Genetically Encoded Lizard Color Divergence for Camouflage and Thermoregulation.

Local adaptation is critical in speciation and evolution, yet comprehensive studies on proximate and ultimate causes of local adaptation are generally scarce. Here, we integrated field ecological experiments, genome sequencing, and genetic verification to demonstrate both driving forces and molecular mechanisms governing local adaptation of body coloration in a lizard from the Qinghai-Tibet Plateau. We found dark lizards from the cold meadow population had lower spectrum reflectance but higher melanin contents than light counterparts from the warm dune population. Additionally, the colorations of both dark and light lizards facilitated the camouflage and thermoregulation in their respective microhabitat simultaneously. More importantly, by genome resequencing analysis, we detected a novel mutation in Tyrp1 that underpinned this color adaptation. The allele frequencies at the site of SNP 459# in the gene of Tyrp1 are 22.22% G/C and 77.78% C/C in dark lizards and 100% G/G in light lizards. Model-predicted structure and catalytic activity showed that this mutation increased structure flexibility and catalytic activity in enzyme TYRP1, and thereby facilitated the generation of eumelanin in dark lizards. The function of the mutation in Tyrp1 was further verified by more melanin contents and darker coloration detected in the zebrafish injected with the genotype of Tyrp1 from dark lizards. Therefore, our study demonstrates that a novel mutation of a major melanin-generating gene underpins skin color variation co-selected by camouflage and thermoregulation in a lizard. The resulting strong selection may reinforce adaptive genetic divergence and enable the persistence of adjacent populations with distinct body coloration.

Collective effects of rising average temperatures and heat events on oviparous embryos.

Survival of the immobile embryo in response to rising temperature is important to determine a species' vulnerability to climate change. However, the collective effects of 2 key thermal characteristics associated with climate change (i.e., rising average temperature and acute heat events) on embryonic survival remain largely unexplored. We used empirical measurements and niche modeling to investigate how chronic and acute heat stress independently and collectively influence the embryonic survival of lizards across latitudes. We collected and bred lizards from 5 latitudes and incubated their eggs across a range of temperatures to quantify population-specific responses to chronic and acute heat stress. Using an embryonic development model parameterized with measured embryonic heat tolerances, we further identified a collective impact of embryonic chronic and acute heat tolerances on embryonic survival. We also incorporated embryonic chronic and acute heat tolerance in hybrid species distribution models to determine species' range shifts under climate change. Embryos' tolerance of chronic heat (T-chronic) remained consistent across latitudes, whereas their tolerance of acute heat (T-acute) was higher at high latitudes than at low latitudes. Tolerance of acute heat exerted a more pronounced influence than tolerance of chronic heat. In species distribution models, climate change led to the most significant habitat loss for each population and species in its low-latitude distribution. Consequently, habitat for populations across all latitudes will shift toward high latitudes. Our study also highlights the importance of considering embryonic survival under chronic and acute heat stresses to predict species' vulnerability to climate change.

