Temporal lags and overlap in the diversification of weevils and flowering plants

Abstract

The extraordinary diversity of herbivorous beetles is usually attributed to coevolution with angiosperms. However, the degree and nature of contemporaneity in beetle and angiosperm diversification remain unclear. Here we present a large-scale molecular phylogeny for weevils (herbivorous beetles in the superfamily Curculionoidea), one of the most diverse lineages of insects, based on approximately 8 kilobases of DNA sequence data from a worldwide sample including all families and subfamilies. Estimated divergence times derived from the combined molecular and fossil data indicate diversification into most families occurred on gymnosperms in the Jurassic, beginning approximately 166 Ma. Subsequent colonization of early crown-group angiosperms occurred during the Early Cretaceous, but this alone evidently did not lead to an immediate and major diversification event in weevils. Comparative trends in weevil diversification and angiosperm dominance reveal that massive diversification began in the mid-Cretaceous (ca. 112.0 to 93.5 Ma), when angiosperms first rose to widespread floristic dominance. These and other evidence suggest a deep and complex history of coevolution between weevils and angiosperms, including codiversification, resource tracking, and sequential evolution.

Fig. 1.

Curculio proboscideus (Curculionidae: Curculioninae) perched atop a flower of Helianthus sp. (Asteraceae). Note the elongation of the head to form the characteristic weevil rostrum or “snout.” In some groups, the rostrum is not only used for feeding, but also for preparing oviposition sites and placing eggs deep inside plant tissues (Photo credit: D. McKenna).

Fig. 2.

Maximum clade credibility tree for weevils based on the minimum age Bayesian analysis. Bayesian PP ≥ 0.50 and maximum likelihood BS values ≥ 50% are shown on the tree (PP/BS). Ninty-five percent confidence intervals for the ages of family- and subfamily-level clades, and for the ingroup, are indicated with blue bars. Letters correspond to fossil calibration points used in the molecular dating analysis. Numbers of described species are from ref. . Images of weevil exemplars are not to scale. Outgroups have been removed.

Fig. 3.

Superimposed plots of stem-group divergence times for the earliest representatives of major weevil clades (maximum fossil age analysis, white circles; minimum fossil age analysis, black circles) and angiosperm dominance over the course of the Cretaceous [black curve (adapted from ref. 9)], reveal evidence for an increase in weevil diversity beginning during the mid Cretaceous, concurrent with the rise of angiosperms to widespread floristic dominance, and well after the first appearance of crown-group angiosperms [fossils ≈132–141 Ma (24), molecules ≈140–180 Ma (25)]. Note that Anthribidae is shown here separate from Nemonychidae (from which it is derived in our analyses), in order to accurately illustrate the disparate timing of origin and magnitude of extant diversity in these 2 groups (the species-poor anthribid subfamily Urodontinae is not shown separately from other Anthribidae). We propose that this temporal lag in the diversification of angiosperm-associated weevils is evidence for the combined major role of ecological-evolutionary opportunity and intrinsic traits (fine-tuned, elaborated, and accumulated over the course of a long history of association with living, dead, dying, and decaying plants and plant organs and tissues) in the evolutionary radiation of weevils. Patterns of weevil diversification during the time interval between the origin of each major weevil clade and the present remain unclear.