Eunuch Supremacy: Evolution of Post-Mating Spider Emasculation
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Behav Ecol Sociobiol (2015) 69:117–126 DOI 10.1007/s00265-014-1824-6 ORIGINAL PAPER Eunuch supremacy: evolution of post-mating spider emasculation Matjaž Kuntner & Urška Pristovšek & Ren-Chung Cheng & Daiqin Li & Shichang Zhang & I-Min Tso & Chen-Pan Liao & Jeremy A. Miller & Simona Kralj-Fišer Received: 11 April 2014 /Revised: 30 September 2014 /Accepted: 1 October 2014 /Published online: 15 October 2014 # Springer-Verlag Berlin Heidelberg 2014 Abstract Emasculation—males becoming effectively sterile via genital plugging and spontaneous death. Emasculation by self-removing their genitals—haslongbeenconsidereda during mating also results in genital plugs, but half eunuchs peculiar evolutionary phenomenon with unknown function, have another chance to mate. So far, the behavior of those taxonomically restricted to few spiders and flies. In spiders, males that become eunuchs post-mating by self-removing emasculation results in half or full eunuchs when males sever disfigured palps has not been investigated empirically. We test one or both sperm transferring organs, palps. Three types of the mechanism and adaptive significance of post-mating emasculation, pre-maturation, mating, and post-mating are emasculation in coin spiders (Herennia multipuncta) and use known in spiders, all having evolved multiple times. Males phylogenetic reconstruction to understand its evolutionary practicing pre-maturation emasculation sever one of their history. Our laboratory assays corroborate three hypotheses palps while still immature, then engage in strict monogyny related to mate monopolization: (1) The plugging hypothe- sis—predicting genital plugs to prevent female remating; (2) The better-fighter hypothesis—predicting enhanced eunuch Communicated by N. Wedell aggressiveness toward rivals; and (3) The gloves-off hypoth- Matjaž Kuntner, Urška Pristovšek, and Simona Kralj-Fišer contributed esis—predicting increased eunuch endurance. The support for equally to this work. these hypotheses in spiders practicing emasculation during M. Kuntner (*) : U. Pristovšek : R.<C. Cheng : S. Kralj-Fišer and after mating reinforces recent phylogenetic interpretations Institute of Biology, Scientific Research Centre, Slovenian Academy of these two emasculation types being evolutionarily linked in of Sciences and Arts, Novi trg 2, 1000, Ljubljana, Slovenia the family Nephilidae. We weigh the evidence in support of e-mail: [email protected] three different, but equally parsimonious scenarios of nephilid M. Kuntner : D. Li emasculation evolution. We conclude that emasculation is an Centre for Behavioural Ecology and Evolution, College of Life adaptive, sexually selected trait that calls for further compar- Sciences, Hubei University, Wuhan, Hubei, China ative and experimental research. M. Kuntner National Museum of Natural History, Smithsonian Institution, Keywords Terminal investment . Sperm competition . Washington, DC, USA Genital plugs . Sexual conflict . Monogyny . Polyandry D. Li : S. Zhang Department of Biological Sciences, National University of Singapore, Singapore, Singapore Introduction < : < I. M. Tso C. P. Liao Emasculation—male genital self-removal in spiders Department of Life Science, Tunghai University, Taichung, Taiwan (Robinson and Robinson 1980) and dipterans (Downes J. A. Miller 1978)—has long been considered an obscure evolutionary Naturalis Biodiversity Center, Leiden, The Netherlands phenomenon. Eunuch spiders have been almost completely neglected, being known only in a few nephilids (genera S. Kralj-Fišer University of Primorska, Faculty of Mathematics, Natural Sciences Herennia, Nephilengys, Nephilingis), araneids (Caerostris, and Information Technologies, Koper, Slovenia Argiope), and in a tiny fraction of theridiids (genera Tidarren 118 Behav Ecol Sociobiol (2015) 69:117–126 and Echinotheridion) (Robinson and Robinson 1980;Kuntner 2012), and Latrodectus (Snow et al. 2006) and of emascula- et al. 2014). Emasculation rendering males sterile imposes tion in Tidarren (Knoflach and van Harten 2001; Ramos et al. high costs on their further mating opportunities and thus future 2004) and in two nephilid species, the SE Asian Nephilengys reproductive output. Relatively recently, however, studies in- malabarensis and the Malagasy Nephilingis livida (Kralj- vestigating reproductive strategies such as sperm competition, Fišer et al. 2011; Kralj-Fišer and Kuntner 2012; Lee et al. genital damage and plugging, male terminal investment, sex- 2012;Lietal.2012). However, mating plugs consisting of ual cannibalism, female polyandry, male monogyny, and sex- male spider genital parts are not always fully effective in ual conflict triggered a shift in focus among researchers of preventing