Efectos colectivos del aumento de las temperaturas promedio y los eventos de calor en embriones ovíparos Resumen La supervivencia de los embriones inmóviles en respuesta al incremento de temperatura es importante para determinar la vulnerabilidad de las especies al cambio climático. Sin embargo, los efectos colectivos de dos características térmicas claves asociadas con el cambio climático (i. e., aumento de temperatura promedio y eventos de calor agudo) sobre la supervivencia embrionaria permanecen en gran parte inexplorados. Utilizamos mediciones empíricas y modelos de nicho para investigar cómo el estrés térmico crónico y agudo influye de forma independiente y colectiva en la supervivencia embrionaria de los lagartos en todas las latitudes. Recolectamos y criamos lagartos de cinco latitudes e incubamos sus huevos en un rango de temperaturas para cuantificar las respuestas específicas de la población al estrés por calor crónico y agudo. Posteriormente, mediante un modelo de desarrollo embrionario parametrizado con mediciones de tolerancia embrionaria al calor, identificamos un impacto colectivo de las tolerancias embrionarias al calor agudo y crónico en la supervivencia embrionaria. También incorporamos la tolerancia embrionaria crónica y aguda al calor en modelos de distribución de especies híbridas para determinar los cambios de distribución de las especies bajo el cambio climático. La tolerancia embrionaria al calor crónico (T­crónico) permaneció constante, mientras que la tolerancia al calor agudo (T­agudo) fue mayor en latitudes altas que en latitudes bajas. La tolerancia al calor agudo ejerció una influencia más pronunciada que la tolerancia al calor crónico. En los modelos de distribución de especies, el cambio climático provocó la pérdida de hábitat más significativa para cada población y especie en su distribución de latitudes bajas. En consecuencia, el hábitat para poblaciones en todas las latitudes se desplazará a latitudes altas. Nuestro estudio también resalta la importancia de considerar la supervivencia embrionaria bajo estrés térmico crónico y agudo para predecir la vulnerabilidad de las especies al cambio climático.

Chromosome-level genome assembly and population genomics of Mongolian racerunner (Eremias argus) provide insights into high-altitude adaptation in lizards.

BACKGROUND: Although the extreme environmental adaptation of organisms is a hot topic in evolutionary biology, genetic adaptation to high-altitude environment remains poorly characterized in ectothermic animals. Squamates are among the most diverse terrestrial vertebrates, with tremendous ecological plasticity and karyotype diversity, and are a unique model system to investigate the genetic footprints of adaptation. RESULTS: We report the first chromosome-level assembly of the Mongolian racerunner (Eremias argus) and our comparative genomics analyses found that multiple chromosome fissions/fusions events are unique to lizards. We further sequenced the genomes of 61 Mongolian racerunner individuals that were collected from altitudes ranging from ~ 80 to ~ 2600 m above sea level (m.a.s.l.). Population genomic analyses revealed many novel genomic regions under strong selective sweeps in populations endemic to high altitudes. Genes embedded in those genomic regions are mainly associated with energy metabolism and DNA damage repair pathways. Moreover, we identified and validated two substitutions of PHF14 that may enhance the lizards' tolerance to hypoxia at high altitudes. CONCLUSIONS: Our study reveals the molecular mechanism of high-altitude adaptation in ectothermic animal using lizard as a research subject and provides a high-quality lizard genomic resource for future research.

State-dependent movement choices of desert lizards: The role of behavioural thermoregulation during summer and winter.

Environmental temperatures are increasing worldwide, threatening desert ectotherms already living at their thermal limits. Organisms with flexible thermoregulatory behaviours may be able to mitigate the effects of extreme temperatures by moving among microhabitats, yet little work has tracked movement patterns of desert ectotherms in the wild over diurnal scales or compared behaviour among seasons. Here, we used camera traps to track the thermoregulatory behaviour and microhabitat choices of 30 desert lizards (Messalina bahaldini) in custom, outdoor arenas that provided access to open, rock, and bush microhabitats. We found that in the summer, lizards preferred to move to the shaded microhabitats and remain there under warmer conditions. During winter, however, lizards' activity was not related to temperature, and lizards mostly chose to remain in the open habitat. Interestingly, in both seasons, lizards tended to remain in their current microhabitat and moved infrequently between certain combinations of microhabitats. Our study shows that thermoregulation (shade-seeking behaviour) is a major factor during summer, helping lizards to avoid extreme temperatures, but not during winter, and shows a novel effect of current microhabitat on movement, suggesting that other biotic or abiotic factors may also drive microhabitat choice. Understanding the complex factors at play in microhabitat choice is critical for developing conservation programs that effectively mitigate the negative impacts of climate change on desert animals.

Ancient Demographics Determine the Effectiveness of Genetic Purging in Endangered Lizards.

