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Stegonotus Cucullatus, Colubridae) Animal Behaviour 77 (2009) 177–182 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/yanbe Sexual selection favours large body size in males of a tropical snake (Stegonotus cucullatus, Colubridae) Sylvain Dubey a,*, Gregory P. Brown a, Thomas Madsen b,1, Richard Shine a a School of Biological Sciences, University of Sydney b School of Biological Sciences, University of Wollongong article info Information on the phenotypic correlates of male reproductive success can provide important insights Article history: into the operation of sexual selection, and the nature of evolutionary forces on phenotypic traits such as Received 19 June 2008 male body size. We combined results from a long-term mark–recapture field study with genetic analyses Initial acceptance 9 July 2008 for identifying paternity of offspring to quantify male reproductive success in a colubrid snake species Final acceptance 30 September 2008 from tropical Australia. Because previous work has shown that male slatey-grey snakes, Stegonotus Published online 21 November 2008 cucullatus, attain larger body sizes than do conspecific females, we predicted that larger males would MS. number: 08-00403R have higher reproductive success. Our paternity assignments of 219 offspring (24 clutches) supported this prediction: larger males fathered more offspring, not because they obtained more matings, but Keywords: because they fathered a higher proportion of offspring within the clutches to which they did contribute. paternity Multiple paternity was common (mean of 2.3 fathers per clutch, range 1–5). Our results demonstrate the reproductive success utility of molecular approaches to clarify mating systems in field populations of snakes, and suggest that reptile Serpentes the evolution of extreme male-biased sexual size dimorphism in this species is attributable to enhanced sexual dimorphism reproductive success afforded by larger body size in males. slatey-grey snake Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Stegenotus cucullaus Variation among individuals in reproductive success is a funda- (e.g. with selection on longevity of spermatozoa: Uller & Olsson mental prerequisite for selection and adaptation. Causal effects of 2008). In addition, the pressures for mate acquisition have resulted phenotypic variation on individual reproductive success thus in intense male–male competition for females and, in many species, provide a critical basis for evolutionary interpretations of inter- female-defence or resource-defence polygyny (e.g. Stamps 1977; specific and intraspecific diversity in phenotypic traits. The central Martins 1994; Shine 2003). importance of individual reproductive success for selection and the Because a male’s body size may often influence its ability to immense diversity of factors that influence the relationship defeat rival males and/or to obtain copulations with females, male- between phenotypic traits and reproductive success have spawned biased sexual size dimorphism might be expected to evolve in taxa a major research field in the analysis of mating systems (e.g. Carson where male mating success is strongly enhanced by larger body 2003; Peterson & Husak 2006; Ramm et al. 2008). size (e.g. in lizards and snakes: Wikelski & Romero 2003; Fearn Sexual selection theory predicts strong selection for traits that et al. 2005). The mechanism linking body size to male reproductive increase reproductive success (in both sexes). In males, mate success may be straightforward: for example, larger males are acquisition is often the most severe limitation on reproductive presumably stronger, so are more likely to win combat bouts with success and, consequently, male strategies to obtain matings with smaller males, and may be better able to obtain matings via coer- more than one female are widespread (e.g. Jehl & Murray 1986; cion of females or via female choice (Shine et al. 2005). In addition, Birkhead & Møller 1998; Say et al. 2003; Uller & Olsson 2008). In larger males may have access to a larger subset of the reproductive reptiles, male reproductive success is mostly driven by the inter- females within the population, and consequently can select females action between (1) rates of copulation, (2) cryptic female choice likely to produce more (or more viable) progeny (e.g. females that and (3) sperm competition, which could occur via sperm storage are larger or are in better physical condition, and thus produce larger litters: e.g. Shine et al. 2001). In addition to such advantages, larger males may also have an * Correspondence: S. Dubey, School of Biological Sciences, University of Sydney, enhanced reproductive success via sperm competition, by pos- Sydney, NSW 2006, Australia. sessing larger ejaculates. Data to test this idea are lacking for many E-mail address: [email protected] (S. Dubey). 