Orthopteran Neo-Sex Chromosomes Reveal Dynamics of Recombination Suppression and Evolution of Supergenes

Abstract

The early evolution of sex chromosomes has remained obscure for more than a century. The Vandiemenella viatica species group of morabine grasshoppers is highly suited for studying the early stages of sex chromosome divergence and degeneration of the Y chromosome. This stems from the fact that neo-XY sex chromosomes have independently evolved multiple times by X-autosome fusions with different autosomes. Here, we generated new chromosome-level assemblies for two chromosomal races representing karyotypes with and without neo-sex chromosomes (P24XY and P24X0), and sequence data of a third chromosomal race with a different neo-XY chromosome system (P25XY). Interestingly, these two neo-XY chromosomal races are formed by different X-autosome fusions (involving chr1 and chrB, respectively), and we found that both neo-Y chromosomes have partly ceased to recombine with their neo-X counterpart. We show that the neo-XY chromosomes have diverged through accumulation of SNPs and structural mutations, and that many neo-Y-linked genes have degenerated since recombination ceased. However, the non-recombining regions of neo-Y chromosomes host non-degenerated genes crucial for sex determination, such as sex-lethal and transformer, alongside genes associated with spermatogenesis, fertility, and reproduction, illustrating their integrative role as a masculinizing supergene. Contrary to expectations, the neo-Y chromosomes showed (slightly) lower density of transposable elements (TEs) compared to other genomic regions. The study reveals the unique dynamics of young sex chromosomes, with evolution of recombination suppression and pronounced decay of (some) neo-sex chromosome genes, and provides a compelling case illustrating how chromosomal fusions and post-fusion mutational processes contribute to the evolution of supergenes.

Keywords: chromosomal rearrangements; genetic degeneration; genomic recombination; neo‐sex chromosomes; repetitive DNA; sexual antagonistic locus; supergenes.

FIGURE 1

Male haploid karyotypes, hypothesized chromosomal changes, and meiosis observed within the analyzed chromosomal races of the Vandiemenella morabine grasshoppers. (a) Overview of male haploid karyotypes and hypothesized chromosomal changes of the morabine grasshoppers V. viatica19, P24X0, P24XY, P25XY, based on White (1978). Chromosomes are sorted by size and centromere position. Noteworthy are two instances of independent neo‐XY sex chromosome formation via centric fusion events between the ancestral X chromosome (red) and one of the autosomes (black). (b) First metaphases of males in P24X0, P24XY and P25XY, modified from White, Blackithr, and Cheney (1967). The largest autosome pairs, the sex chromosomes, and chromosome arms of the neo‐sex chromosomes involved in X‐A centric fusions are indicated. XL refers to the arm originating from the ancestral X chromosome fused to an autosome, while XR designates the autosomal arm of the neo‐X that shares homology with the neo‐Y. The location of chiasmata between neo‐XR and neo‐Y in P24XY (d: Distal) and P25XY (i: Interstitial) is specified.

FIGURE 2

Genome‐wide sex differences in coverage and heterozygosity across 1 Mb windows plotted along chromosomes positions in the Vandiemenella morabine grasshopper genomes. (a) Chromosomal race P24X0, (b) P24XY, and (c) P25XY. Rows depict heterozygosity and genome coverage (unfiltered mismatch setting). The gray background indicates the 95% confidence intervals (CI), with data points exceeding these values marked in red (if higher) or blue (if lower). The data reveal sex‐linked regions encompassing chrX and/or XL across all races, as well as segments of chr1 (257–304 Mb) and chrB (0–75 Mb) in P24XY and P25XY morabine grasshoppers, respectively.

FIGURE 3

Tracks of genes and levels of divergence and degeneration in the sex‐linked regions of the Vandiemenella morabine grasshopper genomes. The sex‐linked regions in (a) P24XY and (b) P25XY span many loci indicated by triangles, some of which (highlighted) affect sex determination, gametogenesis, reproduction, fertility, sexual communication, and behavior. (c) Box plots show neo‐XR and neo‐Y synonymous site divergence estimates (dS values) for the sex‐linked regions in P24XY and P25XY. (d) Box plots shows the rate of non‐synonymous to synonymous substitutions (dN/dS values) for the neo‐XR and neo‐Y in the sex‐linked regions of P24XY and P25XY. The summary statistics in the boxplots represent the median (horizontal black bar), interquartile range (the thick white bar in the center), and the extreme of the distribution (thin black line). (e) Bar plot illustrating the levels of genetic degeneration (loss‐of‐function mutation) in P24XY and P25XY sex‐linked neo‐Y regions. The proportion of nonfunctional pseudogenes is used as proxy of the levels of gene degeneration in each sex‐linked region.

FIGURE 4

Repeat landscapes across Vandiemenella morabine grasshopper genomes. (a‐d) Read‐based repeat content comparison in (a) male versus (b) female of P24XY, and (c) male versus (d) female of P25XY. The inserts depict the satDNA landscapes in each genome. The histograms show the distribution of the BLASTn divergence analysis to the consensus on the x axis and the satDNA abundance (as % of the reads) on the y axis for males and females. Each bin on the x axis represents 1% divergence. (e, f) Assembly‐based repeat content along the neo‐XR chromosomes of P24XY and P25XY. Percentage of repeat‐derived base pairs shown per window of 1 Mb along the neo‐XR chromosomes of P24XY and P25XY, following the same color scheme as (a–d). The alternating black dashed lines below the x axis mark the sex‐linked regions (evolutionary strata) discussed in the main text.

FIGURE 5

Chromosomal rearrangements between the neo‐sex chromosomes and their ancestral counterparts in Vandiemenella morabine grasshoppers. (a) Visualization of syntenic regions and intrachromosomal rearrangements between P24XY neo‐XR and neo‐Y, as well as between neo‐Y and its ancestral counterpart P24X0 chr1. (b) Visualization of syntenic regions and intrachromosomal rearrangements between P25XY neo‐XR and neo‐Y, along with between neo‐Y and its ancestral counterpart P24X0 chrB. The pink shaded area highlights the cumulative count of SNPs and indels within the sex‐linked regions of P24XY and P25XY.