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Plastic Expression of Seminal Fluid Protein Genes in a Simultaneously Behavioral The official journal of the Ecology ISBE International Society for Behavioral Ecology Behavioral Ecology (2019), 30(4), 904–913. doi:10.1093/beheco/arz027 Original Article Plastic expression of seminal fluid protein genes in a simultaneously Downloaded from https://academic.oup.com/beheco/article/30/4/904/5376642 by guest on 02 October 2021 hermaphroditic snail Yumi Nakadera , Athina Giannakara, and Steven A. Ramm Evolutionary Biology Department, Bielefeld University, Germany Morgenbreede 45, 33615 Bielefeld, Germany Received 5 September 2018; revised 30 January 2019; editorial decision 31 January 2019; accepted 8 February 2019; Advance Access publication 18 March 2019. Seminal fluid proteins(SFPs) are components of the ejaculate that often induce drastic changes in female physiology, such as reduc- ing remating rate or shortening longevity. There is compelling evidence that these functions make SFPs a determinant of male repro- ductive success, and some evidence that males can strategically invest in their differential production. However, SFP-mediated effects have received relatively little attention in simultaneous hermaphrodites, that is, organisms that are male and female at the same time. Since this reproductive mode is widespread in animals and their SFPs have unique functions compared to separate-sexed species, examining SFPs of hermaphrodites would help generalize our understanding of the impact of SFPs. We therefore examined if individu- als strategically alter seminal fluid production in response to mate availability and sperm competition in the freshwater snailLymnaea stagnalis. We exposed snails to different social group sizes, and measured the expression of 6 SFP genes. We found that the snails plastically elevated SFP expression in the presence of at least 1 mating partner. Specifically, paired snails showed higher SFP expres- sion than isolated snails, whereas SFP expression of snails exposed to sperm competition, that is, in a larger group size, was equivalent to that of paired snails. Furthermore, 5 out of 6 SFP genes we examined responded to mate availability in a very similar way, implying that overall seminal fluid production increases when the snails have mating opportunities. The plastic expression of seminal fluid depending on mate availability supports that SFPs play important roles in post-copulatory processes in this hermaphroditic species. Key words: ejaculate investment, gene expression, mate availability, seminal fluid, sexual selection, sperm competition. INTRODUCTION plastically adjust their investment in SFPs, for example, depending Variation in reproductive success arises not just from variation in on the presence of rivals or on the females’ mating history (Wigby mating success but also from the differential fertilizing ability of et al. 2009; Fedorka et al. 2011; Sirot et al. 2011; Ramm et al. transferred ejaculates (Parker 1970). Recent studies have revealed 2015; Simmons and Lovegrove 2017; Sloan et al. 2018). Such plas- that non-sperm components in the ejaculate, that is, seminal fluid tic investment in SFPs suggests that these proteins play important proteins (SFPs), play significant roles in determining male repro- roles in determining male reproductive success in post-copulatory ductive success. For example, SFPs induce essential responses sexual selection. in females for reproduction, such as ovulation or sperm trans- To date, most studies of seminal fluid have been conducted in port (Chapman 2001; Poiani 2006; Avila et al. 2011). Thus, their species with separate sexes, and the impact of SFPs has received positive effects on reproduction have also been emphasized in far less attention in simultaneous hermaphrodites, that is, organ- assisted reproductive technology (McGraw et al. 2015; Samanta isms that possess male and female functions within their body at et al. 2018). Moreover, SFPs have sometimes been shown to trig- the same time (hereafter called hermaphrodites). Hermaphroditism ger sexually antagonistic effects on females, seemingly exploiting is a widespread reproductive mode across animals and is found, for them for the male’s own benefits (e.g., shortening females’ life span: example, in snails, slugs, barnacles, flatworms, and fish (Jarne and Chapman et al. 1995, reviewed in Sirot et al. 2015). To further Auld 2006). Recent studies have demonstrated that hermaphrodites underline the significance of seminal fluid, males in several taxa are indeed under sexual selection (e.g., Anthes et al. 2010; Hoffer et al 2017). In particular, several studies in hermaphroditic snails have revealed the presence of multiple paternity in field popula- tions, suggesting that sperm competition occurs commonly (e.g., Address correspondence to Y. Nakadera. E-mail: yumi.nakadera@uni- bielefeld.de. Janssen and Baur 2015; Bürkli and Jokela 2017; Nakadera et al. 2017). © The Author(s) 2019. