Unravelling the evolution of mycetophagy and phytophagy in fungus weevils (Curculionoidea: Anthribidae): Phylogenomic insights into Anthribinae paraphyly and tribal non-monophyly

Abstract

Fungus weevils (family Anthribidae) are morphologically and ecologically diverse, with highly varied feeding habits, mainly mycetophagy but also phytophagy, palynophagy and entomophagy. The phylogeny of the family is virtually unexplored, its evolutionary history obscure; thus, the existing classification is controversial and likely artificial. We generated the first multi-gene higher-level phylogeny estimate of Anthribidae using DNA data from 400 nuclear genes obtained via anchored hybrid enrichment from 40 species representing 17 tribes plus genera incertae sedis. As in previous studies, the family Anthribidae was consistently recovered as the sister group of Nemonychidae. We recovered two main clades in Anthribidae as sister groups with strong statistical support, viz. a monophyletic subfamily Urodontinae and the traditionally recognized Anthribinae, which was rendered paraphyletic by the subfamily Choraginae. Paraphyly and polyphyly among tribes of Anthribinae indicate that current tribal concepts—all based on morphology and without phylogenetic analysis—are artificial. Based on our results, we subsume the subfamily Choraginae into Anthribinae and place its six current tribes (Apolectini, Araecerini, Choragini, Cisanthribini, Valenfriesiini and Xenorchestini) in an expanded subfamily Anthribinae. We also transfer three genera currently treated as Anthribinae incertae sedis to three generally recognized tribes, namely Pleosporius Holloway to Sintorini, Xylanthribus Kuschel to Proscoporhinini and Anthribidus Fåhraeus to Platystomini. The phylogenetic positions of Urodontinae and Trigonorhinini suggest that phytophagy is the ancestral feeding mode of Anthribidae, with a few taxa of Anthribinae having secondarily evolved plant-feeding from mycetophagy, the predominant feeding habit of the subfamily. Overall, our results provide the first molecular phylogenetic context for research on Anthribidae and a first step towards reconstructing a natural tribal classification of the Anthribinae. Our study highlights the need for a phylogenetic approach, sampling of type genera and deeper taxon sampling to identify natural tribal-level groupings.