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Genotype-By-Environment Interactions for Seminal Fluid Expression And bioRxiv preprint doi: https://doi.org/10.1101/727685; this version posted August 6, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Genotype-by-environment interactions for seminal fluid expression and 2 sperm competitive ability 3 4 Bahar Patlar1,2, Steven A. Ramm1 5 1 Evolutionary Biology, Bielefeld University, Morgenbreede 45, 33615 Bielefeld, Germany 6 2 Current address: 515 Portage Ave R3B 2E9, Department of Biology, University of Winnipeg, 7 MB, Canada 8 9 Corresponding authors: 10 [email protected] (BP) +1 204 990 6225 11 [email protected] (SAR) +49 521 106 2719 12 13 bioRxiv preprint doi: https://doi.org/10.1101/727685; this version posted August 6, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 14 Abstract 15 Sperm competition commonly occurs whenever females mate multiply, leading to variation in 16 male paternity success. This can be due to variation in the various traits that might affect sperm 17 competitive ability, which itself depends on both genetic and environmental factors, as well as 18 on genotype-by-environment interactions (GEI). Seminal fluid is a major component of the 19 male ejaculate that is often expected to mediate sperm competition, where different genotypes 20 can differ in their seminal fluid expression as a response to different level of sperm competition 21 (i.e., exhibit GEI). We therefore here focussed on testing for GEI in expression of two recently 22 identified seminal fluid transcripts, suckless-1 and suckless-2, which potentially modulate 23 sperm competitive ability in the simultaneously hermaphroditic flatworm Macrostomum 24 lignano via their effects on manipulating post-mating partner behaviour and ultimately the fate 25 of transferred ejaculates. In addition, we sought to test for GEI in sperm competitive ability, to 26 investigate the relationship between natural variation in the expression of these seminal fluid 27 transcripts generated through GEI and relative paternity success. To do so, we manipulated 28 social group size, which has been shown to successfully alter sperm competition level in M. 29 lignano, in a set of inbred lines (genotypes) and then measured both the expression level of 30 suckless-1 and suckless-2 in focal worms together with their relative paternity success in a 31 standardised sperm competition (P1 & P2) assay. We found GEI for the expression level of 32 suckless-1 and suckless-2, as well as for sperm competitive ability. Moreover, we found a 33 positive relation between the expression of suckless-1 and paternity success. This suggests that 34 natural variation in the expression of this seminal fluid transcript indeed can influence sperm 35 competition outcomes in M. lignano. 36 Keywords: Gene/transcript expression, Macrostomum lignano, Post-mating sexual selection, 37 Simultaneous hermaphrodites, Social group size, Sperm competition bioRxiv preprint doi: https://doi.org/10.1101/727685; this version posted August 6, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 38 Introduction 39 Sperm competition, that is the competition between the ejaculates of two or more males for the 40 fertilization of a given set of ova (Parker, 1970), and cryptic female choice, in which females 41 influence the outcome of sperm competition (Eberhard, 1996), are important evolutionary 42 forces across a diverse range of taxa in which females mate multiply. Variation in paternity 43 success is therefore determined by many factors affecting sperm competitive ability of the 44 ejaculate (Parker, 1970; Lewis & Austad, 1990; Radwan, 1996; Birkhead & Møller, 1998; Gage 45 & Morrow, 2003; Snook, 2005; Simmons & Parker, 2006; Pizzari & Parker, 2009). Numerous 46 adaptations related to the amount and quality of sperm such as sperm number, size, velocity, 47 mobility, and storage capacity affect relative paternity success under sperm competition 48 (Birkhead & Møller, 1998; Wedell et al., 2002; Snook, 2005; Bjork & Pitnick, 2006; Pitnick et 49 al., 2009; Pizzari & Parker, 2009; Parker & Pizzari, 2010; Godwin et al., 2017). Alongside 50 sperm, males typically also transfer large number of seminal fluid proteins/peptides (SFPs) 51 during mating (reviewed by Poiani, 2006; Avila et al., 2011; Hopkins et al., 2017) and these 52 too are theoretically expected to be strongly shaped by sperm competition, favouring the 53 evolution of SFP functions that confer a male fitness benefit through increased competitive 54 fertilization success (Cameron et al., 2007; Dhole & Servedio, 2014; Dapper & Wade, 2016). 