Sex Dev 2010;4:129–140 DOI: 10.1159/000282494 Received: June 10, 2009 Accepted: July 14, 2009 Published online: February 9, 2010 Temperature-Dependent Sex Determination and Contemporary Climate Change N.J. Mitchell a F.J. Janzen b a Centre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, W.A., Australia; b Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, USA Key Words Adaptation ⴢ Climate change ⴢ Conservation ⴢ Extinction ⴢ Heritability ⴢ Reptile ⴢ Sex determination ⴢ Temperature ⴢ TSD Abstract Whether species that have persisted throughout historic climatic upheavals will survive contemporary climate change will depend on their ecological and physiological traits, their evolutionary potential, and potentially upon the resources that humans commit to prevent their extinction. For those species where temperatures influence sex determination, rapid global warming poses a unique risk of skewed sex ratios and demographic collapse. Here we review the specific mechanisms by which reptiles with temperature-dependent sex determination (TSD) may be imperilled at current rates of warming, and discuss the evidence for and against adaptation via behavioural or physiological means. We propose a scheme for ranking reptiles with TSD according to their vulnerability to rapid global warming, but note that critical data on the lability of the sex determining mechanism and on the heritability of behavioural and threshold traits are unavailable for most species. Nevertheless, we recommend a precautionary approach to management of reptiles identified as being at relatively high risk. In such cases, © 2010 S. Karger AG, Basel 1661–5425/10/0042–0129$26.00/0 Fax +41 61 306 12 34 E-Mail karger@karger.ch www.karger.com Accessible online at: www.karger.com/sxd management should aim to neutralise directional sex ratio biases (e.g. by manipulating incubation temperatures or assisted migration) and promote adaptive processes, possibly by genetic supplementation of populations. These practices should aid species’ persistence and buy time for research directed at more accurate prediction of species’ vulnerability. Copyright © 2010 S. Karger AG, Basel Changes in the Earth’s environment, particularly at the boundaries of geological epochs, are implicated in the extinction of many biological lineages [Berner, 2002; Huey and Ward, 2005]. However, many other lineages survived these same events. The survival of reptiles through past changes in climate is notable because this group is characterised extensively by the environmental control of offspring sex (temperature-dependent sex determination, or TSD) and rapid changes in the thermal environment could be expected to result in extreme sex ratio biases. Repeated exposure to conditions that promote highly skewed sex ratios could lead to adaptation (selection to restore the equilibrium sex ratio while retaining TSD), but could feasibly also lead to selection for alternative forms of sex determination (e.g. genotypic sex determination (GSD) or parthenogenesis) or to popu- Nicola Jane Mitchell Centre for Evolutionary Biology, School of Animal Biology The University of Western Australia Crawley, 6009 W.A. (Australia) Tel. +61 8 6488 4510, Fax +61 8 6488 1029, E-Mail nicola.mitchell @ cyllene.uwa.edu.au lation extinction [Bull and Bulmer, 1989; Janzen and Paukstis, 1991; Girondot et al., 2004; Miller et al., 2004; Schwanz and Janzen, 2008]. The four orders of modern non-avian reptiles (Testudines, Crocodilia, Squamata and Rhynchocephalia) originated between 280 and 200 million years ago (MYA) in the Mesozoic, where mean global sea and air temperatures were between 10–20 ° C warmer than at present [Fastovsky and Weishampel, 2005]. These lineages have persisted throughout continuous cycles of cooling and warming associated with glaciation, including the extremely rapid warming in the Pleistocene that followed the ‘Younger Dryas’ period between 12,900 to 11,600 BP, and abrupt changes of up to 5 ° C in the Holocene that occurred in a matter of decades [Steffensen et al., 2008]. However, the geographical extent of ‘abrupt’ climate change events is mostly limited to the Northern hemisphere, and there is no clear evidence of global shifts in temperature occurring at the same rate [Barrows et al., 2007; Ackert et al., 2008]. In contrast, increasing levels of greenhouse gases emitted due to human activity, particularly since the industrial revolution, should result in a minimum 2 ° C global increase in mean surface air temperatures, at a rate of about 0.2 ° C per decade [IPCC, 2007; Ramanathan and Feng, 2008]. Regional warming could be in the order of 0.6 ° C per decade under higher future emission scenarios [IPCC, 2007]. Thus, although contemporary rates of warming may be comparable to more extreme climatic changes in the Earth’s prehistory, the global extent of the current rate of warming is unusual. We have no historical basis on which to judge whether modern reptiles are imperilled by current rates of global warming, because the fossil record leaves no clue as to whether a now extinct lineage had TSD. However, phylogenetic analysis of the evolution of sex determining mechanisms in vertebrates suggests that GSD is the ancestral state, that TSD originated early in the diversification of modern reptiles, and that TSD has subsequently been lost multiple times in turtles, and originated at least three times in lizards [Janzen and Krenz, 2004; Pokorná and Kratochvíl, 2009]. Given that TSD is the dominant mechanism for sex determination in most reptilian lineages (apart from the most speciose lineage – the Squamata), it is clear that reptiles have adapted to past thermal perturbations while TSD has been their sex-determining mechanism. Our objective in this review is: (1) to weigh the evidence for and against the view that extant reptiles with TSD are imperilled by contemporary climate change, (2) to designate criteria that identify those species most at 130 Sex Dev 2010;4:129–140 risk, and (3) to suggest management options that could ameliorate the effects of a warmer climate on such species. While we acknowledge that other features of global climate change including higher sea levels, more frequent storm events, changes in food webs and reductions in habitat will also directly affect reproductive success of reptiles with TSD [for marine turtles see review by Hawkes et al., 2009], here we focus on the impact that increasing air temperatures could have on population dynamics and evolutionary processes. What Are the Threatening Processes? Sex Ratio Bias Leading to Demographic Collapse In reptiles with TSD there is now abundant evidence that unusually warm years produce hatchling sex ratios that are skewed towards the sex produced near the upper limit of tolerated incubation temperatures [Mrosovsky and Provancha, 1992; Janzen, 1994; Freedberg and Wade, 2001; Hays et al., 2003; Glen and Mrosovsky, 2004; Doody et al., 2006; Freedberg and Bowne, 2006; Hawkes et al., 2007; Wapstra et al., 2009]. This trend may exist despite any associated behavioural response to a warmer year (such as earlier nesting) and clearly demonstrates that, without a microevolutionary shift in threshold temperatures or subsequent nesting behaviour, climate warming is