The genetic basis of a plant–insect coevolutionary key innovation

Abstract

Ehrlich and Raven formally introduced the concept of stepwise coevolution using butterfly and angiosperm interactions in an attempt to account for the impressive biological diversity of these groups. However, many biologists currently envision butterflies evolving 50 to 30 million years (Myr) after the major angiosperm radiation and thus reject coevolutionary origins of butterfly biodiversity. The unresolved central tenet of Ehrlich and Raven's theory is that evolution of plant chemical defenses is followed closely by biochemical adaptation in insect herbivores, and that newly evolved detoxification mechanisms result in adaptive radiation of herbivore lineages. Using one of their original butterfly-host plant systems, the Pieridae, we identify a pierid glucosinolate detoxification mechanism, nitrile-specifier protein (NSP), as a key innovation. Larval NSP activity matches the distribution of glucosinolate in their host plants. Moreover, by using five different temporal estimates, NSP seems to have evolved shortly after the evolution of the host plant group (Brassicales) (Ϸ10 Myr). An adaptive radiation of these glucosinolate-feeding Pierinae followed, resulting in significantly elevated species numbers compared with related clades. Mechanistic understanding in its proper historical context documents more ancient and dynamic plant-insect interactions than previously envisioned. Moreover, these mechanistic insights provide the tools for detailed molecular studies of coevolution from both the plant and insect perspectives.adaptive radiation ͉ Brassicales ͉ Pieridae ͉ diversification ͉ Bayesian relaxed molecular clock

Macroevolution and the biological diversity of plants and herbivores

“…In conformity with Ehrlich and Raven's scenario (4), most of the diversification of insect host associations is based on shifts among plant lineages that had evolved earlier, for almost no instances of cospeciation or congruence between plant and insect phylogenies have been described, and molecular dating shows that at least some insect clades are younger than the plant clades with which they are associated (71). For example, the radiation of pierine butterf lies (cabbage white and relatives) began Ϸ10 million years after the diversification of the glucosinolate-containing Brassicales (72). There is some evidence, as yet more intriguing than definitive, that the diversification of insect clades is temporally correlated, although time-lagged, with the diversification of their host-plant clades, a point to which we return later (71).…”

“…The radiation of insect clades associated with specific plant clades shows a degree of temporal correspondence. For example, Zwölfer and Herbst (105) suggested, based on fossil and biogeographic evidence, that the weevil genus Larinus is as old (Oligocene) as the thistle clade with which it is associated, and molecular clock estimates suggest that the butterfly subfamily Pierinae arose within Ϸ10 million years of the origin of its hosts (72). How long such clade-level associations, indicative of phylogenetic conservatism, persist is uncertain.…”

“…Still less do we know whether adaptation to chemically distinct plants fosters adaptive radiation. In perhaps the most convincing example, Wheat et al (72) ascribe the radiation of the butterfly subfamily Pierinae, which is much more diverse than its sister group, to the evolution of a nitrile-specifier protein that detoxifies the glucosinolate defenses of their diverse Brassicales hosts. In this Special Feature, Winkler et al (92), in a new phylogenetic analysis, provide evidence that evolutionary shifts to chemically different plant clades are associated with elevated diversification in leafmining flies.…”

Host plants and immatures as mate-searching cues in Heliconius butterflies

“…Although the influence of host plants in the sexual behaviour of other phytophagous insects is well established (Landolt & Phillips 1997), ours is the first study that has investigated their importance in butterflies. Adaptation allowing shifts to new larval hosts has been widely accepted as an important driver in butterfly diversification (Ehrlich & Raven 1964;Braby & Trueman 2006;Mullen 2006;Weingartner et al 2006;Wheat et al 2007;Pena & Wahlberg 2008). Measuring to what extent host plants are used as matesearching cues is then relevant to understanding how such evolutionary processes have been facilitated by this interaction.…”

Climate and host‐plant associations shaped the evolution of ceutorhynch weevils throughout the Cenozoic

“…Recent studies inferring the timing and pattern of the crucifers’ chemical defense mechanisms (the mustard oil glucosides) and the counter adaptations of Pierinae (the nitrile‐specifier protein gene) provide strong evidence for an ancient arms race between these butterflies and crucifers that escalated in complexity over time (Wheat et al. 2007; Winde and Wittstock 2011; Edger et al. 2015).…”