Strong Signatures of Selection on Candidate Genes Underlying Core Speciation Mechanisms in Desert Tortoises

Abstract

Genomic incompatibilities and differential ecological adaptation are thought to be fundamental mechanisms of speciation. In this study, we generated a chromosome-scale reference genome and annotation for Gopherus morafkai , the Sonoran Desert tortoise, and conducted a detailed analysis of genes under positive selection with its sister species, the Mojave Desert tortoise. They occupy desert habitats with differing seasonal rainfall patterns and have considerable behavioural and reproductive differences, yet maintain a narrow hybrid zone. We find high conservation of synteny with other chelonian species. Results show extensive positive selection (422 candidate genes) relating to eye development and function that may reflect differences in UV exposure, as well as core reproductive isolation mechanisms of sperm-egg recognition, spindle assembly checkpoint and sister chromatid pairing. Together, our results offer strong genomic support and speciation genomic resources for processes shaping reproductive isolation in chelonians.

Keywords: Gopherus; postzygotic; prezygotic; reinforcement; speciation; spindle assembly checkpoint.

FIGURE 1

Summary of habitat and genomic differences. (A) Range maps of G. morafkai and G. agassizii ; (B) UV index differences between G. agassizii and G. morafkai ; (C) schematic of putatively ecologically adaptive PS genes involved in development of the ocular lens, which plays a role in UV filtering; (D) schematic of PS genes putatively related to reproductive isolation and/or reinforcement, including sperm–egg binding and chromosome positioning and spindle assembly checkpoint (SAC). Genes related to those functions are listed and colour‐coded.

FIGURE 2

Synteny comparisons across the most gene‐rich scaffolds in the genome assemblies of G. morafkai and T. s. elegans. Scaffold 16 of the T. s. elegans assembly shows fusion of three scaffolds of the G. morafkai assembly from 21, 22, and 23. See Figure S1 for synteny comparisons between G. morafkai and G. agassizii .

FIGURE 3

STRING interaction network of genes under positive selection between G. morafkai and G. agassizii . The gene function was manually curated and subnetworks were identified by noteworthy themes: Chromosome function and chromatid pairing involved in mitosis/meiosis (gold), cell cycle (pink), reproduction (blue), or vision and eye formation (green).