likely to produce cohorts of hatchlings where sex ratios are significantly skewed. Warmer climates may also extend the breeding season of some species, which may indirectly affect population sex ratios if extra clutches are produced at times when biased sex ratios are more likely [e.g. Tucker et al., 2008]. Some evidence that sex ratio biases in hatchling cohorts translate to adult stages comes from a 17-year study of painted turtles, Chrysemys picta, where the number of females released as hatchlings was an excellent predictor of the number of breeding females recruited in the population [Schwanz et al., 2010]. In most cases, warmer years are likely to produce predominantly females, due to the fact that most reptiles with TSD have a type that produces females at the maximum tolerated incubation temperatures (MF or FMF TSD). Theoretical models support the adaptive value of a female bias in small populations, because the intrinsic rate of increase of the population is enhanced despite a reduction in the effective genetic population size [Wedekind, 2002]. Provided that males are produced periodically and the breeding system is polygynous, then an overproduction of females may pose little immediate threat to population viability [Wapstra et al., 2009]. Mitchell /Janzen An overproduction of male offspring more immediately threatens a population by a reduction in population growth rates due to a scarcity of females. Overproduction of males under climate change is most likely for species with FM TSD, where males are produced above the upper temperature threshold. Tuatara are the only reptile group that exclusively have this pattern, while FM TSD has also been reported for some squamates [Mitchell et al., 2006]. In many cases an FM pattern has subsequently been revised to FMF TSD following additional experimentation [Harlow, 2004]. Significant male population biases are less often reported (or predicted) than female biases in reptiles with TSD, with the exception of tuatara [Nelson et al., 2002a; Mitchell et al., 2009]. However, for species with MF TSD, significantly male biased cohorts are produced in some years or at particular rookeries, usually in cooler years or in sites that receive relatively lower solar radiation [Lance et al., 2000; Kamel and Mrosovsky, 2006]. Spatial and temporal variability in the hatchling sex ratios of species with TSD is widespread and may be inconsequential to population viability given the longevity of many reptiles that have TSD. However, a directional trend toward increasing production of males could have dire demographic consequences. In one study that used population viability analysis (PVA), extinction of a population of around 550 tuatara (Sphenodon guntheri) was predicted once hatchling sex ratios reach about 80% male, or around 65% male if inbreeding was simulated at realistic levels [Mitchell et al., 2009]. This population lives on an offshore island where mechanistic modelling of nest temperatures suggested that almost all available nest sites (and nesting dates) would produce males if air temperatures were 3–4 ° C warmer than at present. Such a temperature shift could occur by 2085 under maximum emission scenarios, and would lead to a technical extirpation of the population (i.e. only males survive) by approximately 2150 [Mitchell et al., 2009]. It is also possible that, if strongly male-biased populations arise as a consequence of climate change, males could drive an ‘extinction vortex’ if they outcompete females for resources [Rankin and Kokko, 2007], or in the case of the common lizard, Lacerta vivipara, if male aggression toward females leads to a reduction in female fecundity and survival [Le Galliard et al., 2005]. ulations may also be eroded by a consistent bias towards one sex. Populations with unequal numbers of males and females will lose heterozygosity at a greater rate than the same sized population with a balanced sex ratio, and this effect is exacerbated if the skew is more extreme [Allendorf and Luikart, 2007]. Loss of heterozygosity is problematic if behavioural or physiological traits associated with TSD in a population are heritable, rather than solely environmentally determined. Mismatching of Emergence Times and Food Availability/Climatic Suitability Annual events in an animal’s lifecycle such as hatching or birth, and the renewal of activity following periods of dormancy are usually tightly coupled to food availability, but numerous studies have demonstrated that climate change is interfering with these ecological linkages [Hughes, 2000; Walther et al., 2002; Edwards and Richardson, 2004]. Species with TSD are no exception – warmer temperatures could lead to unseasonal hatching events in species whose eggs normally overwinter in a nest and hatch in more benign spring conditions. An energetically based model for the Brother’s Island tuatara (Sphenodon guntheri) predicts that males could emerge up to 5 months earlier than females under a warmer climate (3– 4 ° C increase in air temperatures), emerging before the flush of insect prey that sustains hatchlings emerging in the spring [Mitchell et al., 2008]. Conversely, males may overwinter in the nest as hatchlings and still emerge before females in the spring, but may be relatively disadvantaged by a greater depletion of their residual yolk reserve. This effect has been demonstrated empirically in slider turtles (Trachemys scripta) that are obligated to overwinter in the nest; warmer winters cause the neonates to consume more energy reserves, weakening the turtles for the post-nest migration to water [Willette et al., 2005]. Which Species Are Most Vulnerable? Loss of Genetic Diversity/Adaptive Potential via Reductions in Effective Population Size The most dramatic consequence of sex ratio bias is population extinction, but the adaptive potential of pop- Whether a particular species of reptile with TSD will be vulnerable to the current or projected rates of global warming will be influenced by multiple factors. Not only will many of these factors be interrelated, many of them also apply to species that do not have TSD. These factors comprise traits that influence the rate of potential adaptation (e.g. generation length, heritability of nesting behaviour) and those directly attributable to anthropogenic impacts (e.g. habitat fragmentation and loss of genetic variation). We have devised a simple categorical scoring TSD and Contemporary Climate Change Sex Dev 2010;4:129–140 131 system based on 11 factors that allow the ranking of reptile species with TSD by their relative risk of extirpation – with a higher score denoting a greater risk (table 1). Below, we discuss the rationale for our ranking system. A. Lability in the Sex-Determining System Crocodilians and Sphenodontians show no variation in their sex-determining mechanism (all species lack sex chromosomes and have TSD), whereas sex determination in turtles shows some lability, with at least two genera (Kinosternidae and Emydidae) including species with TSD or GSD [Ewert et al., 2004]. In contrast, sex determining processes in squamates are proving remarkably complex [Sarre et al., 2004; Quinn et al., 2007; Radder et al., 2008, 2009; Pokorná and Kratochvíl, 2009], to the extent that GSD and