Alternative reproductive adaptations predict asymmetric responses to climate change in lizards
Alternative reproductive adaptations predict asymmetric responses to climate change in lizards
Manuel Jara 0 1
Roberto Garc?a-Roa 2
Luis E. Escobar 3
Omar t orres-Carvajal 4
Daniel pincheira-Donoso 5
0 School of Life Sciences, University of Lincoln , Brayford Campus, Lincoln, LN6 7DL , United Kingdom
1 Department of Population Health and Pathobiology, college of Veterinary Medicine, north carolina State University , Raleigh, nc , USA
2 ethology Lab, c avanilles institute of Biodiversity and e volutionary Biology, University of Valencia , Valencia , Spain
3 Department of Fish and Wildlife Conservation, Virginia Tech , Blacksburg, Virginia , USA
4 Museo de Zoologi?a, Escuela de Biologi?a, Pontificia Universidad Cato?lica del Ecuador, Avenida 12 de Octubre y Roca , Apartado 17-01-2184, Quito , Ecuador
5 MacroBiodiversity Lab, School of Science and Technology, Department of Biosciences
Published: xx xx xxxx Anthropogenic climate change ranks among the major global-scale threats to modern biodiversity. Extinction risks are known to increase via the interactions between rapid climatic alterations and environmentally-sensitive species traits that fail to adapt to those changes. Accumulating evidence reveals the influence of ecophysiological, ecological and phenological factors as drivers underlying demographic collapses that lead to population extinctions. However, the extent to which life-history traits influence population responses to climate change remains largely unexplored. The emerging 'cul-de-sac hypothesis' predicts that reptilian viviparity ('live-bearing' reproduction), a 'key innovation' facilitating historical invasions of cold climates, increases extinction risks under progressively warming climates compared to oviparous reproduction - as warming advances polewards/mountainwards, historically cold-climates shrink, leading viviparous species to face demographic collapses. We present the first large-scale test of this prediction based on multiple lizard radiations and on future projections of climate-based ecological niche models. Viviparous species were found to experience stronger elevational range shifts (and potentially increased extinctions) in coming decades, compared to oviparous lizards. Therefore, our analyses support the hypothesis's fundamental prediction that elevational shifts are more severe in viviparous species, and highlight the role that life-history adaptations play in the responses of biodiversity to ongoing climate change.
The accelerated rates of climate change recorded over the last half century are known to be driving global-scale
alterations and declines of biodiversity at unprecedented magnitudes1?6. As a result, accumulating evidence
suggests that the planet is entering one of the greatest environmental crises since the origin of life7?9. A prevailing
?biodiversity syndrome? emerging from these climatic changes is the rapid alterations of the geographic ranges
observed across a broad range of species3,10?12. Such geographic shifts are the result of species displacements
tracking their rapidly moving historical niches as warming advances across space10,13,14. However, patterns, rates,
and drivers of geographic range shifts differ across regions and lineages10,14?16. Climate change has consistently
been observed to be spatially heterogeneous, tending to be more severe towards higher latitudes and
elevations3,10,14,15,17. Therefore, species restricted to mountaintops and continental margins are more likely to
experience progressive losses of suitable areas as warming advances, hence, forcing either rapid adaptations to the new
climatic conditions, or extinctions3,10,18,19. The steepness of mountain slopes also increases the severity of climatic
and ecological gradients in a more reduced geographic space (relative to flat regions), further aggravating the
increases of extinction risks in species from high elevations2,19?22. In addition to pressures emerging from the
environment, the magnitude of species? responses to climate change importantly depends on their ecological
tolerance as a function of intrinsic factors such as genetic variation, population size, and generation time23?25.
In recent years, research efforts have focused on identifying mechanisms behind such spatial asymmetries in
responses to contemporary climate change, leading to reinforce the focus on a range of phenological, ecological,
and physiological factors as primary factors underlying extinction risks26?28.
Surprisingly, the influence that life-history adaptations exert on species responses to climate change has only
occasionally been addressed. In fact, although parity-mode transitions (from live-bearing to egg-laying) have
been suggested to play a key role in accelerating extinction risks under rapid climate warming19,26, only a handful
of studies have investigated the ecological basis of this phenomenon19,26,29. Given that life-history traits underlie
reproductive success (?fitness?), and that climate change operates as rapid natural selection on fitness via its
impact on environmentally-sensitive traits, the conceptual disjoint between both dimensions creates a major gap
in our understanding of biodiversity declines via anthropogenic effects. In fact, selection arising from climatic
pressures have been shown to generate predictable patterns of evolution and distribution of reproductive traits
(e.g., parity mode19, transient fecundity30), which therefore creates macroecological patterns of species
interactions with the climate via life-history adaptations19,30?33.
