Ode to Ehrlich and Raven or how herbivorous insects might drive plant speciation

Abstract

Fifty years ago, Ehrlich and Raven proposed that insect herbivores have driven much of plant speciation, particularly at tropical latitudes. There have been no explicit tests of their hypotheses. Indeed there were no proposed mechanisms either at the time or since by which herbivores might generate new plant species. Here we outline two main classes of mechanisms, prezygotic and postzygotic, with a number of scenarios in each by which herbivore-driven changes in host plant secondary chemistry might lead to new plant lineage production. The former apply mainly to a sympatric model of speciation while the latter apply to a parapatric or allopatric model. Our review suggests that the steps of each mechanism are known to occur individually in many different systems, but no scenario has been thoroughly investigated in any one system. Nevertheless, studies of Dalechampia and its herbivores and pollinators, and patterns of defense tradeoffs in trees on different soil types in the Peruvian Amazon provide evidence consistent with the original hypotheses of Ehrlich and Raven. For herbivores to drive sympatric speciation, our findings suggest that interactions with both their herbivores and their pollinators should be considered. In contrast, herbivores may drive speciation allopatrically without any influence by pollinators. Finally, there is evidence that these mechanisms are more likely to occur at low latitudes and thus more likely to produce new species in the tropics. The mechanisms we outline provide a predictive framework for further study of the general role that herbivores play in diversification of their host plants.

Plant–herbivore coevolution and plant speciation

“…However, unlike Marquis et al. (), we do not stress the importance of inviability of hybrids produced in areas of secondary sympatry as a key mechanism maintaining incipient species.…”

“…The latter mechanism, the low fitness of hybrids, was one of the allopatric pathways proposed by Marquis et al. ().…”

“…(), that proposed six different “pathways” whereby the adaptive evolution of plant defense traits indirectly or directly could result in reproductive isolation and plant speciation ( Pathways to the evolution of plant defense driving speciation proposed by Marquis et al. ( ) ). Their first three pathways involve speciation in sympatry.…”

“…The last three pathways proposed by Marquis et al. (; Pathways to the evolution of plant defense driving speciation proposed by Marquis et al. ( ) ) involve parapatric or allopatric speciation, where the major isolating barrier is extrinsic post‐zygotic reproductive isolation caused by the reduced fitness of hybrids that are poorly defended against herbivores.…”

“…(; Pathways to the evolution of plant defense driving speciation proposed by Marquis et al. ( ) ) involve parapatric or allopatric speciation, where the major isolating barrier is extrinsic post‐zygotic reproductive isolation caused by the reduced fitness of hybrids that are poorly defended against herbivores. While extrinsic postzygotic isolation is certainly feasible (Schluter ), we suggest that herbivore‐mediated selection can lead to the evolution of other isolating barriers, and that it is therefore useful to take a broader view of how herbivory might contribute to speciation.…”