ORIGINAL ARTICLE doi:10.1111/evo.13064 Basking behavior predicts the evolution of heat tolerance in Australian rainforest lizards Martha M. Mu ˜ noz, 1,2 Gary M. Langham, 3 Matthew C. Brandley, 4 Dan F. Rosauer, 5,6 Stephen E. Williams, 7 and Craig Moritz 5,6 1 Department of Biology, Duke University, Durham, North Carolina 27708 2 E-mail: [email protected]3 National Audubon Society, Washington, District of Columbia 4 School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia 5 Centre for Biodiversity Analysis, Australian National University, Canberra, Australian Capital Territory, Australia 6 Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia 7 Centre for Tropical Biodiversity and Climate Change, James Cook University, Townsville, Queensland, Australia Received August 31, 2015 Accepted August 31, 2016 There is pressing urgency to understand how tropical ectotherms can behaviorally and physiologically respond to climate warming. We examine how basking behavior and thermal environment interact to influence evolutionary variation in thermal physiology of multiple species of lygosomine rainforest skinks from the Wet Tropics of northeastern Queensland, Australia (AWT). These tropical lizards are behaviorally specialized to exploit canopy or sun, and are distributed across marked thermal clines in the AWT. Using phylogenetic analyses, we demonstrate that physiological parameters are either associated with changes in local thermal habitat or to basking behavior, but not both. Cold tolerance, the optimal sprint speed, and performance breadth are primarily influenced by local thermal environment. Specifically, montane lizards are more cool tolerant, have broader performance breadths, and higher optimum sprinting temperatures than their lowland counterparts. Heat tolerance, in contrast, is strongly affected by basking behavior: there are two evolutionary optima, with basking species having considerably higher heat tolerance than shade skinks, with no effect of elevation. These distinct responses among traits indicate the multiple selective pressures and constraints that shape the evolution of thermal performance. We discuss how behavior and physiology interact to shape organisms’ vulnerability and potential resilience to climate change. KEY WORDS: Australian Wet Tropics, behavioral thermoregulation, climate change, physiological evolution, skinks, thermal physiology. Anthropogenic climate warming presents an unprecedented threat to global biodiversity (Thomas et al. 2004; Parmesan 2006; Barnosky et al. 2011), and its impacts are predicted to be particularly pernicious for tropical ectotherms such as lizards, which already function near their upper physiological limits (Huey et al. 2009; Sinervo et al. 2010; Buckley and Huey 2016). Whether organisms can buffer rising temperatures with behavior or physiology, or adapt genetically, is thus a central question (Deutsch et al. 2008; Hoffman and Sgr` o 2011; Huey et al. 2012; Hoffmann et al. 2013). Evolutionary studies of physiology in lizards have yielded mixed results. Case studies in Caribbean Anolis lizards reported adaptive shifts in cold tolerance (Leal and Gunderson 2012) and the optimal sprinting temperature (Logan et al. 2014), indicating that some physiological traits 1 C 2016 The Author(s). Evolution
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ORIGINAL ARTICLE
doi:10.1111/evo.13064
Basking behavior predicts the evolutionof heat tolerance in Australian rainforestlizardsMartha M. Munoz,1,2 Gary M. Langham,3 Matthew C. Brandley,4 Dan F. Rosauer,5,6 Stephen E. Williams,7
and Craig Moritz5,6
1Department of Biology, Duke University, Durham, North Carolina 277082E-mail: [email protected]
3National Audubon Society, Washington, District of Columbia4School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales, Australia5Centre for Biodiversity Analysis, Australian National University, Canberra, Australian Capital Territory, Australia6Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia7Centre for Tropical Biodiversity and Climate Change, James Cook University, Townsville, Queensland, Australia
Received August 31, 2015
Accepted August 31, 2016
There is pressing urgency to understand how tropical ectotherms can behaviorally and physiologically respond to climate warming.