1 T. Madsen is at the School of Biological Sciences, University of Wollongong, groups of animals, including snakes. Nevertheless, the high inci- Wollongong, NSW 2522, Australia. dence of multiple paternity within clutches of many reptile species, 0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.09.037 178 S. Dubey et al. / Animal Behaviour 77 (2009) 177–182 coupled with the prevalence of multiple mating in female reptiles active snakes. The animals were captured by hand, and returned to (reviewed in Uller & Olsson 2008), suggests that strong selection to the field laboratory for processing (measurement, individual maximize male reproductive success within multiply sired clutches marking by scale clipping, removal of tissue sample) before release should influence traits that enhance success in sperm competition. (typically 1 or 2 days postcapture) at their original capture site. Despite increasing scientific interest in snake ecology and Gravid females were detectable by abdominal palpation, and behaviour (Shine & Bonnet 2000), most studies on this lineage are maintained in captivity until they laid their eggs (median interval based on species from cold climates, where thermoregulatory capture to oviposition ¼ 7 days). They were kept individually in needs render snakes more readily observable. Therefore, our plastic cages (40 Â 30 cm and 20 cm high) at room temperature. knowledge of mating systems in snakes is skewed and woefully Cages were lined with paper and provided with a water dish and incomplete compared to other taxa, such as birds (see Griffith et al. a plastic nest/refuge box. Females in the late stages of gravidity are 2002). For example, there has probably been more detailed mating- arorectic and thus no food was provided. The eggs were incubated system analysis for a single population of garter snakes, Thamno- in the laboratory under a variety of substrate moisture regimes phis sirtalis parietalis, at the extreme northern limit of their range in (to assess incubation effects on hatchling phenotypes), and hatch- Canada (e.g. Mason 1993; Shine et al. 2000a,b,c,d,e) than for all lings were measured, marked and tissue-sampled, as for the adult other snakes combined. Other intensively studied snake species snakes. The hatchlings were then released at their mother’s site of include European adders, Vipera berus, and grass snakes, Natrix capture. The intense sampling schedule meant that most resident natrix, in Sweden (Madsen & Shine 1993, 1994; Madsen et al. 1992, snakes in this population were marked animals (e.g. in 2007, 112 of 1993), northern water snakes, Nerodia sipedon, in Canada (Weath- 123 adult animals were already marked when collected, as were 7 erhead et al. 1995) and prairie rattlesnakes, Crotalus viridis, in the of 12 juveniles). northern U.S.A. (Duvall & Schuett 1997). In the present study, we explored the mating system of Tissue Sampling a secretive tropical snake species by using molecular analyses based on tissue samples from offspring, their mothers and their potential We collected 380 tissue samples from slatey-grey snakes from fathers, to document fundamental parameters of the mating 2001 to 2007, including samples from 144 males and 17 different systems, such as the incidence of multiple paternity and the gravid females (in 2001–2004 and 2006–2007) which provided 24 correlates of male reproductive success. different clutches and 219 hatchlings (some females were captured Slatey-grey snakes, Stegonotus cucullatus (Colubridae) show while gravid in more than 1 year; Table 1). more extreme male-biased sexual size dimorphism than most other snake taxa (Shine 1994). Under the hypothesis that male- biased sexual size dimorphism results from a strong enhancement DNA Extraction and Microsatellite Analysis of male reproductive success by larger body size (e.g. Shine 1978, 1994), we predicted that larger body size would increase repro- Total cellular DNA was isolated from scales. Tissue of each ductive success for male slatey-grey snakes. Previous studies on individual was placed in 200 ml of 5% Chelex containing 0.2 mg/ml mating systems have identified at least three (not mutually of proteinase K, incubated overnight at 56 C, and boiled at 100 C. exclusive) pathways by which such a relationship might arise, and Nine microsatellite loci isolated and characterized from S. cucullatus distinguishing between those pathways can clarify the nature of (Dubey et al. 2008a; Steg_A4, Steg_A5, Steg_A105, Steg_B104, the selective forces working on body size
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