The purging of deleterious alleles has been hypothesized to mitigate inbreeding depression, but its effectiveness in endangered species remains debatable. To understand how deleterious alleles are purged during population contractions, we analyzed genomes of the endangered Chinese crocodile lizard (Shinisaurus crocodilurus), which is the only surviving species of its family and currently isolated into small populations. Population genomic analyses revealed four genetically distinct conservation units and sharp declines in both effective population size and genetic diversity. By comparing the relative genetic load across populations and conducting genomic simulations, we discovered that seriously deleterious alleles were effectively purged during population contractions in this relict species, although inbreeding generally enhanced the genetic burden. However, despite with the initial purging, our simulations also predicted that seriously deleterious alleles will gradually accumulate under prolonged bottlenecking. Therefore, we emphasize the importance of maintaining a minimum population capacity and increasing the functional genetic diversity in conservation efforts to preserve populations of the crocodile lizard and other endangered species.

Oxidative stress mediates the impact of heatwaves on survival, growth and immune status in a lizard.

Climate change often includes increases in the occurrence of extreme environmental events. Among these, heatwaves affect the pace of life and performance of wildlife, particularly ectothermic animals, owing to their low thermoregulatory abilities. However, the underlying mechanisms by which this occurs remain unclear. Evidence shows that heatwaves alter the redox balance of ectotherms, and oxidative stress is a major mediator of life-history trade-offs. Therefore, oxidative stress may mediate the effect of extreme thermal conditions on the life histories of ectotherms. To test this hypothesis, a 2 × 2 experiment was conducted to manipulate the redox balance (through a mitochondrial uncoupler that alleviates oxidative stress) of the desert toad-headed agama (Phrynocephalus przewalskii) exposed to heatwave conditions. We recorded lizard growth and survival rates and quantified their redox and immune statuses. In control lizards (unmanipulated redox balance), heatwave conditions decreased growth and survival and induced oxidative damage and immune responses. By contrast, lizards with alleviated oxidative stress showed close-to-normal growth, survival, and immune status when challenged with heatwaves. These results provide mechanistic insight into the role of oxidative stress in mediating the effects of extreme temperatures on ectothermic vertebrates, which may have major eco-evolutionary implications.

Cool shade and not-so-cool shade: How habitat loss may accelerate thermal stress under current and future climate.

Worldwide habitat loss, land-use changes, and climate change threaten biodiversity, and we urgently need models that predict the combined impacts of these threats on organisms. Current models, however, overlook microhabitat diversity within landscapes and so do not accurately inform conservation efforts, particularly for ectotherms. Here, we built and field-parameterized a model to examine the effects of habitat loss and climate change on activity and microhabitat selection by a diurnal desert lizard. Our model predicted that lizards in rock-free areas would reduce summer activity levels (e.g. foraging, basking) and that future warming will gradually decrease summer activity in rocky areas, as even large rocks become thermally stressful. Warmer winters will enable more activity but will require bushes and small rocks as shade retreats. Hence, microhabitats that may seem unimportant today will become important under climate change. Modelling frameworks should consider the microhabitat requirements of organisms to improve conservation outcomes.

Distinct responses and range shifts of lizard populations across an elevational gradient under climate change.

Ongoing climate change has profoundly affected global biodiversity, but its impacts on populations across elevations remain understudied. Using mechanistic niche models incorporating species traits, we predicted ecophysiological responses (activity times, oxygen consumption and evaporative water loss) for lizard populations at high-elevation (<3600 m asl) and extra-high-elevation (≥3600 m asl) under recent (1970-2000) and future (2081-2100) climates. Compared with their high-elevation counterparts, lizards from extra-high-elevation are predicted to experience a greater increase in activity time and oxygen consumption. By integrating these ecophysiological responses into hybrid species distribution models (HSDMs), we were able to make the following predictions under two warming scenarios (SSP1-2.6, SSP5-8.5). By 2081-2100, we predict that lizards at both high- and extra-high-elevation will shift upslope; lizards at extra-high-elevation will gain more and lose less habitat than will their high-elevation congeners. We therefore advocate the conservation of high-elevation species in the context of climate change, especially for those populations living close to their lower elevational range limits. In addition, by comparing the results from HSDMs and traditional species distribution models, we highlight the importance of considering intraspecific variation and local adaptation in physiological traits along elevational gradients when forecasting species' future distributions under climate change.

