Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera

Homeobox genes encode transcription factors with essential roles in patterning and cell fate in developing animal embryos. Many homeobox genes, including Hox and NK genes, are arranged in gene clusters, a feature likely related to transcriptional control. Sparse taxon sampling and fragmentary genome assemblies mean that little is known about the dynamics of homeobox gene evolution across Lepidoptera or about how changes in homeobox gene number and organization relate to diversity in this large order of insects. Here we analyze an extensive data set of high-quality genomes to characterize the number and organization of all homeobox genes in 123 species of Lepidoptera from 23 taxonomic families. We find most Lepidoptera have around 100 homeobox loci, including an unusual Hox gene cluster in which the lab gene is repositioned and the ro gene is next to pb. A topologically associating domain spans much of the gene cluster, suggesting deep regulatory conservation of the Hox cluster arrangement in this insect order. Most Lepidoptera have four Shx genes, divergent zen-derived loci, but these loci underwent dramatic duplication in several lineages, with some moths having over 165 homeobox loci in the Hox gene cluster; this expansion is associated with local LINE element density. In contrast, the NK gene cluster content is more stable, although there are differences in organization compared with other insects, as well as major rearrangements within butterflies. Our analysis represents the first description of homeobox gene content across the order Lepidoptera, exemplifying the potential of newly generated genome assemblies for understanding genome and gene family evolution

Evolution of the insect Hox gene cluster: comparative analysis across 243 species

The Hox gene cluster is an iconic example of evolutionary conservation between divergent animal lineages, providing evidence for ancient similarities in the genetic control of embryonic development. However, there are differences between taxa in gene order, gene number and genomic organisation implying conservation is not absolute. There are also examples of radical functional change of Hox genes; for example, the ftz, zen and bcd genes in insects play roles in segmentation, extraembryonic membrane formation and body polarity, rather than specification of anteroposterior position. There have been detailed descriptions of Hox genes and Hox gene clusters in several insect species, including important model systems, but a large-scale overview has been lacking. Here we extend these studies using the publiclyavailable complete genome sequences of 243 insect species from 13 orders. We show that the insect Hox cluster is characterised by large intergenic distances, consistently extreme in Odonata, Orthoptera, Hemiptera and Trichoptera, and always larger between the ‘posterior’ Hox genes. We find duplications of ftz and zen in many species and multiple independent cluster breaks, although certain modules of neighbouring genes are rarely broken apart suggesting some organisational constraints. As more high-quality genomes are obtained, a challenge will be to relate structural genomic changes to phenotypic change across insect phylogeny