TSD may co-occur within a population. For example, in the Australian montane skink, Bassiana duperreyi – a species with heteromorphic sex chromosomes – warmer years favour GSD and produce balanced sex ratios, whereas cooler years seem to cause a switch to TSD and produce predominantly males [Telemeco et al., 2009]. It is clear that GSD can be overridden by environmental effects in some species (e.g. Pogona barbata and Bassiana duperreyi), but the apparent TSD pattern detected under certain (often unusual) incubation conditions could also be driven by alternative factors such as sex-biased fertilisation or the quantity of yolk steroids. Nonetheless, the lability in the processes influencing offspring sex ratios in some squamates means that rapid global warming could exert strong selection for GSD, or for plastic or evolved responses that allow adaptive sex ratios to be produced under TSD. However, when temperature is the primary signal regulating sexual differentiation and, ultimately, population sex ratios, then species with true TSD (i.e. those that lack sex chromosomes) are at the greatest risk from rapid warming. B. Patterns of TSD The three expressed patterns of TSD (MF, FM and FMF) differ in the sex-ratio biases that could result from warmer nest temperatures, and we have concluded above that male biases are more directly threatening than female biases. Male biases would be predicted for species with FM TSD (tuatara and some squamates), whereas female biases are more likely for species with the MF pattern (most turtles). A recent review suggests that at least 44% of turtle populations with MF TSD currently produce mixed sex nests, and the real proportion may be higher because skewed sex ratios are more likely to be reported [Hulin et al., 2009]. It is most difficult to predict 132 Sex Dev 2010;4:129–140 the sex ratio expected under an FMF pattern if nest temperatures increase, because for most species there are few field data to reveal whether females are primarily produced above or below the threshold temperature for the production of males [reviewed in Deeming, 2004; Janzen, 2008]. However, in this latter group we assume that the possession of two temperature thresholds for sex determination would provide the greatest capacity to buffer population sex ratios from sideways shift in incubation temperatures – provided that the extreme temperatures that produce females do not compromise embryonic viability. C. Width of the Transitional Range of Temperatures (TRTs) Reptiles with TSD are characterised by diversity in the TRTs that produce mixed sexes; for example, in turtles with MF TSD, TRTs range between 0.7 ° C to at least 8.5 ° C [Hulin et al., 2009]. A modelling study has suggested that TRT width is positively associated with populations that produce greater proportions of mixed sex nests. Moreover, species with relatively large TRTs are likely to evolve more readily than species with narrower TRTs because more heritable genetic variation can be expressed at intermediate temperatures, which may place them at a lower risk of sex ratio bias under climate change [Hulin et al., 2009]. D. Generation Length The generation lengths of some reptiles are among the longest known for any vertebrates and will be a critical limiting factor in determining the rates of adaptation to warmer climates. There is a strong correlation between extinction risk and generation lengths in vertebrates, with species with relatively long generation times being the least likely to persist at small population sizes [O’Grady et al., 2009]. While there are no clear delineations between short, intermediate and long generation lengths, we have based our categories on the range of generation lengths reported for species with TSD. Species with short generation lengths (GLs) include agamid lizards (e.g. Ctenophorus pictus – GL = 1 year) [Bradshaw, 1971], whilst the longest generation times include those recorded for turtles (GL = 23–35 years) [O’Grady et al., 2009] and tuatara (GL = ⬃40 years) [Mitchell et al., 2009]. E. Climatic Zone for Egg Development Reptiles that occur at or near to the equator may be particularly vulnerable to climate change because they are adapted to a relatively stable climate with markedly Mitchell /Janzen smaller daily and seasonal temperature fluctuations than their counterparts at higher latitudes [Tewksbury et al., 2008]. Consequently, such climate-induced stabilizing selection should deplete adaptive genetic variation compared to fluctuating selection experienced by reptile populations that occur toward the poles. Hence, relative to equatorial species, temperate-zone reptiles are more likely to have retained genetic variation that will allow them to respond adaptively to climate change. F. Extent of Habitat Fragmentation Habitat fragmentation is a major factor that will influence whether nonmarine reptiles with TSD will persist through climate change. At least 28% of the Earth’s terrestrial and freshwater habitats have been converted to human-dominated uses [Hoekstra, 2005] and other habitats have been severely degraded, leaving many reptiles isolated in pockets of remnant habitat that may have limited or no connectivity to other suitable areas [Driscoll, 2004; Berry et al., 2005]. Hence, many populations of reptiles with TSD are now less able to shift their distributions to remain in suitable climatic envelopes, as may have been a response to past changes in climate. Most species will be stranded in a warmer and perhaps otherwise altered (wetter or drier) environment. A significant consequence of habitat fragmentation is isolation from other populations and a reduction in gene flow, coupled with the gradual depletion of genetic diversity through the chance loss of rare alleles [e.g. Sarre, 1995]. G. Adult Population Size The size of the adult population has obvious implications for assessing extinction risk, because stochastic events (such as extreme weather conditions) can exert a disproportionally large effect on small populations [Caughley, 1994]. A recent analysis of 16 factors commonly used to predict extinction concluded that population size was the best correlate of extinction risk when PVA was applied to 45 vertebrate taxa [O’Grady et al., 2004]. While largely arbitrary, the adult population size categories we assign in table 1 reflect those used by the International Union for the Conservation of Nature for designating threatened species categories [IUCN, 1994]. rapid reduction in size) may retain residual genetic diversity for some time, particularly for long-lived species – hence our justification for considering these factors in separate categories. In practice, conservation managers will at best have access to information on the genetic diversity of neutral genetic markers in a reptile population. Indicators of neutral genetic variation, such as the heterozygosity of microsatellite DNA markers, are only relevant to predicting extinction risk if they reflect concordant variation in the underpinning adaptive traits [Bekessy et al., 2003]. Meta-analysis suggests that neutral genetic diversity is a poor predictive of additive genetic variation for traits that influence fitness [Reed and Frankham, 2001], and a more productive approach may