Divergent effects of climate change on the egg-laying opportunity of species in cold and warm regions.

Climate warming can substantially impact embryonic development and juvenile growth in oviparous species. Estimating the overall impacts of climate warming on oviparous reproduction is difficult because egg-laying events happen throughout the reproductive season. Successful egg laying requires the completion of embryonic development as well as hatching timing conducive to offspring survival and energy accumulation. We propose a new metric-egg-laying opportunity (EO)-to estimate the annual hours during which a clutch of freshly laid eggs yields surviving offspring that store sufficient energy for overwintering. We estimated the EO within the distribution of a model species, Sceloporus undulatus, under recent climate condition and a climate-warming scenario by combining microclimate data, developmental functions, and biophysical models. We predicted that EO will decline as the climate warms at 74.8% of 11,407 sites. Decreasing hatching success and offspring energy accounted for more lost EO hours (72.6% and 72.9%) than the occurrence of offspring heat stress (59.9%). Nesting deeper (at a depth of 12 cm) may be a more effective behavioral adjustment for retaining EO than using shadier (50% shade) nests because the former fully mitigated the decline of EO under the considered warming scenario at more sites (66.1%) than the latter (28.3%). We advocate for the use of EO in predicting the impacts of climate warming on oviparous animals because it encapsulates the integrative impacts of climate warming on all stages of reproductive life history.

Efectos divergentes del cambio climático sobre la oportunidad de desove de las especies en regiones cálidas y frías Resumen El calentamiento global puede tener un impacto considerable sobre el desarrollo embrionario y el crecimiento juvenil de las especies ovíparas. Es complicado estimar el impacto general que tiene el calentamiento global sobre la reproducción ovípara ya que los eventos de desove suceden durante la época reproductiva. El desove exitoso requiere que se complete el desarrollo embrionario y que el momento de eclosión sea favorable para la supervivencia de las crías y la acumulación de energía. Proponemos una nueva medida-oportunidad de desove (OD)-para estimar las horas anuales durante las cuales una puesta de huevos recién desovados produce crías que sobreviven y almacenan suficiente energía para invernar. Estimamos la OD dentro de un modelo de distribución de la especie Sceloporus undulatus bajo las recientes condiciones climáticas y bajo un escenario de calentamiento global mediante la combinación de datos microclimáticos, funciones del desarrollo y modelos biofísicos. Pronosticamos que la OD declinará conforme la temperatura aumente en 74.8% de los 11407 sitios. La disminución del éxito de eclosión y de la energía de las crías explicó más horas perdidas de OD (72.6% y 72.9%) que la presencia de estrés por calor en las crías (59.9%). Una anidación más profunda (a una profundidad de 12 cm) puede ser un ajuste conductual más efectivo para la retención de la OD que los nidos con mayor sombreado (50% de sombra) porque el primero mitigó por completo la declinación de la OD bajo el escenario de calentamiento en más sitios (66.1%) que el segundo ajuste (28.3%). Defendemos el uso de la OD en el pronóstico del impacto del calentamiento global sobre los animales ovíparos porque encapsula los impactos integrales que tiene el calentamiento global sobre todas las etapas de la vida reproductiva. 气候变化在寒冷和温暖地区对物种产卵机会造成不同影响.

Temperate and tropical lizards are vulnerable to climate warming due to increased water loss and heat stress.

