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Phylogenetic Escalation and Decline of Plant Defense Strategies

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Phylogenetic Escalation and Decline of Plant Defense Strategies Phylogenetic escalation and decline of plant defense strategies Anurag A. Agrawal*† and Mark Fishbein‡ *Department of Ecology and Evolutionary Biology, Cornell Center for a Sustainable Future, and Department of Entomology, Cornell University, Corson Hall, Ithaca, NY 14853-2701; and ‡Department of Biology, Portland State University, P.O. Box 751, Portland, OR 97207 Edited by Douglas J. Futuyma, Stony Brook University, Stony Brook, NY, and approved May 8, 2008 (received for review March 13, 2008) As the basal resource in most food webs, plants have evolved eages diversify (17–20)? This last prediction was made explicitly myriad strategies to battle consumption by herbivores. Over the by Vermeij (19) and is a special case of Ehrlich and Raven’s (17) past 50 years, plant defense theories have been formulated to ‘‘escape and radiate’’ hypothesis where the evolution of novel explain the remarkable variation in abundance, distribution, and traits that promote speciation is incremental (and directional) diversity of secondary chemistry and other defensive traits. For through the diversification process. example, classic theories of enemy-driven evolutionary dynamics To test our predictions, we grew replicate plants of each of 36 have hypothesized that defensive traits escalate through the Asclepias species and two from the genus Gomphocarpus (repre- diversification process. Despite the fact that macroevolutionary sentative of the sister clade to Asclepias) from seed in a common patterns are an explicit part of defense theories, phylogenetic environment and measured cardenolides, latex, trichomes, growth analyses have not been previously attempted to disentangle spe- rate, and regrowth ability after severe damage. Phylogenetically cific predictions concerning (i) investment in resistance traits, (ii) explicit analyses were conducted by using a molecular phylogeny of recovery after damage, and (iii) plant growth rate. We constructed Asclepias estimated by using Bayesian inference (Fig. 1). The a molecular phylogeny of 38 species of milkweed and tested four phylogeny was estimated from sequence data obtained from three major predictions of defense theory using maximum-likelihood noncoding regions of the chloroplast genome, and branch lengths methods. We did not find support for the growth-rate hypothesis. were estimated by maximum likelihood. Our key finding was a pattern of phyletic decline in the three most potent resistance traits (cardenolides, latex, and trichomes) and an Results and Discussion escalation of regrowth ability. Our neontological approach com- Contrary to prediction 1, we found no tradeoffs between the plements more common paleontological approaches to discover three most potent resistance traits (pairwise correlations: car- directional trends in the evolution of life and points to the impor- denolides–latex [raw correlation (rc): r ϭ 0.279, P ϭ 0.094, tance of natural enemies in the macroevolution of species. The phylogenetically corrected (pic): P ϭ 0.317, cardenolides– finding of macroevolutionary escalating regowth ability and de- trichomes (rc: r ϭ 0.175, P ϭ 0.300, pic: P ϭ 0.121), latex– clining resistance provides a window into the ongoing coevolu- trichomes (rc: r ϭ 0.647, P Ͻ 0.001, pic: P ϭ 0.001)]. Indeed, the tionary dynamics between plants and herbivores and suggests a strongly positive phylogenetically independent correlation be- revision of classic plant defense theory. Where plants are primarily tween latex and trichomes is consistent with our previous field consumed by specialist herbivores, regrowth (or tolerance) may be experiment on a subset of these species (1). Positive correlated favored over resistance traits during the diversification process. evolution appears to be a general phenomenon in the evolution of plant defense against herbivory, because tradeoffs between cardenolides ͉ coevolution ͉ macroevolutionary trends ͉ resistance traits are relatively uncommon in inter- and intraspe- milkweed Asclepias ͉ plant defense theory cific comparisons in other systems (1, 12, 21). Consequently, we sought to use a multivariate index of composite investment across the three traits. We used a recently proposed index, the EVOLUTION ilkweeds (Asclepias spp., Apocynaceae) are prime candi- sum of the Z scores for the three traits (22), which was also highly Mdates for a clade-based approach to testing plant defense correlated with the factor scores of the first principal component theories because of their well known defensive strategies and estimated from the same data (r ϭ 0.998, P Ͻ 0.001) [supporting tremendous variation in expression of these traits (1–3). Three information (SI) Table