Sex chromosomes have evolved independently multiple times in eukaryotes and are therefore considered a prime example of convergent genome evolution. Sex chromosomes are known to emerge after recombination is halted between a homologous pair of chromosomes, and this leads to a range of non-adaptive modifications causing gradual degeneration and gene loss on the sex-limited chromosome. However, the proximal causes of recombination suppression and the pace at which degeneration subsequently occurs remain unclear. Here, we use long- and short-read single-molecule sequencing approaches to assemble and annotate a draft genome of the basket willow, Salix viminalis, a species with a female heterogametic system at the earliest stages of sex chromosome emergence. Our single-molecule approach allowed us to phase the emerging Z and W haplotypes in a female, and we detected very low levels of Z/W single-nucleotide divergence in the non-recombining region. Linked-read sequencing of the same female and an additional male (ZZ) revealed the presence of two evolutionary strata supported by both divergence between the Z and W haplotypes and by haplotype phylogenetic trees. Gene order is still largely conserved between the Z and W homologs, although the W-linked region contains genes involved in cytokinin signaling regulation that are not syntenic with the Z homolog. Furthermore, we find no support across multiple lines of evidence for inversions, which have long been assumed to halt recombination between the sex chromosomes. Our data suggest that selection against recombination is a more gradual process at the earliest stages of sex chromosome formation than would be expected from an inversion and may result instead from the accumulation of transposable elements. Our results present a cohesive understanding of the earliest genomic consequences of recombination suppression as well as valuable insights into the initial stages of sex chromosome formation and regulation of sex differentiation.

中文翻译：

---

篮柳（Salix viminalis）的基因组组装揭示了性染色体扩张的最早阶段。

性染色体在真核生物中独立进化了多次，因此被认为是趋同基因组进化的主要例子。已知在一对同源染色体之间的重组停止后会出现性染色体，这会导致一系列非适应性修饰，从而导致限性染色体逐渐退化和基因丢失。然而，重组抑制的近端原因和随后发生退化的速度仍不清楚。在这里，我们使用长读长和短读长单分子测序方法来组装和注释篮柳 Salix viminalis 的基因组草图，这是一种在性染色体出现的最早阶段具有雌性异配子系统的物种。我们的单分子方法使我们能够在女性中分阶段出现的 Z 和 W 单倍型，并且我们在非重组区域检测到非常低水平的 Z/W 单核苷酸分歧。同一名女性和另一名男性 (ZZ) 的连锁阅读测序揭示了 Z 和 W 单倍型之间的差异以及单倍型系统发育树支持的两个进化层的存在。Z 和 W 同系物之间的基因顺序在很大程度上仍然是保守的，尽管 W 连锁区域包含参与细胞分裂素信号调节的基因，这些基因与 Z 同系物不同步。此外，我们发现没有多条证据支持倒位，长期以来人们一直认为倒位会停止性染色体之间的重组。我们的数据表明，在性染色体形成的最早阶段，针对重组的选择比倒位所预期的过程更为渐进，并且可能是由转座因子的积累引起的。我们的结果呈现了对重组抑制的最早基因组后果的统一理解，以及对性染色体形成和性别分化调节初始阶段的宝贵见解。