Origin and evolution of Y chromosomes: Drosophila tales

Abstract

Classically, Y chromosomes are thought to originate from X chromosomes through a process of degeneration and gene loss. Now, the availability of 12 Drosophila genomes provides an opportunity to study the origin and evolution of Y chromosomes in an informative phylogenetic context. Surprisingly, the majority of Drosophila Y-linked genes are recent acquisitions from autosomes and Y chromosome gene gains are more frequent than gene losses. Moreover, the Drosophila pseudoobscura Y chromosome lacks homology with the Y of most Drosophila species. Thus, the Drosophila Y has a different evolutionary history from canonical Y chromosomes (such as the mammalian Y) and it also might have a different origin.

FIGURE 1. Origins of Y chromosomes

Panel A. Y-linked genes in humans and D. melanogaster. Genes ancestrally shared with the X are shown in blue bars, and those acquired from autosomes, in red bars. Genes with unknown origin or that are later additions to both the X and the Y are grouped in the “other” class (green bar). Genes on the human Y chromosome encode 27 different proteins. The majority of these genes are ancestrally shared with the X-chromosome, indicating that these chromosomes are homologous [6,7]. This class of genes is absent among the 12 known single-copy genes in the D. melanogaster Y chromosome, suggesting that X and Y are not homologous [9]. Several human Y-linked genes are multi-copy; we counted them only once. Panel B. Main paths for the origin of Y chromosomes. Only male karyotypes are shown (autosomes in blue, mature sex-chromosomes in red, and extra chromosomes such as a B chromosome in yellow). The canonical path (top) starts when an autosome acquires a strong male determining gene M, becoming a nascent Y (its homologous became a nascent X). Degeneration of the nascent Y and the evolution of dosage compensation in the X originate mature sex chromosomes [–5]. The neo-Y path (middle; shown here in a species with X0/XX sex-determination) starts with a X-autosome fusion, transforming the fused autosome into a neo-X. The free homolog became a neo-Y, which then degenerates [1]. The non-canonical path (bottom) starts when a parasitic B chromosome (which usually do not pair) acquires the capacity to pair with the X. Improvement of B-X pairing and the acquisition of male-fertility genes (F) originate a chromosome that will be termed as Y [,–36]. However, in contrast with the two other paths, these non-canonical Y chromosomes do not share any homologous region with the X, and is not formed by degeneration. Note that only canonical Y chromosomes are expected to have male-determining function (imparted by the M gene), and that the neo-Y and non-canonical paths can be distinguished because the former reduces the number of autosomes [1].

FIGURE 1. Origins of Y chromosomes

Panel A. Y-linked genes in humans and D. melanogaster. Genes ancestrally shared with the X are shown in blue bars, and those acquired from autosomes, in red bars. Genes with unknown origin or that are later additions to both the X and the Y are grouped in the “other” class (green bar). Genes on the human Y chromosome encode 27 different proteins. The majority of these genes are ancestrally shared with the X-chromosome, indicating that these chromosomes are homologous [6,7]. This class of genes is absent among the 12 known single-copy genes in the D. melanogaster Y chromosome, suggesting that X and Y are not homologous [9]. Several human Y-linked genes are multi-copy; we counted them only once. Panel B. Main paths for the origin of Y chromosomes. Only male karyotypes are shown (autosomes in blue, mature sex-chromosomes in red, and extra chromosomes such as a B chromosome in yellow). The canonical path (top) starts when an autosome acquires a strong male determining gene M, becoming a nascent Y (its homologous became a nascent X). Degeneration of the nascent Y and the evolution of dosage compensation in the X originate mature sex chromosomes [–5]. The neo-Y path (middle; shown here in a species with X0/XX sex-determination) starts with a X-autosome fusion, transforming the fused autosome into a neo-X. The free homolog became a neo-Y, which then degenerates [1]. The non-canonical path (bottom) starts when a parasitic B chromosome (which usually do not pair) acquires the capacity to pair with the X. Improvement of B-X pairing and the acquisition of male-fertility genes (F) originate a chromosome that will be termed as Y [,–36]. However, in contrast with the two other paths, these non-canonical Y chromosomes do not share any homologous region with the X, and is not formed by degeneration. Note that only canonical Y chromosomes are expected to have male-determining function (imparted by the M gene), and that the neo-Y and non-canonical paths can be distinguished because the former reduces the number of autosomes [1].

FIGURE 2

Gene movements in the Drosophila Y chromosome. Gene gains by the Y chromosome are marked with red arrows and gene losses by blue arrows. The genes assigned with dashed red arrows are probable gains, which could not yet be confirmed due to lack of close outgroups [9]. The green bar in the D. pseudoobscura/D. persimilis lineage marks the incorporation of the ancestral Y into an autosome, and its replacement by a new Y chromosome [8]. Due to the experimental design, gene gains basically can only be detected in the D. melanogaster lineage, and gene losses only in the other lineages. After correction of this ascertainment bias it was found that the rate of gene gain is 11-fold higher than the rate of gene loss [9]. Note that the majority of D. melanogaster Y-linked genes (7 out 12) were acquired after the split between the Drosophila and Sophophora subgenera, which happened ~ 63 Myr ago [64]. Modified from ref [9], with permission.