Supplementary Files S5 Output of the WhatGene pipeline for paradise crow, chicken, zebra finch and emu. from The avian W chromosome is a refugium for endogenous retroviruses with likely effects on female-biased mutational load and genetic incompatibilities

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, likely leading to female-biased mutational load that may influence female physiology similar to the ‘toxic-Y’ effect in <i>Drosophila</i>. 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)’.

学界已普遍观测到一类典型模式：限性染色体（sex-limited chromosomes）的非重组区域（即Y与W染色体），相较于基因组其余区域会累积更多重复序列，即便在全基因组重复序列含量较低的鸟类等物种中亦是如此。本研究针对具有高度异形性染色体（heteromorphic sex chromosomes）的鸟类展开分析，结果显示其W染色体的转座因子（transposable element, TE）密度超过55%，而全基因组转座因子密度不足10%；且该染色体承载了全基因组超过半数的全长内源性逆转录病毒（endogenous retroviruses, ERVs，此类序列潜在具备活性）。借助转录组测序（RNA-seq）与蛋白质质谱（protein mass spectrometry）数据，本研究成功检测到雌性特异性ERV表达的特征信号。我们提出如下假说：鸟类W染色体可作为活性ERV的避难所，这大概率会引发雌性偏向的突变负荷，进而影响雌性生理机能，其机制与果蝇（Drosophila）中的‘毒性Y’（toxic-Y）效应类似。此外，霍尔丹法则（Haldane's rule）预测，异配性别个体的杂交后代育性会出现下降。我们认为，W染色体上活性ERV的富集程度高于基因组其余区域，这一现象可作为霍尔丹法则的额外解释变量：杂交个体中转座因子与阻遏蛋白的错配，可能引发物种间的遗传不相容性。综上，本研究结果表明，雌性特异性W染色体的序列组成，其生物学影响远不止性别决定与基因剂量调控。本文属于《挑战性染色体演化范式：以脊椎动物为重点的实证与理论洞察（第二部分）》主题专栏文章。