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals. [email protected] Nakadera et al. • Plastic seminal fluid expression in hermaphrodites 905 These observations imply that SFPs in hermaphrodites could play Here we examined whether L. stagnalis alters SFP production important roles in sperm competition, just as they do in separate- in different social group sizes. We aimed to investigate the devel- sexed species (e.g., Clark et al. 1995; Chapman et al. 2003; Zhang opmental plasticity of SFP expression, so we exposed the snails to et al. 2013), since many of the mechanisms through which male different social group sizes continually prior to and after sexual mat- reproductive success can be maximized will be common to both uration. At the end of the experiment, we measured the abundance reproductive modes. Moreover, a recent study demonstrated that of mRNA from 6 SFP genes in the prostate glands of adult snails SFPs of hermaphrodites can have unique functions compared to using quantitative polymerase chain reaction (qPCR). This measure separate-sexed species. That is, the receipt of specific SFPs reduces serves as our estimate of SFP production. Since transcription is a the investment of male function in mating partners (Nakadera et al. key machinery of protein synthesis, we would expect that the abun- 2014), which may be one instance of an adaptive strategy in her- dance of mRNA broadly correlates with the abundance of protein maphrodites of targeting the sex allocation of a mating partner produced (e.g., Lovrić 2011; Bonilla et al. 2015) and so we assume (Charnov 1979; Schärer and Ramm 2016). Therefore, examining here that our measure of gene expression results in downstream SFPs in hermaphrodites could contribute to generalizing the cur- differences in SFP production. In our first experiment (Exp. 1), we Downloaded from https://academic.oup.com/beheco/article/30/4/904/5376642 by guest on 02 October 2021 rent insights about the functional and evolutionary significance of tested whether the snails exhibit higher SFP gene expression and seminal fluid to a wider range of animals and reproductive modes. thus presumably produce more seminal fluid when a mate is avail- As one aspect of investigating the role of SFPs in hermaphro- able (isolated vs. paired), as well as if isolated snails adjust SFP dites, we here focus on plasticity in SFP production under sperm gene expression within 24 h of being exposed to a potential mate competition. Based on the general framework of sperm competi- (isolated vs. iso-paired, see Material and Methods). The latter com- tion theory, males are expected to increase ejaculate production parison would thus inform us about the time window to adjust SFP when they are exposed to high sperm competition risk or inten- production in this species. In our second experiment (Exp. 2), we sity (e.g., Parker and Ball 2005). Our predictions in this study are tested if SFP production differs across varying social group sizes based on general sperm competition theory, rather than predictions (isolated vs. paired vs. grouped), to examine developmental plastic- concerning SFP allocation (e.g., Cameron et al. 2007; Alonzo and ity in seminal fluid production at different sperm competition levels. Pizzari 2010; Dhole and Servedio 2014), since the link between By comparing the isolated to the other 2 treatments (i.e., paired and such allocation decisions and measures of production is uncertain. grouped), we tested if the presence or absence of a mate (hereafter Several empirical studies on SFP production provide evidence for “mate availability”) affects SFP gene expression. The comparison plastic investment according to different sperm competition lev- between paired and grouped snails then allowed us to further test els (Fedorka et al. 2011; Mohorianu et al. 2017; Simmons and if the presence or absence of sperm competition alters SFP gene Lovegrove 2017; Patlar et al. forthcoming; Sloan et al. 2018; Ramm expression. et al. forthcoming). For example, a study on house mouse explicitly Note that, although the paired treatment enforced monogamy showed that males increase SFP production when they perceive a and so sperm competition is strictly absent, it is possible that this risk of sperm competition, and
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