Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation

Abstract

A tremendous diversity of plants exude sticky and toxic latex upon tissue damage, and its production has been widely studied as a defensive adaptation against insect herbivores. Here, we address variation in latex production and its constituent chemical properties (cardenolides and cysteine proteases) in 53 milkweeds [ Asclepias spp. (Apocynaceae)], employing a phylogenetic approach to test macroevolutionary hypotheses of defense evolution. Species were highly variable for all three traits, and they showed little evidence for strong phylogenetic conservatism. Latex production and the constituent chemical defenses are thus evolutionarily labile and may evolve rapidly. Nonetheless, in phylogenetically independent analyses, we show that the three traits show some correlations (and thus share a correlated evolutionary history), including a positive correlation between latex exudation and cysteine protease activity. Conversely, latex exudation and cysteine protease activity both showed a trade-off with cardenolide concentrations in latex. We also tested whether these traits have increased in their phenotypic values as the milkweeds diversified, as predicted by plant defense escalation theory. Alternative methods of testing this prediction gave conflicting results -there was an overall negative correlation between amount of evolutionary change and amount of latex exudation; however, ancestral state reconstructions indicated that most speciation events were associated with increases in latex. We conclude by (i) summarizing the evidence of milkweed latex itself as a multivariate defense including the amount exuded and toxin concentrations within, (ii) assessing the coordinated evolution of latex traits and how this fits with our previous notion of 'plant defense syndromes' , and finally, (iii) proposing a novel hypothesis that includes an 'evolving community of herbivores' that may promote the escalation or decline of particular defensive strategies as plant lineages diversify.

Evidence for adaptive radiation from a phylogenetic study of plant defenses

“…(24) and latex (29) showed declining expression during the diversification of Asclepias, trichomes showed no trend (30), and phenolics and plant tolerance to damage showed evidence for escalation (7,24). In this new, larger dataset we have evaluated not only the presence of directional trends in these and other traits, but importantly have evaluated the tempo of evolutionary changes.…”

“…3). As an index of overall defense investment, we also assess trait evolution of the sum of the Z-scores (standard normal scores) for cardenolides, latex, and trichomes (29,31). Although this approach certainly omits some potentially important defensive traits of milkweeds (e.g., phenolics, cysteine proteases, waxes), given our previous demonstration of covarying evolution of milkweed Models were fit under 2 modes of evolution: gradual, in which phylogenetic distance is scaled as time, and speciational, in which phylogenetic distance is scaled as number of nodes (speciation events).…”

Role of phytohormones in insect-specific plant reactions

“…Specialist herbivores in particular may have found ways to suppress plant defenses (Box1) or to circumvent them via behavioral adaptations, which, in analogy to the PTI/ETI model in plant-pathogen interactions, may have led to the counter-evolution of specifically adapted defense mechanisms in plants [120, 121]. Until today, few mechanistic examples of plant-counter adaptations to specialists are known (but see other articles in this special issue), and further research is required to disentangle whether differential responses of plants to chewing herbivores are truly specific, and whether plants have evolved to tailor their response to different chewing attackers.…”

Macroevolutionary chemical escalation in an ancient plant–herbivore arms race

“…In Asclepias, complex cardenolides appear to be phylogenetically novel (8). Nevertheless, one of the few studies to use explicit phylogenetic models of character evolution actually reported a pattern of phyletic decline of defensive cardenolides in Asclepias (9,10).…”