Evolutionary success of a parasitic B chromosome rests on gene content

et al. 2021

Phil. Trans. R. Soc. B

It is a broadly observed pattern that the non-recombining regions of sex-limited chromosomes (Y and W) accumulate more repeats than the rest of the genome, even in species like birds with a low genome-wide repeat content. Here, we show that in birds with highly heteromorphic sex chromosomes, the W chromosome has a transposable element (TE) density of greater than 55% compared to the genome-wide density of less than 10%, and contains over half of all full-length (thus potentially active) endogenous retroviruses (ERVs) of the entire genome. Using RNA-seq and protein mass spectrometry data, we were able to detect signatures of female-specific ERV expression. We hypothesize that the avian W chromosome acts as a refugium for active ERVs, probably leading to female-biased mutational load that may influence female physiology similar to the ‘toxic-Y’ effect in Drosophila males. Furthermore, Haldane's rule predicts that the heterogametic sex has reduced fertility in hybrids. We propose that the excess of W-linked active ERVs over the rest of the genome may be an additional explanatory variable for Haldane's rule, with consequences for genetic incompatibilities between species through TE/repressor mismatches in hybrids. Together, our results suggest that the sequence content of female-specific W chromosomes can have effects far beyond sex determination and gene dosage. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

Section: Methodsmentioning

confidence: 99%

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

Peona

Palacios-Gimenez

et al. 2021

Phil. Trans. R. Soc. B

“…Interestingly, Orthofinder suggested that genes in CNV regions were three times more likely to derive from a duplication event than genes found in other places of the genome. This indicates that duplications had a role in the origin of these CNV-regions, which incidentally has some resemblance to the proposed early evolution of B-chromosomes [25,26].…”

Section: Discussionmentioning

confidence: 84%

Genome structure ofBrachionus asplanchnoidis, a Eukaryote with intrapopulation variation in genome size

Stelzer

Waldvogel

et al. 2021

Preprint

Eukaryotic genomes vary greatly in size due to variation in the proportion of non-coding DNA, a pattern that emerges both in comparisons at a larger taxonomic scale and at the level of individuals within a species. The rotifer Brachionus asplanchnoidis represents one of the most extreme cases of intraspecific genome size variation among Eukaryotes, displaying almost 2-fold variation within a geographic population. Here we used a whole-genome sequencing approach to identify the underlying DNA sequence differences by assembling a high-quality reference genome draft for one individual of the population and aligning short-reads of 15 individuals from the same geographic population. We identified large, contiguous copy number variable regions (CNVs), which exhibited significant coverage differences among individuals, and whose coverage overall scaled with genome size. CNVs were mainly composed of tandemly repeated satellite DNA, with only few interspersed genes or other sequences, and were characterized by an elevated GC-content. Judging from their distributions across contigs, some CNVs are fragments of accessory (B-)chromosomes while others resemble large insertions to normal chromosomes. CNV patterns in offspring of two parents with divergent genome size, and CNV patterns in several individuals from an inbred line differing in genome size demonstrated inheritance and accumulation of CNVs across generations. Our study provides unprecedented insights into genome size evolution at microevolutionary time scales and thus paves the way for studying genome size evolution in contemporary populations rather than inferring patterns and processes a posteriori from species comparisons.

“…To identify W-linked SNVs from male/female read mapping, we used the WhatGene pipeline developed by [108] for SNV analyses of B chromosomes and germline-restricted chromosomes [109] where we mapped male and female genome re-sequencing reads to the consensus sequences of our repeat library. We considered variants to be W-linked if they were present in all females but absent in males.…”

Section: Methodsmentioning

confidence: 99%

The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

Peona

Palacios-Gimenez

et al. 2020

Preprint

It is a broadly observed pattern that the non-recombining regions of sex-limited chromosomes (Y and W) accumulate more repeats than the rest of the genome, even in species like birds with a low genome-wide repeat content. Here we show that in birds with highly heteromorphic sex chromosomes, the W chromosome has a transposable element (TE) density of >55% compared to the genome-wide density of <10%, and contains over half of all full-length (thus potentially active) endogenous retroviruses (ERVs) of the entire genome. Using RNA-seq and protein mass spectrometry data, we were able to detect signatures of female-specific ERV expression. We hypothesise that the avian W chromosome acts as a refugium for active ERVs, likely leading to female-biased mutational load that may influence female physiology similar to the "toxic-Y" effect in Drosophila. Furthermore, Haldane's rule predicts that the heterogametic sex has reduced fertility in hybrids. We propose that the excess of W-linked active ERVs over the rest of the genome may be an additional explanatory variable for Haldane's rule, with consequences for genetic incompatibilities between species through TE/repressor mismatches in hybrids. Together, our results suggest that the sequence content of female-specific W chromosomes can have effects far beyond sex determination and gene dosage.