Evidência para radiação adaptiva de um estudo filogenético de defesas de plantas

Evidence for adaptive radiation from a phylogenetic study of plant defenses

Anurag A. Agrawala,b,1, Mark Fishbeinc,2, Rayko Halitschkea, Amy P. Hastingsa, Daniel L. Raboskya and Sergio Rasmanna

+ Author Affiliations

aDepartment of Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, NY 14853-2701;

bCornell Center for a Sustainable Future and Department of Entomology, Cornell University, Ithaca, NY 14853; and

cDepartment of Biology, Portland State University, P.O. Box 751, Portland, OR 97207

↵2Present address: Department of Botany, Oklahoma State University, 104 Life Sciences East, Stillwater, OK 74078.

Edited by Douglas J. Futuyma, Stony Brook University, Stony Brook, NY, and approved August 6, 2009 (received for review May 4, 2009)

Abstract

One signature of adaptive radiation is a high level of trait change early during the diversification process and a plateau toward the end of the radiation. Although the study of the tempo of evolution has historically been the domain of paleontologists, recently developed phylogenetic tools allow for the rigorous examination of trait evolution in a tremendous diversity of organisms. Enemy-driven adaptive radiation was a key prediction of Ehrlich and Raven's coevolutionary hypothesis [Ehrlich PR, Raven PH (1964) Evolution 18:586–608], yet has remained largely untested. Here we examine patterns of trait evolution in 51 North American milkweed species (Asclepias), using maximum likelihood methods. We study 7 traits of the milkweeds, ranging from seed size and foliar physiological traits to defense traits (cardenolides, latex, and trichomes) previously shown to impact herbivores, including the monarch butterfly. We compare the fit of simple random-walk models of trait evolution to models that incorporate stabilizing selection (Ornstein-Ulenbeck process), as well as time-varying rates of trait evolution. Early bursts of trait evolution were implicated for 2 traits, while stabilizing selection was implicated for several others. We further modeled the relationship between trait change and species diversification while allowing rates of trait evolution to vary during the radiation. Species-rich lineages underwent a proportionately greater decline in latex and cardenolides relative to species-poor lineages, and the rate of trait change was most rapid early in the radiation. An interpretation of this result is that reduced investment in defensive traits accelerated diversification, and disproportionately so, early in the adaptive radiation of milkweeds.

Asclepias cardenolides coevolution macroevolutionary trends latex
Footnotes

1To whom correspondence should be addressed. E-mail: agrawal@cornell.edu

Author contributions: A.A.A. and M.F. designed research; A.A.A., M.F., R.H., A.P.H., D.L.R., and S.R. performed research; A.A.A. and R.H. contributed new reagents/analytic tools; A.A.A., M.F., and D.L.R. analyzed data; and A.A.A., M.F., and D.L.R. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

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