Abstract
Gene duplications within the conserved Hox cluster are rare in animal evolution, but in Lepidoptera an array of divergent Hox-related genes (Shx genes) has been reported between pb and zen. Here, we use genome sequencing of five lepidopteran species (Polygonia c-album, Pararge aegeria, Callimorpha dominula, Cameraria ohridella, Hepialus sylvina) plus a caddisfly outgroup (Glyphotaelius pellucidus) to trace the evolution of the lepidopteran Shx genes. We demonstrate that Shx genes originated by tandem duplication of zen early in the evolution of large clade Ditrysia; Shx are not found in a caddisfly and a member of the basally diverging Hepialidae (swift moths). Four distinct Shx genes were generated early in ditrysian evolution, and were stably retained in all descendent Lepidoptera except the silkmoth which has additional duplications. Despite extensive sequence divergence, molecular modelling indicates that all four Shx genes have the potential to encode stable homeodomains. The four Shx genes have distinct spatiotemporal expression patterns in early development of the Speckled Wood butterfly (Pararge aegeria), with ShxC demarcating the future sites of extraembryonic tissue formation via strikingly localised maternal RNA in the oocyte. All four genes are also expressed in presumptive serosal cells, prior to the onset of zen expression. Lepidopteran Shx genes represent an unusual example of Hox cluster expansion and integration of novel genes into ancient developmental regulatory networks.
Highlights
The characterization of Hox genes in the 1980s awakened the idea that there may be similar processes controlling body patterning in divergent animals and gave the first opportunity to compare the control of developmental processes between taxa at a molecular level
Hox genes are often arranged in a genomic cluster, which was generated by tandem gene duplication early in animal evolution [2,3]
We have examined gene duplication in a set of ancient genes used in patterning of animal embryos: the Hox genes
Summary
The characterization of Hox genes in the 1980s awakened the idea that there may be similar processes controlling body patterning in divergent animals and gave the first opportunity to compare the control of developmental processes between taxa at a molecular level. Conservation of Hox gene function is reflected in their constrained evolution. Hox genes are often arranged in a genomic cluster, which was generated by tandem gene duplication early in animal evolution [2,3]. After expansion of the Hox cluster in early animal evolution there has been relatively little variation in gene number. The ancestor of all Ecdysozoa, Lophotrochozoa and Deuterostomia possessed 7 to 10 Hox genes [3], and most bilaterian animals still have approximately this number despite hundreds of millions of years of subsequent evolution. The lack of expansion of the Hox gene cluster within Bilateria is intriguing and is in contrast to the pattern
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