; see Additional file 1: Table S6 for details)
Exposure of sperm to own seminal fluid significantly increased the proportion of motile sperm by 29.8%, significantly increased sperm swimming speed by 20% (VCL = 24.2%; Velocity average path (VAP) = 22.2%; Velocity straight-line (VSL) = 21.2%), and made sperm swim 10.1% more linearly compared to sperm in the control treatment not containing any seminal fluid

Summary

Introduction

Promiscuous mating and sperm competition often induce arms races between the sexes with detrimental outcomes for females. While traveling through the reproductive tract of females after insemination, sperm typically experience environmental changes in temperature or pH, increasing or decreasing concentrations of organic molecules or emerging immune challenges [1]. These female factors often mediate viability selection of sperm and have led to the evolution of sophisticated olfactory recognition mechanisms that allow sperm to reach fertilization or storage sites despite of female-imposed handicaps [2, 3]. Because seminal fluid is ejaculated together with sperm, these glandular secretions can play a key role in securing sperm viability and paternity in female tracts where interactions between secretions by females and rival males set the rules for sperm competition. Male fowls (Gallus gallus) can adjust the velocity of their spermatozoa through allocating more seminal fluid when mating with more attractive females [22] and male morphs of externally fertilizing grass gobies (Zosterisessor ophiocephalus) and Arctic charr (Salvelinus alpinus) produce seminal fluids

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