An emerging idea, the ?cul-de-sac? hypothesis, predicts that the evolution of viviparity ? a key life-history
adaptation believed to have facilitated the radiation of reptiles into cold climates19,33,34 ? is driving reptiles to
extinctions due to climate change, relative to oviparous reproducers19. Thanks in part to evolving viviparity,
reptiles have successfully proliferated across extreme high elevations and latitudes, where low temperatures create
strong natural selection against multiple components of fitness via thermal demands on ecological (e.g., embryo
survival and development19,26 and life-history (e.g., limitations on reproductive output for viviparous species)
functions26,32,35. In contrast, these pressures are relaxed in warm climates, where oviparous reptiles dominate.
In viviparous squamates, embryo retention in the maternal body acts similar to an incubator to counteract the
lethal effects that low and fluctuating environmental temperatures impose on egg development19,36?38. However,
cold-climate reptiles may be approaching an evolutionary dead-end in the face of climate change19. Given that
most cold-climate reptiles are viviparous30,32,39, that the oviparity-to-viviparity transitions are largely irreversible
(thus, fundamentally unidirectional)19,32,39,40, and that live-bearing parity (relative to oviparity) entails high
fitness costs (e.g., reduced reproductive frequency, increased pregnancy-burden, prolonged basking time)32,35,41, the
cul-de-sac hypothesis suggests that, as climate warming advances towards higher elevations and latitudes,
viviparous reptiles will remain trapped in rapidly retracting cold environments19, while oviparous species are expected
to colonize previously cold sites19,26. As viviparous species progressively run out of suitable environments as they
approach mountaintops and continental edges, populations are expected to experience demographic collapse that
will lead to extinctions10,14,19,42. So far, evidence consistent with this hypothesis remains limited to a few studies
that have approached the question in a preliminary fashion19,26,43. However, a replicated, large-scale
macroecological test assessing the responses of species to climate change as a function of life-history adaptations proposed
by this hypothesis remains lacking.
Here, we present a comprehensive test of the cul-de-sac hypothesis, based on fine-scale distributional data
spanning three prolific and evolutionarily contrasting lizard radiations that have diversified in the Andes and
adjacent areas in South America. Their natural histories span all scenarios of parity mode variation: Liolaemus,
with 270+ species is the world?s second most diverse genus of living amniotes44, in which viviparity has evolved
in several independent phylogenetic events19,45; Phymaturus, a strictly cold-climate, viviparous genus of 60+
species46; finally, Stenocercus consists of 60+ oviparous species, despite their distributions up to above 4000 m in the
Andes47. Using an ecological niche modeling framework and future climate scenarios (IPPC Fifth Assessment48)
we tested whether viviparous (relative to oviparous) species (i) are predicted to experience greater range
contractions, (ii) higher overall spatial displacements, and (iii) greater displacement towards higher elevations in relation
with oviparous species.
Our ecological niche model (ENM) analyses reveal that the geographic ranges and their changes are
predominantly influenced by temperature-related variables across all three lineages (in 93.7% of the species), while
precipitation-related variables tend to be considerably less relevant (only dominant in 6.3% of the species;
Supplementary Table?S1). Also, we found that potential impacts of climate change on species ranges were not
evenly distributed across space. Range expansions and contractions were more likely in certain regions (e.g., the
high Andes), and absent from other regions (e.g., Patagonian steppe, Temperate broadleaf and mixed forests in
Southern Chile; Moran?s spatial autocorrelation index >0.7, P < 0.001; Supplementary Table?S8). Such range shifts
patterns were observed consistently in viviparous species (Figs?1a,b and S1a,b). Although MIROC5-based
models supported the hypothesis of a geographic directionality in the spatial shifts (Rayleigh?s test range, P = 0.05?
0.01), GISS-ER-based models showed centroid shifts that were not distinguishable from uniform (Fig.?1c;
Supplementary Table?S6; Supplementary Fig.?S1c).
Geographic range shifts. Our analyses revealed that shifts in the percentage of range expansions or
contractions driven by estimated magnitudes of climate change do not significantly differ between viviparous species
combined (regardless of taxonomic group) and oviparous species combined (Table?1; Fig.?1a,b, Supplementary
Tables?S2?S5, Supplementary Fig.?S1a,b). Likewise, the effects of climate change on the magnitude of spatial
displacements of species? geographic range centroids (Fig.?2a,b) and their spatial direction (Fig.?1c, Supplementary
Table?S6, Supplementary Fig.?S1c) do not significantly differ between viviparous species combined and oviparous
species combined, in concordance with observations on expansions and contractions.
