The turtle shell is often described as an evolutionary novelty that facilitated the radiation of the clade Testudines. The scutes, or keratinous plates, of the turtle shell are hypothesized to be patterned by reaction-diffusion dynamics, and this property of their development provides explanatory power to mechanisms of anomalous variation. A mathematical model of scute development predicts that anomalous variation in the phylogenetically stable pattern of scutes is achieved by environmental influence on the developmental program. We test this prediction with data on patterns of scute variation from natural nests and controlled incubation of sea turtle eggs in Florida and Western Australia. We find that high temperatures are sufficient to produce anomalous patterns in turtle scutes, and that this correlation is even stronger when conditions are dry. Furthermore, we find that the patterns of variation are not random; greater anomalous variation is found in the midline vertebral scutes and during a critical period of turtle development.

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Oviparous reptile embryos are expected to breach their critical thermal maxima if temperatures reach those predicted under current climate change models due to the lack of the maternal buffering processes and parental care. Heat-shock proteins (HSPs) are integral in the molecular response to thermal stress, and their expression is heritable, but the roles of other candidate families such as the heat-shock factors (HSFs) have not been determined in reptiles. Here, we subject embryonic sea turtles (Caretta caretta) to a biologically realistic thermal stress and employ de novo transcriptomic profiling of brain tissue to investigate the underlying molecular response. From a reference transcriptome of 302 293 transcripts, 179 were identified as differentially expressed between treatments. As anticipated, genes enriched in the heat-shock treatment were primarily associated with the Hsp families, or were genes whose products play similar protein editing and chaperone functions (e.g. bag3, MYOC and serpinh1). Unexpectedly, genes encoding the HSFs were not significantly upregulated under thermal stress, indicating their presence in unstressed cells in an inactive state. Genes that were downregulated under thermal stress were less well functionally defined but were associated with stress response, development and cellular organization, suggesting that developmental processes may be compromised at realistically high temperatures. These results confirm that genes from the Hsp families play vital roles in the thermal tolerance of developing reptile embryos and, in addition with a number of other genes, should be targets for evaluating the capacity of oviparous reptiles to respond adaptively to the effects of climate change.

Marine turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 MYA, yet the genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remain largely unknown. Additionally, many populations have declined drastically due to anthropogenic activities over the past two centuries, and their recovery is a high global conservation priority. We generated and analyzed high-quality reference genomes for green (Chelonia mydas) and leatherback (Dermochelys coriacea) turtles, representing the two extant marine turtle families (MRCA ~60 MYA). Generally, these genomes are highly syntenic and homologous. Non-collinearity was associated with higher copy numbers of immune, zinc-finger, or olfactory receptor (OR) genes in green turtles. Gene family analyses suggested that ORs related to waterborne odorants have expanded in green turtles and contracted in leatherbacks, which may underlie immunological and sensory adaptations assisting navigation and occupancy of neritic versus pelagic environments, and diet specialization. Microchromosomes showed reduced collinearity, and greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, demographic history and diversity analyses showed stark contrasts between species, indicating that leatherback turtles have had a low yet stable effective population size, extremely low diversity when compared to other reptiles, and a higher proportion of deleterious variants, reinforcing concern over the persistence of this species under future climate scenarios. These highly contiguous genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage.