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Multiple Paternity and Postcopulatory Sexual Selection in a Hermaphrodite: What Influences Sperm Precedence in the Garden Snail

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Multiple Paternity and Postcopulatory Sexual Selection in a Hermaphrodite: What Influences Sperm Precedence in the Garden Snail View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Serveur académique lausannois Molecular Ecology (2005) 14, 805–812 doi: 10.1111/j.1365-294X.2005.02449.x MultipleBlackwell Publishing, Ltd. paternity and postcopulatory sexual selection in a hermaphrodite: what influences sperm precedence in the garden snail Helix aspersa? GUILLAUME EVANNO,* LUC MADEC† and JEAN-FRANÇOIS ARNAUD‡ *Département d’Ecologie et Evolution, Bâtiment de Biologie, Université de Lausanne, CH-1015 Lausanne, Switzerland, †UMR CNRS 6553, Université de Rennes 1, Campus de Beaulieu, Avenue du Général, Leclerc, 35042 Rennes cedex, France, ‡UMR CNRS 8016, Laboratoire de Génétique et Evolution des Populations Végétales, Bât. SN2, Université de Lille 1, 59655 Villeneuve d’Ascq cedex, France Abstract Sperm competition has been studied in many gonochoric animals but little is known about its occurrence in simultaneous hermaphrodites, especially in land snails. The reproductive behaviour of the land snail Helix aspersa involves several features, like multiple mating, long-term sperm storage and dart-shooting behaviour, which may promote sperm competition. Cryptic female choice may also occur through a spermatheca subdivided into tubules, which potentially allows compartmentalized sperm storage of successive mates. In order to determine the outcome of postcopulatory sexual selection in this species, we designed a cross-breeding experiment where a recipient (‘female’) mated with two sperm donors (‘males’). Mates came from either the same population as the recipient or from a distinct one. To test for the influence a recipient can have on the paternity of its offspring, we excluded the effects of dart shooting by using only virgin snails as sperm donors because they do not shoot any dart before their first copulation. We measured the effects of size of mates as well as time to first and second mating on second mate sperm precedence (P2; established using microsatellite markers). Multiple paternity was detected in 62.5% of clutches and overall there was first-mate sperm precedence with a mean P2 of 0.24. Generalized linear modelling revealed that the best predictors of paternity were the time between matings and the time before first mating. Overall, both first and second mates that copulated quickly got greater parentage, which may suggest that postcopulatory events influence patterns of sperm precedence in the garden snail. Keywords: cryptic female choice, Helix aspersa, hermaphroditic snail, P2, sperm competition Received 5 September 2004; revision received 12 November 2004; accepted 29 November 2004 sexual selection (Birkhead & Pizzari 2002). Indeed, in Introduction species where multiple inseminations occur, there will be Sexual selection is the evolutionary process that favours competition among the sperm provided by different fathers. selection for traits associated with mating success and By definition, sperm competition is the competition partner choice. Mating success often trades off with survival between the sperm of different males to fertilize the ova of and sexual selection accounts for many of the attractive a female (Parker 1970). Females, on their part can potentially ornaments of various plants and animals (Andersson 1994). choose sperm from different donors if for instance the Sexual selection is generally viewed as a process operating sperm carry information on male quality. Such a cryptic on the diploid stage of the life cycle. However, it has been female choice designates the influence a female can have documented that females of several species actively seek on fertilization of her eggs after intromission or sperm multiple copulation partners, leading to postcopulatory transfer. This choice is exercised through molecular and physiological mechanisms and/or morphological structures Correspondence: Guillaume Evanno, Fax: + 41 21 692 42 65; E- in the female reproductive tract (Eberhard 1996). Overall, mail: [email protected] recent studies suggest that relative reproductive rates of © 2005 Blackwell Publishing Ltd 806 G. EVANNO, L. MADEC and J.