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Sex Determination and Ovarian Development in Reptiles and Amphibians: From Genetic Pathways to Environmental InfluencesBackground: Reptiles and amphibians provide untapped potential for discovering how a diversity of genetic pathways and environmental conditions are incorporated into developmental processes that can lead to similar functional outcomes. These groups display a multitude of reproductive strategies, and whereas many attributes are conserved within groups and even across vertebrates, several aspects of sexual development show considerable variation. Summary: In this review, we focus our attention on the development of the reptilian and amphibian ovary. First, we review and describe the events leading to ovarian development, including sex determination and ovarian maturation, through a comparative lens. We then describe how these events are influenced by environmental factors, focusing on temperature and exposure to anthropogenic chemicals. Lastly, we identify critical knowledge gaps and future research directions that will be crucial to moving forward in our understanding of ovarian development and the influences of the environment in reptiles and amphibians. Key Messages: Reptiles and amphibians provide excellent models for understanding the diversity of sex determination strategies and reproductive development. However, a greater understanding of the basic biology of these systems is necessary for deciphering the adaptive and potentially disruptive implications of embryo-by-environment interactions in a rapidly changing world.Free, publicly-accessible full text available November 15, 2023
Genome‐wide DNA methylation patterns harbour signatures of hatchling sex and past incubation temperature in a species with environmental sex determinationAbstract Conservation of thermally sensitive species depends on monitoring organismal and population‐level responses to environmental change in real time. Epigenetic processes are increasingly recognized as key integrators of environmental conditions into developmentally plastic responses, and attendant epigenomic data sets hold potential for revealing cryptic phenotypes relevant to conservation efforts. Here, we demonstrate the utility of genome‐wide DNA methylation (DNAm) patterns in the face of climate change for a group of especially vulnerable species, those with temperature‐dependent sex determination (TSD). Due to their reliance on thermal cues during development to determine sexual fate, contemporary shifts in temperature are predicted to skew offspring sex ratios and ultimately destabilize sensitive populations. Using reduced‐representation bisulphite sequencing, we profiled the DNA methylome in blood cells of hatchling American alligators ( Alligator mississippiensis ), a TSD species lacking reliable markers of sexual dimorphism in early life stages. We identified 120 sex‐associated differentially methylated cytosines (DMCs; FDR < 0.1) in hatchlings incubated under a range of temperatures, as well as 707 unique temperature‐associated DMCs. We further developed DNAm‐based models capable of predicting hatchling sex with 100% accuracy (in 20 training samples and four test samples) and past incubation temperature with a mean absolute error of 1.2°C (in four testmore »Free, publicly-accessible full text available November 1, 2023
Transcriptional networks underlying a primary ovarian insufficiency disorder in alligators naturally exposed to EDCsFree, publicly-accessible full text available November 1, 2023
Acute Copper Toxicity Displays a Nonmonotonic Relationship with Age Across the Medaka ( Oryzias latipes ) Life Span
The ability of an organism to cope with environmental stressors varies across the life span because of developmental stage–specific responses and age‐related functional declines. In the present study, we examined the effect of age on acute copper toxicity in Japanese medaka (
Oryzias latipes). We first determined the median lethal concentration (LC50) at 96 h for embryos, 7‐day‐old fry, and 6‐month‐old medaka. Embryos were exposed to 0, 15, 30, 60, 125, 250, and 500 ppb CuSO4through hatching. Fry were exposed to 0, 20, 50, 75, 100, 150, 250, and 500 ppb CuSO4for 96 h. Adult fish were exposed to 0, 100, 150, 200, 250, and 300 ppb CuSO4for 96 h. The 96‐h LC50 was 804 ppb for embryos, 262 ppb for embryonically exposed larvae, 60.3 ppb for 7‐day‐old fry, and 226 ppb for adults. We then challenged cohorts of fish aged 2, 3, 5, 6, 7, 8, 9, 10, 11, 13, 14, 15, and 16 months with a 225‐ppb CuSO4exposure to determine the acute toxicity across the life span. The fish exhibited a bimodal tolerance to copper, with tolerance peaking in 2‐ and 3‐month‐old fish and again at 10 and 11 months of age. Our data demonstrate that copper sensitivity is dynamic throughout the medaka life span and may bemore »
Differential early‐life survival underlies the adaptive significance of temperature‐dependent sex determination in a long‐lived reptile
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 manipulationmore »
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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Incubation Temperature and Maternal Resource Provisioning, but Not Contaminant Exposure, Shape Hatchling Phenotypes in a Species with Temperature-Dependent Sex DeterminationThe 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 withmore »
Transient Copper Exposure During Embryogenesis and Temperature Affect Developmental Rate, Survival, and Fin Regeneration in Japanese Medaka ( Oryzias latipes )
Combined environmental stressors that an organism experiences can have both immediate and lasting consequences. In the present study, we exposed Japanese medaka (
Oryzias latipes) embryos to sublethal copper sulfate (CuSO4; 0, 10, and 100 ppb) in combination with different rearing temperatures (27, 30, and 33 °C) to assess acute and latent effects on development, growth, and regenerative capacity. Embryos exposed to CuSO4and/or higher temperatures hatched significantly earlier. At 4 months post‐exposure, fish exposed to low levels of CuSO4during development had higher survival, whereas fish exposed to both 100 ppb CuSO4and 33 °C temperatures had significantly lower survival. In addition, a sex‐specific effect of embryonic CuSO4exposure was observed as female mass decreased with increasing Cu dose. We also assessed caudal fin regenerative capabilities in both embryo‐exposed fish at 4 months of age and adult medaka that were exposed to 0, 10, and 100 ppb CuSO4at room temperature during a 14‐day trial. Whereas fin regeneration was unaffected by adult exposure to Cu, fish transiently exposed during embryogenesis displayed an initial increase in fin growth rate and an increased incidence of abnormal fin morphology following regrowth. Collectively, these data suggest that developmental Cu exposure has the potential to exert long‐lasting impacts to organismal growth, survival, and function. Environmore »2022;41:748–757. © 2021 SETAC
Spatial and temporal variation in nest temperatures forecasts sex ratio skews in a crocodilian with environmental sex determinationSpecies 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 themore »