Climate warming has imposed profound impacts on species globally. Understanding the vulnerabilities of species from different latitudinal regions to warming climates is critical for biological conservation. Using five species of Takydromus lizards as a study system, we quantified physiological and life-history responses and geography range change across latitudes under climate warming. Using integrated biophysical models and hybrid species distribution models, we found: (i) thermal safety margin is larger at high latitudes and is predicted to decrease under climate warming for lizards at all latitudes; (ii) climate warming will speed up embryonic development and increase annual activity time of adult lizards, but will exacerbate water loss of adults across all latitudes; and (iii) species across latitudes are predicted to experience habitat contraction under climate warming due to different limitations-tropical and subtropical species are vulnerable due to increased extremely high temperatures, whereas temperate species are vulnerable due to both extremely high temperatures and increased water loss. This study provides a comprehensive understanding of the vulnerability of species from different latitudinal regions to climate warming in ectotherms, and also highlights the importance of integrating environmental factors, behaviour, physiology and life-history responses in predicting the risk of species to climate warming.

The eggshell-matrix protein gene OC-17 is functionally lost in the viviparous Chinese crocodile lizard.

Thickness reduction or loss of the calcareous eggshell is one of major phenotypic changes in the transition from oviparity to viviparity. Whether the reduction of eggshells in viviparous squamates is associated with specific gene losses is unknown. Taking advantage of a newly generated high-quality genome of the viviparous Chinese crocodile lizard (Shinisaurus crocodilurus), we found that ovocleidin-17 gene (OC-17), which encodes an eggshell matrix protein that is essential for calcium deposition in eggshells, is not intact in the crocodile lizard genome. Only OC-17 transcript fragments were found in the oviduct transcriptome, and no OC-17 peptides were identified in the eggshell proteome of crocodile lizards. In contrast, OC-17 was present in the eggshells of the oviparous Mongolia racerunner (Eremias argus). Although the loss of OC-17 is not common in viviparous species, viviparous squamates show fewer intact eggshell-specific proteins than oviparous squamates. Our study implies that functional loss of eggshell-matrix protein genes may be involved in the reduction of eggshells during the transition from oviparity to viviparity in the crocodile lizard.

Effects of climate and human activity on the current distribution of amphibians in China.

In China, as elsewhere, amphibians are highly endangered. Anthropogenic environmental change has affected the distribution and population dynamics of species, and species distributions at a broad scale are strongly driven by climate and species' ability to disperse. Yet, current knowledge remains limited on how widespread human activity affects the distribution patterns of amphibians in China and whether this effect extends beyond climate. We compiled a relatively comprehensive database on the distribution of 196 amphibian species in China from the literature, public databases, and field data. We obtained 25,826 records on almost 50% of known species in China. To test how environmental factors and human activities influence the current distribution of amphibians (1960-1990), we used range filling, which is species realized ranges relative to their potential climate distribution. We used all species occurrence records to represent realized range and niche models to predict potential distribution range. To reduce uncertainty, we used 3 regression methods (beta regression, generalized boosted regression models, and random forest) to test the associations of species range filling with human activity, climate, topography, and range size. The results of the 3 approaches were consistent. At the species level, mean annual precipitation (climate) had the most effect on spatial distribution pattern of amphibians in China, followed by range size. Human activity ranked last. At the spatial level, mean annual precipitation remained the most important factor. Regions in southeastern of China that are currently moist supported the highest amphibian diversity, but were predicted to experience a decline in precipitation under climate change scenarios. Consequently, the distributions of amphibians will likely shift to the northwest in the future, which could affect future conservation efforts.

