Divergent sensory and immune gene evolution in sea turtles with contrasting demographic and life histories

Sea turtles represent an ancient lineage of marine vertebrates that evolved from terrestrial ancestors over 100 Mya. The genomic basis of the unique physiological and ecological traits enabling these species to thrive in diverse marine habitats remains largely unknown. Additionally, many populations have drastically declined 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 the leatherback (Dermochelys coriacea) and green (Chelonia mydas) turtles, representing the two extant sea turtle families. These genomes are highly syntenic and homologous, but localized regions of noncollinearity were associated with higher copy numbers of immune, zinc-finger, and olfactory receptor (OR) genes in green turtles, with ORs related to waterborne odorants greatly expanded in green turtles. Our findings suggest that divergent evolution of these key gene families may underlie immunological and sensory adaptations assisting navigation, occupancy of neritic versus pelagic environments, and diet specialization. Reduced collinearity was especially prevalent in microchromosomes, with greater gene content, heterozygosity, and genetic distances between species, supporting their critical role in vertebrate evolutionary adaptation. Finally, diversity and demographic histories starkly contrasted between species, indicating that leatherback turtles have had a low yet stable effective population size, exhibit extremely low diversity compared with other reptiles, and harbor a higher genetic load compared with green turtles, reinforcing concern over their persistence under future climate scenarios. These genomes provide invaluable resources for advancing our understanding of evolution and conservation best practices in an imperiled vertebrate lineage. This work was completed in part with resources provided by the University of Massachusetts' Green High Performance Computing Cluster (GHPCC). Funding was provided by the University of Massachusetts Amherst, NSF-IOS (grant #1904439 to L.M.K.), NOAA-Fisheries, National Research Council postdoctoral fellowship program to L.M.K., VGP, Rockefeller University, to E.D.J., HHMI to E.D.J., the Sanger Institute, Max-Planck-Gesellschaft, and grant contributions from Tom Gilbert, Paul Flicek, R.W.M., Karen A. Bjorndal, Alan B. Bolten, Ed Braun, N.J.G., T.M.-B., and A.F.S. We acknowledge CONICYT-DAAD for scholarship support to T.C.-V., the São Paulo Research Foundation to E.K.S.R.–FAPESP (grant #2020/10372-6). BeGenDiv is partially funded by the German Federal Ministry of Education and Research (BMbF, Förderkennzeichen 033W034A). The work of F.T.-N. and P.M. was supported by the Intramural Research Program of the National Library of Medicine, NIH. The work of M.P. was partially funded through the Federal Ministry of Education and Research (grant 01IS18026C). H.P. was supported by a Formació de Personal Investigador fellowship from Generalitat de Catalunya (FI_B100131). M.K. was supported by “la Caixa” Foundation (ID 100010434; code LCF/BQ/PR19/11700002), the Vienna Science and Technology Fund (WWTF), and the City of Vienna (VRG20-001). Funding for green turtle resequencing was provided by a Welsh Government Sêr Cymru II and the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No. 663830-BU115 and the Sea Turtle Conservancy, Florida Sea Turtle Grants Program (17-033R).