Complex Evolutionary History of the Y Chromosome in Flies of the Drosophila obscura Species Group.

Ryan Bracewell,Doris Bachtrog,Esther Betran

doi:10.1093/gbe/evaa051

Ryan Bracewell, Doris Bachtrog + Show 1 more

Open Access

https://doi.org/10.1093/gbe/evaa051

Copy DOI

Abstract

The Drosophila obscura species group shows dramatic variation in karyotype, including transitions among sex chromosomes. Members of the affinis and pseudoobscura subgroups contain a neo-X chromosome (a fusion of the X with an autosome), and ancestral Y genes have become autosomal in species harboring the neo-X. Detailed analysis of species in the pseudoobscura subgroup revealed that ancestral Y genes became autosomal through a translocation to the small dot chromosome. Here, we show that the Y-dot translocation is restricted to the pseudoobscura subgroup, and translocation of ancestral Y genes in the affinis subgroup likely followed a different route. We find that most ancestral Y genes have translocated to unique autosomal or X-linked locations in different taxa of the affinis subgroup, and we propose a dynamic model of sex chromosome formation and turnover in the obscura species group. Our results suggest that Y genes can find unique paths to escape unfavorable genomic environments that form after sex chromosome–autosome fusions.

Highlights

Sex chromosomes have formed independently many times from a pair of ordinary autosomes by acquiring a sexdetermining gene (Bull 1983)
De novo transcriptome assemblies from males generated from a subobscura subgroup species (D. guanche) and an obscura subgroup species (D. obscura) recovered several transcripts with clear sequence similarity to D. melanogaster Y transcripts, indicating that ancestral Y genes are present in these lineages and located on the Y chromosome
These results are consistent with the hypothesis that the formation of the neo-sex chromosomes causes problems in meiosis, driving the fusion or translocation of the ancestral Y chromosome and the dot

Summary

Introduction

Sex chromosomes have formed independently many times from a pair of ordinary autosomes by acquiring a sexdetermining gene (Bull 1983). In some species groups, such as many fish or reptiles, the proto-X and proto-Y keep recombining over most of their length and evolve little differentiation beyond the sex-determining gene (homomorphic sex chromosomes) (Kitano and Peichel 2012; Miura 2017). Sex chromosome turnover can be frequent in some groups, especially if the X and Y show little differentiation (Vicoso 2019), but is thought to be rare for heteromorphic sex chromosomes (Bachtrog et al 2014). The highly specialized gene content of old sex chromosomes (i.e., male-fertility genes on the Y) and chromosome-wide regulatory mechanisms (dosage compensation of the X, heterochromatin formation on the Y) is thought to make reversals of highly differentiated sex chromosomes into autosomes increasingly difficult (Bachtrog et al 2014). The identity of the X chromosome was found to have changed multiple times across Diptera clades (Vicoso and Bachtrog 2015)

Methods

Results

Conclusion