En China, como en todos lados, los anfibios están gravemente en peligro. El cambio ambiental antropogénico ha afectado la distribución y dinámica poblacional de especies, y la distribución de especies a gran escala están muy influidas por el clima y la habilidad de dispersión de las especies. Sin embargo, el conocimiento actual sigue siendo limitado sobre cómo la actividad humana generalizada afecta a los patrones de distribución de anfibios en China y si este efecto se extiende más allá del clima. A partir de literatura, bases de datos públicas y datos de campo, integramos una base datos relativamente completa sobre la distribución de 196 especies de anfibios en China. Obtuvimos 25,826 registros de casi 50% de las especies conocidas en China. Para probar cómo los factores ambientales y las actividades humanas influyen en la distribución actual de anfibios (1960-1990), utilizamos la ocupación de rango, que contrasta los rangos de distribución observada de las especies en relación con su distribución climática potencial. Utilizamos los registros de ocurrencia de todas las especies para representar el rango observado y modelos de nicho para predecir el rango de distribución potencial. Para reducir la incertidumbre, utilizamos 3 métodos de regresión (regresión beta, modelos de regresión acelerada generalizada y bosque aleatorio) para probar las asociaciones de la ocupación de rango de especies con la actividad humana, clima, topografía y extensión de rango. Los resultados de los tres métodos fueron consistentes. A nivel de especie, la precipitación media anual (clima) tuvo el mayor efecto sobre el patrón de distribución de anfibios en China, seguida por la extensión del rango. La actividad humana ocupó el último lugar. A nivel espacial, la precipitación media anual siguió como el factor más importante. Las regiones en el sureste de China que aun son húmedas sostuvieron la mayor diversidad de anfibios, pero se pronosticó que la precipitación declinará bajo escenarios de cambio climático. Consecuentemente, la distribución de anfibios muy probablemente cambiará hacia el noreste, lo cual podría afectar esfuerzos futuros de conservación.

Grow fast but don't die young: Maternal effects mediate life-history trade-offs of lizards under climate warming.

As postulated by life-history theory, not all life-history traits can be maximized simultaneously. In ectothermic animals, climate warming is predicted to increase growth rates, but at a cost to overall life span. Maternal effects are expected to mediate this life-history trade-off, but such effects have not yet been explicitly elucidated. To understand maternal effects on the life-history responses to climate warming in lizard offspring, we conducted a manipulative field experiment on a desert-dwelling viviparous lacertid lizard Eremias multiocellata, using open-top chambers in a factorial design (maternal warm climate and maternal present climate treatments × offspring warm climate and offspring present climate treatments). We found that the maternal warm climate treatment had little impact on the physiological and life-history traits of adult females (i.e. metabolic rate, reproductive output, growth and survival). However, the offspring warm climate treatment significantly affected offspring growth, and both maternal and offspring warm climate treatments interacted to affect offspring survival. Offspring from the warm climate treatment grew faster than those from the present climate treatment. However, the offspring warm climate treatment significantly decreased the survival rate of offspring from maternal present climate treatment, but not for those from the maternal warm climate treatment. Our study demonstrates that maternal effects mediate the trade-off between growth and survival of offspring lizards, allowing them to grow fast without a concurrent cost of low survival rate (short life span). These findings stress the importance of adaptive maternal effects in buffering the impact of climate warming on organisms, which may help us to accurately predict the vulnerability of populations and species to future warming climates.

Effects of hypoxia on the thermal physiology of a high-elevation lizard: implications for upslope-shifting species.

Montane reptiles are predicted to move to higher elevations in response to climate warming. However, whether upwards-shifting reptiles will be physiologically constrained by hypoxia at higher elevations remains unknown. We investigated the effects of hypoxic conditions on preferred body temperatures (Tpref) and thermal tolerance capacity of a montane lizard (Phrynocephalus vlangalii) from two populations on the Qinghai-Tibet Plateau. Lizards from 2600 m a.s.l. were exposed to O2 levels mimicking those at 2600 m (control) and 3600 m (hypoxia treatment). Lizards from 3600 m a.s.l. were exposed to O2 levels mimicking those at 3600 m (control) and 4600 m (hypoxia treatment). The Tpref did not differ between the control and hypoxia treatments in lizards from 2600 m. However, lizards from 3600 m selected lower body temperatures when exposed to the hypoxia treatment mimicking the O2 level at 4600 m. Additionally, the hypoxia treatment induced lower critical thermal minimum (CTmin) in lizards from both populations, but did not affect the critical thermal maximum (CTmax) in either population. Our results imply that upwards-shifting reptiles may be constrained by hypoxia if a decrease in Tpref reduces thermally dependent fitness traits, despite no observed effect on their heat tolerance.

