Macroevolution and the biological diversity of plants and herbivores

Abstract

Terrestrial biodiversity is dominated by plants and the herbivores that consume them, and they are one of the major conduits of energy flow up to higher trophic levels. Here, we address the processes that have generated the spectacular diversity of flowering plants (>300,000 species) and insect herbivores (likely >1 million species). Long-standing macroevolutionary hypotheses have postulated that reciprocal evolution of adaptations and subsequent bursts of speciation have given rise to much of this biodiversity. We critically evaluate various predictions based on this coevolutionary theory. Phylogenetic reconstruction of ancestral states has revealed evidence for escalation in the potency or variety of plant lineages' chemical defenses; however, escalation of defense has been moderated by tradeoffs and alternative strategies (e.g., tolerance or defense by biotic agents). There is still surprisingly scant evidence that novel defense traits reduce herbivory and that such evolutionary novelty spurs diversification. Consistent with the coevolutionary hypothesis, there is some evidence that diversification of herbivores has lagged behind, but has nevertheless been temporally correlated with that of their host-plant clades, indicating colonization and radiation of insects on diversifying plants. However, there is still limited support for the role of host-plant shifts in insect diversification. Finally, a frontier area of research, and a general conclusion of our review, is that community ecology and the long-term evolutionary history of plant and insect diversification are inexorably intertwined.

Fig. 1.

A conceptualization of escape and radiate coevolution hypothesized by Ehrlich and Raven (4). In this hypothetical scenario, a plant phylogeny is on the left and insect herbivore phylogeny is on the right; arrows between the phylogenies indicate host use (species missing arrows feed on plants that are not shown here). For the plant lineage, black indicates the ancestral defensive phenotype, yellow indicates the evolution of some new defense, and yellow with red hatches indicates the evolution of an additional novel defense. The evolution of counteradaptations is similarly indicated on the insect phylogeny. Note that the evolution of novel traits related to the interaction is associated with an increased diversification rate (i.e., species accumulation per unit time). Insect counteradaptations have allowed for the colonization of differentially defended plant clades, but in this case the counteradaptations have not escalated by adding on new phenotypes; rather, two counteradaptations have independently evolved. Insect host use shows some phylogenetic signal (i.e., closely related species feed on related plants), but some insects also colonize distantly related plants. The insect lineage did not cospeciate with the plant lineage. In other words, the phylogenies are not parallel (i.e., mirror images of each other), but rather the pattern indicates that insects radiated onto existing plants (fossil evidence or other means of dating could verify this pattern of insect speciation on to a diversified group of plants). Parallel phylogenies are not predicted by coevolution, and could simply be a consequence of joint vicariance events that result in both insect and plant speciation.