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

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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. Butterflies and moths (called the Lepidoptera) are a large and diverse group of insects that has long captured the attention of biologists and laymen. The colorful patterns on the wings of butterflies, in particular, offer an ideal system to investigate which genes and developmental mechanisms contribute to evolutionary diversification. Genetic analyses that try to find the position of genes along chromosomes are invaluable for such efforts, also because they allow researchers to compare chromosome content between species. Here, we report on a study which built a gene-based map for the chromosomes of a butterfly “lab rat” and identified chromosomes carrying color pattern genes. We compare our map to that of the reference lepidopteran species, the silkworm. Despite these species having diverged some 100 million years ago, there is much conservation in terms of which genes are found together in chromosomes and even how genes are ordered within chromosomes. However, because we were able to compare positioning of many more genes than had ever been reported before for this group, we also found evidence of several large- and small-scale chromosomal rearrangements. We discuss the advantages of gene-based maps in understanding the genetic basis of color pattern evolution.