We examine how basking behavior and thermal environment interact to influence evolutionary variation in thermal physiology of
multiple species of lygosomine rainforest skinks from the Wet Tropics of northeastern Queensland, Australia (AWT). These tropical
lizards are behaviorally specialized to exploit canopy or sun, and are distributed across marked thermal clines in the AWT. Using
phylogenetic analyses, we demonstrate that physiological parameters are either associated with changes in local thermal habitat
or to basking behavior, but not both. Cold tolerance, the optimal sprint speed, and performance breadth are primarily influenced by
local thermal environment. Specifically, montane lizards are more cool tolerant, have broader performance breadths, and higher
optimum sprinting temperatures than their lowland counterparts. Heat tolerance, in contrast, is strongly affected by basking
behavior: there are two evolutionary optima, with basking species having considerably higher heat tolerance than shade skinks,
with no effect of elevation. These distinct responses among traits indicate the multiple selective pressures and constraints that
shape the evolution of thermal performance. We discuss how behavior and physiology interact to shape organisms’ vulnerability
PGLS models were fit comparing physiological traits to environmental temperature (left) and environmental temperature + basking behavior (center and
right panels). For analyses including behavior, the coefficients for the additional behavioral term are given. As described in the Methods, when treated as a
continuous variable, basking behavior is represented as the arcsine square-root transformed proportion of basking observations during ecological surveys.
Based on the hypotheses described in the text, CTmin and B95 were regressed against the mean minimum environmental temperature of the month prior to
capture, whereas Topt and CTmax were regressed against the mean maximum environmental temperature of the month prior to capture. The best-supported
models (based on AICC score) are shown in italics.
in CTmax was driven by differences in basking behavior (thermal
microhabitat), with little to no effects due to elevation (Fig. 2B).
One possibility is that the physiological variation among
lizards that we observed was due to environment-induced plastic-
ity, rather than genetic differences. However, the range of varia-
tion observed for these traits was much greater than that typically
induced through experimental acclimation. Targeted ecological
studies within lizard species (e.g., Kolbe et al. 2012; Munoz et al.
2014a; Phillips et al. 2016) and broader meta-analyses of accli-
mation (Gunderson and Stillman 2015) all find that physiological
traits typically only shift by 1–2°C in response to acute or sus-
tained environmental shifts (but see meta-analysis of CTmin ac-
climation in Pintor et al. 2016), whereas our measurements often
differed by up to 12°C (Fig. 4). This indicates that, while plasticity
8 EVOLUTION 2016
PHYSIOLOGICAL EVOLUTION IN AUSTRALIAN SKINKS
24
CT m
ax (°
C)
15 20 25 30
36
32
28
44
42
40
38
36
Max. Environmental Temperature (°C)
Max. Environmental Temperature (°C)
Min. Environmental Temperature (°C)
Min. Environmental Temperature (°C)
T opt
(°C
)
15 20 25 30
10 14 18 22
9
8
7
6
5
4
B95
(°C
)
10
16
14
12
18
10 14 18 22
CT m
in (°
C)
Figure 4. Population means for critical thermal minimum (CTmin),
the optimal performance range (B95), the optimal sprinting tem-
perature (Topt), and the critical thermal maximum (CTmax). The
x-axis denotes mean maximum environmental temperature for
CTmax and Topt and mean minimum environmental temperature for
CTmin and B95. Species are denoted in different colors and shapes
as follows: Carlia rubrigularis, circle; Gnypetoscincus queenslan-
lis robertsi, diamond; Saproscincus basiliscus, square; S. czechurae,
x mark; S. tetradactyla, cross. Basking species are shown in red and
shade dwellers in blue.
can be expected to contribute, there is likely a genetic basis for
much of the variation observed among lizards.
