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MBE Advance Access originally published online on February 23, 2008
Molecular Biology and Evolution 2008 25(5):809-820; doi:10.1093/molbev/msn014
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© The Author 2008. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Evolutionary Origins of a Novel Host Plant Detoxification Gene in Butterflies

Hanna M. Fischer*, Christopher W. Wheat{dagger}, David G. Heckel* and Heiko Vogel*

* Department of Entomology, Max-Planck-Institute for Chemical Ecology, Beutenberg Campus, Jena, Germany
{dagger} Department of Biological Sciences, Pennsylvania State University

E-mail: hvogel{at}ice.mpg.de.

Accepted for publication December 26, 2007.

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.

Key Words: molecular evolution • tandem duplication • Pieridae • Brassicaceae • host plant shift • detoxification

Adriana Briscoe, Associate Editor


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