Do Operational Sex Ratios Influence Sex Allocation in Viviparous Lizards
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doi:10.1111/j.1420-9101.2006.01086.x Do operational sex ratios influence sex allocation in viviparous lizards with temperature-dependent sex determination? D. J. ALLSOP, D. A. WARNER, T. LANGKILDE,1 W. DU2 & R. SHINE School of Biological Sciences, The University of Sydney, Sydney, New South Wales 2006, Australia Keywords: Abstract litter sex ratio; Under certain environmental situations, selection may favour the ability of maternal effects; females to adjust the sex ratio of their offspring. Two recent studies have sex allocation; suggested that viviparous scincid lizards can modify the sex ratio of the sex-biased investment; offspring they produce in response to the operational sex ratio (OSR). Both of temperature-dependent sex determination. the species in question belong to genera that have also recently been shown to exhibit temperature-dependent sex determination (TSD). Here we test whether pregnant montane water skinks (Eulamprus tympanum) utilise TSD to select offspring sex in response to population wide imbalances in the OSR, by means of active thermoregulation. We use a combination of laboratory and field-based experiments, and conduct the first field-based test of this hypothesis by maintaining females in outdoor enclosures of varying OSR treatments throughout pregnancy. Although maternal body temperature during pregnancy was influenced by OSR, the variation in temperature was not great enough to affect litter sex ratios or any other phenotypic traits of the offspring. where the environment might have sex specific fitness Introduction effects on the offspring, and ask whether mothers In most sexually reproducing species, females are expec- facultatively adjust their offspring sex ratios in response ted to allocate equal effort to producing sons and to imbalances in the population adult sex ratio (termed daughters, assuming that the fitness returns from the the Operational Sex Ratio (OSR)). sexes are equal (Fisher, 1930). However, sex specific The OSR is defined as the ratio of males to females that fitness returns may differ under a wide variety of are ready to mate in a population at any one time (Emlen circumstances (Bull, 1981; Bull & Charnov, 1988). For & Oring, 1977), and this ratio can have a large impact on example, when relatives interact with each other in the level of mating competition, and thus sexual competition for mates or resources, and these inter- selection (Kvarnemo & Ahnesjo, 1996,2002). A bias in actions differ between the sexes, fitness returns may be the OSR will usually result in increased competition for sex specific (Hamilton, 1967). In circumstances where mates or resources amongst individuals of the more fitness returns differ between sons and daughters, abundant sex, and the extent of the OSR bias will selection may favour maternal ability to shift sex determine the level of competition and the intensity of allocation to produce the ‘best’ sex for the prevailing sexual selection (Clutton-Brock & Parker, 1992). For social and ecological conditions (Hamilton, 1967; Trivers example, males of the common spider mite (Tetranychus & Willard, 1973; Charnov, 1982; Frank, 1990; West et al., urticae) increase their level of mating competition as the 2002; West & Sheldon, 2002). Here we investigate a case OSR shifts towards a male bias, and consequently sexual selection leads to an increase in male body size relative to Correspondence: David J. Allsop, School of Biological Sciences, The female size (Enders, 1993). In a sex-role-reversed shore- University of Sydney, Sydney, New South Wales 2006, Australia. bird (Wilson’s phalarope, Phalatropus tricolor), the inten- Tel.: 61 02 9351 4661; fax: 61 02 9351 5609; sity of female–female competition diminishes as more e-mail: [email protected] males arrive at breeding grounds, levelling out the OSR 1Present address: T. Langkilde, School of Forestry and Environmental Studies, Yale University, New Haven, CT 06511, USA (Colwell & Oring, 1988). 2Present address: W. Du, School of Life Sciences, Hangzhou Normal Sex allocation theory predicts that if the OSR is College, Hangzhou, 310012, China perturbed from unity (either in time or space), facultative ª 2006 THE AUTHORS 19 (2006) 1175–1182 JOURNAL COMPILATION ª 2006 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1175 1176 D. J. ALLSOP ET AL. sex ratio adjustment should cause females to over- context. To do so we combine the realism of field produce the rare sex. In this way, mothers can reduce conditions with the power of experimentation, by competition within the over-abundant sex, and thus allowing females to gestate in field enclosures in which maximise offspring fitness (Werren & Charnov, 1978; we have manipulated OSR. We further extend