Previous studies on closely related ectotherms generally re-
port stable heat tolerances (Hoffmann 2010; Sunday et al 2011;
Kellermann et al. 2012; but see Gilchrist and Huey 1999). How-
ever, among the lizard taxa we sampled, CTmax varied consider-
ably, ranging from 35.1°C (S. czechurae—AU 1000) to 45.2°C (C.
rubrigularis—AU 1000). This range—more than 10°C—is par-
ticularly remarkable given that those lizards were from the same
locality. The differences in heat tolerance that we observe between
sympatric lizards are usually observed over substantially greater
geographic scales or across biomes (e.g., between temperate and
tropical taxa; Huey et al. 2009).
Heat tolerance evolved toward two distinct optima, with
edge habitat species (Carlia and Lampropholis) exhibiting con-
siderably higher heat tolerance (�6°C) than the shade specialists
(Gnypetoscincus and Saproscincus). Nonetheless, we found
no additional effects of local thermal environment on CTmax,
indicating that heat tolerance evolution largely occurred when
species behaviorally specialized to a specific microhabitat—
forest interior or canopy gaps/forest edges. The evolutionary
differences in heat tolerance between shade skinks and baskers
emphasize that tropical landscapes, though more thermally stable
than temperate habitats, provide sufficient within-site thermal
heterogeneity for marked physiological trait specialization.
Although basking behavior exerted a strong influence on
CTmax, it had no clear effects on any of the other traits. Rather,
thermal macroenvironment was the primary driver of variation in
CTmin, Topt, and B95. All lizards, regardless of basking behav-
ior, were more cold tolerant in cooler (higher elevation) habitats.
This finding is broadly concordant with a variety of geographic
studies on ectotherms. Interspecific studies, for example, have
demonstrated that CTmin exhibits considerably more geographic
variation than CTmax (Sunday et al. 2011; Araujo et al. 2013),
lower phylogenetic signal (Kellermann et al. 2012), and faster
rates of evolution than other physiological traits (Munoz et al.
2014a). Basking species and shade dwellers alike are confronted
with cool, thermally stable conditions at night, which greatly limit
their ability to thermoregulate efficiently (Ghalambor et al. 2006;
Munoz et al. 2014a). In the absence of behavioral refuges from
the cold, lizards have no option but to adjust their physiology.
As organisms become more cold tolerant (while also remaining
equally heat tolerant), the performance curve becomes progres-
sively more left-skewed, explaining why performance breadth is
considerably greater in montane habitats and why CTmin and B95
were strongly correlated.
In addition to more constricted performance breadths, lizards
in warm environments also had lower optimal sprinting tempera-
tures (Topt). This pattern, which we observe in a broad interspecific
study, is supported by a detailed interpopulational study in L.
EVOLUTION 2016 9
MARTHA M. MUNOZ ET AL.
Table 3. Model comparisons for heat tolerance (CTmax) evolution.
AICC θ σ2Loglikelihood
BM 65.90529 NA 15.912 −30.553OU single
peak69.54214 39.138 19.621 −30.914
OU multipeak
50.12621 43.006,37.146
18.659 −19.525
For each model, the AICC score is given, along with θ (optimal trait values),
σ2 (Brownian motion rate parameter), and the log-likelihood. Bold indicates
the best-supported model.
coggeri (Llewelyn et al. 2016). One possibility is that counter-
gradient selection is occurring, such that lizards in cooler habitats
exhibit greater behavioral sensitivity to temperature (e.g., Schultz
et al. 1996; Laugen et al. 2003). The inverse relationship between
Topt and environmental temperature may thus be a by-product of
reduced surface activity in hotter environments. At low elevation,
lizards are at much greater risk of overheating than freezing and
should be expected to alter their activity patterns to avoid heat
stress (Kearney et al. 2009). Recent empirical work on Honduran
Anolis lizards by Logan et al. (2015) supports this idea—whereas
lizards became less active when temperatures exceeded Topt,
activity patterns were unrelated to temperatures when the habitat
was cooler than Topt. Similarly, Vickers et al. (2011) found that
Carlia skinks thermoregulated most effectively during summer
months, when environmental temperatures were highest (and,
therefore, the risk of overheating was greatest). In a recent meta-
analysis of various lizard species, Huey et al. (2012) also detected
an inverse (though nonsignificant) correlation between maximum
summer temperature and optimal sprinting speed. Fine-scale stud-
ies of thermoregulatory behavior across thermal gradients would
help resolve the mechanism(s) underlying this physiological
pattern.
