The genetic basis of a plant–insect coevolutionary key innovation

doi:10.1073/pnas.0706229104

The genetic basis of a plant–insect coevolutionary key innovation

*Max Planck Institute for Chemical Ecology, Beutenberg Campus, Hans Knoell Strasse 8, 07745 Jena, Germany;
^¶School of Botany and Zoology, Australian National University, Canberra ACT 0200, Australia;
**California State University, 1250 Bellflower Boulevard, Long Beach, CA 90840; and
^††Department of Biology, Duke University, Durham, NC 27708

Edited by May R. Berenbaum, University of Illinois at Urbana–Champaign, Urbana, IL, and approved October 23, 2007 (received for review July 5, 2007)

Abstract

Ehrlich and Raven formally introduced the concept of stepwise coevolution using butterfly and angiosperm interactions in an attempt to account for the impressive biological diversity of these groups. However, many biologists currently envision butterflies evolving 50 to 30 million years (Myr) after the major angiosperm radiation and thus reject coevolutionary origins of butterfly biodiversity. The unresolved central tenet of Ehrlich and Raven's theory is that evolution of plant chemical defenses is followed closely by biochemical adaptation in insect herbivores, and that newly evolved detoxification mechanisms result in adaptive radiation of herbivore lineages. Using one of their original butterfly-host plant systems, the Pieridae, we identify a pierid glucosinolate detoxification mechanism, nitrile-specifier protein (NSP), as a key innovation. Larval NSP activity matches the distribution of glucosinolate in their host plants. Moreover, by using five different temporal estimates, NSP seems to have evolved shortly after the evolution of the host plant group (Brassicales) (≈10 Myr). An adaptive radiation of these glucosinolate-feeding Pierinae followed, resulting in significantly elevated species numbers compared with related clades. Mechanistic understanding in its proper historical context documents more ancient and dynamic plant–insect interactions than previously envisioned. Moreover, these mechanistic insights provide the tools for detailed molecular studies of coevolution from both the plant and insect perspectives.

Footnotes

^‡To whom correspondence should be addressed. E-mail: cww10{at}psu.edu
Author contributions: C.W.W. and T.M.-O. designed research; C.W.W., H.V., and U.W. performed research; U.W., M.F.B., D.U., and T.M.-O. contributed new reagents/analytic tools; C.W.W., H.V., and U.W. analyzed data; and C.W.W., H.V., and U.W. wrote the paper.
↵ ^†Present Address: Pennsylvania State University, Department of Biology, 208 Mueller Laboratories, University Park, PA 16802.
↵ ^§Present Address: Institute of Pharmaceutical Biology, Braunschweig University of Technology, 38106 Braunschweig, Germany.
↵ ^‖Present Address: Biodiversity Conservation Division, Department of Natural Resources, Environment and the Arts, P.O. Box 496, Palmerston NT 0831, Australia.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0706229104/DC1.