title: Evolutionary origins of a novel host plant detoxification gene in butterflies.
abstract: Chemical interactions between plants and their insect herbivores provide an excellent opportunity to study the evolution of species interactions on a molecular level. Here, we investigate the molecular evolutionary events that gave rise to a novel detoxifying enzyme (nitrile-specifier protein [NSP]) in the butterfly family Pieridae, previously identified as a coevolutionary key innovation. By generating and sequencing expressed sequence tags, genomic libraries, and screening databases we found NSP to be a member of an insect-specific gene family, which we characterized and named the NSP-like gene family. Members consist of variable tandem repeats, are gut expressed, and are found across Insecta evolving in a dynamic, ongoing birth-death process. In the Lepidoptera, multiple copies of single-domain major allergen genes are present and originate via tandem duplications. Multiple domain genes are found solely within the brassicaceous-feeding Pieridae butterflies, one of them being NSP and another called major allergen (MA). Analyses suggest that NSP and its paralog MA have a unique single-domain evolutionary origin, being formed by intragenic domain duplication followed by tandem whole-gene duplication. Duplicates subsequently experienced a period of relaxed constraint followed by an increase in constraint, perhaps after neofunctionalization. NSP and its ortholog MA are still experiencing high rates of change, reflecting a dynamic evolution consistent with the known role of NSP in plant-insect interactions. Our results provide direct evidence to the hypothesis that gene duplication is one of the driving forces for speciation and adaptation, showing that both within- and whole-gene tandem duplications are a powerful force underlying evolutionary adaptation.
authors.affiliation: Department of Entomology, Max-Planck-Institute for Chemical Ecology, Beutenberg Campus, Jena, Germany.
authors.forename: Hanna M
authors.initials: HM
authors.lastname: Fischer
authors.forename: Christopher W
authors.initials: CW
authors.lastname: Wheat
authors.forename: David G
authors.initials: DG
authors.lastname: Heckel
authors.forename: Heiko
authors.initials: H
authors.lastname: Vogel
mesh_terms: D000818:Animals; D019607:Brassicaceae / Q000469:parasitology / Q000633:toxicity; D002080:Butterflies / Q000201:enzymology / Q000235:genetics* / Q000502:physiology; D030541:Databases, Genetic; D019143:Evolution, Molecular; D005091:Exons; D020224:Expressed Sequence Tags; D015723:Gene Library; D017344:Genes, Insect; D006790:Host-Parasite Interactions; D019476:Insect Proteins / Q000235:genetics; D007438:Introns; D005810:Multigene Family; D010802:Phylogeny; D017434:Protein Structure, Tertiary
chemical_list: D019476:Insect Proteins