Variable juvenile growth rates and offspring size: a response to anthropogenic shifts in prey size among populations.

Environmental variables, such as resource quality, shape growth in organisms, dictating body size, an important correlate of fitness. Variation in prey characteristics among populations is frequently associated with similar variation in predator body sizes. Anthropogenic alterations to prey landscapes impose novel ecological pressures on predators that may shift predator phenotypes. Research has focused on determining the adaptability of the phenotypic response by testing its genetic heritability. Here, we asked if anthropogenic shifts in prey size across the landscape correlate with juvenile growth rates among populations of watersnakes with divergent life-history phenotypes. We sought to determine if growth rate variation is the product of genetic adaptation or a non-heritable phenotypic response. Using a common-garden design, we measured growth of neonate snakes from fish farms varying in prey size. We found juvenile growth rates are faster for snakes with larger initial body sizes and from populations with larger average prey sizes. Our data suggest variability in juvenile grow rates within and among populations are not the product of genetic adaptation, but the indirect consequence of initial offspring size variation and prey consumption. We propose larger offspring sizes may favor increased juvenile growth rates, mediated through a larger morphological capacity to consume and process energy resources relative to smaller individuals. This experiment provides evidence supporting the growing body of literature that non-heritable responses may be significant drivers of rapid phenotypic divergence among populations across a landscape. This mechanism may explain the stability and colonization of populations in response to rapid, human-mediated, landscape changes.

3D printed models are an accurate, cost-effective, and reproducible tool for quantifying terrestrial thermal environments.

Predicting ecological responses to rapid environmental change has become one of the greatest challenges of modern biology. One of the major hurdles in forecasting these responses is accurately quantifying the thermal environments that organisms experience. The distribution of temperatures available within an organism's habitat is typically measured using data loggers called operative temperature models (OTMs) that are designed to mimic certain properties of heat exchange in the focal organism. The gold standard for OTM construction in studies of terrestrial ectotherms has been the use of copper electroforming which creates anatomically accurate models that equilibrate quickly to ambient thermal conditions. However, electroformed models require the use of caustic chemicals, are often brittle, and their production is expensive and time intensive. This has resulted in many researchers resorting to the use of simplified OTMs that can yield substantial measurement errors. 3D printing offers the prospect of robust, easily replicated, morphologically accurate, and cost-effective OTMs that capture the benefits but alleviate the problems associated with electroforming. Here, we validate the use of OTMs that were 3D printed using several materials across eight lizard species of different body sizes and living in habitats ranging from deserts to tropical forests. We show that 3D printed OTMs have low thermal inertia and predict the live animal's equilibration temperature with high accuracy across a wide range of body sizes and microhabitats. Finally, we developed a free online repository and database of 3D scans (https://www.3dotm.org/) to increase the accessibility of this tool to researchers around the world and facilitate ease of production of 3D printed models. 3D printing of OTMs is generalizable to taxa beyond lizards. If widely adopted, this approach promises greater accuracy and reproducibility in studies of terrestrial thermal ecology and should lead to improved forecasts of the biological impacts of climate change.

Temporal climatic variability predicts thermal tolerance in two sympatric lizard species.

Thermal acclimatization, plastic shifts in thermal physiology in response to recent climatic conditions, is thought to be adaptive in highly seasonal environments where thermal variability is high but predictable. Thus, lizards from mid-latitude, desert environments should exhibit plasticity in their thermal tolerance limits, the upper (CTmax) and lower (CTmin) body temperatures they can withstand while maintaining physiological functioning, associated with changes in seasonal changes in climatic variation (i.e., when daily fluctuations in temperature are greater, lizards should have wider thermal tolerance breadths [CTmax-CTmin]). We measured the thermal tolerance limits of two Phrynosomatid lizard species, Uta stansburiana and Sceloporus tristichus, occurring in sympatry at three time points to test for temporal variation in thermal physiology in response to climatic variation. We found that lizards of both species measured during times when climatic variability was high had wider thermal tolerance breadths than lizards measured when climatic variability was lower. While CTmax was largely invariable, CTmin varied in response to minimum air temperature, driving the observed difference in thermal tolerance breadth among the sampling periods.