S1]. traits—cardenolides, latex, and trichomes—have been strongly Resource-availability theory, which has been well supported in implicated in providing milkweed resistance against herbivores. studies of tropical trees and some temperate herbaceous species, Each of these traits has been demonstrated to quantitatively predicts that plant growth rate determines investment in resistance affect the behavior (4, 5), performance (1, 6, 7), and abundance (14, 15, 23). However, despite Ͼ20-fold variation in plant growth (8) of herbivores in the field. The resistance provided by these rate, this did not explain investment in the composite resistance of three traits occurs despite the fact that most milkweed herbivores milkweeds (Fig. 2A). We do not interpret this result to mean that are specialists and have adaptations to cope with each defense the production of resistance traits is cost-free, but rather that there (4, 5, 9). Our central goal was thus to evaluate what factors is no evolutionary signature of intrinsic plant growth rate dictating predict variation in defense investment across the clade. investment in resistance traits across the clade. We tested four major predictions of classic plant defense theory using phylogenetically explicit analyses employing max- imum-likelihood estimation of defense trait evolution (10, 11). Author contributions: A.A.A. and M.F. designed research, performed research, contributed First, do the individual resistance traits used by plants trade off new reagents/analytic tools, analyzed data, and wrote the paper. due to redundancy, or do they repeatedly evolve together as a The authors declare no conflict of interest. suite of covarying traits (12, 13)? Second, does plant growth rate This article is a PNAS Direct Submission. covary with investment in resistance traits as predicted by Data deposition: The sequences reported in this paper have been deposited in the GenBank resource availability theory (14, 15)? Third, do resistance and database (accession nos. are available in Table S4). regrowth ability (a measure of tolerance) trade off as alternative †To whom correspondence should be addressed. E-mail: [email protected]. defensive strategies to cope with herbivores (16)? And finally, as This article contains supporting information online at www.pnas.org/cgi/content/full/ predicted by some (co)evolutionary theory, is there evidence for 0802368105/DCSupplemental. phenotypic escalation in defense trait expression as plant lin- © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802368105 PNAS ͉ July 22, 2008 ͉ vol. 105 ͉ no. 29 ͉ 10057–10060 Downloaded by guest on September 23, 2021 Fig. 1. Phylogeny of 36 species of Asclepias and two of Gomphocarpus, with branch lengths estimated by maximum likelihood. DNA sequences from three, noncoding, plastid DNA regions (rpl16 intron, trnC-rpoB spacer, trnS-trnG spacer/trnG intron) were analyzed. The phylogeny was inferred by Bayesian inference; the 50%-majority-rule consensus of trees sampled from the stationary distribution in an analysis of a broader sample of 145 species formed the starting tree from which the depicted tree was pruned (see Materials and Methods). Posterior probabilities (Ͼ0.5) are indicated near nodes. Images on the right (top to bottom): A. californica, leaf beetle Labidomera clivicollis feeding on A. syriaca after deactivation of latex by clipping of the laticifers, Monarch butterfly caterpillar Danaus plexippus shaving trichomes of A. syriaca, and the longhorn beetle Tetraopes tetraophthalmus feeding after clipping the midrib of A. syriaca. We tested two predictions about the ability of plants to regrow number of intervening nodes or molecular branch length from after damage. First, early models and intraspecific data from A. root to tip) against trait values. The benefit of this framework is syriaca suggested that regrowth may be predicted by the root- that the regression of path length against the phenotype is to-shoot ratio, whereby those species that invest relatively more estimated while correcting for phylogenetic nonindependence. underground will be able to better recover from aboveground Our data were remarkably consistent with classic theory; how- damage (3, 24). Indeed, we found that root-to-shoot ratio was a ever, the evolutionary escalation we report is in regrowth after good predictor of regrowth, but that the association between damage but not in resistance traits (Fig. 2B). Indeed, the dominant high investment in roots and ability to regrow after damage was evolutionary trend for our index of the three resistance traits was phylogenetically constrained (rc: r ϭ 0.387, P ϭ 0.022, pic: P ϭ to strongly decline during the diversification of Asclepias (Fig. 2C). 0.841). Second, defense theories have suggested that investment The directional trends for regrowth and resistance were not
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