Daniel A. Warner

The environment can alter the physiological condition of parents during reproduction, resulting in variation in energy allocation that can affect offspring performance. In addition, differences in energy allocation can affect how offspring respond to their own environmental heterogeneity. Consequently, specific parental effects can alter the developmental plasticity of offspring when both parents and offspring experience environmental variation. In this study, we assess how offspring developmental plasticity is affected by parental allocation using a breeding colony of brown anoles (Anolis sagrei) that varied in their caloric intake. Mothers fed a high-food diet laid larger eggs and were more fecund than mothers fed a low-food diet. Embryos from these mothers were then incubated across a range of ecologically relevant developmental temperatures. The reaction norm of hatchling body size, a trait crucial for fitness across ontogeny, differed between eggs laid from high-food and low-food mothers, suggesting that parental effects alter the developmental plasticity of offspring. This effect might be driven by the combination of an energetic constraint on reproduction and a thermodynamic constraint on development. Our results suggest that environmental variation experienced by previous generations affects the capacity of future generations to respond to their own environments.

Although directional selection and additive genetic variance are frequently detected in wild populations, evolutionary responses are often weak or absent, giving rise to a “paradox of stasis.” To explore the relationship between selection and evolution, we used a pedigreed wild population of lizards (Anolis sagrei) to quantify natural selection, estimate additive genetic (co)variances, and track phenotypic and genetic change in adult body size while addressing several factors that could lead to evolutionary stasis. Selection via adult reproductive success consistently favored larger body size in both sexes and was stronger in males. Body size was heritable and genetically correlated with adult reproductive success in both sexes, indicating that selection acted on underlying additive genetic variance. Across five annual cohorts, mean phenotypic values and breeding values for body size increased in both sexes, exceeding expectations under genetic drift. This rapid evolutionary response was not obscured by several processes commonly invoked to explain stasis. For example, accounting for phenotypic skew strengthened expected responses, and prior viability selection on juveniles did not phenotypically or genetically oppose selection on adult body size. Our results show that rapid evolutionary change is detectable in the wild when directional selection is consistent, acts on additive genetic variance, and is not genetically opposed by early-life viability selection.

Using organismal-level data to predict population-level responses to climate change is a common, yet complicated challenge. Studies concerned with estimating the costs of living in warmer environments use designs that are often unable to quantitatively link their results to population persistence. Because of the reliance of ectotherms on environmental temperature to regulate metabolism and behavior, most aspects of their reproduction and survival are temperature sensitive. Consequently, relationships between the environment that parents experience during reproduction, the environment offspring experience during development, and interactions across generations can help us link changes in fitness-relevant phenotypes directly to population growth and recruitment. To that end, some experiments use multi-generational study designs to describe the effects of warming on current and future generations. These experiments provide more detail and accuracy on population-level responses to climate change than those that examine responses within a single generation, and we stand to learn much from the continued use and development of multi-generational experiments to describe responses to climate change. In this Review, we examine the multi-generational effects of climate change on ectothermic animals, focusing on the ecophysiological consequences of warming, and the evidence for transgenerational phenotypic plasticity. In addition to reviewing the breadth of transgenerational climate change studies, we highlight some persistent gaps that future work could be well poised to address.

Conditions experienced during early life stages may influence an array of fitness‐relevant phenotypes, especially in oviparous ectotherms. The pond slider ( Trachemys scripta ) has two life stages particularly vulnerable to the influence of ambient conditions: the egg stage and hatchling overwintering stage. We aimed to determine the influence of both incubation temperature and overwinter environment on hatchling turtle performance. In 2019 and 2020, we incubated pond slider eggs at five constant temperatures (24°C, 26°C, 28°C, 30°C, 32°C). After hatching, turtles were distributed to two housing treatments that simulated overwintering in a terrestrial nest or an aquatic environment. In the spring following hatching, we conducted righting response trials, which are frequently used performance measures that may be associated with coordination and neuromuscular function. Our linear mixed‐effects models show that incubation temperature, overwinter environment, and their interaction significantly influenced hatchling phenotypes (e.g., shell and tail dimensions, body mass) and righting performance (e.g., total righting response time, latency to right). Aquatically overwintering hatchlings that were incubated at cooler temperatures righted themselves faster than those incubated at warmer temperatures. This relationship did not exist in terrestrially overwintering hatchlings, which had faster overall righting times that were not affected by incubation temperature, suggesting overwintering in the nest may better equip hatchlings for post‐emergence dispersals over land.

