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Strategic Ejaculation in Simultaneously Hermaphroditic Land Snails: More Sperm Into Virgin Mates Kazuki Kimura* and Satoshi Chiba

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Strategic Ejaculation in Simultaneously Hermaphroditic Land Snails: More Sperm Into Virgin Mates Kazuki Kimura* and Satoshi Chiba Kimura and Chiba BMC Evolutionary Biology 2013, 13:264 http://www.biomedcentral.com/1471-2148/13/264 RESEARCH ARTICLE Open Access Strategic ejaculation in simultaneously hermaphroditic land snails: more sperm into virgin mates Kazuki Kimura* and Satoshi Chiba Abstract Background: It has been theorised that sperm competition promotes the strategic usage of costly sperm. Although sperm competition is thought to be an important driving force of reproductive traits in simultaneous hermaphrodites as well as in species with separate sexes, empirical studies on strategic ejaculation in simultaneous hermaphrodites are scarce. Results: In the present study, we tested whether the simultaneously hermaphroditic land snail Euhadra quaesita adjusts the number of sperm donated according to the condition of the mate and whether the pattern of strategic ejaculation is in line with previously suggested theories. We found that individuals donated much more sperm when they copulated with a virgin mate than when they copulated with a non-virgin. Conclusion: The virgin-biased pattern of ejaculation matches the theoretical prediction and suggests that sperm competition significantly influence the reproductive traits of simultaneously hermaphroditic land snails. Keywords: Sperm competition, Strategic ejaculation, Sperm allocation, Simultaneous hermaphrodites, Land snails Background expected fertility in a mating event, which include mate If a female copulates with more than one male and condition and sperm competition levels [10,11]. Indeed, stores the resulting sperm, sexual selection is likely to such strategic ejaculation has been reported in many an- continue after copulation via sperm competition and imals, including insects, fish, and mammals [12]. As in cryptic female choice. Although the outcome of sperm species with separate sexes, post-copulatory sexual selec- competition can be influenced by non-numerical factors tion is thought to be an important evolutionary force such as sperm length and seminal fluid composition leading to morphological and behavioral diversification [1,2], the relative number of sperm transferred by com- in simultaneous hermaphrodites, which have male and peting males is a key predictor of fertilization success female functions at the same time [13,14]. Moreover, under post-copulatory reproductive conditions in several previous empirical studies have shown that such organ- species [3-5]. Because sperm cells are relatively small isms are careful about the use of resources for and require less energy to produce than eggs, males are reproduction and can adjust the allocation of resources expected to evolve an undiscriminating eagerness to between their male and female functions [15]. Therefore, copulate and transfer their sperm, whereas females are simultaneous hermaphrodites are also expected to be expected to show a discriminating passivity [6]. How- prudent with their limited male reserves. However, the ever, accumulating evidence has suggested that sperm literature on this point has been dominated by studies and seminal fluids are, in fact, costly to produce [7-9]. on species with separate sexes. Selection would therefore favour males that adjust their Several factors are known to be involved in the stra- ejaculate expenditure according to the indicators of tegic usage of limited male reserves. Among these fac- tors, sperm competition risk and intensity have been well studied from both theoretical [16-18] and empirical * Correspondence: [email protected] Department of Environmental Life Sciences, Graduate School of Life perspectives [19-21]. The sperm competition risk model Sciences, Tohoku University, Kawauchi 41, Aoba-ku, Sendai 980-8576, Japan considers the probability that sperm competition occurs © 2013 Kimura and Chiba; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Kimura and Chiba BMC Evolutionary Biology 2013, 13:264 Page 2 of 7 http://www.biomedcentral.com/1471-2148/13/264 in a focal female [18]. Alternatively, the sperm competi- sperm transfer [30]. When individuals reciprocally tion intensity model applies the number of competitors intromit their penises in a single mating event, they may when females mate with more than two males [17]. For alter the amount of sperm transferred to their mates example, animals use the number of rivals and the mat- (autosperm) based on the amount of sperm received ing history of their mates as indicators in these cases. (allosperm). Although a pattern of strategic ejaculation