The mechanisms connecting environmental conditions to plasticity in biological aging trajectories are fundamental to understanding individual variation in functional traits and life history. Recent findings suggest that telomere biology is especially dynamic during early life stages and has long‐term consequences for subsequent reproduction and survival. However, our current understanding is mostly derived from studies investigating ecological and anthropogenic factors separately, leaving the effects of complex environmental interactions unresolved. American alligators (
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- NSF-PAR ID:
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- Molecular Ecology
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- p. 6114-6127
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- National Science Foundation
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null (Ed.)The environment experienced during embryonic development is a rich source of phenotypic variation, as environmental signals have the potential to both inform adaptive plastic responses and disrupt normal developmental programs. Environment-by-embryo interactions are particularly consequential for species with temperature-dependent sex determination, a mode of sex determination common in non-avian reptiles and fish, in which thermal cues during a discrete period of development drive the formation of either an ovary or a testis. Here we examine the impact of thermal variation during incubation in combination with developmental exposure to a common endocrine-disrupting contaminant on fitness-related hatchling traits in the American alligator (Alligator mississippiensis), a species with temperature-dependent sex determination. Using a factorial design, we exposed field-collected eggs to five thermal profiles (three constant temperatures, two fluctuating temperatures) and two environmentally relevant doses of the pesticide metabolite dichlorodiphenyldichloroethylene; and we quantified incubation duration, sex ratios, hatchling morphometric traits, and growth (9–10 days post-hatch). Whereas dichlorodiphenyldichloroethylene exposure did not generally affect hatchling traits, constant and fluctuating temperatures produced diverse phenotypic effects. Thermal fluctuations led to subtle changes in incubation duration and produced shorter hatchlings with smaller heads when compared to the constant temperature control. Warmer, male-promoting incubation temperatures resulted in larger hatchlings with more residual yolk reserves when compared to cooler, female-promoting temperatures. Together, these findings advance our understanding of how complex environmental factors interact with developing organisms to generate phenotypic variation and raise questions regarding the mechanisms connecting variable thermal conditions to responses in hatchling traits and their evolutionary implications for temperature-dependent sex determination.more » « less
A central objective of evolutionary biology is understanding variation in life‐history trajectories and the rate of aging, or senescence. Senescence can be affected by trade‐offs and behavioural strategies in adults but may also be affected by developmental stress. Developmental stress can accelerate telomere degradation, with long‐term longevity and fitness consequences. Little is known regarding whether variation in developmental stress and telomere dynamics contributes to patterns of senescence during adulthood. We investigated this question in the dimorphic white‐throated sparrow (
Zonotrichia albicollis), a species in which adults of the two morphs exhibit established differences in behavioural strategy and patterns of senescence, and also evaluated the relationship between oxidative stress and telomere length. Tan morph females, which exhibit high levels of unassisted parental care, display faster reproductive senescence than white females, and faster actuarial senescence than all of the other morph–sex classes. We hypothesized that high oxidative stress and telomere attrition in tan female nestlings could contribute to this pattern, since tan females are small and potentially at a competitive disadvantage even as nestlings. Nestlings that were smaller than nest mates had higher oxidative stress, and nestlings with high oxidative stress and fast growth rates displayed shorter telomeres. However, we found no consistent morph–sex differences in oxidative stress or telomere length. Results suggest that oxidative stress and fast growth contribute to developmental telomere attrition, with potential ramifications for adults, but that developmental oxidative stress and telomere dynamics do not account for morph–sex differences in senescence during adulthood.
