Abstract

Sex chromosome evolution remains an evolutionary puzzle despite its importance in understanding sexual development and genome evolution. The seemingly random distribution of sex-determining systems in reptiles offers a unique opportunity to study sex chromosome evolution not afforded by mammals or birds. These reptilian systems derive from multiple transitions in sex determination, some independent, some convergent, that lead to the birth and death of sex chromosomes in various lineages. Here we focus on turtles, an emerging model group with growing genomic resources. We review karyotypic changes that accompanied the evolution of chromosomal systems of genotypic sex determination (GSD) in chelonians from systems under the control of environmental temperature (TSD). These transitions gave rise to 31 GSD species identified thus far (out of 101 turtles with known sex determination), 27 with a characterized sex chromosome system (13 of those karyotypically). These sex chromosomes are varied in terms of the ancestral autosome they co-opted and thus in their homology, as well as in their size (some are macro-, some are micro-chromosomes), heterogamety (some are XX/XY, some ZZ/ZW), dimorphism (some are virtually homomorphic, some heteromorphic with larger-X, larger W, or smaller-Y), age (the oldest system could be ~195 My old and the youngest < 25 My old). Combined, all data indicate that turtles follow some tenets of classic theoretical models of sex chromosome evolution while countering others. Finally, although the study of dosage compensation and molecular divergence of turtle sex chromosomes has lagged behind research on other aspects of their evolution, this gap is rapidly decreasing with the acceleration of ongoing research and growing genomic resources in this group.

Highlights

  • A paramount event in the history of life is the early evolution of sexual reproduction

  • Sex chromosomes and sex determination in many species of reptiles have been studied, the genomic basis of sexual development has yet to be fully characterized in reptiles

  • There is no evidence reported for the influence of environmental factors overriding sex chromosomes in genotypic sex determination (GSD) turtles

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Summary

Introduction

A paramount event in the history of life is the early evolution of sexual reproduction. Genes 2020, 11, 416 chromosomes (the sex chromosomes) [2] In other animals, this decision is plastic and occurs in response to environmental cues (ESD), of which the most common in vertebrates is temperature (TSD) [3]. TSD and GSD is not the same in all reptiles [3,7]. GSD reptiles vary, as some possess female- and others male-heterogametic sex chromosomes, including homomorphic or heteromorphic ZZ/ZW, XX/XY, X1 X2 Y, Z1 Z2 W, and ZW1 W2 systems [3,8]. We concentrate on turtles, an emerging model group with growing genomic resources, and explore the karyotypic changes that accompanied the evolution of the genomic architecture of sexual development during transitions between TSD and GSD in this group.

Sex Chromosome Evolution
Sex Chromosomes were Gained and Lost Multiple Times in Turtles
Independent and Convergent Evolution of Turtle Sex Chromosomes
The Architecture of Sex Determination with and without Sex Chromosomes
Consequences of Sex Chromosome Evolution—Dosage Compensation and Faster
Conclusions
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