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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
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Abstract Many ectotherms rely on temperature cues experienced during development to determine offspring sex. The first descriptions of temperature‐dependent sex determination (TSD) were made over 50 years ago, yet an understanding of its adaptive significance remains elusive, especially in long‐lived taxa.
One novel hypothesis predicts that TSD should be evolutionarily favoured when two criteria are met—(a) incubation temperature influences annual juvenile survival and (b) sexes mature at different ages. Under these conditions, a sex‐dependent effect of incubation temperature on offspring fitness arises through differences in age at sexual maturity, with the sex that matures later benefiting disproportionately from temperatures that promote juvenile survival.
The American alligator (
Alligator mississippiensis ) serves as an insightful model in which to test this hypothesis, as males begin reproducing nearly a decade after females. Here, through a combination of artificial incubation experiments and mark‐recapture approaches, we test the specific predictions of the survival‐to‐maturity hypothesis for the adaptive value of TSD by disentangling the effects of incubation temperature and sex on annual survival of alligator hatchlings across two geographically distinct sites.Hatchlings incubated at male‐promoting temperatures (MPTs) consistently exhibited higher survival compared to those incubated at female‐promoting temperatures. This pattern appears independent of hatchling sex, as females produced from hormone manipulation at MPT exhibit similar survival to their male counterparts.
Additional experiments show that incubation temperature may affect early‐life survival primarily by affecting the efficiency with which maternally transferred energy resources are used during development.
Results from this study provide the first explicit empirical support for the adaptive value of TSD in a crocodilian and point to developmental energetics as a potential unifying mechanism underlying persistent survival consequences of incubation temperature.
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null (Ed.)Synopsis An organism’s ability to integrate transient environmental cues experienced during development into molecular and physiological responses forms the basis for adaptive shifts in phenotypic trajectories. During temperature-dependent sex determination (TSD), thermal cues during discrete periods in development coordinate molecular changes that ultimately dictate sexual fate and contribute to patterns of inter- and intra-sexual variation. How these mechanisms interface with dynamic thermal environments in nature remain largely unknown. By deploying thermal loggers in wild nests of the American alligator (Alligator mississippiensis) over two consecutive breeding seasons, we observed that 80% of nests exhibit both male- and female-promoting thermal cues during the thermosensitive period, and of these nests, all exhibited both male- and female-promoting temperatures within the span of a single day. These observations raise a critical question—how are opposing environmental cues integrated into sexually dimorphic transcriptional programs across short temporal scales? To address this question, alligator embryos were exposed to fluctuating temperatures based on nest thermal profiles and sampled over the course of a daily thermal fluctuation. We examined the expression dynamics of upstream genes in the temperature-sensing pathway and find that post-transcriptional alternative splicing and transcript abundance of epigenetic modifier genes JARID2 and KDM6B respond rapidly to thermal fluctuations while transcriptional changes of downstream effector genes, SOX9 and DMRT1, occur on a delayed timescale. Our findings reveal how the basic mechanisms of TSD operate in an ecologically relevant context. We present a hypothetical hierarchical model based on our findings as well as previous studies, in which temperature-sensitive alternative splicing incrementally influences the epigenetic landscape to affect the transcriptional activity of key sex-determining genes.more » « less
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null (Ed.)Species displaying temperature-dependent sex determination (TSD) are especially vulnerable to the effects of a rapidly changing global climate due to their profound sensitivity to thermal cues during development. Predicting the consequences of climate change for these species, including skewed offspring sex ratios, depends on understanding how climatic factors interface with features of maternal nesting behaviour to shape the developmental environment. Here, we measure thermal profiles in 86 nests at two geographically distinct sites in the northern and southern regions of the American alligator's ( Alligator mississippiensis ) geographical range, and examine the influence of both climatic factors and maternally driven nest characteristics on nest temperature variation. Changes in daily maximum air temperatures drive annual trends in nest temperatures, while variation in individual nest temperatures is also related to local habitat factors and microclimate characteristics. Without any compensatory nesting behaviours, nest temperatures are projected to increase by 1.6–3.7°C by the year 2100, and these changes are predicted to have dramatic consequences for offspring sex ratios. Exact sex ratio outcomes vary widely depending on site and emission scenario as a function of the unique temperature-by-sex reaction norm exhibited by all crocodilians. By revealing the ecological drivers of nest temperature variation in the American alligator, this study provides important insights into the potential consequences of climate change for crocodilian species, many of which are already threatened by extinction.more » « less
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Abstract 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 (
Alligator mississippiensis ) are long‐lived apex predators that rely on incubation temperature during a discrete period during development and endocrine cues to determine sex, making them especially vulnerable to current climatic variability and exposure to anthropogenic contaminants interfering with hormone function. Here, we combine field studies with a factorial design to understand how the developmental environment, along with intrinsic biological variation contribute to persistent telomere variation. We found that exposure to a common endocrine disrupting contaminant, DDE, affects telomere length, but that the directionality is highly dependent upon incubation temperature. Variation in hatchling growth, underlies a strong clutch effect. We also assess concentrations of a panel of glucocorticoid hormones and find that contaminant exposure elicits an increase in circulating glucocorticoids. Consistent with emerging evidence linking stress and aging trajectories, GC levels also appear to trend with shorter telomere length. Thus, we add support for a mechanistic link between contaminants and glucocorticoid signalling, which interacts with ecological aspects of the developmental environment to alter telomere dynamics. -
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Abstract Contaminants such as mercury are pervasive and can have immunosuppressive effects on wildlife. Impaired immunity could be important for forecasting pathogen spillover, as many land‐use changes that generate mercury contamination also bring wildlife into close contact with humans and domestic animals. However, the interactions among contaminants, immunity and infection are difficult to study in natural systems, and empirical tests of possible directional relationships remain rare.
We capitalized on extreme mercury variation in a diverse bat community in Belize to test association among contaminants, immunity and infection. By comparing a previous dataset of bats sampled in 2014 with new data from 2017, representing a period of rapid agricultural land conversion, we first confirmed bat species more reliant on aquatic prey had higher fur mercury. Bats in the agricultural habitat also had higher mercury in recent years. We then tested covariation between mercury and cellular immunity and determined if such relationships mediated associations between mercury and bacterial pathogens. As bat ecology can dictate exposure to mercury and pathogens, we also assessed species‐specific patterns in mercury–infection relationships.
Across the bat community, individuals with higher mercury had fewer neutrophils but not lymphocytes, suggesting stronger associations with innate immunity. However, the odds of infection for haemoplasmas and
Bartonella spp. were generally lowest in bats with high mercury, and relationships between mercury and immunity did not mediate infection patterns. Mercury also showed species‐ and clade‐specific relationships with infection, being associated with especially low odds for haemoplasmas inPteronotus mesoamericanus andDermanura phaeotis . ForBartonella spp., mercury was associated with particularly low odds of infection in the genusPteronotus but high odds in the subfamily Stenodermatinae.Synthesis and application . Lower general infection risk in bats with high mercury despite weaker innate defense suggests contaminant‐driven loss of pathogen habitat (i.e. anemia) or vector mortality as possible causes. Greater attention to these potential pathways could help disentangle relationships among contaminants, immunity and infection in anthropogenic habitats and help forecast disease risks. Our results also suggest that contaminants may increase infection risk in some taxa but not others, emphasizing the importance of considering surveillance and management at different phylogenetic scales.
