Cross-species genomic survey reveals a single origin of the soft-shelled turtles

Abstract

Turtles have a have a complicated sex determination system; however, Trionychidae species, as a unique group, have evolved a conserved genetic sex determination, which provides an excellent case to study the evolution of environmental sex determination to genetic sex determination. Analysis of the chromosome-level genome assembly, construction of the first sex chromosomes of Trionychidae, and embryonic transcriptome revealed that P. sinensis has a ZW-type sex determination system, and that the key sex-determining genes, including Dmrt1, Amh, Foxl2, etc., and their homologs, are not located on the sex chromosomes, which rejects the involvement of Dmrt1s SDGs or dosage compensation effect in the sex determination of P. sinensis ZW system and also indicates that the ZW chromosomes in birds, turtles, frogs, and fishes originated from different chromosome pairs in the common ancestors. Subsequently, comparative genomic studies demonstrated that a conserved ZW-type sex determination system exists in Trionychidae species, and inferred that their sex chromosomes originate from the same chromosome pair of the common ancestor. More importantly, we found a single origin of the sex chromosomes in Trionychidae species, approximately 56 million years ago, which is highly coincident with the Paleocene-Eocene thermal maximum, PETM, event. Therefore, we hypothesize that the PETM event and the loss of embryonic self-thermal regulation are two critical dynamics that drive the adaptive evolution of sex chromosomes for the common ancestor of Trionychidae species in response to extreme temperature changes. Finally, we link the ancestral sex chromosome origin time, the species divergence time, the PETM event, and the continental plate movements to paint a picture of a single origin and radiation route for extant Trionychidae species. Collectively, our findings provide novel insights into the mechanisms of sex determination in P. sinensis, and the single origin of sex chromosomes and species in extant soft-shelled turtles.