Temperature-Dependent Sex Determination and ... - Seaturtle.org

Sexual 

Development 

Sex Dev 2010;4:129-140 

001: 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 

aCentre for Evolutionary Biology, School of Animal Biology, The University of Western Australia, Crawley, W.A., 

Australia; bDepartment of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, USA 

KeyWords 

Adaptation' Climate change' Conservation' Extinction' 

Heritability' Reptile' Sex determination' Temperature' 

TSO 

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 (TSO) 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 TSO 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, 

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 ofgeological 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 ofsex determination (e.g. genotypic sex 

determination (GSD) or parthenogenesis) or to popu- 

KARGER 

Fax +41 61 306 1234 

E-Mail karger@karger.ch 

www.karger.com 

© 2010 S. Karger AG, Basel 

1661-5425/10/0042-0129$26.00/0 

Accessible online at: 

www.karger.com/sxd 

Nicola Jane Mitchell 

Centre for Evolutionary Biology, School of Animal Biology 

The University ofWestern Australia 

Crawley, 6009 W.A. (Australia) 

Tel. +61864884510, Fax +61864881029, E-Mail nicola.mitchell@cyllene.uwa.edu.au

lation extinction [Bull and Bulmer, 1989; Janzen and 

Paukstis, 1991; Girondot et aI., 2004; Miller et aI., 2004; 

Schwanz and Janzen, 2008]. 

The four orders ofmodern 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 1O-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 ofup 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 aI., 

2007; Ackert et aI., 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 o.rc 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 ofglobal 

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; Pokorna 

and Kratochvil, 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 contemporaryclimate change, 

(2) to designate criteria that identify those species most at 

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 ofglobal 

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 withTSD [formarineturtles see reviewbyHawkes 

et aI., 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 aI., 2003; Glen and Mrosovsky, 2004; Doodyet 

aI., 2006; Freedberg and Bowne, 2006; Hawkes et aI., 

2007; Wapstra et aI., 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 ofhatchlings where sex ratios 

are significantly skewed. Warmer climates may also extend 

the breeding season ofsome 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 aI., 2008]. Some evidence that sex ratio biases 

in hatchling cohorts translate to adult stages comes 

from a 17-year study ofpainted turtles, Chrysemys picta, 

where the number of females released as hatchlings was 

an excellent predictor ofthe number ofbreeding females 

recruited in the population [Schwanz et aI., 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 ofa 

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 aI., 2009]. 

130 Sex Dev 2010;4;129-140 Mitchell/Janzen

An overproduction of male offspring more immediately 

threatens a population by a reduction in population 

growth rates due to a scarcity offemales. 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 aI., 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 oftuatara [Nelson 

et aI., 2002a; Mitchell et aI., 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 aI., 2000; Kamel and Mrosovsky, 

2006]. 

Spatial and temporal variability in the hatchling sex 

ratios ofspecies 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 ofmales could have 

dire demographic consequences. In one study that used 

population viability analysis (PVA), extinction ofa 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, andwould lead to a technicalextirpation 

ofthe population (Le. only males survive) byapproximately 

2150 [Mitchell et aI., 2009]. Itis 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 ofthe common 

lizard, Lacerta vivipara, if male aggression toward females 

leads to a reduction in female fecundity and survival 

[Le Galliard et aI., 2005]. 

Loss ofGenetic Diversity/Adaptive Potential via 

Reductions in Effective Population Size 

The most dramatic consequence of sex ratio bias is 

population extinction, but the adaptive potential ofpopulations 

may also be eroded by a consistent bias towards 

one sex. Populations with unequal numbers ofmales 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 ofEmergence Times and Food 

Availability/Climatic Suitability 

Annual events in an animal's lifecycle such as hatching 

or birth, and the renewal ofactivity follOWing periods 

ofdormancy 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 aI., 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 ofinsect prey that sustains hatchlings emerging in 

the spring [Mitchell et aI., 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 oftheir 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 aI., 2005]. 

Which Species Are Most Vulnerable? 