Theoretical studies have shown that the properties of according to the mate’s mating status (virgin or non- the mates with which males should spend more ejaculate virgin) was reported in a simultaneously hermaphroditic are species or population specific [11]. Engqvist & freshwater snail, there remains the possibility that the Reinhold [22] have shown that when ejaculates from patterns of resource allocation to a female function differ more than two males compete to fertilize ova (i.e., the between virgin and non-virgin mates, and thus the effect sperm competition intensity model), the remating fre- of mate’s fecundity was unclear [31]. Moreover, although quency of the mates and the fertilization pattern of the large individuals of the hermaphroditic land snail sperm from several mates determine the evolutionary Succinea putris adjust their ejaculate expenditures ac- consequences of strategic ejaculation. Their model has cording to the body sizes of their mates, this result may predicted that a strategy in which larger ejaculations are be explainable in terms of sperm transfer number of the invested in favour of non-virgin mates is evolutionary mates because body size is significantly correlated with stable whenever the remating rate is low. On the other ejaculation size in this species [32]. Therefore, experi- hand, when the remating rate is high, last-male sperm ments that examine these factors at the same time are precedence (i.e., the fertilization priority of sperm from needed to test the theories of sperm competition inten- the latter male) is necessary for the evolution of the sity in simultaneous hermaphrodites. Although only a strategy focusing on non-virgins. Conversely, first-male limited literature exists on strategic ejaculation in simul- sperm precedence or random fertilization lead to stra- taneous hermaphrodites, Baur et al. [33] examined it tegic ejaculation that prioritizes virgin mates. Simultan- and found no evidence of strategic ejaculation according eous hermaphrodites that have a habit of mating with to either mate mating status, mate body size, and mate reciprocal intromission (i.e., they play both male and sperm transfer number in the simultaneously hermaph- female roles and exchange sperm in a single mating roditic land snail Arianta arbustorum. However, it has event) are expected to satisfy the conditions of sperm been suggested that sexual selection including sperm competition intensity models. Such hermaphroditic ani- competition is weak in Arianta arbustorum [34-36]. mals are thought to be intensely promiscuous because Moreover, although Anthes et al. [37] found that copula- the fertilization success of their male function is ex- tion duration was correlated with sperm competition pected to increase with an increasing number of matings intensity in a simultaneously hermaphroditic sea slug, [23], but see [24], which leads to high remating rates Lange et al. [38] revealed that copulation duration was and sperm competition among several individuals. In not a reliable proxy for sperm transfer number in that hermaphrodites, therefore, the strategy of ejaculation species. Therefore, whether the pattern of strategic should be determined by the sperm priority pattern ac- ejaculation in simultaneous hermaphrodites is in line cording to the theoretical models proposed by Engqvist with the theories of sperm competition games remains & Reinhold [22]. Contrary to the theoretical prediction, an unclear, controversial issue. however, the simultaneously hermaphroditic earthworm In this study, we examined the effects of the mating Eisenia andrei, in which the fertilization pattern is history of the mate (virgin or non-virgin) and other po- thought to be random, exhibits greater ejaculate expend- tential factors (quality and sperm transfer of mates) on iture during copulation with a non-virgin mate than that ejaculate size in the simultaneously hermaphroditic land with a virgin mate [25]. snail Euhadra quaesita. In contrast to the reproductive Other factors have been proposed as important for the traits of A. arbustorum, those of E. quaesita have been allocation of the costly ejaculate of males. Female quality suggested to be influenced by sexual selection [39]. In (e.g., fecundity) is thought to influence ejaculate expend- Cornu aspersum, it has been determined that allosperm iture [26-28]. Moreover, because of their unique repro- near the internal wall of the allosperm storage organ of a ductive systems, another potential factor affects ejaculate mate can survive longer and may have a better chance size in simultaneous hermaphrodites. When there is a of successful fertilisation [40]. Therefore, allosperm from difference in the expected fitness gain between sex roles, the first donor would reach this limited hospitable individuals
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