Metabolic consequences of sex reversal in two lizard species: a test of the like-genotype and like-phenotype hypotheses.

Vertebrate sex is typically determined genetically, but in many ectotherms sex can be determined by genes (genetic sex determination, GSD), temperature (temperature-dependent sex determination, TSD), or interactions between genes and temperature during development. TSD may involve GSD systems with either male or female heterogamety (XX/XY or ZZ/ZW) where temperature overrides chromosomal sex determination to cause a mismatch between genetic sex and phenotypic sex (sex reversal). In these temperature-sensitive lineages, phylogenetic investigations point to recurrent evolutionary shifts between genotypic and temperature-dependent sex determination. These evolutionary transitions in sex determination can occur rapidly if selection favours the reversed sex over the concordant phenotypic sex. To investigate the consequences of sex reversal on offspring phenotypes, we measured two energy-driven traits (metabolism and growth) and 6 month survival in two species of reptile with different patterns of temperature-induced sex reversal. Male sex reversal occurs in Bassiana duperreyi when chromosomal females (female XX) develop male phenotypes (maleSR XX), while female sex reversal occurs in Pogona vitticeps when chromosomal males (male ZZ) develop female phenotypes (femaleSR ZZ). We show metabolism in maleSR XX was like that of male XY; that is, reflective of phenotypic sex and lower than genotypic sex. In contrast, for Pogona vitticeps, femaleSR ZZ metabolism was intermediate between male ZZ and female ZW metabolic rate. For both species, our data indicate that differences in metabolism become more apparent as individuals become larger. Our findings provide some evidence for an energetic advantage from sex reversal in both species but do not exclude energetic processes as a constraint on the distribution of sex reversal in nature.

Developmental environments do not affect thermal physiological traits in reptiles: an experimental test and meta-analysis.

On a global scale, organisms face significant challenges due to climate change and anthropogenic disturbance. In many ectotherms, developmental and physiological processes are sensitive to changes in temperature and resources. Developmental plasticity in thermal physiology may provide adaptive advantages to environmental extremes if early environmental conditions are predictive of late-life environments. Here, we conducted a laboratory experiment to test how developmental temperature and maternal resource investment influence thermal physiological traits (critical thermal maximum: CTmax and thermal preference: Tpref) in a common skink (Lampropholis delicata). We then compared our experimental findings more broadly across reptiles (snakes, lizards and turtles) using meta-analysis. In both our experimental study and meta-analysis, we did not find evidence that developmental environments influence CTmax or Tpref. Furthermore, the effects of developmental environments on thermal physiology did not vary by age, taxon or climate zone (temperate/tropical). Overall, the magnitude of developmental plasticity on thermal physiology appears to be limited across reptile taxa suggesting that behavioural or evolutionary processes may be more important. However, there is a paucity of information across most reptile taxa, and a broader focus on thermal performance curves themselves will be critical in understanding the impacts of changing thermal conditions on reptiles in the future.

Evolutionary stability inferred for a free ranging lizard with sex-reversal.

The sex of vertebrates is typically determined genetically, but reptile sex can also be determined by developmental temperature. In some reptiles, temperature interacts with genotype to reverse sex, potentially leading to transitions from a chromosomal to a temperature-dependent sex determining system. Transitions between such systems in nature are accelerated depending on the frequency and fitness of sex-reversed individuals. The Central Bearded Dragon, Pogona vitticeps, exhibits female heterogamety (ZZ/ZW) but can have its sex reversed from ZZ male to ZZ female by high incubation temperatures. The species exhibits sex-reversal in the wild and it has been suggested that climate change and fitness of sex-reversed individuals could be increasing the frequency of reversal within the species range. Transitions to temperature-dependent sex determination require low levels of dispersal and high (>50%) rates of sex-reversal. Here, we combine genotype-by-sequencing, identification of phenotypic and chromosomal sex, exhaustive field surveys, and radio telemetry to examine levels of genetic structure, rates of sex-reversal, movement, space use, and survival of P. vitticeps in a location previously identified as a hot spot for sex-reversal. We find that the species exhibits low levels of population structure (FST ~0.001) and a modest (~17%) rate of sex-reversal, and that sex-reversed and nonsex-reversed females have similar survival and behavioural characteristics to each other. Overall, our data indicate this system is evolutionary stable, although we do not rule out the prospect of a more gradual transition in sex-determining mechanisms in the future in a more fragmented landscape and as global temperatures increase.