55 SFPs can either decrease the risk of sperm competition, for example by preventing female re- 56 mating, or increase the chance of sperm to fertilize eggs by serving as offensive or defensive 57 tools against rival sperm in female genital tracts. Their well-known functions decreasing sperm 58 competition risk include manipulation of female propensity to re-mate and/or attractiveness 59 (e.g. Chapman et al., 2003; LaFlamme, Ravi Ram, & Wolfner, 2012; Lung & Wolfner, 2001) 60 and blocking her genital tract by forming plugs to prevent additional successful copulations, as 61 commonly occurs in many taxa (Barker, 1994; Jia et al., 2002; Mangels et al., 2016; Sutter & bioRxiv preprint doi: https://doi.org/10.1101/727685; this version posted August 6, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 62 Lindholm, 2016). On the other hand, the role of SFPs in sperm displacement has been reported 63 for example in the fruit fly Drosophila melanogaster (Harshman & Prout, 1994) and in the seed 64 beetle Callosobruchus maculatus (Yamane et al., 2015), in which seminal fluid of the second 65 male to mate with a female causes a reduction in the number of sperm from the previous mating 66 and correlations have been found between allelic variation at SFP loci and levels of sperm 67 displacement, as well as resisting ability to being displaced (Clark et al., 1995; Fiumera et al., 68 2005). Moreover, in polyandrous ants and bees, seminal fluid enhances the survival of own 69 sperm, while preferentially eliminating sperm of rival males (Den Boer et al., 2008, 2010). 70 So far, the literature on varying functions of seminal fluid modulating sperm competitive ability 71 focuses mainly on separate-sexed organisms, but similar functions could also have evolved in 72 hermaphrodites. Indeed, post-mating sexual selection has been suggested as a major 73 evolutionary force shaping reproductive traits especially in simultaneous hermaphrodites (i.e. 74 organisms with both male and female reproductive functions) (Charnov, 1979; Charnov & City, 75 1996; Michiels, 1998; Schärer et al., 2015; Marie-Orleach et al., 2016). Because frequent 76 multiple mating is common in many reciprocally copulating simultaneous hermaphrodites, and 77 individuals are capable of storing sperm from multiple ejaculate donors, there is an opportunity 78 for selection to operate on differential fertilization success and resulting sperm competition 79 among ejaculate donors (Baur, 1998; Michiels, 1998; Koene, 2005; Leonard, 2006; Anthes, 80 2010; Domínguez & Velando, 2013). 81 Our study organism, the flatworm Macrostomum lignano, is a reciprocally copulating 82 simultaneous hermaphrodite in which self-fertilization does not occur (Schärer & Ladurner, 83 2003; Ladurner et al., 2005b), and is an emerging model organism to study ejaculate adaptations 84 driven by sperm competition and sexual conflict (e.g. Janicke & Schärer, 2009a; Schärer et al., 85 2011; Marie-Orleach et al., 2016; Patlar et al., 2019, submitted). M. lignano can adjust its sex 86 allocation, that is the strategic investment to produce eggs and sperm, in response to sperm bioRxiv preprint doi: https://doi.org/10.1101/727685; this version posted August 6, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 87 competition level (e.g. Schärer & Ladurner, 2003; Janicke & Schärer, 2009a, 2010; Ramm et 88 al., 2019). It has been clearly shown that in larger social groups, where sperm competition 89 intensity is high compared to small groups, worms invest more in their male sex function, as 90 captured by traits such as testis size, testicular activity (Schärer et al., 2004b), sperm production 91 rate (Schärer & Vizoso, 2007) and spermatogenesis speed (Giannakara et al., 2016). Moreover, 92 it has been established that increasing investment in testis size and sperm production increases 93 relative paternity success (Sekii et al., 2013; Vellnow et al., 2018). M. lignano also exhibits 94 high mating rates, potentially due to the fact that individuals are motivated to donate sperm 95 more than to receive it, just as in many other simultaneous hermaphrodites (Michiels, 1998; 96 Schärer et al., 2015; Greeff & Michiels, 2017). However, the high motivation to mate more, in 97 general, also increases the risk of receiving (excess) sperm and/or seminal fluid, and 98 concomitantly increases risks of polyspermy, sexually transmitted pathogens and/or receipt of 99 manipulative SFPs (Charnov, 1979;
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