Abstract

Weevils (Coleoptera: Curculionoidea) represent one of the most diverse groups of organisms on Earth; interactions with their host plants have been recognized to play a central role in their remarkable diversity, yet the exact mechanisms and factors still remain poorly understood. Using phylogenetic comparative analyses, here we investigate the evolution of host use and its possible role in diversification processes of Rhinusa and Gymnetron, two closely related groups of weevils that feed and develop inside plant tissues of hosts within the families Scrophulariaceae and Plantaginaceae. We found strong evidence for phylogenetic conservatism of host use at the plant family level, most likely due to substantial differences in the chemical composition of hosts, reducing the probability of shifts between host families. In contrast, the use of different plant organs represents a more labile ecological trait and ecological niche expansion that allows a finer partitioning of resources. Rhinusa and Gymnetron weevils initially specialized on plants within Scrophulariaceae and then shifted to the closely related Plantaginaceae; likewise, a gall inducing behavior evolved from non-galler weevils, possibly in response to resource competition, as galls facilitate larval development by providing enhanced nutrition and a favorable microhabitat. Results from trait-dependent diversification analyses suggest that both use of hosts within Plantaginaceae and parasitism on fruits and seed capsules are associated with enhanced diversification of Rhinusa and Gymnetron via low extinction rates. Our study provides quantitative evidence and insights on the ecological factors that can promote diversification in phytophagous insects that feed and develop inside plant tissues.

Highlights

  • Comprising approximately 5,800 genera and more than 60,000 described species (Oberprieler, Anderson & Marvaldi, 2014; Oberprieler, Marvaldi & Anderson, 2007), weevils (Coleoptera: Curculionoidea) have been described as one of the most successful adaptive radiations on Earth (Mayr, 1963; McKenna et al, 2009)

  • Phylogenetic conservatism of traits associated with host plant use Rhinusa and Gymnetron represent two non-reciprocally monophyletic groups with deep genetic divergences between southern Africa and Palearctic lineages (Hernández-Vera et al, 2013)

  • When host plant use is categorized according to the plant parts being parasitized and as gall inducer vs. non gall inducer, the distribution of characters over the Bayesian consensus tree is marginally significant at the 0.05 confidence level, that is, in both cases the difference between the expected and observed number of parsimony steps is only one

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Summary

Introduction

Comprising approximately 5,800 genera and more than 60,000 described species (Oberprieler, Anderson & Marvaldi, 2014; Oberprieler, Marvaldi & Anderson, 2007), weevils (Coleoptera: Curculionoidea) have been described as one of the most successful adaptive radiations on Earth (Mayr, 1963; McKenna et al, 2009). We focus attention on species from the closely related genera Rhinusa and Gymnetron (Curculionidae: Curculioninae), endophagous parasitic weevils whose larvae feed and develop within tissues of plant species in the families Scrophulariaceae and Plantaginaceae. The genus Rhinusa comprises approximately 40 species with a Palearctic distribution (Caldara, 2001, 2013) that feed on species within the plant genera Verbascum and Scrophularia in the family Scrophulariaceae and Linaria, Kickxia, Chaenorhinum, Antirrhinum and Misopates within the family Plantaginaceae (Caldara, Sassi & Toševski, 2010). Mitochondrial and nuclear DNA sequence data has revealed cryptic host-associated diversity within the species Rhinusa antirrhini (Hernández-Vera et al, 2010) and R. pilosa (Toševski et al, 2015); several evolutionary lineages were found to be associated with species and subspecies in the genus Linaria, suggesting host specialization as a likely driver for diversification

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