Populations during early stages of establishment are sensitive to forms of demographic regulation coinciding with rapid growth, which may also coincide with specific patterns of natural selection due to demographic variation. Understanding how selection varies during the establishment of new populations, however, is complicated by the constraint of knowing the precise age of a population as it grows over time. To address this, we established six brown anole (Anolis sagrei) populations on spoil islands in Florida and manipulated initial sex ratios to understand how natural selection is influenced by the demographic composition of founding populations. We found that initial sex ratios of founding populations led to age-specific patterns of natural selection. Juveniles experienced stronger selection in populations that began with a female-biased sex ratio, and the strength of natural selection on juvenile size strengthened with increasing population density. We also found substantial variation in selection, suggesting that the relationship between phenotypes and fitness across early generations of a population is not consistent over time. As a result, variation in natural selection driven by demographic aspects within populations may provide opportunities for rapid population growth and novel evolutionary trajectories during the earliest stages of establishment.

Theory predicts that thermal developmental plasticity evolves in response to thermal heterogeneity, suggesting that plasticity may be an important trait for establishment in novel climates. However, few studies use multispecies comparisons to examine how plasticity evolves, meaning that there is little empirical basis with which to examine key theoretical predictions. We estimate patterns of thermal developmental plasticity in morphological and performance traits for 7 Anolis lizard species inhabiting South Florida, USA. We found interspecific differences as well as intraspecific variation in reaction norms across species. Neither temperature heterogeneity in present-day invasive ranges in Florida nor historical temperature heterogeneity from the contemporary native ranges predicted reaction norm variation. Phylogeny and species identity typically predicted around 90%–95% of reaction norm variation. Overall, these results suggest that thermal developmental plasticity in these traits exhibits variation that could be inconsistent with patterns expected under adaptive evolution to macroclimate. Examining the role of maternal nesting behavior and sampling of additional species can help to distinguish between neutral variation and selection toward multiple adaptive peaks. Our comparative study of thermal developmental plasticity in lizards provides new insights about macroevolutionary dynamics behind the evolution of developmental plasticity and the conditions under which adaptive plasticity is expected to evolve.

The embryonic environment is critical for the development of many ectothermic vertebrates, which makes them highly vulnerable to environmental change. Changes in temperature and moisture, in particular, are known to influence embryo survival and offspring phenotypes. Although most papers concerning phenotypic development of terrestrial ectotherms focus on the role of temperature on eggs and embryos, the comparatively small number of studies on the effects of substrate moisture are well suited for quantitative analysis aimed at guiding future research. To accomplish this goal, we compiled data from 37 studies on 28 different reptile species and used a meta-analytic approach to quantify the effect of substrate moisture on several offspring outcomes: hatching success (survival), incubation duration, hatchling mass and length, and sex ratio. We found that substrate moisture had a small effect across most traits but significantly affected body size (i.e. length and mass), with wetter conditions producing longer and heavier hatchlings. Temperature also moderated the effect of moisture on hatching success, with higher temperatures resulting in lower success. Additionally, the effect of moisture on hatching success and hatchling mass was enhanced by larger differences in moisture concentration between treatments, yet the effect was small. Lastly, substrate moisture affected sex ratio in turtles, but not in other squamates. Overall, these analyses provide a foundation for further research investigating the effects of moisture on oviparous reptile development. Increasing the diversity of environmental variables for which we understand their impact on animal phenotype will be beneficial in an era with wide-ranging global change.

Water availability has critical impacts on numerous physiological functions in all organisms and can have different effects across life stages. For example, water available to reproductive females can influence offspring production, and has the potential to influence how early‐stage offspring (e.g., embryos) respond to moisture in their developmental environment. In this study, we use the brown anole lizard (Anolis sagrei) to examine the effects of water availability on reproductive investment. We tested the hypothesis that water available to mothers influences embryonic development under different levels of moisture in their incubation environment. We demonstrate that a substantial reduction in water availability to mothers (~70% reduction) has no observable effect on fecundity, egg size, or egg hydration. We also provide evidence that our water restriction to mothers does not influence how embryos respond to moisture conditions during egg incubation. However, moisture in the egg incubation substrate positively affected egg water uptake, egg hatching success and hatchling body size (but not hatchling hydration). Overall, our study shows that reproduction in adult female A. sagrei is robust to variation in water availability, but survival during early life stages is sensitive to this variable. Thus, the effect of water availability on different fitness components varies between life stages.

Developmental plasticity is the capacity of a single genotype to express multiple phenotypes in response to different early‐life environments. Such responses are defined by reaction norms, which may vary among individuals or populations. Variation in developmental reaction norms allows natural selection to operate on plasticity and is rarely examined in vertebrates. We quantified variation in embryonic developmental plasticity within and between populations using the brown anole lizard. We captured lizards from two islands in the Matanzas River (Florida, USA) and incubated their eggs under one of two multivariate treatments that mimicked the temperature, moisture and substrates of nest sites in either a shaded or open habitat. We measured hatchling morphology, performance, and physiology to quantify variation in family‐level reaction norms. We observed evidence of family‐level variation in reaction norms for morphology but not for performance or physiology, indicating an opportunity for natural selection to shape plasticity in hatchling body size. Overall, the results indicate that multiple abiotic conditions in natural nests combine to increase or reduce phenotypic variation, and that family‐level variation in reaction norms provides a potential for natural selection to shape plasticity.