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Maternal hormones such as estrogens deposited into the yolk of turtle eggs follow circulating levels in adult females, and they may alter the sexual fate of developing embryos in species with temperature-dependent sex determination (TSD). In temperate regions, this deposition occurs during the spring when estrogens increase in adult females as ambient temperatures rise, drop after the first clutch, and peak again (albeit less) in the fall. Global warming alters turtle nesting phenology (inducing earlier nesting), but whether it affects circulating hormones remains unknown, hindering our understanding of all potential challenges posed by climate change and the adaptive potential (or lack thereof) of turtle populations. Here, we addressed this question in painted turtles (Chrysemys picta) by quantifying estradiol, estrone, and testosterone via mass spectrometry in the blood of wild adult females exposed to 26 °C and 21 °C in captivity between mid-August and mid-October (15 females per treatment). Results from ANOVA and pairwise comparisons revealed no differences between treatments in circulating hormones measured at days 0, 2, 7, 14, 28, and 56 of the experiment. Further research is warranted (during the spring, using additional temperatures) before concluding that females are truly buffered against the indirect risk of climate change via maternal hormone allocation. 

Temperature-dependent sex determination (TSD) decides the sex fate of an individual based on incubation temperature. However, other environmental factors, such as pollutants, could derail TSD sexual development. Cadmium is one such contaminant of soils and water bodies known to affect DNA methylation, an epigenetic DNA modification with a key role in sexual development of TSD vertebrate embryos. Yet, whether cadmium alters DNA methylation of genes underlying gonadal formation in turtles remains unknown. Here, we investigated the effects of cadmium on the expression of two gene regulators of TSD in the painted turtle, Chrysemys picta, incubated at male-producing and female-producing temperatures using qPCR. Results revealed that cadmium alters transcription of Dmrt1 and aromatase, overriding the normal thermal effects during embryogenesis, which could potentially disrupt the sexual development of TSD turtles. Results from a preliminary DNA methylation-sensitive PCR assay implicate changes in DNA methylation of Dmrt1 as a potential cause that requires further testing (aromatase methylation assays were precluded). 

During meiotic prophase I, tightly regulated processes take place, from pairing and synapsis of homologous chromosomes to recombination, which are essential for the generation of genetically variable haploid gametes. These processes have canonical meiotic features conserved across different phylogenetic groups. However, the dynamics of meiotic prophase I in non-mammalian vertebrates are poorly known. Here, we compare four species from Sauropsida to understand the regulation of meiotic prophase I in reptiles: the Australian central bearded dragon ( Pogona vitticeps ), two geckos ( Paroedura picta and Coleonyx variegatus ) and the painted turtle ( Chrysemys picta ). We first performed a histological characterization of the spermatogenesis process in both the bearded dragon and the painted turtle. We then analyzed prophase I dynamics, including chromosome pairing, synapsis and the formation of double strand breaks (DSBs). We show that meiosis progression is highly conserved in reptiles with telomeres clustering forming the bouquet , which we propose promotes homologous pairing and synapsis, along with facilitating the early pairing of micro-chromosomes during prophase I (i.e., early zygotene). Moreover, we detected low levels of meiotic DSB formation in all taxa. Our results provide new insights into reptile meiosis. 

Understanding genome‐wide responses to environmental conditions during embryogenesis is essential for discerning the evolution of developmental plasticity and canalization, two processes generating phenotypic variation targeted by natural selection. Here, we present the first comparative trajectory analysis of matched transcriptomic developmental time series from two reptiles incubated under identical conditions, a turtle with a ZZ/ZW system of genotypic sex determination (GSD),Apalone spinifera, and a turtle with temperature‐dependent sex determination (TSD),Chrysemys picta. Results from our genome‐wide, hypervariate gene expression analysis of sexed embryos across five developmental stages revealed that substantial transcriptional plasticity in the developing gonads can persist for >145 Myr, long after the canalization of sex determination via the evolution of sex chromosomes, while some gene‐specific thermal sensitivity drifts or evolves anew. Such standing thermosensitivity represents an underappreciated evolutionary potential harbored by GSD species that may be co‐opted during future adaptive shifts in developmental programing, such as a GSD to TSD reversal, if favored by ecological conditions. Additionally, we identified novel candidate regulators of vertebrate sexual development in GSD reptiles, including sex‐determining candidate genes in a ZZ/ZW turtle.