be to target markers linked to regions of the genome that code for functional traits [van Tienderen et al., 2002]. I. Dispersal Ability (Vagility) Reptiles with TSD have varying levels of vagility, ranging from marine turtles that cross major oceans and that produce hatchlings that disperse on ocean currents [Boyle et al., 2009], to freshwater turtles and crocodilians that undergo seasonal migrations across wetland and river systems, to terrestrial tortoises and tuatara that have small home ranges and may move less than 1 km in their lifetime [Pough et al., 2004]. Animal species with low vagility (and their plant counterparts that have limited seed dispersal) may be most likely to require ‘assisted migration’ (see below) to relocate to more suitable habitats. H. Genetic Diversity Population size and genetic diversity are usually interrelated; small populations are expected to lose genetic variation more rapidly than large populations due to genetic drift and inbreeding [Allendorf and Luikart, 2007]. However, a population subject to a recent bottleneck (a J, K. Heritability of Traits (Threshold Temperatures and Nesting Behaviour) Heritability describes the degree to which the variation in a trait is attributable to additive genetic variance, which can be viewed as governing the adaptive response of a trait to selection. One of the most important factors that will influence the adaptability of reptiles to rapid climate change is the heritability of traits that influence offspring sex, and the extent to which heritable traits can be overridden by environmental effects [Rhen and Lang, 1988; Janzen, 1992; Hulin et al., 2009]. These data are currently unavailable for the vast majority of reptile species. Although difficult to obtain, this information is essential for generating quantitative predictions of adaptive potential. We applied our scoring scheme to 5 reptile species representing the 4 extant reptile orders, with our scores being largely based on our personal knowledge of the species in question. Even for these relatively well-studied species the data are incomplete (notably data on the heritability of traits), hence we have tallied only the scores TSD and Contemporary Climate Change Sex Dev 2010;4:129–140 133 Table 1. A categorical system designed to rank species by likelihood that they will survive contemporary climate change, with 5 ex- amples Risk category Common and species name (order) American alligator, Brothers Island tuatara, Jacky dragon, Loggerhead turtle, Painted turtle, Chrysemys picta Amphibolurus mu- Alligator mississip- Sphenodon guntheri Caretta caretta ricatus (Squamata) piensis (Crocodilia) (Rhyncocephalia) (Testudines) (Testudines) A Lability in sex 1. Co-existence of GSD and TSD determining system 2. GSD in congeners 3. TSD in all related species B TSD pattern C Width of TRTs D Generation length 2 3 3 1. FMF 2. MF 3. FM 2 2 1. ≥5° C 2. >1–≤5° C 3. ≤1° C 2 1. Short (1–5 years) 2. Medium (6–19 years) 3. Long (20+ years) 1 3 1 G Adult population size 1. Large (≥10,000) 2. Medium (>250–≤2,500) 3. Small (≤250) 1 H Genetic diversity 1. High 2. Intermediate 3. Low K Heritability of nesting behaviour a Includes 1 3 1 2 2 2 2 3 1 1 1 2 1 2 2 2 3 1. Highly heritable 2. Moderate heritability 3. Not heritable 2 1. Highly heritable 2. Moderate heritability 3. Not heritable 1 2 3 3 17 17 13 17 24 only categories A–I, as data on heritability (J, K) are unavailable for most species. A higher score indicates a greater risk of extinction. from categories A–I. Of the species we considered, we conclude that the Brothers Island tuatara is most threatened by climate change (score = 24) and an agamid lizard the least (score = 13; table 1). Equivalent scores for other reptiles with TSD could feasibly be calculated from published literature or personal communication with re134 1 2 2 Score 2 3 1. Highly mobile/migratory 1 2. Short-range mobility 3. Small, relatively constant home ranges a 2 1 1. Not fragmented 2. Partially fragmented 3. Extremely fragmented Heritability of pivotal temperature and TRT 2 2 F Fragmentation of current habitat J 1 3 1. Temperate 2. Subtropical 3. Equatorial Dispersal ability/vagility 3 3 E Climatic zone for egg development I 3 Sex Dev 2010;4:129–140 searchers, and ranking species by their risk score could provide a useful framework for allocating scarce conservation resources. However, increasing our knowledge of the heritability of traits associated with sex ratio allocation will be a major step forward in forecasting the relative risks faced by different species. Mitchell /Janzen Adaptation comprises a blend of selection with varying degrees of phenotypic plasticity and inheritance. While phenotypic plasticity might afford an intragenerational response to selection, inheritance allows a more permanent evolutionary solution. With climate change possibly exerting sex-ratio selection on reptiles with TSD, it is thus important to identify traits that can influence sex ratios (i.e., the targets of selection) as well as the phenotypic plasticity and genetic architecture that underpin those traits. Four traits are likely to serve as primary targets of sexratio selection in species with TSD: pivotal temperature (Tpiv), TRT, nest-site choice, and nesting phenology. The first two traits embody the intercept and slope of the temperature-sex ratio reaction norm for developing embryos, whereas the latter two traits encompass spatial and temporal targeting of the embryonic thermal environment. For only one of these traits – nesting phenology – are there extensive data on the response of the trait to warmer climates. Longer-term studies are revealing that a variety of reptiles with TSD are nesting earlier in warmer years [e.g. Iverson, 1991; Weishampel et al., 2004; Doody et al., 2006; Hawkes et al., 2007; Tucker et al., 2008; Zhang et al., 2009], with the most dramatic shift reported in slider turtles (Trachemys scripta) that have shifted the onset of the nesting season forward by 27 days over 13 years of monitoring, during which period the mean annual temperature has warmed by about 2 ° C [Schwanz and Janzen, 2008]. This forward shift in the average egglaying date has also been widely observed in invertebrates, amphibians, and birds [Beebee, 1995; Crick and Sparks, 1999; Walther et al., 2002]. The outcome in terms of offspring sex for reptiles with TSD is largely unknown, and will depend on whether the thermosensitive period (TSP) for sex determination falls in a cooler or warmer portion of the year relative to typical nesting dates. In tuatara, where the TSP occurs between 30–35% of embryonic development [Nelson et al., in press], mechanistic models suggest that the effect of earlier nesting in response to a climate 3–4 ° C warmer than at present would need to be dramatic (e.g. a forward shift of approximately 90 days by 2085) in order to avoid male-biased sex ratios [Mitchell et al., 2009]. Changes in nesting phenology to offset the impact of climate change on offspring sex ratio are similarly predicted to be ineffective in painted turtles (Chrysemys picta) [Schwanz and Janzen, 2008]. Despite discouraging modelling outcomes [Morjan, 2003a], the likelihood that one or more of these traits can change swiftly enough to facilitate