Evidence for adaptive radiation from a phylogenetic study of plant defenses

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.

Fig. 1.

Phylogeny of milkweed species sampled for phenotypic traits. The phylogeny is the all-compatible consensus of trees sampled in a Bayesian analysis of the complete dataset of 155 samples, pruned to the 53 taxa investigated here. Branch lengths are drawn in proportion to the number of speciation events between nodes; they are not equivalent in length because multiple speciation events in the complete phylogeny may occur on a single branch of the pruned phylogeny. Bayesian posterior probabilities >0.50 are indicated.

Fig. 2.

Two possible relationships between trait values and amount of phylogenetic divergence. (A) Directional evolutionary trend: root-to-tip phylogenetic distance is proportional to phenotypic trait value (e.g., body size, defense). When the x-axis is scaled as the number of nodes, this signifies a correlation between speciation events and trait evolution, possibly implicating the trait as a driver of diversification. When the x-axis is scaled as substitutions/site, this suggests a correlation between molecular divergence and phenotypic evolution. Such directional trends can be estimated with Pagel's scaling parameter β (2). (B) Shifting tempo of phenotypic evolution: scaled phylogenetic distances are proportional to phenotypic trait value. An exponent scales the relationship between phylogenetic distance and trait value; thus, the tempo of phenotypic change varies over time. In this study we used Pagel's δ as the scaling exponent (2). The commonly assumed constant rate of trait change would be represented by a flat line. Here, we assume that the rate of trait change decelerates, as is predicted during adaptive radiation, with early diverging lineages predicted to exhibit higher rates of trait change (and greater variance) as compared to later diverging lineages.

Fig. 3.

Phylogenetic deceleration of declining investment in cardenolides across 53 milkweeds. The x-axis shows the number of intervening nodes between the root and each taxon, calculated from the comprehensive phylogeny. Note that the decline is not linear, but is best fit by an exponential decrease (δ) in the rate of trait evolution during the radiation (see Table 2). The reduction of investment in cardenolides occurred disproportionately early in the diversification process.