-F. ARNAUD males and females, sperm competition, and quality variation H. aspersa. To address this issue, a cross-breeding experiment among mates affect the strength of sexual selection was designed with the following scheme: a group of recipi- (Birkhead & Pizzari 2002). ents from one population successively mates with two Simultaneous hermaphrodites can also experience sperm donors either belonging to the same population as sexual selection (Charnov 1979; Michiels 1998). However, the recipient or to a different one. The resulting pattern of postcopulatory sexual selection has been rarely investi- sperm precedence could highlight a higher siring success gated in these organisms: multiple mating appears of allopatric or sympatric mates (Chapman et al. 2003). If widespread but evidence of mate choice is rare and usually partial premating isolation occurs, sympatric mates should consists of assortative mating. In the particular case of outcompete allopatric ones. To avoid this effect, we sam- studied helicid land snails that mate multiply (for instance pled snails from northwestern Europe because H. aspersa three times per year for Helix aspersa, Fearnley 1993), mating populations do not display any incompatibility because of seems generally random with respect to size and related- marked differences in distal genitalia in this geographical ness (Baur 1992; Baur & Baur 1997). This may be because area (Madec & Guiller 1994). According to the theory of (i) characters involved in mate choice are difficult to detect, sexual conflict, allopatric mates may sire more offspring or (ii) sexual selection acts essentially during or after co- because local snails would be supposed to have only pulation. Nonetheless, the long-term sperm-storage ability evolved resistance to sympatric mates (Leonard 1992; Rice characteristic of land snails (Murray 1964; Duncan 1975) & Holland 1997; Parker & Partridge 1998; Landolfa 2002). may increase the potential for postcopulatory sexual The limited dispersal capabilities of snails often lead to selection. The dart-shooting behaviour exhibited by a strong population isolation that can result in matings some helicid species, including the land snail H. aspersa between relatives (Arnaud et al. 1999, 2001). Such matings (Gastropoda: Helicidae), may also promote some forms by proximity are likely to increase inbreeding and its of postcopulatory sexual selection (Koene & Chase potential deleterious effects (Chen 1993). Consequently, 1998). Just before copulation, snails attempt to push a from a female perspective, favouring migrant individuals calcareous dart into their partners, which eventually should be advantageous. enhances the number of sperm stored by the recipient In H. aspersa, potential mechanisms involved in post- through a temporary modification of its female genitalia copulatory sexual selection include dart-shooting behaviour, caused by chemicals in the mucus covering the dart sperm digestion ability and/or cryptic female choice. The (Koene & Chase 1998; Rogers & Chase 2001, 2002). The donor role of dart-shooting behaviour has been widely investigated thus avoids the digestion of most of its sperm in the bursa and many studies have shown its influence in postcopula- copulatrix (sperm-digesting organ) of the recipient, and tory sexual selection (Koene & Chase 1998; Landolfa et al. therefore increases its reproductive success (Landolfa et al. 2001; Rogers & Chase 2001, 2002). However, little is known 2001). about the influence of a recipient on the paternity of Land snails are also especially suitable organisms to test its offspring through allosperm digestion and cryptic for postcopulatory sexual selection because cryptic female female choice. For this reason, we focused on the female choice could occur owing to the presence of a spermatheca perspective and excluded the effects of dart-shooting subdivided into several tubules, which possibly allow for behaviour by using only virgin snails that are unable to separate storage of sperm from successive mates (Haase & shoot darts before their first copulation. Baur 1995; Baminger & Haase 1999). The ability to exercise cryptic female choice theoretically increases with the number Materials and methods of sperm stores (Hellriegel & Ward 1998), therefore this phenomenon is potentially important in H. aspersa whose Study populations and their maintenance spermatheca can have up to 13 tubules (mean ± SD = 7.2 ± 2.4; G. Evanno and L. Madec, unpublished). In this species, Three French populations were sampled for mating trials: cryptic female choice might be based on (i) size of mate, one group of recipients (‘females’) and two others used larger individuals displaying heritable differences in sev- only as sperm donors (‘males’) in the mating experiments. eral fitness related traits, e.g. size and number of progeny All sampled snails were immature (less than 1 year) and (Madec et al. 1998, 2000); or (ii) relatedness, because land thus virgin prior to mating experiments. Therefore, dart- snails exhibit poor dispersal capacities so that maximizing shooting effects were excluded because virgin snails do not paternity of migrant individuals establishing in a pre- shoot darts during courtship prior to their first copulation existing colony may counteract deleterious effects of (Chung 1986). inbreeding in local populations (see Fearnley 1993; Recipients were collected in a snail farm from Rennes
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