sex-ratio adaptation in response to expected rapid climate change remains an empirical question. We can gain useful insight into the adaptive potential of these traits in (at least) two ways. First, intraspecific variation, particularly among populations occupying areas with substantially different thermal environments, can provide guidance regarding historical adaptation of TSD. For example, female water dragons, Physignathus lesueurii, from populations closer to the equator prefer shadier nest sites than do females from more polar populations, with the result that developmental temperatures are reasonably consistent across the range of this species [Doody et al., 2006]. While observations of the trait values in these populations are helpful, their utility is enhanced if accompanied by experimental manipulation, such as with a common-garden or reciprocal-transplant design. Second, work on intraspecific variation in TSD is complemented by quantitative genetic assessments of within-population variation. Quantifying phenotypic plasticity can provide a measure of the resiliency of a trait in a population whereas estimates of the heritability of a trait, or genetic covariance among traits, yield quantitative assessments of evolutionary potential. What do we know about intraspecific and intrapopulation variation in our TSD traits of interest? What information we have is largely comprised of studies of Tpiv and TRT in turtles [e.g. Hulin et al., 2009]; we know almost nothing about intraspecific variation for either measure of nesting behaviour. Even for Tpiv, many of the studies are plagued by inadequate sample sizes or concerns about proper measures of incubation temperatures, rendering questionable the biological value of many of the estimates [sensu Janzen and Paukstis, 1991]. Having said that, the general sense from studies of Tpiv is that variation exists among populations, but with scant support for substantial adaptive variation [but see Ewert et al., 2005], despite evidence of heritable variation within populations [reviewed in Janzen, 2008]. To our knowledge, only one study has specifically quantified intraspecific variation in the TRT, finding a positive relationship between the width of the TRT and latitude among populations of Northern Hemisphere snapping turtles [Ewert et al., 2005]. Quantitative studies of intraspecific variation in nesting behaviour are scarce as well. In addition to the Physignathus and Chelydra work referenced above, Morjan [2003b] quantified differences in nest-site choice spatially and with respect to canopy cover by painted turtles (Chrysemys picta) in two distantly separated populations. Similarly, intraspecific variation in nesting phe- TSD and Contemporary Climate Change Sex Dev 2010;4:129–140 Is Adaptation Possible? 135 nology is poorly quantified for all but a few species [e.g., Doody et al., 2006], because relatively long-term studies are needed to build datasets of sufficient quality to separate meaningful among-population differences from annual noise. Our understanding of within-population phenotypic plasticity and inheritance of TSD traits is no better. This lacuna likely arises because studies of the former necessitate repeated assessments of individuals across reproductive episodes, and the latter require complex quantitative genetic evaluations. We are aware of no explicit studies of within-population phenotypic plasticity of either Tpiv or TRT, although female painted dragons (Ctenophorus pictus) in captivity exhibit repeatable sex ratios among clutches within years [Uller et al., 2006], whereas painted turtles in the wild seemingly do not [Valenzuela and Janzen, 2001]. Several studies have examined repeatability of nest-site choice in reptile populations with TSD, generally finding low but significant levels of consistent nesting behaviour, mostly with respect to habitat variables linked to nest thermal environments [Bull et al., 1988; Janzen and Morjan, 2001; Kamel and Mrosovsky, 2005]. In contrast, the one study of plasticity in nesting phenology found little evidence of such repeatability in a population of painted turtles [Schwanz and Janzen, 2008]. As mentioned above, a handful of experiments have estimated quantitative genetic variation in thermal sensitivity of offspring sex in species with TSD but have focused almost exclusively on turtles and not at all on nesting behaviour. The species most suited to such investigations will be a relatively fast maturing species with large clutches, in which the best candidates may be agamid lizards, such as the Australian water dragon (Physignathus lesueurii). How Should Populations at Risk Be Managed? Active management of reptiles with TSD is already in place for many species listed as locally or globally threatened, although to a large extent current management practices are directed at preventing more immediate threats to species viability, such as habitat loss, illegal harvesting and predation or competition from invasive species [Gibbons et al., 2000]. Although these threats will continue, management directed at neutralising directional biases in sex ratios will become increasingly important as the climate changes. Management can take two main forms. In situ management occurs when populations are managed to maintain adaptive sex ratios at current nesting sites, usually by 136 Sex Dev 2010;4:129–140 shading rookeries to lower nest temperatures [e.g. Chu et al., 2008]. Manipulation of sex ratios by increasing shade will be most achievable if nesting locations are predictable and spatially aggregated. For example, erection of shadecloth over nests would be a practical measure for terrestrial reptiles such as tuatara that are confined to small areas (e.g. islands) and have established rookeries [Mitchell et al., 2008]. In contrast, shading may be impractical for wide ranging marine species such as Hawksbill turtles (Eretmochelys imbricata) that nest at low densities. Maintenance of nest site heterogeneity will be critical to the success of programs that aim to conserve reptiles with TSD, for homogeneous nesting areas offer few mechanisms by which behavioural plasticity could influence nest temperatures. Hence management should also be directed at preserving natural nesting habitat that is shaded, or that otherwise offers a cooler thermal environment (e.g. nest sites that retain more moisture). For example, deforestation of the nesting beaches of Hawksbill turtles is reducing the heterogeneity of nesting habitat so that the majority of suitable nesting areas are unshaded and likely to produce females [Kamel and Mrosovsky, 2006]. Increases in sand temperatures as a response to climate change will only exacerbate this effect. Harvesting eggs from nests shortly after oviposition, or inducing oviposition by injecting oxytocin into gravid females [Booth, 2004], is an alternative form of in situ management. Hatchlings can be incubated at favourable temperatures and released at natal rookeries. This approach is labour intensive, but should result in higher hatching success than eggs that develop in natural nests, which are more likely to experience desiccation or depredation. However, induction of eggs is not a panacea; premature induction can result in poorly