In contrast, as predicted by theory, we found significant differences in the magnitude of elevational shifts
between parity modes (Liolaemus-viviparous + Phymaturus versus Liolaemus-oviparous + Stenocercus; Fig.?2c,d),
expressed as higher elevational shifts for viviparous species relative to oviparous species (Phylogenetic t-test
Future range overlaps between oviparous and viviparous species. Compared with the current
range overlap between the geographic areas covered by oviparous and viviparous species combined regardless of
taxonomy (currently 15.3%), our analyses suggest that climate change-driven range shifts are likely to cause an
increase in the current levels of overlap between species with both parity modes. More specifically, range overlaps
are projected to increase with the magnitude of greenhouse gas emissions (RCPs): while under the minimum
climate change scenario (RCP 2.6), range overlap was observed to remain as today (~15% of overlap, relative to the
modern 15.3%), under the maximum scenario (RCP 8.5) the predicted overlap is projected to increase up to 3%,
leading to ~18% of overlap between both parity modes (Supplementary Table?S9 and Fig.?S2).
Our study presents the first comprehensive and broad-scale quantitative test of the ?cul-de-sac? hypothesis19,
which predicts that viviparous species are more vulnerable to extinctions as climate warming progressively
shrinks the cold regions they are adapted to19. Our findings across three highly-diverse lizard radiations support
the effects that parity modes are expected to exert on the patterns of elevational shifts projected for these
organisms as climate warms up (whereas, no such differences were observed for direction of shifts in range centroids).
Specifically, our findings revealed that the prediction strongly holds for alterations in elevational distributions,
where viviparous species combined experience greater elevational shifts relative to oviparous species (see Fig.?1d).
These elevational displacements observed in viviparous species were stronger in Phymaturus (strictly viviparous),
suggesting the potential for greater magnitudes of demographic impacts, and potentially extinction risks faced
by these lizards under the ongoing climate trends49. Importantly, our findings also suggest that as the degrees of
emissions of greenhouse gases increase, the extent of spatial overlap between oviparous and viviparous
reproducers will increase, thus leading to the predicted scenarios of novel forms of competition between oviparous and
viviparous species19,26. Collectively, therefore, our study reinforces the need to add the life-history dimension to
the search for factors that trigger mechanisms underlying biodiversity alterations caused by increased
anthropogenic climate change19. It also adds a further component to the sustained efforts to establish the combination
of factors that define the ?profile? (i.e., shared combinations of traits) of species that have entered a current phase
of extinction risk (or, on the other hand, of species which have seen their populations remain stable or even
increase) as a result of environmental alterations.
At a more general level, the pathway towards species declines is a function of alterations to the ecological and
demographic stability of populations, which can occur due to different mechanisms. For example, as a
consequence of loss of their suitable distributional area, which can erode the genetic diversity to respond to rapidly
changing selection regimes42,50?52. However, other species may not be experiencing shrinking of their geographic
ranges, and yet, may still face demographic alterations via other mechanisms such as novel forms of
competition with species in newly encountered assemblages53, or exposure to climatically suitable, but not necessarily
structurally suitable (e.g., topographically) environments. Therefore, range shifts in diverse directions rather than
towards higher latitudes (Fig.?1) are expected to impact on the ecological and demographic stability of those
species by exposing them to novel environments and networks of species where selection regimes will be different.
In some cases, these impacts may lead to population declines and thus, to increased risk of extinction via factors
not necessarily connected directly with changing temperatures. For instance, a recent study on Liolaemus lizards
showed that, in contrast with the traditionally established ?cold-climate hypothesis? that declines in environmental
temperatures operate as drivers of natural selection for viviparity32,54, reductions in atmospheric oxygen levels
play a central role as agents of selection, promoting embryo retention and evolution of viviparity34. Whether
oxygen levels influence the magnitude and direction of alterations in range shifts of viviparous species via their
interactions with thermal gradients remains an open question. However, this ?hypoxia? hypothesis contributes
to the more general view that species? range stability can be broken down into interactions between a range of
external factors (e.g., climate, topography) and population features (e.g., abundance, morphology, life-history,
physiology). Future studies could develop predictions about the effects of environmental factors on parity modes
taking into account this strong role of oxygen, in combination with classic ecophysiological factors. Such
predictions could expand the findings of, for example, Medina et al. Medina, et al.29, who observed that the preferred
body temperature in the laboratory (Tpref) does not differ among Liolaemus species with different parity models
(while, however, field body temperature in the laboratory (Tpref) does not differ among Liolaemus species with
different parity models (while, however, field body temperature, Tb, does).
