Macroevolutionary chemical escalation in an ancient plant-herbivore arms race

Abstract

A central paradigm in the field of plant-herbivore interactions is that the diversity and complexity of secondary compounds in plants have intensified over evolutionary time, resulting in the great variety of secondary products that currently exists. Unfortunately, testing of this proposal has been very limited. We analyzed the volatile chemistry of 70 species of the tropical plant genus Bursera and used a molecular phylogeny to test whether the species' chemical diversity or complexity have escalated. The results confirm that as new species diverged over time they tended to be armed not only with more compounds/species, but also with compounds that could potentially be more difficult for herbivores to adapt to because they belong to an increasing variety of chemical pathways. Overall chemical diversity in the genus also increased, but not as fast as species diversity, possibly because of allopatric species gaining improved defense with compounds that are new locally, but already in existence elsewhere.

Fig. 1.

Squirt defense in Bursera. In some species resins are stored under pressure in a grid of canals that run throughout the cortex of the stems and in the leaves. When these canals are severed or punctured by an insect, a high-pressure flow of resins is released, soaking the attacker.

Fig. 2.

Diversity of secondary compounds (Upper) and complexity of chemical mixtures (Lower) of extant species of Bursera over time. Chemical diversity and complexity of individual species have increased during the genus' diversification as predicted by coevolutionary theory. The yellow stars indicate values of squirting Burseras. Significant P values for directional evolutionary trends are reported in the text.

Fig. 3.

Accumulation of Bursera lineages (blue diamonds) and compounds (red squares) through time.

Fig. 4.

The cumulative number of compounds divided by the cumulative number of species is plotted against time. In the last 30 My Bursera species have tended to contribute fewer new compounds.