calcified and/or smaller eggs that may have reduced fitness relative to wild-collected eggs [Nelson et al., 2004]. An advantage of harvesting eggs is that hatchlings can be headstarted (raised in captivity) and released into a population at an age when their rates of survival are appreciably greater than their survival rates as hatchlings. For example, release of headstarted Mona Island iguana (Cyclura cornuta stejnegeri – a species with GSD) at 3 years of age has resulted in an increase in the density of adults on Mona Island relative to islands where headstarting programs were not in effect [Pérez-Buitrago et al., 2008]. Elasticity analysis generally supports the principle that increasing the survivorship of juvenile age classes will enhance the growth rates of reptile populations [e.g. Enneson and Litzgus, 2008], particularly if the Mitchell /Janzen cohort to be released is female biased [Wedekind, 2002]. Moreover, adoption of practices such as headstarting in semi-natural conditions [e.g. Gruber, 2007] and imposing quarantine periods prior to release may increase the survivorship of released animals and reduce the risk of introduction of captive-borne diseases into a wild population. The obvious alternative to in situ conservation is translocation – the deliberate (or in some cases accidental) reintroduction of a species to an area that was formerly part of its historic range. Translocation has met with mixed success when applied to reptiles of conservation concern, but the successful establishment of translocated reptiles [e.g. Nelson et al., 2002b; Cook, 2004; Germano and Bishop, 2009] demonstrates that it could be an important tool for allowing species to persist under a changing climate. Translocation to more southern reserves has been proposed for the Brothers’ Island tuatara (S. guntheri) as a means of mitigating the impact of climate change – in this case, translocated populations already occur for this species and proposed translocation sites are potentially within the species’ historic range [Mitchell et al., 2008]. In contrast, ‘assisted migration’ – the deliberate introduction of species to novel regions that may be more climatically favourable in the long term – is more controversial [e.g. Ricciardi and Simberloff, 2009], but for some species the potential benefits of assisted migration may outweigh the risks [Hoegh-Guldberg et al., 2008; Richardson et al., 2009]. The slider turtle (Trachemys scripta elegans) would be an excellent model for assessing the potential costs and benefits of translocation, as it has successfully colonized habitats worldwide despite originating from the near tropical conditions in the southern United States [Cadi et al., 2004]. mentation, but as far as we are aware, there have been no deliberate attempts to introduce animals that are preadapted to warmer regions. Genetic supplementation may be viewed by some conservation practitioners as being less extreme intervention than assisted migration. However, we are hesitant to advocate genetic supplementation of reptile populations without first testing its effects empirically using rigorous field experiments. Genetic Supplementation The genetic rescue hypothesis is based on the idea that immigrants increase the likelihood of population persistence by providing additional genetic diversity [Ingvarsson, 2001]. To date genetic supplementation has largely been applied to critically endangered species to limit the deleterious impacts of inbreeding depression [e.g. Masden et al., 1999; Pimm et al., 2006], yet it could potentially also provide increased resilience to climate change. In particular, relocating animals from more polar populations to populations closer to the equator may introduce heritable genetic variation (e.g. for Tpiv) upon which selection can act. In essence, translocation of animals into existing populations is already a form of genetic supple- Contemporary climate change has already exerted an impact, and will continue to threaten the viability of many species, largely through interactions with other deleterious processes such as habitat fragmentation and disease. Data available on the factors that threaten individual species of reptiles are scarce relative to data that are available for mammals and birds, yet a recent assessment by the International Union for Conservation of Nature (IUCN) concludes that 22% of the world’s reptile species are at risk of extinction – a proportion similar to the 25% for mammals and birds [Sampled Red List Index; Baillie et al., 2008]. Again, insufficient data prohibit analysis of whether there is an upward trend in the relative risk of extinction for reptiles, but climate change will TSD and Contemporary Climate Change Sex Dev 2010;4:129–140 The Importance of Population Monitoring under Climate Change Regular assessment of population sex ratios and sizes will be critical to determining how reptiles with TSD respond to future climate change. In many species, particularly marine turtles, population size is predominantly estimated from the numbers of females that nest each year at established rookeries, and a decline in the number of males would be less obvious than a decline in the size of the female population [Kamel and Mrosovsky, 2006]. The cost of regular assessment of population sizes and sex ratios may be prohibitive for wide-ranging species, and indirect techniques such as measuring changes in gene frequencies, or modelling approaches, are viable alternatives. Modelling techniques in particular are increasingly being used in preference to direct assessment for predicting hatchling sex ratios [e.g. Janzen, 1994; Hays et al., 2003; Glen and Mrosovsky, 2004; Kamel and Mrosovsky, 2006; Hawkes et al., 2007; Mitchell et al., 2008], and the accuracy and applicability of models will increase with further knowledge of threshold temperatures, thermosensitive periods and the variability and heritability of these traits. Conclusions 137 continue to exert significant demographic pressures on populations that are already under threat from other adverse factors. Ultimately, reptiles with TSD may serve as ‘canaries in the coalmine’ for the biological impacts of rapid climate change, because few threshold traits are as fundamental to population viability as those that determine sex. Acknowledgements We thank Ettore Olmo for the invitation to contribute to this themed edition and Rick Shine for helpful comments on a draft of the manuscript. Our most recent work on this topic has been supported by the Australian Research Council (N.J.M.) and the National Science Foundation (F.J.J. – Grant DEB-0640932). References Ackert RP Jr, Becker RA, Singer BS, Kurz MD, Caffee MW, Mickelson DM: Patagonian glacier response during the late glacial-Holocene transition. Science 321:392–395 (2008). Allendorf FW, Luikart G: Conservation and the Genetics of Populations (Blackwell Publishing, Oxford 2007). Baillie JEM, Collen B, Amin R, Akcakaya HR, Butchart SHM, et al: Towards monitoring global biodiversity. Conserv Lett 1: 18–26 (2008). Barrows TT, Lehman SJ, Fifield LK, De Deckker P: Absence of cooling in New Zealand and the adjacent ocean during the Younger Dryas chronozone. Science 318:86–89 (2007). Beebee TJC: Amphibian breeding and