New Insights into the Evolution of the W Chromosome in Lepidoptera

Abstract

Moths and butterflies (Lepidoptera) represent the most diverse group of animals with heterogametic females. Although the vast majority of species has a WZ/ZZ (female/male) sex chromosome system, it is generally accepted that the ancestral system was Z/ZZ and the W chromosome has evolved in a common ancestor of Tischeriidae and Ditrysia. However, the lack of data on sex chromosomes in lower Lepidoptera has prevented a formal test of this hypothesis. Here, we performed a detailed analysis of sex chromosomes in Tischeria ekebladella (Tischeriidae) and 3 species representing lower Ditrysia, Cameraria ohridella (Gracillariidae), Plutella xylostella (Plutellidae), and Tineola bisselliella (Tineidae). Using comparative genomic hybridization we show that the first 3 species have well-differentiated W chromosomes, which vary considerably in their molecular composition, whereas T. bisselliella has no W chromosome. Furthermore, our results suggest the presence of neo-sex chromosomes in C. ohridella. For Z chromosomes, we selected 5 genes evenly distributed along the Z chromosome in ditrysian model species and tested their Z-linkage using qPCR. The tested genes (Henna, laminin A, Paramyosin, Tyrosine hydroxylase, and 6-Phosphogluconate dehydrogenase) proved to be Z-linked in all species examined. The conserved synteny of the Z chromosome across Tischeriidae and Ditrysia, along with the W chromosome absence in the lower ditrysian families Psychidae and Tineidae, suggests a possible independent origin of the W chromosomes in these 2 lineages.

Identification and characterization of a Masculinizer homologue in the diamondback moth, Plutella xylostella

“…For this system to function across such broad phylogenetic distances, splicing sites within the PBW dsx cassette must be recognized by endogenous splicing regulators within each of these two distantly related lepidopteran species. We therefore hypothesized that homologues of the key regulator of this splicing in silkworm, Masc, would also be present in DBMa species with a confirmed WZ/ZZ sex chromosome arrangement (Dalikova et al, 2017). Previous research on B. mori Masc identified the amino acid region between 304 and 310 aa and particularly the two cysteine residues (cysteinecysteine domain) as being necessary for promoting male-specific splicing of dsx .…”

Absence of W Chromosome in Psychidae Moths and Implications for the Theory of Sex Chromosome Evolution in Lepidoptera

“…The Z chromosome resembles autosomes and contains many genes. Multiple studies have shown a highly conserved synteny of Z-linked genes between species across the phylogenetic tree of Lepidoptera [2][3][4][5]. In contrast, the W chromosome is largely composed of repetitive sequences and is partially or completely degenerated, possibly as a result of the absence of recombination in lepidopteran females [6].…”

“…Nevertheless, the origin of the W chromosome remains elusive. There are several hypotheses about when and how the W chromosome arose [5,11,12]. The generally accepted hypothesis of Lukhtanov [12] assumed that the W chromosome evolved in a common ancestor of Tischeriidae (Tischeriina in the original paper), a small group of leaf-mining moths, and Ditrysia, an evolutionary younger, multidiverse group comprising 98% of lepidopteran species.…”

Construction of a bacterial artificial chromosome library of Endoclita excrescens as a tool for comparative gene mapping in Lepidoptera

“…Endoclita excrescens belongs to a primitive lepidopteran family, the Hepialidae, which is one of the key families to elucidate the origin of the lepidopteran W chromosome (Lukhtanov ; Dalíková et al . ; Fraïsse et al . ).…”