This study adds a further conceptual and empirical layer to the urgent need to develop ?profiles? of species
facing risks of extinction. These profiles aim to summarize our current understanding of factors that contribute
to altering the historical stability of populations, and thus, to reinforce the efficiency of actions developed to
mitigate ongoing declines of biodiversity. However, one of the main limitations of this study is the bias generated by
not considering the extremely endemic species in our analysis, which is related to the lack of enough geographic
information to predict the potential distribution of these species.
Overall, this study shows that life-history adaptations, favoured by natural selection, can turn into
determinant factors pushing species to decline under contemporary climate change. Life-history traits, given their direct
effects on fitness, are therefore primary candidate traits to disentangle factors that contribute to extinction, and
thus must be incorporated into empirical and theoretical studies aiming to develop estimations of climate change
effects on life on earth.
Species geographic distribution. We gathered a large-scale dataset encompassing three lizard radiations
differing in their patterns of geographic distribution and in parity modes, which spans large species-samples of
Liolaemus (40 oviparous and 52 viviparous species), Phymaturus (11 species, exclusively viviparous ? although
our dataset contained data for most species within this genus, we excluded most of them given their extremely
limited geographic range sizes, which makes it inviable to perform the analyses employed to address our core
predictions), and Stenocercus (40 species, exclusively oviparous) (Supplementary Fig.?S1). The distributional
and life-history data comprise 4,532 geographic occurrence records (after all duplicated points collected from
different individuals at same localities were removed). This includes all known records of presence of these
lizards following 20+ years of field and museum work, and museum-validated published occurrences45,47,55?61.
All the occurrences were individually checked and confirmed by experts (i.e., Daniel Pincheira-Donoso:
Liolaemus + Phymaturus and Omar Torres-Carvajal: Stenocercus, to assure accuracy).
Environmental predictors. To analyse the environmental space occupied by lizard lineages, we used the
bioclimatic variables characterizing climate during the 1970?2000 period, obtained from the WorldClim 2 data
repository62 (available at: http://www.worldclim.org/version2) at a spatial resolution of 30 seconds (~1 km). To
reduce collinearity between the environmental variables, we used VIF (Variance Inflation Factors) implemented
in the ?usdm? R-package63. Using this approach, we excluded all the highly correlated variables from the model
(VIF greater than 10), which is associated with a signal that the model has a collinearity problem64. This method
is based on the square of the multiple correlation coefficient (R2) resulting from regressing the predictor variable
against all other predictor variables. We used the remaining uncorrelated variables to calibrate models: mean
annual temperature (bio1), mean diurnal range (bio2), isothermality (bio3), temperature seasonality (bio4),
max temperature of warmest month (bio5), min temperature of coldest month (bio6), temperature annual range
(bio7), mean temperature of warmest quarter (bio10), mean temperature of coldest quarter (bio11), annual
precipitation (bio12) precipitation of wettest month (bio13), precipitation of driest month (bio14), and precipitation
seasonality (bio15), precipitation of wettest quarter (bio16), and precipitation of driest quarter (bio17).
To explore the occupation of environmental space by Liolaemus, Phymaturus, and Stenocercus and their
reproductive modes, we performed a principal component analysis (PCA) of present-day climate conditions in South
America using NicheA v3.0 software65 (available at: http://nichea.sourceforge.net), an open-source application
that analyses ecological niches (or ?climatic spaces?) in both environmental and geographic space (Supplementary
To estimate impacts of climate change on distributions of species, we employed two models of future climate
conditions, the GISS-ER and the MIROC5 general circulation models for the period around 2070 (2061?2080).
Each model consists of two Representative Concentration Pathways (RCPs) versions representing a stringent
mitigation scenario (RCP2.6, which predicts magnitude of climatic variation for the parameters of the model) and
one scenario assuming high anthropogenic greenhouse gas (GHG) emissions (RCP8.5, which predicts the highest
magnitude of climatic change for the parameters of the model) as alternative scenarios of climate change66 (IPCC,
Fifth Assessment), because it is extremely likely that human activities caused more than half of the observed
increase in GMST (Global Mean Surface Temperature) from 1951 to 201067. We selected these models based on
their high resolution and incorporation of covariates68,69.