Population origin, maternal effects, and hydric conditions during incubation determine embryonic and offspring survival in a desert-dwelling lizard.

While the effects of incubation environment on embryonic development and offspring traits have been extensively studied in oviparous vertebrates, studies into how genetic inheritance (population origin), maternal effects, and incubation environment interact to produce varying phenotypes, are rare. To elucidate the interactive role of those three factors during incubation in shaping offspring phenotypes through hydric conditions, we conducted a fully factorial experiment [arid and semiarid populations × maternal dry and wet treatments (MDT and MWT) × embryonic dry and wet treatments (EDT and EWT)] with a desert-dwelling lacertid lizard (Eremias argus). Female lizards in dry conditions produced larger clutch sizes but smaller eggs. The incubation period and hatching success were significantly affected by embryonic but not by maternal moisture treatments. Eggs in the EDT hatched later than those in the EWT in both arid and semiarid populations. Hatching success was lower in EDT than in EWT in the semiarid population, but not in the arid population. Hatchlings from the EDT had a slower post-hatch increase in body mass than those from the EWT. EDT would decrease the survival rates of hatchlings in the semiarid population only. In addition, structural equation models revealed that population had a stronger effect on embryonic and offspring survival than maternal and embryonic moisture. Our study demonstrates locally adaptive strategies of drought resistance at multiple life-history stages in lizard populations from diverse hydric habitats and highlights the importance of genetic factors in determining embryonic drought resistance in oviparous lizards.

A reciprocal egg-swap experiment reveals sources of variation in developmental success among populations of a desert lizard.

Identifying intrinsic and extrinsic sources of variation in life history traits among populations has been well-studied at the post-embryonic stage but rarely at the embryonic stage. To reveal these sources of variation in the developmental success of embryos, we measured the physical characteristics of nest environments and conducted reciprocal egg-swap experiments in two populations of the toad-headed agamid lizard (Phrynocephalus przewalskii), isolated from each other by a mountain range. We determined the effects of population origin and nest environment on embryonic and offspring traits related to developmental success, including incubation period, hatching success, and offspring growth and survival. Females from the northern population constructed deeper nests that were colder and wetter than those from the southern population. Northern embryos had higher hatching success than the southern embryos when incubated at the northern nest environment, but not when they were incubated at the southern nest environment. The southern hatchlings grew faster than the northern hatchlings when incubated at the southern nest environment, but not after incubation at the northern nest environment. These phenomena likely reflect local adaptation of embryonic development to their nest environments among populations in lizards. In addition, the southern hatchlings had higher survivorship than the northern hatchlings regardless of nest environment, suggesting the southern population has evolved a superior phenotype at the hatchling stage to maximize its fitness.

Behavioural thermoregulation by the endangered crocodile lizard (Shinisaurus crocodilurus) in captivity.

Understanding the factors that may affect behavioural thermoregulation of endangered reptiles is important for their conservation because thermoregulation determines body temperatures and in turn physiological functions of these ectotherms. Here we measured seasonal variation in operative environmental temperature (Te), body temperature (Tb), and microhabitat use of endangered crocodile lizards (Shinisaurus crocodilurus) from a captive population, within open and shaded enclosures, to understand how they respond to thermally challenging environments. Te was higher in open enclosures than in shaded enclosures. The Tb of lizards differed between the open and shaded enclosures in summer and autumn, but not in spring. In summer, crocodile lizards stayed in the water to avoid overheating, whereas in autumn, crocodile lizards perched on branches seeking optimal thermal environments. Crocodile lizards showed higher thermoregulatory effectiveness in open enclosures (with low thermal quality) than in shaded enclosures. Our study suggests that the crocodile lizard is capable of behavioural thermoregulation via microhabitat selection, although overall, it is not an effective thermoregulator. Therefore, maintaining diverse thermal environments in natural habitats for behavioural thermoregulation is an essential measure to conserve this endangered species both in the field and captivity.