female remating (Schneider and Elgar 2001; spider biology (Andrade 1996; Elgar and Fahey 1996; Schneider and Elgar 2002; Kralj-Fišer et al. 2011;Fromhage Schneider and Lubin 1998; Schneider et al. 2000;Elgar and Schneider 2012) and thus the plugging spider male may et al. 2003a, b; Andrade and Kasumovic 2005; Fromhage increase his monopolization of the female through post- and Schneider 2006; Miller 2007; Fromhage et al. 2008; copulatory mate guarding (Robinson and Robinson 1980; Kuntner et al. 2009b, c; Uhl et al. 2010;Fromhageand Fromhage and Schneider 2006; Kralj-Fišer et al. 2011). In Schneider 2012; Herberstein et al. 2012). These studies solid- accordance with the “asset protection principle” (Clark 1994), ified the view that most sexual strategies, including those that predicting that a male should adjust his behavior to its future relate to genital and body sacrifice pose certain fitness advan- residual reproductive potential, the better-fighter hypothesis tages such as securing paternity and monopolizing partners predicts escalated eunuch aggressiveness toward rival males (Austad 1984; Andrade 1996; Kuntner et al. 2009c; Uhl and with intact genitals (Kralj-Fišer et al. 2011). A male with Busch 2009; Welke and Schneider 2010). damaged genitalia and thus low future residual reproductive Male insects and spiders sometimes damage their genitals potential is expected to be more aggressive and to take more during copulation (Monnin and Peeters 1998; Fromhage and risk in male–male contests than a male with intact genitalia Schneider 2006;Snowetal.2006; Nessler et al. 2007, 2009; and high future residual reproductive potential (Fromhage and Uhl et al. 2010; Ghione and Costa 2011; Herberstein et al. Schneider 2005). 2012). In spiders, however, genital mutilation ranges from The remaining hypotheses explaining the adaptiveness simple embolic breakage (i.e., breakage of the genital tip) to of emasculation are specific to eunuchs (those spiders practic- emasculation, where males break off the entire genital or- ing emasculation) and do not apply to other spiders practicing gan(s). Kuntner et al. (2014) established a distinction between lesser genital damage. In this case, the possession of the “lesser genital damage,” a widespread practice where male disproportionally heavy palp should be more costly than its spiders break only a distal part of the embolus (i.e., the removal. In fact, the proximate cause of eunuch superior terminal portion of the male palp—the intrommitent organ in fighting abilities has been explained by the gloves-off spiders) (Uhl et al. 2010), and “(full) emasculation” (hence- hypothesis, which predicts the male endurance and stamina forth emasculation) resulting in palpless eunuchs (Robinson to increase with each severance of the heavy palp (Ramos and Robinson 1980; Kuntner 2005, 2007). Beyond the obvi- et al. 2004; Kuntner et al. 2009c; Lee et al. 2012). ous anatomical distinction (Kuntner et al. 2014), the former Accordingly, Tidarren males remove one of their palps before does not necessarily result in functional sterility (Snow et al. mating rendering them more agile and thereby likely allowing 2006), while the latter does (Kuntner et al. 2014). In this paper, them to win contests against rival males (Ramos et al. 2004). we follow this distinction and only discuss genital damage if it In an untested hypothesis, Kuntner (2005) suggested that relates to emasculation. males chew off their damaged palps in order to avoid Various hypotheses have been proposed to explain male haemolymph leakage. Finally, it has been reported that the emasculating behaviors (reviewed in Kuntner et al. 2014). The entire male genital severance resulting in whole palp plug plugging hypothesis predicts that the broken male genital parts allows for continuous sperm transfer into female spermathecae lodged in female copulatory organs must effectively prevent after the eunuch male has been “detached” from copula (Li female remating, thereby reducing sperm competition and et al. 2012). This remote-copulation hypothesis predicts con- increasing paternity share (Kuntner 2005; Kuntner et al. tinuous sperm transfer into female spermatheca after palpal 2009c; Uhl et al. 2010). However, as genital plugs are a removal (Kralj-Fišer et al. 2011;Lietal.2012). Recent empir- widespread phenomenon in spiders, this hypothesis may ap- ical research has demonstrated adaptive function of emascula- ply to any genital damage and is not strictly restricted to tion in the South-East Asian N. malabarensis, with support for emasculating eunuchs. In general support of the plugging the above hypotheses (haemolymph leakage not tested), and in hypothesis, numerous studies demonstrate paternity benefits part in the Malagasy N. livida, with support for the plugging of plugs made of male genital parts. For