Accumulation of retrotransposons contributes to W chromosome differentiation in the willow beauty Peribatodes rhomboidaria (Lepidoptera: Geometridae)

Abstract

The W chromosome of Lepidoptera is typically gene-poor, repeat-rich and composed of heterochromatin. Pioneering studies investigating this chromosome reported an abundance of mobile elements. However, the actual composition of the W chromosome varies greatly between species, as repeatedly demonstrated by comparative genomic hybridization (CGH) or fluorescence in situ hybridization (FISH). Here we present an analysis of repeats on the W chromosome in the willow beauty, Peribatodesrhomboidaria (Geometridae), a species in which CGH predicted an abundance of W-enriched or W-specific sequences. Indeed, comparative analysis of male and female genomes using RepeatExplorer identified ten putative W chromosome-enriched repeats, most of which are LTR or LINE mobile elements. We analysed the two most abundant: PRW LINE-like and PRW Bel-Pao. The results of FISH mapping and bioinformatic analysis confirmed their enrichment on the W chromosome, supporting the hypothesis that mobile elements are the driving force of W chromosome differentiation in Lepidoptera. As the W chromosome is highly underrepresented in chromosome-level genome assemblies of Lepidoptera, this recently introduced approach, combining bioinformatic comparative genome analysis with molecular cytogenetics, provides an elegant tool for studying this elusive and rapidly evolving part of the genome.

W chromosome sequences of two bombycid moths provide an insight into the origin of Fem

“…We estimated that explosive proliferation of W‐linked LTRs occurred very recently in both species because less differentiated LTRs (with divergence value of 1 or 2) account for the most significant proportion. This result is consistent with previous studies showing that lepidopteran insects' W chromosomes tend to accumulate transposons (Hejníčková et al., 2023; Lewis et al., 2021). The epigenetic environment specific to the W chromosomes, which was formed by a lack of meiotic recombination, could have acted to increase the copy number for the transposons.…”

“…In contrast, the W chromosome of another butterfly species, Dryas iulia , is derived from the B chromosome (Lewis et al., 2021). Lepidopteran W chromosomes tend to accumulate retrotransposons and often have complex structures (Hejníčková et al., 2023; Lewis et al., 2021), and B. mori represents a prime example; because the nested structures of the W‐linked retrotransposons were of considerable degree (Abe, Mita, et al., 2005; Abe, Seki, et al., 2005), chromosome‐scale assembly of the W chromosome of B. mori has been considered impossible. For this reason, previous genome projects have used male individuals for genomic DNA (Kawamoto et al., 2019; Mita et al., 2004; Xia et al., 2004).…”

Transposon fusion gave birth toFem,Bombyx morifemale determining gene

“…The collinearity between the W and Z chromosomes of two Pieris butterflies, namely Pieris manni and Pieris rapae , exists, suggesting that the W chromosomes of P. mannii and P. rapae have evolved from Z chromosomes [3] while the W chromosome of another butterfly species, Dryas iulia , is derived from the B chromosome [4]. Lepidopteran W chromosomes tend to accumulate retrotransposons and often have complex structures [4,5], and B. mori represents a prime example: because the nested structures of the W- linked retrotransposons were of considerable degree [6,7], chromosome-scale assembly of the W chromosome of B. mori has been considered impossible. For this reason, in the genome projects organized in the past [8–10], male individuals have been used as the donor of genomic DNA.…”