Adaptive responses of the embryos of birds and reptiles to spatial and temporal variations in nest temperatures.

Natural nests of egg-laying birds and reptiles exhibit substantial thermal variation, at a range of spatial and temporal scales. Rates and trajectories of embryonic development are highly sensitive to temperature, favouring an ability of embryos to respond adaptively (i.e. match their developmental biology to local thermal regimes). Spatially, thermal variation can be significant within a single nest (top to bottom), among adjacent nests (as a function of shading, nest depth etc.), across populations that inhabit areas with different weather conditions, and across species that differ in climates occupied and/or nest characteristics. Thermal regimes also vary temporally, in ways that generate differences among nests within a single population (e.g. due to seasonal timing of laying), among populations and across species. Anthropogenic activities (e.g. habitat clearing, climate change) add to this spatial and temporal diversity in thermal regimes. We review published literature on embryonic adaptations to spatio-temporal heterogeneity in nest temperatures. Although relatively few taxa have been studied in detail, and proximate mechanisms remain unclear, our review identifies many cases in which natural selection appears to have fine-tuned embryogenesis to match local thermal regimes. Developmental rates have been reported to differ between uppermost versus lower eggs within a single nest, between eggs laid early versus late in the season, and between populations from cooler versus warmer climates. We identify gaps in our understanding of thermal adaptations of early (embryonic) phases of the life history, and suggest fruitful opportunities for future research.

Impacts of maternal characteristics and temperature on juvenile survival in the crocodile lizard: Implications for conservation.

Captive breeding is an important conservation measure that may restore and enhance wild populations of rare and endangered species. Multiple anthropogenic hazards have brought the crocodile lizard, Shinisaurus crocodilurus, to the brink of extinction. We initiated a captive breeding program and quantified female reproductive traits, including reproductive timing, litter size, litter mass, and neonate size. To identify the internal and external factors affecting female reproductive function, we then analyzed how maternal age is related to body size, temperature, and female reproductive traits. We found that larger female crocodile lizards produced more offspring than smaller ones, as both litter size and litter mass were positively related to maternal body size. In contrast, neonate size was independent of maternal body size. Maternal reproductive output varied among different age groups. Young and old females had significantly smaller living litter size and mass than middle-aged females. Among captive females, one-third exhibited early parturition in autumn and winter instead of the following spring, a pattern probably associated with higher ambient temperatures in captivity. Although female reproductive output and neonatal body size did not differ between early- and normal-parturition females, offspring from the former group died earlier than those from the latter. Our study highlights the danger of climate change in hastening parturition, a phenomenon that could significantly hamper neonate survival and impede population recruitment.

Anticipatory parental effects in a subtropical lizard in response to experimental warming.

Parental effects may produce adaptive or maladaptive plasticity that either facilitates persistence or increases the extinction risk of species and populations in a changing climate. However, empirical evidence of transgenerational adaptive plastic responses to climate change is still scarce. Here we conducted thermal manipulation experiments with a factorial design in a Chinese lacertid lizard (Takydromus septentrionalis) to identify the fitness consequences of parental effects in response to climate warming. Compared to present climate conditions, a simulated warming climate significantly advanced the timing of oviposition, depressed the immune capability of post-partum females, and decreased the hatching success of embryos, but did not affect female reproductive output (clutch size and egg mass). These results indicate that maternal warming negatively affects female health, and embryonic hatchability. More interestingly, we found that offspring from parents exposed to warming environments survived well under a simulated warming climate, but not under a present climate scenario. Accordingly, our study demonstrates anticipatory parental effects in response to a warming climate in an ectothermic vertebrate. However, the fitness consequences of this parental effect will depend on future climate change scenarios.