Rival seminal fluid induces enhanced sperm motility in a polyandrous ant

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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1144-y) contains supplementary material, which is available to authorized users.

Long‐term sperm storage in eusocial Hymenoptera

“…Apis florea , Apis andrenifromis (Koeniger, Koeniger & Wongsiri, 1989; Koeniger et al ., 2000); leaf cutter ants (den Boer et al ., 2015)], in eusocial Hymenoptera sperm are typically stored in the bursa copulatrix before being transferred to the spermatheca (Pascini & Martins, 2017; Gotoh & Furukawa, 2018). The role of the bursa copulatrix in these species remains largely unknown to date (Oppelt & Heinze, 2007; Liberti et al ., 2018). Proteomic analyses of the fluid from the bursa copulatrix could reveal the presence of proteins involved in the elimination of toxic compounds (e.g.…”

“…Over recent decades, this unique reproductive system has received much attention, with investigations focusing on sperm production (Page, 1986; Schlüns et al ., 2003; Baer & Boomsma, 2004; Holman et al ., 2011; Aron et al ., 2016; Dávila & Aron, 2017; Metzler, Schrempf & Heinze, 2018); sperm size (Baer et al ., 2003; Fitzpatrick & Baer, 2011; Aron et al ., 2016; Metzler et al ., 2018); sperm viability (Locke & Peng, 1993; Dávila & Aron, 2017; Chérasse & Aron, 2018; Fisher & Rangel, 2018; Metzler et al ., 2018); sperm motility (Lensky & Schindler, 1967; Werner & Simmons, 2008; Pearcy et al ., 2014; Ciereszko et al ., 2017; Liberti, Baer & Boomsma, 2018); and seminal fluid composition (Mann, 1954; Blum, Glowska & Taber, 1962; Baer et al ., 2000, 2009 b ; Brown et al ., 2002; King et al ., 2011; Poland et al ., 2011; Gotoh et al ., 2017 a ; Dosseli et al ., 2019), and its role in sexual conflict (Liberti et al ., 2019) and sperm competition (den Boer, Baer & Boomsma, 2010). Boomsma, Baer & Heinze (2005) reviewed the evolution of male mating traits in eusocial insects, including sperm number and size, while Baer (2016) addressed how sperm characteristics are affected by polyandry (multiple mating by queens) and sperm competition.…”

Sperm Storage Costs Determine Survival and Immunocompetence in Newly Mated Queens of the Leaf-Cutting Ant Atta colombica

“…of the sister genus Acromyrmex (Liberti et al, 2018) receive sperm into the bursa copulatrix or the lateral oviducts first, before it is stored during a secondary process. Such two-step sperm storage procedures offer more opportunities for postcopulatory sexual selection, and may allow more sperm to be competitively removed without damaging queen health.…”

Transcriptomic analysis of the honey bee (Apis mellifera) queen spermathecae reveals genes that may be involved in sperm storage after mating

“…In the ant Atta colombica , secretions from the male accessory glands greatly increase sperm viability upon ejaculation inside the female [ 13 ]. In Acromyrmex echinatior ants, sperm have a “self-non-self” recognition system in which sperm motility is lower in the presence of a male’s own seminal fluids, but it is higher when mixed with the seminal fluids of other males’ sperm, suggesting that enhanced sperm motility is costly and thus is only implemented as needed during competition between males [ 14 ].…”