An individual's telomere length early in life may reflect or contribute to key life‐history processes sensitive to environmental variation. Yet, the relative importance of genetic and environmental factors in shaping early‐life telomere length is not well understood as it requires samples collected from multiple generations with known developmental histories. We used a confirmed pedigree and conducted an animal model analysis of telomere lengths obtained from nestling house sparrows (
Passer domesticus) sampled over a span of 22 years. We found significant additive genetic variation for early‐life telomere length, but it comprised a small proportion (9%) of the total biological variation. Three sources of environmental variation were important: among cohorts, among‐breeding attempts within years, and among nestmates. The magnitude of variation among breeding attempts and among nestmates also differed by cohort, suggesting that interactive effects of environmental factors across time or spatial scales were important, yet we were unable to identify the specific causes of these interactions. The mean amount of precipitation during the breeding season positively predicted telomere length, but neither weather during a given breeding attempt nor date in the breeding season contributed to an offspring's telomere length. At the level of individual nestlings, offspring sex, size and mass at 10 days of age also did not predict telomere length. Environmental effects appear especially important in shaping early‐life telomere length in some species, and more focus on how environmental factors that interact across scales may help to explain some of the variation observed among studies.
Population‐scale responses of key ecological traits to local environmental conditions provide insight into their adaptive potential. In species with temperature‐dependent sex determination (TSD), short‐term, individual developmental responses to the incubation environment have long‐term consequences for populations.
We took a model‐based approach to study within‐ and among‐population variation in the physiological components of TSD in 12 populations of painted turtles (
Chrysemys picta). We used laboratory and field incubation data to quantify variation in thermal reaction norms at both population and clutch scales, focusing on the pivotal temperature that produces a 1:1 sex ratio ( P) and the transitional range of incubation temperatures (TRTs) that produce mixed sex ratios.
Defying theoretical expectations, among‐population variation in
Pwas not convincingly explained by geography or local thermal conditions. However, within some populations, Pvaried by >5°C at the clutch scale, indicating that the temperature sensitivity of gonadal differentiation can vary substantially among individual nesting females. In addition, the TRT was wider at lower latitudes, suggesting responsiveness to local incubation conditions.
Our results provide a potential explanation for discrepancies observed between constant‐temperature experimental results and outcomes of fluctuating incubation conditions experienced in natural nests, exposing important knowledge gaps in our understanding of local adaptation in TSD and identifying shortcomings of traditional laboratory studies. Understanding individual variation and the timing of gonadal differentiation is likely to be far more useful in understanding local adaptation than previously acknowledged.
Plain Language Summarycan be found within the Supporting Information of this article.
Phenotypic variation within populations is influenced by the environment via plasticity and natural selection. How phenotypes respond to the environment can vary among traits, populations and life stages in ways that can influence fitness.
Plastic responses during early development are particularly important because they can affect components of fitness throughout an individual's life. Consequently, how natural selection shapes developmental plasticity could be influenced by fitness consequences across different life stages. Moreover, spatial variation in selection pressures could generate differences in plastic responses among populations.
To gain insight into sources of variation in phenotypes and survival, we used a laboratory egg incubation experiment using brown anole lizards
Anolis sagreifrom mainland (ancestral) and island (descendent) populations, combined with a mark–release–recapture experiment in the field. Our study was designed to (a) quantify the effects developmental temperature on embryo development and offspring morphology, (b) assess how developmental temperature influences offspring survival across different life stages and (c) quantify how thermal reaction norms vary among ancestral and descendant populations.
Developmental temperature influenced offspring morphology, but thermal reaction norms of embryos showed little variation among populations. Developmental temperature influenced offspring survival, but the patterns differed between embryo and hatchling stages; the optimal temperature for embryos was about 5℃ lower than that for hatchlings. High temperatures were thermally stressful to embryos, but they reduced incubation duration and led to early hatching. In turn, earlier hatching increased the probability of survival to adulthood. Moreover, the effect of developmental temperature on hatchling survival was most pronounced for offspring that hatched late in the season.
The difference in optimal developmental temperatures between life stages may be driven by physiological tolerance for embryos and by ecological factors for hatchlings. Moreover, the fitness consequences of the developmental environment depend on the phenology of hatching. Overall, these results highlight how the developmental environment can differentially affect fitness across life stages and show that temporal thermal heterogeneity can influence survival of embryos, but the consequences on post‐hatching stages may vary at different times of the season.
Plain Language Summarycan be found within the Supporting Information of this article.