 

Triggers and biological processes controlling male or female gonadal differentiation vary in vertebrates, with sex determination (SD) governed by environmental factors or simple to complex genetic mechanisms that evolved repeatedly and independently in various groups. Here, we review sex evolution across major clades of vertebrates with information on SD, sexual development and reproductive modes. We offer an up-to-date review of divergence times, species diversity, genomic resources, genome size, occurrence and nature of polyploids, SD systems, sex chromosomes, SD genes, dosage compensation and sex-biased gene expression. Advances in sequencing technologies now enable us to study the evolution of SD at broader evolutionary scales, and we now hope to pursue a sexomics integrative research initiative across vertebrates. The vertebrate sexome comprises interdisciplinary and integrated information on sexual differentiation, development and reproduction at all biological levels, from genomes, transcriptomes and proteomes, to the organs involved in sexual and sex-specific processes, including gonads, secondary sex organs and those with transcriptional sex-bias. The sexome also includes ontogenetic and behavioural aspects of sexual differentiation, including malfunction and impairment of SD, sexual differentiation and fertility. Starting from data generated by high-throughput approaches, we encourage others to contribute expertise to building understanding of the sexomes of many key vertebrate species. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’. 

Global climate is warming rapidly, threatening vertebrates with temperature-dependent sex determination (TSD) by disrupting sex ratios and other traits. Less understood are the effects of increased thermal fluctuations predicted to accompany climate change. Greater fluctuations could accelerate feminization of species that produce females under warmer conditions (further endangering TSD animals), or counter it (reducing extinction risk). Here we use novel experiments exposing eggs of Painted Turtles (Chrysemys picta) to replicated profiles recorded in field nests plus mathematically-modified profiles of similar shape but wider oscillations, and develop a new mathematical model for analysis. We show that broadening fluctuations around naturally male-producing (cooler) profiles feminizes developing embryos, whereas embryos from warmer profiles remain female or die. This occurs presumably because wider oscillations around cooler profiles expose embryos to very low temperatures that inhibit development, and to feminizing temperatures where most embryogenesis accrues. Likewise, embryos incubated under broader fluctuations around warmer profiles experience mostly feminizing temperatures, some dangerously high (which increase mortality), and fewer colder values that are insufficient to induce male development. Therefore, as thermal fluctuations escalate with global warming, the feminization of TSD turtle populations could accelerate, facilitating extinction by demographic collapse. Aggressive global CO₂mitigation scenarios (RCP2.6) could prevent these risks, while intermediate actions (RCP4.5 and RCP6.0 scenarios) yield moderate feminization, highlighting the peril that insufficient reductions of greenhouse gas emissions pose for TSD taxa. If our findings are generalizable, TSD squamates, tuatara, and crocodilians that produce males at warmer temperatures could suffer accelerated masculinization, underscoring the broad taxonomic threats of climate change.

 

Vertebrate sex‐determining mechanisms (SDMs) are triggered by the genotype (GSD), by temperature (TSD), or occasionally, by both. The causes and consequences ofSDMdiversity remain enigmatic. Theory predictsSDMeffects on species diversification, and life‐span effects onSDMevolutionary turnover. Yet, evidence is conflicting in clades with labileSDMs, such as reptiles. Here, we investigate whetherSDMis associated with diversification in turtles and lizards, and whether alterative factors, such as lifespan's effect on transition rates, could explain the relative prevalence ofSDMs in turtles and lizards (including and excluding snakes). We assembled a comprehensive dataset ofSDMstates for squamates and turtles and leveraged large phylogenies for these two groups. We found no evidence thatSDMs affect turtle, squamate, or lizard diversification. However,SDMtransition rates differ between groups. In lizardsTSD‐to‐GSDsurpassGSD‐to‐TSDtransitions, explaining the predominance ofGSDlizards in nature.SDMtransitions are fewer in turtles and the rates are similar to each other (TSD‐to‐GSDequalsGSD‐to‐TSD), which, coupled withTSDancestry, could explainTSD's predominance in turtles. These contrasting patterns can be explained by differences in life history. Namely, our data support the notion that in general, shorter lizard lifespan rendersTSDdetrimental favoringGSDevolution in squamates, whereas turtle longevity permitsTSDretention. Thus, based on the macro‐evolutionary evidence we uncovered, we hypothesize that turtles and lizards followed different evolutionary trajectories with respect toSDM, likely mediated by differences in lifespan. Combined, our findings revealed a complex evolutionary interplay betweenSDMs and life histories that warrants further research that should make use of expanded datasets on unexamined taxa to enable more conclusive analyses.