climate. Nature 374:219–220 (1995). Bekessy SA, Ennos RA, Burgman MA, Newton AC, Ades PK: Neutral DNA markers fail to detect genetic divergence in an ecologically important trait. Biol Conserv 110: 267–275 (2003). Berner RA: Examination of hypotheses for the Permo-Triassic boundary extinction by carbon cycle modeling. Proc Natl Acad Sci USA 99:4172–4177 (2002). Berry O, Tocher MD, Gleeson DM, Sarre SD: Effect of vegetation matrix on animal dispersal: Genetic evidence from a study of endangered skinks. Conserv Biol 19: 855–864 (2005). Booth DT: Artificial incubation, in Deeming DC (ed): Reptilian Incubation: Environment, Evolution and Behaviour, pp 253–263 (Nottingham University Press, Nottingham 2004). Boyle MC, FitzSimmons NN, Limpus CJ, Kelez S, Velez-Zuazo X, Waycott M: Evidence for transoceanic migrations by loggerhead sea turtles in the southern Pacific Ocean. Proc Biol Sci Ser B 276: 1993–1999 (2009). Bradshaw SD: Growth and mortality in a field population of Amphibolurus lizards exposed to seasonal cold and aridity. J Zool 165: 1–25 (1971). Bull JJ, Bulmer MG: Longevity enhances selection of environmental sex determination. Heredity 63:315–320 (1989). Bull J, Gutzke W, Bulmer M: Nest choice in a captive lizard with temperature-dependent sex determination. J Evol Biol 1: 177–184 (1988). 138 Sex Dev 2010;4:129–140 Cadi A, Delmas V, Prévot-Julliard A-C, Joly P, Pieau C, Girondot M: Successful reproduction of the introduced slider turtle (Trachemys scripta elegans) in the South of France. Aquatic Conservation: Marine and Freshwater Ecosystems 14:237–246 (2004). Caughley G: Directions in conservation biology. J Anim Ecol 63: 215–244 (1994). Chu TC, Booth DT, Limpus CJ: Estimating the sex ratio of loggerhead turtle hatchlings at Mon Repos rookery (Australia) from nest temperatures. Aust J Zool 56:57–64 (2008). Cook RP: Dispersal, home range establishment, survival, and reproduction of translocated eastern box turtles, Terrapene c. carolina. Appl Herpetol 1: 197–228 (2004). Crick HQP, Sparks TH: Climate change related to egg-laying trends. Nature 399: 423–424 (1999). Deeming DC: Prevalence of TSD in crocodilians, in Valenzuela N, Lance VA (eds): Temperature-Dependent Sex Determination in Vertebrates, pp 33–41 (Smithsonian Institution Press, Washington 2004). Doody JS, Guarino F, Georges A, Corey B, Murray G, Ewert MW: Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evol Ecol Res 20:307–330 (2006). Driscoll DA: Extinction and outbreaks accompany fragmentation of a reptile community. Ecol Appl 14: 220–240 (2004). Edwards M, Richardson AJ: Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430: 881–884 (2004). Enneson JJ, Litzgus JD: Using long-term data and a stage-classified matrix to assess conservation strategies for an endangered turtle (Clemmys guttata). Biol Conserv 141: 1560– 1568 (2008). Ewert MA, Etchberger CR, Nelson CE: Turtle sex-determining modes and TSD patterns, and some TSD pattern correlates, in Valenzuela N, Lance VA (eds): Temperature-Dependent Sex Determination in Vertebrates, pp 21–32 (Smithsonian Institution Press, Washington 2004). Ewert MA, Lang JW, Nelson CE: Geographic variation in the pattern of temperature-dependent sex determination in the American snapping turtle (Chelydra serpentina). J Zool 265:81–95 (2005). Fastovsky DE, Weishampel DB: The Evolution and Extinction of the Dinosaurs. (Cambridge University Press, Cambridge 2005). Freedberg S, Bowne DR: Monitoring juveniles across years reveals non-Fisherian sex ratios in a reptile with environmental sex determination. Evol Ecol Res 8:1499–1510 (2006). Freedberg S, Wade MJ: Cultural inheritance as a mechanism for population sex-ratio bias in reptiles. Evolution 55:1049–1055 (2001). Germano JM, Bishop PJ: Suitability of amphibians and reptiles for translocation. Conserv Biol 23: 7–15 (2009). Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, et al: The global decline of reptiles, déjà vu amphibians. Bioscience 50: 653–666 (2000). Girondot M, Delmas V, Rivalan P, Courchamp F, Prévot-Julliard A-C, Godfrey M: Implications of temperature-dependent sex determination for population dynamics, in Valenzuela N, Lance VA (eds): TemperatureDependent Sex Determination in Vertebrates, pp 148–155 (Smithsonian Institution Press, Washington 2004). Glen F, Mrosovsky N: Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach. Global Change Biol 10: 2036–2045 (2004). Gruber MAM: Conservation of tuatara (Sphenodon): an evaluation of the survival and growth of artificially incubated, head-started juveniles. B Sc (hons) thesis, University of Wellington, Victoria (2007). Harlow PS: Temperature-dependent sex determination in lizards, in Valenzuela N, Lance VA (eds): Temperature-Dependent Sex Determination in Vertebrates, pp 42–52 (Smithsonian Institution Press, Washington 2004). Hawkes LA, Broderick AC, Godfrey MH, Godley BJ: Investigating the potential impacts of climate change on a marine turtle population. Global Change Biol 13: 923–932 (2007). Hawkes LA, Broderick AC, Godfrey MH, Godley BJ: Climate change and marine turtles. Endangered Species Res 7:137–154 (2009). Hays GC, Broderick AC, Glen F, Godley BJ: Climate change and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Global Change Biol 9:642–646 (2003). Mitchell /Janzen Hoegh-Guldberg O, Hughes H, McIntyre S, Lindenmayer DB, Parmesan C, et al: Assisted colonization and rapid climate change. Science 321:345–346 (2008). Hoekstra JM: Confronting a biome crisis: global disparities of habitat loss and protection. Ecol Lett 8:23 (2005). Huey RB, Ward PD: Hypoxia, global warming, and terrestrial late Permian extinctions. Science 308:398–401 (2005). Hughes L: Biological consequences of global warming: is the signal already apparent? Trends Ecol Evol 15:56–61 (2000). Hulin V, Delmas V, Girondot M, Godfrey M, Guillon JM: Temperature-dependent sex determination and global change: are some species at greater risk? Oecologia 160: 493– 506 (2009). Ingvarsson PK: Restoration of genetic variation lost – the genetic rescue hypothesis. Trends Ecol Evol 16: 62 (2001). IPCC – Summary for Policymakers: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge University Press, Cambridge 2007). IUCN 1994: IUCN Red List Categories (Gland, Switzerland 1994). Iverson JB: Life-history and demography of the yellow mud turtle, Kinosternon flavescens. Herpetologica 47: 373–395 (1991). Janzen FJ: Heritable variation for sex-ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina). Genetics 131:155–161 (1992). Janzen FJ: Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci USA 91:7487–7490 (1994). Janzen FJ: Sex determination in Chelydra, in Steyermark AC, Finkler MS, Brooks RJ (eds): Biology of the Snapping Turtle (Chelydra serpentina), pp 146–157 (Johns Hopkins University Press, Baltimore 2008). Janzen FJ, Krenz JG: Which was first, TSD or GSD?, in Valenzuela N, Lance VA (eds): Temperature-Dependent Sex Determination in Vertebrates, pp 121–130 (Smithsonian Institution Press, Washington 2004). Janzen FJ, Morjan CL: Repeatability of microenvironment-specific nesting behaviour in a turtle with environmental sex determination. Anim Behav 63:73–82 (2001). Janzen FJ, Paukstis GL: Environmental sex determination in reptiles: ecology, evolution and experimental