Sex Chromosome Turnover in Moths of the Diverse Superfamily Gelechioidea

GBE Sex Chromosome Turnover in Moths of the Diverse Superfamily Gelechioidea Leonela Z. Carabajal Paladino1,2,†, Irena Provaznıkova1,3,†, Madeleine Berger4, Chris Bass5, pez7, Frantisek Marec1, and Petr Nguyen1,3,* Nayanie S. Aratchige6, Silvia N. Lo  e Budejovice, Czech Republic Biology Centre of the Czech Academy of Sciences, Institute of Entomology, Cesk 1 2 The Pirbright Institute, Surrey, United Kingdom 4 Rothamsted Research, Department of Biointeractions and Crop Protection, Herts, United Kingdom 5 University of Exeter, College of Life and Environmental Sciences, Biosciences, Penryn, Cornwall, United Kingdom 6 Coconut Research Institute of Sri Lanka, Crop Protection Division, Bandirippuwa Estate, Lunuwila, Sri Lanka 7 Instituto Nacional de Tecnologıa Agropecuaria, Instituto de Microbiologıa y Zoologıa Agrıcola, Hurlingham, Buenos Aires, Argentina † These authors contributed equally to this work. *Corresponding author: E-mail: . Accepted: April 5, 2019 Data deposition: This project has been deposited at GenBank under accession numbers MG265651, MG265652, MG265654–MG265661, MG265664–MG265670, MG265672–MG265675, MG265678–MG265690, and MG265692–MG265694. 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. Key words: Coleophora, Depressaria, Hofmannophila, Opisina, Phthorimaea, Sitotroga. Introduction 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). Indeed, 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. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Genome Biol. Evol. 11(4):1307–1319. doi:10.1093/gbe/evz075 Advance Access publication April 8, 2019 1307  e Budejovice, Czech Republic University of South Bohemia, Faculty of Science, Cesk 3 GBE Carabajal Paladino et al. 1308 sex chromosomes in an invasive gelechiid pest, the tomato leafminer Tuta absoluta (Gelechiidae). To test for the presence of neo-sex chromosomes in their genomes, we examined the karyotypes of several pests of the diverse superfamily Gelechioidea, which contains 18,500 species (van Nieukerken et al. 2011) and comprises among others the above-mentioned Oecophoridae and Gelechiidae families. Our results confirmed a sex chromosome–autosome fusion, which occurred in a common ancestor of all three main lineages of Gelechioidea, namely the Gelechiid, Scythridid, and Depressariid assemblages (Sohn et al. 2016). A synteny block involved in the fusion was identified as an autosome homoeologous to the chromosome 7 of the ancestral karyotype represented by the peppered moth Biston betularia (Geometridae) (cf. Van’t Hof 2013). Furthermore, we discovered another fusion between the neo-sex chromosomes and homoeologue of the B. betularia chromosome 27 within the tribe Gnorimoschemini (Gelechiinae). A potential role of the sex chromosome turnover in the divergence of Gelechioidea is discussed. Materials and Methods Insects Representatives of five families within Gelechioidea were either obtained from laboratory stocks or collected from natural populations. A laboratory stock of the potato tuber moth, Phthorimaea operculella (Gelechiidae), was provided by the Atomic Energy Commission of Syria (Damascus, Syria). Larvae were reared on wax-coated potato slices as described in Saour and Makee (1997). Cultures of the Angoumois grain moth, Sitotroga cerealella (Gelechiidae), from the Instituto de Microbiologıa y Zoologıa Agrıcola (IMYZA), Instituto Nacional de Tecnologıa Agropecuaria (INTA) (Buenos Aires, Argentina), and the Institute for Biological Control JKI, Federal Research Centre for Cultivated Plants (Darmstadt, Germany) were kept on wheat grains (Mendez et al. 2016). A laboratory colony of the tomato leafminer, T. absoluta (Gelechiidae), from IMYZA, INTA was maintained on potted tomato plants under the conditions detailed in Cagnotti et al. (2012). Specimens of the coconut black-headed caterpillar, Opisina arenosella (Xylorictidae), were obtained from the colony maintained on coconut leaflets at the Crop Protection Division of the Coconut Research Institute of Sri Lanka (Lunuwila, Sri Lanka). The larch case-bearer Coleophora laricella (Coleophoridae) and the brown house-moth Hofmannophila pseudospretella (Oecophoridae) were collected as larvae from wild populations in Levın (Lisov, Czech Republic). The dingy flat-body moth Depressaria daucella (Depressaridae) was collected as larvae and pupae in Slapy u Tabora (Tabor, Czech Republic). The material obtained in the field was immediately processed for its future analysis, an (...truncated)