Whether a particular species ofreptile with TSD will 

be vulnerable to the current or projected rates of global 

warming will be influenced by multiple factors. Not only 

will many ofthese factors be interrelated, many ofthem 

also apply to species that do not have TSD. These factors 

comprise traits that influence the rate ofpotential adaptation 

(e.g. generation length, heritability of nesting behaviour) 

and those directly attributable to anthropogenic 

impacts (e.g. habitat fragmentation and loss ofgenetic 

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 ofextirpation 

- 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 aI., 2004]. In contrast, sex determining 

processes in squamates are proving remarkably 

complex [Sarre et aI., 2004; Quinn et al., 2007; Radder et 

aI., 2008, 2009; Pokorna and Kratochvil, 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 andproduce predominantly males [Telemeco 

et aI., 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 ofyolk 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 (Le. those that lack sex chromosomes) 

are at the greatest risk from rapid warming. 

B. Patterns ofTSD 

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 aI., 2009]. It is most difficult to predict 

the sex ratio expected under an FMF pattern ifnest 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 ofmales [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 ofthe Transitional Range ofTemperatures 

(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 aI., 2009]. A modelling study has suggested that 

TRT width is positively associated with populations that 

producegreaterproportions ofmixed 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 aI., 2009]. 

D. Generation Length 

The generation lengths of some reptiles are among 

the longest known for any vertebrates and will be a criticallimiting 

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 aI., 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 aI., 2009] and tuatara (GL = ~40 years) 

[Mitchell et aI., 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 

132 Sex Dev 2010;4:129-140 Mitchell/Janzen

smaller daily and seasonal temperature fluctuations than 

their counterparts at higher latitudes [Tewksbury et aI., 

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 ofHabitat 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 ofremnant habitat that may have limited 

or no connectivity to other suitable areas [Driscoll, 

2004; Berry et aI., 2005]. Hence, manypopulations ofreptiles 

with TSD are nowless 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 

PYA was applied to 45 vertebrate taxa [O'Grady et aI., 

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]. 

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 [Allendorfand Luikart, 2007]. 

However, a population subject to a recent bottleneck (a 

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 

ofneutral genetic markers in a reptile population. 

Indicators ofneutral genetic variation, such as the heterozygosity 

ofmicrosatellite DNA markers, are only relevant 

to predicting extinction risk if they reflect concordant 

variation in the underpinning adaptive traits [Bekessy et 

aI., 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]. 

1. Dispersal Ability (Vagility) 

Reptiles with TSD have varying levels ofvagility, ranging 

from marine turtles that cross major oceans and that 

producehatchlings thatdisperse on oceancurrents [Boyle 

et aI., 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 aI., 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. 

J, K. Heritability ofTraits (Threshold Temperatures 

and Nesting Behaviour) 

Heritabilitydescribes the degree to which thevariation 

in a trait is attributable to additive genetic variance, which 

can be viewed as governing the adaptive response ofa trait 

to selection. One of the most important factors that will 

influence the adaptability of reptiles to rapid climate 

change is the heritability oftraits 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 aI., 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 ofadaptive potential. 

We applied ourscoring 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 


Table 1. A categorical system designed to rank species by likelihood that they will survive contemporary climate change, with 5 examples 

A Lability in sex 1. Co-existence ofGSD and TSD 

determining system 2.·GSD in congeners---.---..---------...- 2 

. -_.._-_._--------_.. 

3. TSD in all"~~latedspecies 

3 3 3 3 

B TSD pattern 1.FMF 

2.MF 2 2 

3.FM 3 

C Width ofTRTs 

D Generation length 

1. ~5°C 

2. >1-~5°C 2 2 2 2 

3. ~1°C 3 

1. Short (1-5 years) 

-----_._----_. 

2Medium (6=-19 ye~-s)--·-----···· 

_..._._--. 

2 

3. Long (20+ ye~rs) 

3 3 3 

E Climatic zone for 1. Temperate 

egg development 2. Subtropical 2 2 

3. Equatorial 

F Fragmentation of 1. Not fragmented 

current habitat 2. Partially fragmented 2 2 2 

3. Extremely fragmented 3 

G Adult population 1. Large (~1 0,000) 

size 2. Medium (>250-:Q,500) 2 

3. Small ($250) 

H Genetic diversity 1. High 

2. Intermediate 2 2 2 

3. Low 3 

Dispersal 

1. Highly mobile/migratory 

ability/vagility 2. Short-range mobility 2 2 

3. Small, relatively constant horne ranges 3 

Heritability of 1. Highly heritable 

pivotal tempera- 2. Moderate heritability 2 

ture and TRT 3. Not heritable - 

K Heritability of 1. Highly heritable 

nesting behaviour 2. Moderate heritability 

3. Not heritable 3 

Score" 17 17 13 17 24 

a Includes only categories A-I, as data on heritability 0, K) are unavailable for most species. A higher score indicates a greater risk ofextinction. 