previous Werren & Taylor, 1984; West & Godfray, 1997). For such work by asking whether the two environmentally labile an effect to occur, there must be considerable overlap in sex allocation strategies (OSR and TSD) are linked in this generations, such that offspring have the opportunity to species, by measuring the thermal behaviour of pregnant compete with their mothers’ adult conspecifics. In addi- females throughout gestation in the laboratory whilst tion, mothers must have the ability to accurately perceive housed in varying OSR treatments. Our prediction is that the OSR and to make the relevant sex ratio adjustments pregnant females utilise TSD to alter their sex allocation (Werren & Charnov, 1978). Empirical evidence that OSR decisions in response to an unbalanced OSR, via active can influence sex ratio has come from disparate maternal thermoregulation during gestation. phylogenetic lineages, including plants (Lopez & Dominguez, 2003), insects (McLain & Marsh, 1990), Materials and methods and humans (Lummaa et al., 1998; Lazarus, 2002). Two recent studies on viviparous scincid lizards in The model system Australia have suggested the same ability in reptiles. The first of these studies, using free ranging populations of The southern water-skink, E. tympanum is a medium the Tasmanian snow skink, Niveoscincus microlepidotus, sized (mean adult snout-vent length (SVL) 82 mm) used correlational evidence to suggest that females insectivorous scincid lizard with a geographic range perceive the OSR through the number of potential mates stretching throughout much of montane SE Australia they encounter during the breeding season. They then (Cogger, 2000). Eulamprus tympanum is viviparous and is shift their litter sex ratios to track the OSR both among predominantly lecithotrophic, providing nutrients for the and within years (Olsson & Shine, 2001). The second developing embryos in a yolk sac (Thompson et al., example used the southern water skink, Eulamprus 2001a). Ovulation and mating occur in October, and the tympanum, and conducted laboratory experiments with females gestate their young over summer, giving birth to animals held in small sex-biased populations (Robert between one and five offspring in January/February et al., 2003). Robert et al. (2003) concluded that pregnant (Schwarzkopf & Shine, 1991). females use facultative sex allocation in response to OSR, by overproducing the sex that is in short supply. Laboratory experiment However, the mechanism by which female E. tympanum perceives the OSR remains elusive (Robert, 2003). Adult male and female E. tympanum were collected early Intriguingly, although the taxa involved belong to two in the breeding season (early October, 2004) from widely separated phylogenetic lineages, both belong to Kanangra-Boyd National Park (33 °58.270S, genera that have been reported to shift offspring sex 150 °03.346E), 160 km west of Sydney, New South ratios in response to thermal conditions during gestation Wales, in eastern Australia. Lizards were measured (temperature-dependant sex determination (TSD): Rob- (mass, SVL, tail length), sexed (by hemipene eversion: ert & Thompson, 2001; Wapstra et al., 2004). Harlow, 1996), and given a unique toe clip for individual The mechanism of sex determination in these vivipar- identification. Lizards were then kept in experimental ous lizards is poorly understood and remains controver- groups in animal housing facilities at the University of sial (Valenzuela et al., 2003). In the southern water Sydney. skink, E. tympanum, offspring sex ratio is sensitive to Animals were kept in plastic nally bins (645 · maternal temperature during gestation, suggesting a 413 · 276 mm) and provided with basking heat using possible role for TSD (Robert & Thompson, 2001). under-cage heating tape set to 40°C (average field Temperature-dependant sex determination is commonly basking temperature in field is 30°C (Schwarzkopf & associated with a lack of heteromorphic sex chromo- Shine, 1991). Thus, lizards in these enclosures were able somes (Bull, 1980), and karyotype analysis demonstrates to regulate their own temperatures behaviourally that the Eulamprus genus indeed shows no overt sex whenever the heating tape was switched on, from chromosome dimorphism (Donnellan, 1985). However approximately 16°C (air temperature) to 40°C (the the co-occurrence of TSD and genetic sex determination hottest point above the heat tape). Heat strips were (GSD) in sister taxa and even within a single species controlled with an electronic timer set to one of two (Wibbels et al., 1994; Shine et al., 2002) suggest that the contrasting basking length regimes in an attempt to boundary between TSD and GSD is blurred, and that the mimic thermal variation in the field. Half of the animals two mechanisms comprise points on a continuum rather were offered a limited