Developmental plasticity of thermal ecology traits in reptiles: Trends, potential benefits, and research needs.

A variety of phenotypic traits in reptiles are affected by conditions during embryonic development, a phenomenon known as developmental plasticity. In particular, many traits in which expression changes with temperature, such as locomotor performance or growth rates, are also developmentally plastic. However, much less is known about the extent to which traits associated with thermal ecology, such as thermal tolerance and behavioral thermoregulation, are developmentally plastic. Here, we review the literature on developmental plasticity in physiological and behavioral traits associated with thermal ecology in reptiles. Most studies on developmental plasticity of thermal traits have assessed plasticity in behavioral traits, such as selected temperature or time spent basking, and these studies have found mixed support for the presence of developmental plasticity in behavioral thermal traits. In contrast, very few studies have assessed developmental plasticity in physiological traits, yet these studies generally support a developmentally plastic basis for thermal tolerance. Most studies have only tested for developmental plasticity in thermal ecology traits at the hatchling stage, which limits our understanding of the benefits of developmental plasticity to individuals, or the adaptive significance of developmental plasticity in populations. We recommend that research on developmental plasticity in reptile thermal ecology be expanded to include incubation conditions other than mean temperature, consider traits associated with cold-tolerance, and endeavor to understand how developmental plasticity in thermal ecology traits is beneficial. In particular, determining how long differences persist over ontogeny, and testing for benefits of developmental plasticity across multiple life stages, are crucial first steps towards understanding the adaptive significance of developmental plasticity in thermal ecology traits.

Cellular and whole-organism effects of prolonged versus acute heat stress in a montane, desert lizard.

Global climate change involves both prolonged periods of higher-than-normal temperatures and short but extreme heat waves. Both types of temperature increases are likely to be detrimental to ectotherms, and even if such temperature increases do not cause mortality directly, compensating for such temperature increases will likely entail costs to organisms. We tested the effects of prolonged periods of higher-than-average temperatures and short-term, acute heat stress in wild populations of greater short-horned lizards (Phrynosoma hernandesi), a temperate, montane lizard of the Colorado Plateau, UT, USA. We transplanted one group of lizards from a high- to a low-elevation site, exposing them to a prolonged period of warmer temperatures. These lizards, exposed to prolonged periods of higher-than-average temperatures, experienced no change in sprint speed, endurance, or heat shock protein (HSP) production after treatment compared to baseline levels; however, they had lower water content after the transplant to a warmer climate compared to before the transplant. We exposed a second group of lizards to acute heat stress by exposing them to thermally stressful temperatures for 4 h. These lizards, exposed to a short period of acute heat stress, had no change in endurance, water content, or HSP production following acute heat stress; however, lizards exposed to acute heat stress had slower sprint speeds than control lizards. Our results demonstrate that both prolonged temperature increases and acute heat stress, each of which are predicted to occur with climate change, had different cellular and/or whole organismal-level effects on lizards.

Role of phenotypic plasticity in morphological differentiation between watersnake populations.

An individual's morphology is shaped by the environmental pressures it experiences, and the resulting morphological response is the culmination of both genetic factors and environmental (non-genetic) conditions experienced early in its life (i.e. phenotypic plasticity). The role that phenotypic plasticity plays in shaping phenotypes is important, but evidence for its influence is often mixed. We exposed female neonate diamond-backed watersnakes (Nerodia rhombifer) from populations experiencing different prey-size regimes to different feeding treatments to test the influence of phenotypic plasticity in shaping trophic morphology. We found that snakes in a large-prey treatment from a population frequently encountering large prey exhibited a higher growth rate in body size than individuals in a small-prey treatment from the same population. This pattern was not observed in snakes from a population that regularly encounters small prey. We also found that regardless of treatment, snakes from the small-prey population were smaller at birth than snakes from the large-prey population and remained so throughout the study. These results suggest that the ability to plastically respond to environmental pressures may be population-specific. These results also indicate a genetic predisposition towards larger body sizes in a population where large prey items are more common.