The draft genomes of soft-shell turtle and green sea turtle yield insights into the development and evolution of the turtle-specific body plan

TLDR

Turtles possess unique anatomical features that raise questions about the origin of their distinctive body plan. The study aimed to generate and analyze draft genomes of the soft‑shell and green sea turtles to investigate their evolutionary relationship to birds and crocodilians. Draft genomes were produced and phylogenetically analyzed for Pelodiscus sinensis and Chelonia mydas. The genomes revealed a close sister relationship to birds and crocodilians, extensive expansion of olfactory receptor genes, an hourglass‑like divergence in embryogenesis with conservation at the phylotypic period, Wnt5a expression in the dorsal shell growth zone, and turtle evolution involving a conservative phylotypic period followed by shell‑specific developmental repatterning.

Abstract

Naoki Irie and colleagues report the draft genomes of the soft-shell and green sea turtles. Their genome-wide phylogenetic analysis supports the hypothesis that turtles are a sister group of crocodilians and birds. The unique anatomical features of turtles have raised unanswered questions about the origin of their unique body plan. We generated and analyzed draft genomes of the soft-shell turtle (Pelodiscus sinensis) and the green sea turtle (Chelonia mydas); our results indicated the close relationship of the turtles to the bird-crocodilian lineage, from which they split ∼267.9–248.3 million years ago (Upper Permian to Triassic). We also found extensive expansion of olfactory receptor genes in these turtles. Embryonic gene expression analysis identified an hourglass-like divergence of turtle and chicken embryogenesis, with maximal conservation around the vertebrate phylotypic period, rather than at later stages that show the amniote-common pattern. Wnt5a expression was found in the growth zone of the dorsal shell, supporting the possible co-option of limb-associated Wnt signaling in the acquisition of this turtle-specific novelty. Our results suggest that turtle evolution was accompanied by an unexpectedly conservative vertebrate phylotypic period, followed by turtle-specific repatterning of development to yield the novel structure of the shell.