design. Quart Rev Biol 66: 149–179 (1991). Kamel SJ, Mrosovsky N: Repeatability of nesting preferences in the hawksbill sea turtle, Eretmochelys imbricata, and their fitness consequences. Anim Behav 70:819–828 (2005). Kamel SJ, Mrosovsky N: Deforestation: risk of sex ratio distortion in hawksbill sea turtles. Ecol Appl 16: 923–931 (2006). Lance VA, Elsey RM, Lang JW: Sex ratios of American alligators (Crocodylidae): Male or female biased? J Zool 252:71–78 (2000). TSD and Contemporary Climate Change Le Galliard JF, Fitze PS, Ferrière R, Clobert J: Sex ratio bias, male aggression, and population collapse in lizards. Proc Natl Acad Sci USA 102:18231–18236 (2005). Madsen T, Shine R, Olsson M, Wittzell H: Restoration of an inbred adder population. Nature 402:34–35 (1999). Miller D, Summers J, Silber S: Environmental versus genetic sex determination: a possible factor in dinosaur extinction? Fertil Steril 81: 954–964 (2004). Mitchell NJ, Nelson NJ, Cree A, Pledger S, Keall SN, Daugherty CH: Support for a unique pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon). Front Zool 3:9 (2006). Mitchell NJ, Kearney MR, Nelson NJ, Porter WP: Predicting the fate of a living fossil: how will global warming affect sex determination and hatching phenology in tuatara? Proc Biol Sci Ser B 275: 2185–2193 (2008). Mitchell NJ, Allendorf FW, Keall SN, Daugherty CH, Nelson NJ: Demographic effects of temperature-dependent sex determination: will tuatara survive global warming? Global Change Biol 16:60–72 (2010). Morjan CL: How rapidly can maternal behaviour affecting primary sex ratio evolve in a reptile with environmental sex determination? Am Nat 162:205–219 (2003a). Morjan CL: Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination. Behav Ecol Sociobiol 53: 254–261 (2003b). Mrosovsky N, Provancha J: Sex ratios of hatchling loggerhead sea turtles: data and estimates from a 5-year study. Can J Zool 70: 530–538 (1992). Nelson NJ, Keall SN, Pledger S, Daugherty CH: Male-biased sex ratio in a small tuatara population. J Biogeogr 29: 633–640 (2002a). Nelson NJ, Keall SN, Brown D, Daugherty CH: Establishing a new wild population of tuatara (Sphenodon guntheri). Conserv Biol 16: 887–894 (2002b). Nelson NJ, Thompson MB, Pledger S, Keall SN, Daugherty CLH: Induction of oviposition produces smaller eggs in tuatara (Sphenodon punctatus). N Z J Zool 31:283–289 (2004). Nelson NJ, Moore J, Pillai S, Keall SN: Thermosensitive period for sex determination in tuatara. Herpetol Conserv Biol, in press. O’Grady JJ, Reed DH, Brook BW, Frankham R: What are the best correlates of predicted extinction risk? Biol Conserv 118:513 (2004). O’Grady JJ, Reed DH, Brook BW, Frankham R: Extinction risk scales better to generations than to years. Anim Conserv 11: 442–451 (2009). Pérez-Buitrago N, García MA, Sabat A, Delgado J, Álvarez A, et al: Do headstart programs work? Survival and body condition in headstarted Mona Island iguanas Cyclura cornuta stejnegeri. Endangered Species Res 6: 55–65 (2008). Sex Dev 2010;4:129–140 Pimm SL, Dollar L, Bass OLJ: The genetic rescue of the Florida panther. Anim Conserv 9:115– 122 (2006). Pokorná M, Kratochvíl L: Phylogeny of sex-determining mechanisms in squamate reptiles: are sex chromosomes an evolutionary trap? Zool J Linn Soc 156:168–183 (2009). Pough FH, Andrews RM, Cadle JE, Crump ML, Savitsky AH, Wells KD: Herpetology, 3rd edition (Benjamin Cummings, Pearson 2004). Quinn AE, Georges A, Sarre SD, Guarino F, Ezez T, Graves JAM: Temperature sex reversal implies sex gene dosage in a reptile. Science 316: 411 (2007). Radder RS, Quinn AE, Georges A, Sarre S, Shine R: Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol Lett 4: 176 (2008). Radder RS, Pike DA, Quinn AE, Shine R: Offspring sex in a lizard depends on egg size. Curr Biol 19: 1–4 (2009). Ramanathan V, Feng Y: On avoiding dangerous anthropogenic interference with the climate system: formidable challenges ahead. Proc Natl Acad Sci USA 105:14245–14250 (2008). Rankin DJ, Kokko H: Do males matter? The role of males in population dynamics. Oikos 116: 335–348 (2007). Reed DH, Frankham R: How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103 (2001). Rhen T, Lang JW: Among-family variation for environmental sex determination in reptiles. Evolution 52:1514–1520 (1998). Ricciardi A, Simberloff D: Assisted colonization is not a viable conservation strategy. Trends Ecol Evol 24: 248–253 (2009). Richardson DM, Hellmann JJ, McLachlan JS, Sax DF, Schwartz MW, et al: Multidimensional evaluation of managed relocation. Proc Natl Acad Sci USA 106: 9721–9724 (2009). Sarre S: Mitochondrial DNA variation among populations of Oedura reticulata (Gekkonidae) in remnant vegetation: implications for metapopulation structure and population decline. Mol Ecol 4:395–406 (1995). Sarre SD, Georges A, Quinn A: The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26:639–645 (2004). Schwanz LE, Janzen FJ: Climate change and temperature-dependent sex determination: can individual plasticity in nesting phenology prevent extreme sex ratios? Physiol Biochem Zool 81:826–834 (2008). Schwanz LE, Spencer RJ, Bowden RM, Janzen FJ: Climate and predation dominate early life demography and adult recruitment in a turtle with temperature-dependent sex determination: insight from a long-term study. Ecology, in press (2010). 139 Steffensen JP, Andersen KK, Bigler M, Clausen HB, Dahl-Jensen D, et al: High-resolution Greenland ice core data show abrupt climate change happens in few years. Science 321: 680–684 (2008). Telemeco R, Elphick M, Shine R: Nesting lizards (Bassiana duperreyi) compensate partly, but not completely, for climate change. Ecology 90:17–22 (2009). Tewksbury JJ, Huey RB, Deutsch CA: Putting the heat on tropical animals. Science 320: 1296–1297 (2008). Tucker JK, Dolan CR, Lamer JT, Dustman EA: Climatic warming, sex ratios, and red-eared sliders (Trachemys scripta elegans) in Illinois. Chelonian Conserv Biol 7: 60–69 (2008). 140 Sex Dev 2010;4:129–140 Uller T, Mott B, Odierna G, Olsson M: Consistent sex ratio bias of individual female dragon lizards. Biol Lett 22: 569–572 (2006). Valenzuela N, Janzen FJ: Nest-site philopatry and the evolution of temperature-dependent sex determination. Evol Ecol Res 3: 779–794 (2001). van Tienderen PH, de Haan AA, van der Linden CG, Vosman B: Biodiversity assessment using markers for ecologically important traits. Trends Ecol Evol 17:577–582 (2002). Walther G-R, Post E, Convey P, Menzel A, Parmesan C, et al: Ecological responses to recent climate change. Nature 416:389–395 (2002). Wapstra E, Uller T, Sinn D, Olsson M, Mazurek K, et al: Climate effects on offspring sex ratio in a viviparous lizard. J Anim Ecol 78:84–90 (2009). Wedekind C: Manipulating sex ratios for conservation: short-term risks and long-term benefits. Anim Conserv 5:13–20 (2002). Weishampel JF, Bagley DA, Ehrhart LM: Earlier nesting by loggerhead sea turtles following sea surface warming. Global Change Biol 10: 1424–1457 (2004). Willette DA, Tucker JK, Janzen FJ: Linking climate and physiology at the population level for a key life-history stage of turtles. Can J Zool 83: 845–850 (2005). Zhang F, Li Y, Guo Z, Murray BR: Climate warming and reproduction in Chinese alligators. Anim Conserv 12:128–137 (2009). Mitchell /Janzen