The sampling strategy employed here maximized the num-
ber of populations sampled, and focused on capturing physiolog-
ical variation across phylogenetic splits and geographic clines.
Despite relatively modest sample sizes within populations, we
feel that our sampling strategy accurately captured the range of
physiological trait variation, particularly because of the high trait
variation observed (Table 1; Fig. 4), and because we focused on
sampling across the altitudinal ranges of species (Bonino et al.
2011; Munoz et al. 2014a). Nonetheless, more detailed intraspe-
cific studies would be useful to further explore the relationships
described here. For example, in a detailed study of L. coggeri,
Llewelyn et al. (2016) found extensive among-population varia-
tion in CTmin and considerably less among-population variation
for CTmax, a pattern concordant with the results presented here.
BEHAVIOR AND PHYSIOLOGY INFLUENCE
VULNERABILITY TO CLIMATE CHANGE
By examining the physiological traits of ectotherms from an evo-
lutionary perspective, we can predict their potential for adaptive
response to rising temperatures, and hence vulnerability to fu-
ture climate change (Williams et al. 2008; Huey et al. 2012). Our
empirical data underscore the especially high vulnerability of the
shade-specialist lizards, Gnypetoscincus and Saproscincus, due
to their low heat tolerance as compared to edge habitat species.
These results indicate that even in tropical rainforests, which tend
to be relatively thermally stable habitats, there is enough envi-
ronmental heterogeneity for even closely related species to differ
substantially in their vulnerability to climate change (discussed
in Huey et al. 2009).
The shifts we observed in all species for CTmin, Topt, and B95
across elevation suggest high evolutionary lability in these traits.
It is important to note, however, that an accelerated evolutionary
rate—a process often inferred from such relationships—may in
fact reflect a number of different possible evolutionary processes
(Revell et al. 2008). Whatever the cause, it is clear that these traits
shift strongly across thermal gradients, due to genetic changes,
plastic shifts, or a combination of both, whereas CTmax does not.
The fact that CTmax does not shift with elevation may sug-
gest that this trait is unable to respond adaptively, or to do so fast
enough to meet the predicted pace of environmental warming.
Stability in CTmax is a general pattern observed across a variety
of ectotherms (Araujo et al. 2013), and is alarming because the
imminent challenge facing such organisms is to avoid overheat-
ing. In the case of these rainforest skinks, once lizards adapt to
a given thermal microhabitat, heat tolerance remains stable. Al-
though rigidity in CTmax suggests a limited capacity for lizards
to adaptively respond to warming, plasticity in thermal traits is
predicted to confer greater resilience in the face of rising tempera-
tures (Seebacher et al. 2015). Heat hardening, or a rapid, transient
increase in CTmax in response to heat shock, may provide phys-
iological buffering against greater and more intense heat waves.
Indeed, Phillips et al. (2016) found that one of our target species,
L. coggeri, exhibits a marked heat hardening response. However,
they also found that organisms in environments that are already
approaching thermal limits have a reduced capacity to shift heat
tolerance, which has also been observed in flies (Kristensen et al.
2015) and crabs (Stillman 2003). Hence, either through a limited
ability to shift heat tolerance, heat hardening, or both, ectotherms
are likely to be confronted with increasingly hostile thermal
environments.
Examining intraspecific variation in physiology across
altitudinal clines revealed patterns that would not have been
evident by averaging species’ means alone (Munoz et al. 2014b).