Responses of a forest-dwelling terrestrial turtle, Terrapene Carolina, to prescribed fire in a Longleaf Pine ecosystem.

Prescribed fire is commonly used as a tool to meet a range of forest management goals. Owing to their limited movement abilities, terrestrial turtles are likely to be at high risk of injury and mortality, and to experience other fitness consequences with population-level implications from fire. Using radiotelemetry, we studied the responses of Eastern Box Turtles, Terrapene carolina carolina, to prescribed fire management in a sandhills Longleaf Pine forest system over a five-year period and compared our results to a nearby population in an unburned coastal plain location. Individual variation in turtle survival was strongly dependent on how frequently and extensively the areas were burned, with annual survival rates of 94.5% in unburned areas decreasing to 45.9 % in the most extensively burned areas. Turtles at the fire-maintained sandhills site had annual survival rates 4.9 % less than at the unburned coastal plain site, and females had annual survival rates 6.8 % less than males. Survival varied seasonally, with greatest mortality rates in winter and spring, especially among females. Growth rates and body condition did not differ between sites, nor did they vary according to fire extent and frequency at the fire-maintained site. Although mortality was greater and spatially variable at the fire-maintained site, annual survival rates across the site (86 - 90 % for females and males, respectively) were comparable to other stable populations of T. carolina. The lesser than expected mortality rate at the fire-maintained site was likely the result of turtles' strong selection of mesic hardwood forests near bottomlands and streams - habitats that may serve as refugia from fire. In areas where T. carolina conservation is a priority, land managers should integrate maintenance of fire refuge habitats into burn planning to minimize unintended negative impacts to this imperiled species.

Inter- and Intra-population Variation in Habitat Selection for a Forest-dwelling Terrestrial Turtle, Terrapene carolina carolina.

Habitat selection, where observed use of a resource is disproportionate to availability, is an important behavior allowing individuals to position themselves spatially relative to critical resources in heterogeneous environments. For species that experience variable environments across broad geographic ranges, we expect resource selection templates to vary among populations accordingly. Using radiotelemetry, we examined habitat selection for populations of Eastern Box Turtles, Terrapene carolina, in fire-maintained forests of the sandhills compared to nearby unburned coastal plain forests in south-central North Carolina. Turtles at the fire-maintained sandhills site preferred bottomland habitats and areas near steams, whereas turtles in the unburned coastal plain environment preferred uplands and used streams randomly. In addition, turtles in the fire-maintained sandhills avoided Longleaf Pine and more strongly preferred hardwood and non-Longleaf Pine forests compared to turtles at the unburned coastal plain site. Body size, but not sex, was also an important source of variation in habitat selection within populations, with smaller turtles more strongly preferring areas near water. Selection of habitat structural components in the immediate area of locations did not differ between sites, sexes, or body sizes. These results highlight the variety of resource selection templates in T. carolina, underscoring a potential need for population- or region-specific conservation and management strategies.

Thermal biology of eastern box turtles in a longleaf pine system managed with prescribed fire.

Fire can influence the microclimate of forest habitats by removing understory vegetation and surface debris. Temperature is often higher in recently burned forests owing to increased light penetration through the open understory. Because physiological processes are sensitive to temperature in ectotherms, we expected fire-maintained forests to improve the suitability of the thermal environment for turtles, and for turtles to seasonally associate with the most thermally-optimal habitats. Using a laboratory thermal gradient, we determined the thermal preference range (Tset) of eastern box turtles, Terrapene carolina, to be 27-31°C. Physical models simulating the body temperatures experienced by turtles in the field revealed that surface environments in a fire-maintained longleaf pine forest were 3°C warmer than adjacent unburned mixed hardwood/pine forests, but the fire-maintained forest was never of superior thermal quality owing to wider Te fluctuations above Tset and exposure to extreme and potentially lethal temperatures. Radiotracked turtles using fire-managed longleaf pine forests maintained shell temperatures (Ts) approximately 2°C above those at a nearby unburned forest, but we observed only moderate seasonal changes in habitat use which were inconsistent with thermoregulatory behavior. We conclude that turtles were not responding strongly to the thermal heterogeneity generated by fire in our system, and that other aspects of the environment are likely more important in shaping habitat associations.