Species distribution modeling. Based on the occurrence data (Supplementary Fig.?1), we calibrated
Ecological Niche Models (ENMs) to estimate current and future potential distribution for each lizard species. To
mitigate oversampling effects in our model, occurrences were re-sampled to one point per pixel with respect to
the environmental grids. Coordinates were divided into two groups for calibration and other evaluation, based
on four quadrants with similar numbers of points, using two off-diagonal quadrants for calibration and two for
evaluation. ENMs were developed using Maxent 3.3.3k70, a presence-background software that estimates
environmental suitability via an index of similarity that resembles a heterogeneous occurrence process or logistic
regression function70,71. We used Maxent with clamping and extrapolation turned off (i.e., no prediction outside
the range of environmental conditions in the calibration areas). To facilitate interpretations, we used the relative
probability of presence as a proxy of environmental suitability71. Suitable area for each species was estimated as
a Boolean (presence/absence) map that was thresholded based on the minimum training presence72. To
determine the model parametrization with the best fit to the data available, we assessed six models for each species
under different regularization multiplier values (i.e., 0.5, 1, 5, 10, 15, and 20)73. Then, we assessed AIC (Akaike
Information Criterion; implemented in ENMTools74) values to choose the model with the best performance
(i.e., descriptive-model evaluation; Supplementary Table?S10). Once the models with the best fit were selected,
we assessed their performance using the software PartialROC74, considering an ? = 0.05 to determine whether
models anticipate independent occurrences better than by random expectations.
To determine changes between the current and future potential distributions, we identified the expansion,
contraction, and stability (?no change?) of areas predicted climatically suitable by using the SDM toolbox in
ArcGIS v.10.275. Direction of the potential distributional changes was calculated based on the centroid of the
species? potential ranges. We applied Rayleigh?s Test of Uniformity76 to compare direction of centroid shifts vs a
uniform circular distribution reflecting a null hypothesis of random centroid shifts. Rayleigh?s statistic quantifies
the angular dispersion among the vectors from 0 (representing uniform dispersion) to 1 (indicating complete
concentration in a single direction).
Finally, to determine the spatial relationships between oviparous and viviparous species, we quantified the
range overlap among the predicted distributions of oviparous and viviparous species. These calculations were
made using the predicted present-day and future SDMs under GISS-ER and the MIROC5 models and each
greenhouse emission scenarios (RCP 2.6 and 8.5).
Climate change impacts on life-histories. To determine effects of climate change on parity mode, we
performed an independent-sample t-test using the variables: (i) range extents of current and future ENMs, (ii)
magnitude and direction of distributions based on range centroids, and (iii) average elevation of current and
future ranges. Analyses were corrected for phylogenetic non-independence to test whether the predicted impacts
of climate change (i.e., as geographic range, centroid or elevational shifts) were statistically significant between
species with different parity mode (i.e., oviparous and viviparous), as well as among ?parity-by-taxonomy? groups
(i.e., Stenocercus, Liolaemus-oviparous, Liolaemus-viviparous and Phymaturus) using the fully-sampled
phylogeny of Squamates recently published by Tonini, et al.77 which spans all 143 species in our dataset. We performed
phylogenetic analyses (t-test and ANOVA) implemented in the R-package ?phytools?78. Additionally, to calculate
the differences between each independent pair of groups we applied ANOVA test with ?holm? post-hoc pairwise
method, owing to it is one of the most powerful multitests when the sample sizes of the groups are different, to
perform this analysis, we used the R-package ?DescTools?. These analyses were performed for the two models of
climate change (GISS-ER and MIROC5) and for each scenario of greenhouse gases emissions indicated above
(RCP 2.6 and 8.5). Finally, we performed a spatial autocorrelation analysis (Global Moran?s I) using the Spatial
Statistics toolbox in ArcGIS to evaluate whether geographic rage shifts were clustered, dispersed, or randomly
We thank A. Townsend Peterson for his valuable comments and suggestions to improve this manuscript. MJ
thanks the University of Lincoln?s School of Life Sciences for a PhD scholarship. DPD thanks the University of
Lincoln for a Research Investment Fund (RIF) Grant that supported this paper. RGR benefited from an FPI grant
number BES-2012-054387 (MICIIN-CGL2011-24150/BOS). LEE was supported by the Global Change Center
Seed Grant 2017-18.
Competing Interests: The authors declare no competing interests. Publisher?s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Additional Information Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-019-41670-8.