Our finding that Topt is higher in montane populations was
not predicted a priori (although there is substantial theoretical
1 0 EVOLUTION 2016
PHYSIOLOGICAL EVOLUTION IN AUSTRALIAN SKINKS
support), and provides an unexpected source of adaptive diversity
and promising new options for mitigation strategies, such as
assisted migration (Aitken and Whitlock 2013). Because the rela-
tionship between Topt and thermal environment is known to vary
in many ways among species (reviewed in Angilletta 2009), it is
only through targeted intraspecific studies that we can discover
how adaptive diversity in this trait is distributed across species’
ranges.
Consistent with what other studies have posited in various
geographic regions (Kearney et al. 2009; Sinervo et al. 2010; Sun-
day et al. 2014), simple extrapolations to future climate scenarios
for the Wet Tropics indicate that maximum temperatures could
exceed Topt of these lizards in lowland environments (e.g., Table
S7), and so challenge the persistence of these populations. The
shade skinks are mostly active early mornings and evenings (C.
Moritz and S. E. Williams pers. obs.), and in the warmer months
basking species such as Carlia also become more crepuscular
(Vickers et al. 2011). Whether these species will shift their di-
urnal rhythms and structural habitat use remains to be explored,
and requires microclimatic measurements to capture the full ef-
fects of behavior on energy budgets (Kearney et al. 2009). We
further point out that rising temperatures represent only one di-
mension of climate warming—other key factors, such as shifts in
humidity and cloud cover, could also stress ectotherms, particu-
larly those from tropical environments (e.g., Pounds et al. 1999;
Vickers 2014).
By examining variation both within and among species, we
were able to reveal patterns in basking behavior and their effect
on heat tolerance evolution. Intraspecific analyses revealed cli-
nal variation in CTmin, Topt, and B95 that would be absent at the
species level. Conversely, interspecific analyses revealed marked
differences in CTmax due to basking behavior that would not have
been apparent by examining clinal variation within species. Such
patterns reveal how ecologically relevant phenotypic diversity
is distributed across species’ ranges. Hence, understanding the
potential impacts of climate change on reptiles requires a more
detailed consideration of how behavioral and physiological phe-
notypes interact, and is best accomplished by studies integrating
information both within and among species.
ACKNOWLEDGMENTSWe thank C. Storlie, and B. Phillips for assistance with analyses. R. Huey,D. Miles, M. Sears, A. Gunderson, P. Cooper, and G. Bakken provideduseful comments and feedback on this manuscript. Funding was providedby a National Science Foundation postdoctoral fellowship (GML) and theAustralian Research Council (CM). Fieldwork support was provided byEarthwatch Institute Australia and the Tropical Ecosystems National En-vironmental Research Program. Intersect Australia Ltd. provided highperformance computing resources. Use of animals in this study was ap-proved by the University of California, Berkeley IACUC (Moritz 278)and the Australian National University (A2013-08). Fieldwork and phys-iological experiments in the Wet Tropics were conducted under a permit
from the Queensland Department of Environment and Resource Man-agement to SEW (WITK05468508). The authors declare no conflict ofinterest.
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Associate Editor: E. DerryberryHandling Editor: R. Shaw
Supporting InformationAdditional Supporting Information may be found in the online version of this article at the publisher’s website:
Table S1. PGLS models comparing physiological traits to environmental temperature (left) and environmental temperature + basking behavior (right).Table S2. Partitions for the molecular dataset used in the Bayesian phylogenetic analyses.Table S3. Comparison of model likelihoods for PGLS analyses when different branch transformations are employed.Table S4. Correlations among traits determined using regression of independent contrasts through the origin.Table S5. Marginal likelihood values for ancestral state reconstruction of basking behavior for each node in the phylogeny.Table S6. Extended model comparisons for heat tolerance (CTmax) evolution.Table S7. As a heuristic indicator of temperature change due to environmental warming, we determined the predicted increase in average daily maximumtemperature for each site, using gridded climate data sourced from WorldClim (worldclim.org) at 30 arcsec (�900 m) resolution (Hijmans et al. 2005).