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 researchers, 

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. 


Is Adaptation Possible? 

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 ofselection) as well as the phenotypic 

plasticity and genetic architecture that underpin 

those traits. 

Four traits are likely to serve as primary targets ofsexratio 

selection in species with TSD: pivotal temperature 

(Tpiv), TRT, nest-site choice, and nesting phenology. The 

first two traits embody the intercept and slope ofthe 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 ofthese 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 aI., 2004; 

Doody et al., 2006; Hawkes et aI., 2007; Tucker et aI., 2008; 

Zhang et aI., 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 aI., 2002]. The outcome in terms 

ofoffspring 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% ofembryonic 

development [Nelson et aI., 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 ofapproximately 

90 days by 2085) in order to avoid male-biased sex ratios 

[Mitchell et aI., 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 ofthese 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 aI., 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 ofwithin-populationvariation. 

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 ofevolutionary 

potential. 

What do we know about intraspecific and intrapopulation 

variation in our TSD traits ofinterest? What information 

we have is largely comprised ofstudies ofTpivand 

TRT in turtles [e.g. Hulin et aI., 2009]; we know almost 

nothing about intraspecific variation for either measure 

of nesting behaviour. Even for Tpiv> many of the studies 

are plaguedby inadequate sample sizes orconcerns about 

proper measures ofincubation 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 ofheritable 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 ofthe TRT and latitude among populations 

ofNorthern Hemisphere snapping turtles [Ewert et 

aI., 2005]. Quantitative studies ofintraspecific 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- 


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 ofsufficient quality to separate 

meaningful among-population differences from annual 

noise. 

Our understanding of within-population phenotypic 

plasticity and inheritance ofTSD traits is no better. This 

lacuna likely arises because studies ofthe former necessitate 

repeated assessments of individuals across reproductive 

episodes, andthe latter require complex quantitative 

genetic evaluations. We are aware ofno explicit studies 

of within-population phenotypic plasticity of either 

T piv or TRT, although female painted dragons (Ctenophorus 

pictus) in captivityexhibit repeatable sex ratios among 

clutches within years [Vller 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 ofplasticity in nesting phenology 

found little evidence ofsuch repeatability in a population 

ofpainted turtles [Schwanz and Janzen, 2008]. As 

mentioned above, a handful ofexperiments have estimated 

quantitative genetic variation in thermal sensitivity of 

offspring sex in species with TSD buthave 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 ofreptiles 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 

shading rookeries to lower nest temperatures [e.g. Chu et 

al., 2008]. Manipulation ofsex 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 ofnest 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 ofHawksbill turtles 

is reducing the heterogeneityofnesting habitat so that the 

majority ofsuitable 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 ofeggs 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 ofharvesting 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 [Perez-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 ifthe 


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 ofcaptive-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 ofconservation 

concern, but the successful establishment of translocated 

reptiles [e.g. Nelson et aI., 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 ofclimate 

change - in this case, translocated populations already 

occur for this species and proposed translocation 

sites are potentially within the species' historic range 

[Mitchell et aI., 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 aI., 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]. 

Genetic Supplementation 

The genetic rescue hypothesis is based on the idea that 

immigrants increase the likelihood ofpopulation 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 aI., 1999; Pimm et aI., 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 equatormayintroduce 

heritable genetic variation (e.g. for T piv ) upon which selection 

can act. In essence, translocation ofanimals into existing 

populations is already a form of genetic supplementation, 

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. 

The Importance ofPopulation Monitoring under 

Climate Change 

Regular assessment ofpopulation sex ratios and sizes 

will be critical to determining how reptiles with TSD respond 

to future climate change. In manyspecies, particularly 

marine turtles, population size is predominantly estimated 

from the numbers offemales 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 ofregular assessment ofpopulation 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 

aI., 2003; Glen and Mrosovsky, 2004; Kamel and Mrosovsky, 

2006; Hawkes et aI., 2007; Mitchell et aI., 2008], 

and the accuracyand applicabilityofmodels will increase 

with further knowledge ofthreshold temperatures, thermosensitive 

periods and the variability and heritability of 

these traits. 

Conclusions 

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 ofNature 

(IUCN) concludes that 22% of the world's reptile 

species are at risk ofextinction - a proportion similar to 

the 25% for mammals and birds [Sampled Red List Index; 

Baillie et aI., 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 


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 (EJ.J. - Grant DEB-0640932). 

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