A Gene-Based Linkage Map for Bicyclus anynana Butterflies Allows for a Comprehensive Analysis of Synteny with the Lepidopteran Reference Genome

Abstract

Lepidopterans (butterflies and moths) are a rich and diverse order of insects, which, despite their economic impact and unusual biological properties, are relatively underrepresented in terms of genomic resources. The genome of the silkworm Bombyx mori has been fully sequenced, but comparative lepidopteran genomics has been hampered by the scarcity of information for other species. This is especially striking for butterflies, even though they have diverse and derived phenotypes (such as color vision and wing color patterns) and are considered prime models for the evolutionary and developmental analysis of ecologically relevant, complex traits. We focus on Bicyclus anynana butterflies, a laboratory system for studying the diversification of novelties and serially repeated traits. With a panel of 12 small families and a biphasic mapping approach, we first assigned 508 expressed genes to segregation groups and then ordered 297 of them within individual linkage groups. We also coarsely mapped seven color pattern loci. This is the richest gene-based map available for any butterfly species and allowed for a broad-coverage analysis of synteny with the lepidopteran reference genome. Based on 462 pairs of mapped orthologous markers in Bi. anynana and Bo. mori, we observed strong conservation of gene assignment to chromosomes, but also evidence for numerous large- and small-scale chromosomal rearrangements. With gene collections growing for a variety of target organisms, the ability to place those genes in their proper genomic context is paramount. Methods to map expressed genes and to compare maps with relevant model systems are crucial to extend genomic-level analysis outside classical model species. Maps with gene-based markers are useful for comparative genomics and to resolve mapped genomic regions to a tractable number of candidate genes, especially if there is synteny with related model species. This is discussed in relation to the identification of the loci contributing to color pattern evolution in butterflies.

Extensive synteny conservation of holocentric chromosomes in Lepidoptera despite high rates of local genome rearrangements

“…Overall conservation of synteny in Lepidoptera has been reported in several studies (16)(17)(18)(19)(20) suggesting that, over the 100 My separating the Bombyx and butterfly lineages, some degree of gene synteny has thus been maintained. However, a more detailed study was warranted to allow more general conclusions.…”

“…LG10 had 15 genes and LG 21 four genes in conserved order (19). The remainder of the chromosomes showed one or more rearrangements or inversions.…”

Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism

“…Linkage maps have been most frequently constructed for the primary purpose of identifying loci controlling specific phenotypic traits (Sturtevant, 1913); however, genome-wide linkage maps are also an efficient starting point for exploring genome architecture and chromosome dynamics (Beldade et al, 2009), complementing the current revolution in next-generation whole-genome sequencing (Wang et al, 2005). Lepidoptera are an interesting group in this respect, characterized by wide variation in chromosome number (Suomalainen and Brown, 1984;Kandul et al, 2007) around a strong, putatively ancestral mode (haploid n ¼ 31), encountered in approximately one-third of the species (White, 1973).…”

“…Lepidoptera are an interesting group in this respect, characterized by wide variation in chromosome number (Suomalainen and Brown, 1984;Kandul et al, 2007) around a strong, putatively ancestral mode (haploid n ¼ 31), encountered in approximately one-third of the species (White, 1973). The dynamism implied by high rates of chromosome fission/fusion contrasts with a highly conserved synteny of genes between chromosomes across distantly related taxa (Pringle et al, 2007;Sahara et al, 2007;Beldade et al, 2009;Yasukochi et al, 2009;d'Alenc¸on et al, 2010;Baxter et al, 2011). This latter feature allows unambiguous identification of orthologous chromosomal regions in different species to reconstruct the events that produced the current pattern of structural diversity.…”

A single major QTL controls expression of larval Cry1F resistance trait in Ostrinia nubilalis (Lepidoptera: Crambidae) and is independent of midgut receptor genes

“…For species of Lepidoptera, linkage maps have relied mainly upon the use of AFLP markers with inclusion of a few single locus markers (Dopman et al 2004;Heckel et al 1999;Baxter et al 2005;Gahan et al 2005). Recently, linkage maps composed exclusively of locus-specific co-dominant markers have been constructed for species of Lepidoptera (Miao et al 2005;Yamamoto et al 2006;Beldade et al 2009). The 123 markers within our O. nubilalis backcross pedigree FQ4 was relatively low compared to that within other segregating populations.…”