Abstract

Sex chromosomes play a central role in genetics of speciation and their turnover was suggested to promote divergence. In vertebrates, sex chromosome–autosome fusions resulting in neo-sex chromosomes occur frequently in male heterogametic taxa (XX/XY), but are rare in groups with female heterogamety (WZ/ZZ). We examined sex chromosomes of seven pests of the diverse lepidopteran superfamily Gelechioidea and confirmed the presence of neo-sex chromosomes in their karyotypes. Two synteny blocks, which correspond to autosomes 7 (LG7) and 27 (LG27) in the ancestral lepidopteran karyotype exemplified by the linkage map of Biston betularia (Geometridae), were identified as sex-linked in the tomato leafminer, Tuta absoluta (Gelechiidae). Testing for sex-linkage performed in other species revealed that while LG7 fused to sex chromosomes in a common ancestor of all Gelechioidea, the second fusion between the resulting neo-sex chromosome and the other autosome is confined to the tribe Gnoreschemini (Gelechiinae). Our data accentuate an emerging pattern of high incidence of neo-sex chromosomes in Lepidoptera, the largest clade with WZ/ZZ sex chromosome system, which suggest that the paucity of neo-sex chromosomes is not an intrinsic feature of female heterogamety. Furthermore, LG7 contains one of the major clusters of UDP-glucosyltransferases, which are involved in the detoxification of plant secondary metabolites. Sex chromosome evolution in Gelechioidea thus supports an earlier hypothesis postulating that lepidopteran sex chromosome–autosome fusions can be driven by selection for association of Z-linked preference or host-independent isolation genes with larval performance and thus can contribute to ecological specialization and speciation of moths.

Highlights

  • Sex chromosomes represent intriguing portions of the genome which play an important role in many evolutionary processes including sexual and intragenomic conflict and speciation (Masly and Presgraves 2007; Mank et al 2014).the formation of postzygotic isolation can be characterized by two empirical rules, both involving sex chromosomes, inferred from analyses of hybrid fitness

  • Two synteny blocks, which correspond to autosomes 7 (LG7) and 27 (LG27) in the ancestral lepidopteran karyotype exemplified by the linkage map of Biston betularia (Geometridae), were identified as sex-linked in the tomato leafminer, Tuta absoluta (Gelechiidae)

  • The F:M ratio for ket, using acetylcholinesterase 1 (Ace-1) as reference, gave a value of 0.498 6 0.090, which significantly differed from 1 (P < 0.05) but not from 0.5 (P > 0.05). These results indicated that females and males had the same copy number of both Ace-1 and elongation factor 1 alpha (EF-1a) genes, and that females had half the number of copies of ket with respect to males, which was expected as this gene represents a standard marker for the lepidopteran Z chromosome

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Summary

Introduction

The formation of postzygotic isolation can be characterized by two empirical rules, both involving sex chromosomes, inferred from analyses of hybrid fitness. The first of these known as the large-X effect refers to the disproportionately large effect of the X chromosome compared with ß The Author(s) 2019. Evol. 11(4):1307–1319. doi:10.1093/gbe/evz Advance Access publication April 8, 2019

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