Plant–herbivore coevolution and plant speciation

Abstract

More than five decades ago, Ehrlich and Raven proposed a revolutionary idea–that the evolution of novel plant defense could spur adaptive radiation in plants. Despite motivating much work on plant–herbivore coevolution and defense theory, Ehrlich and Raven never proposed a mechanism for their "escape and radiate" model. Recent intriguing mechanisms proposed by Marquis et al. include sympatric divergence, pleiotropic effects of plant defense traits on reproductive isolation, and strong postzygotic isolation, but these may not be general features of herbivore‐mediated speciation. An alternate view is that herbivores may impose strong divergent selection on defenses in allopatric plant populations, with plant–herbivore coevolution driving local adaptation resulting in plant speciation. Building on these ideas, we propose three scenarios that consider the role of herbivores in plant speciation. These include (1) vicariance, subsequent coevolution within populations and adaptive divergence between geographically isolated populations, (2) colonization of a new habitat lacking effective herbivores followed by loss of defense and then re‐evolution and coevolution of defense in response to novel herbivores, and (3) evolution of a new defense followed by range expansion, vicariance, and coevolution. We discuss the general role of coevolution in plant speciation and consider outstanding issues related to understanding: (1) the mechanisms behind cospeciation of plants and insects, (2) geographic variation in defense phenotypes, (3) how defensive traits and geography map on plant phylogenies, and (4) the role of herbivores in driving character displacement in defense phenotypes of related species in sympatry.

Testing Host-Plant Driven Speciation in Phytophagous Insects: A Phylogenetic Perspective

“…In addition, as underlined by contemporary researchers of Ehrlich and Raven's, it is difficult to conceive how the selection pressures exerted by insects on plant defences can drive plant speciation (Jermy 1976;Jermy 1984). Plant traits that reduce phytophagous insect attacks are rarely linked with reproductive isolation between plant populations (but see Marquis et al 2016;Maron, Agrawal & Schemske, 2019 for a review of scenarios of herbivore-induced speciation in plants) and the evidence for bursts of speciation in plants following the evolution of chemical defence is scant (Futuyma, Agrawal 2009). However this study has been and remains a great source of inspiration for studies on the diversification of plant-insect associations.…”

Evaluating species interactions as a driver of phytophagous insect divergence

“…Divergence following host shifts is pervasive in phytophagous insects and their parasitoids [26], despite the large variation in interaction outcomes. Even though coevolution might be an important driver of diversification in some cases [79,1,85,35,45,55], evolution without reciprocal adaptation might be sufficient to explain many or most cases of insect specialization. One possibility is that sensory biases, unrelated to performance on host plants, are a more general driver of divergence across phytophagous insects [41,42].…”

“…Insects comprise about two thirds of the 1.5 million described species of animals [86], and current estimates predict that another 4 million insect species remain unknown [76]. This spectacular diversity is thought to be in a large degree a result of interactions with plants [27,25,79,40,55]. Antagonism between plants and insects could lead to accelerated rates of diversification, with the diversity of defenses among plants resulting from host specialization that in turn may spur radiations in insects circumventing those defenses [40,70,21,55].…”

“…This spectacular diversity is thought to be in a large degree a result of interactions with plants [27,25,79,40,55]. Antagonism between plants and insects could lead to accelerated rates of diversification, with the diversity of defenses among plants resulting from host specialization that in turn may spur radiations in insects circumventing those defenses [40,70,21,55]. Alternatively, mutualism could also lead to highly specialized interactions and thereby promote diversification in insects and plants [83,45,46].…”

The nature of interspecific interactions and co‐diversification patterns, as illustrated by the fig microcosm

“…Finally, interactions that involve host and antagonist partners, like predation, herbivory, or parasitism, promote a third set of possible evolutionary responses (Nyman, ; Yoder & Nuismer, ; Barraclough, ; Maron et al ., ). Such interactions are generally viewed as promoting arms races, whereby evolution of new host defences favours evolution of new antagonist weapons, prompting new host defences, and so on (Janz, ; Marquis et al ., ).…”