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
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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
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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).
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