Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle

Abstract

The existence of males and females, which are often strikingly different in morphology, reproductive strategies and behavior, is one of the most widespread phenomena in biology. However, the genetic mechanisms that generate this ubiquitous pattern are surprisingly diverse and do not follow a phylogenetic pattern. Sex-determination mechanisms can differ between even closely related species and arise frequently and independently. Fish provide a paradigmatic example, as their sex-determination mechanisms range from environmental to different modes of genetic determination. The evolutionary meaning of this remarkable plasticity is unknown. For genetic sex determination, where the trigger for female or male development comes from the genetic constitution of the individual, the evolution of sex-determination mechanisms is connected to a very peculiar genomic process, namely the formation of sex chromosomes [1][2][3][4] .To improve understanding of the function and evolution of sex chromosomes, their genetic organization must be deciphered.However, owing to their degenerate nature and high repetitive DNA content, sex chromosomes pose almost insurmountable problems in deciphering their gene content and organization. So far, only the human 5 , chimpanzee 6 and rhesus macaque Y chromosomes 7 and the male-specific region on the Y chromosome of one fish, the medaka 8 , have been sequenced. These analyses have nevertheless provided important insights into the evolution of Y chromosomes, their genomic organization and their degeneration processes, as well as predictions as to their likely evolutionary fate 9-12 .Much less genomic information exists on W chromosomes because, as with Y chromosomes, they are predominantly highly repetitive in nature. The prevailing theory of the evolution of sex chromosomes predicts that degeneration of the heterogametic sex chromosome is a stepwise process that occurs over an extended period of time. We therefore reasoned that an evolutionarily young W chromosome Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle Genetic sex determination by W and Z chromosomes has developed independently in different groups of organisms. To better understand the evolution of sex chromosomes and the plasticity of sex-determination mechanisms, we sequenced the whole genomes of a male (ZZ) and a female (ZW) half-smooth tongue sole (Cynoglossus semilaevis). In addition to insights into adaptation to a benthic lifestyle, we find that the sex chromosomes of these fish are derived from the same ancestral vertebrate protochromosome as the avian W and Z chromosomes. Notably, the same gene on the Z chromosome, dmrt1, which is the male-determining gene in birds, showed convergent evolution of features that are compatible with a similar function in tongue sole. Comparison of the relatively young tongue sole sex chromosomes with those of mammals and birds identified events that occurred during the early phase of sex-chromosome evolution. Pertinent to...

Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes

“…In fish, transgenerational effects of heat exposure have been recently described (67). In the tongue sole, Cynoglossus semilaevis, which has a ZW/ZZ sex-determining system as in wild zebrafish, heat-induced neomales were responsible for the epigenetic transmission of DNA-altered states, resulting in the production of masculinized offspring even at normal temperatures (68). DNA methylation changes occur due to the activity of DNA methyltransferases (Dnmts).…”

Did sex chromosome turnover promote divergence of the major mammal groups?

“…Some reptile species have sex chromosome systems that can be overridden by temperature 28, 29; these dual systems are extremely labile, able to change rapidly to TSD systems and even between ZW and XY 30, 31. Similar GSD‐TSD transitions may be common in some fish and may also facilitate changes in sex determination 32, 33, 34.…”

“…The homology between monotreme and bird sex chromosomes initially suggested that the mammalian ancestor had a bird‐like ZW system, driven by DMRT1 dosage. However, this need not represent identity by descent, for a flatfish also has a ZW sex pair with homology to the bird ZW, and uses DMRT1 dosage to determine sex 32. DMRT1 has also been pressed into service independently by spawning copies that became a dominant male‐determiner in medaka 16, 65 or female determiner in Xenopus 66; clearly this gene is simply good at sex determination and has been independently recruited in several lineages 67.…”

High-density linkage mapping aided by transcriptomics documents ZW sex determination system in the Chinese mitten crab Eriocheir sinensis

“…In addition, transcriptomic data assist in identifying the genes of sex chromosome and sex differentiation pathways. For example, the linkage map in combination with transcriptomes of the flatfish successfully facilitates the assembly and sequence assignment of chromosomes, providing the basis for understanding the evolution of sex chromosomes and the sex determination mechanism (Chen et al, 2014). Determination of full-length transcripts of W-chromosome genes and their expression profiles in early avian embryos provide a complete annotation of the W chromosome (Ayers et al, 2013).…”