THE PERMIAN ORIGIN OF WOOD-BORING BEETLES AND THEIR ECOLOGICAL CONTEXT

Beetles have been the most diverse group of macroscopic organisms probably since the mid Mesozoic. This elevated level of speciosity is reflected by diverse feeding strategies that involve interactions with plant substrates such as leaves, seeds and wood. Wood boring is a life habit present in numerous lineages of beetles representing several taxonomic families that, in conjunction with fungi from their gut and ambient microenvironment, allows nutritional access to consumed tissues such as bark and heartwood, as well as more nutritional phloem and cambium tissues. Nevertheless, the life habits and early evolution of wood-boring beetles remain clouded in a mystery from a poor, uninformative fossil record. We report new data from exceptionally preserved woods from the upper Permian (254–252 Ma) of China that document a microcosm of ecological associations involving a beetle wood-borer (Clade Polyphaga), deuteromycete fungi, pygmephorid and oribatid mites, a chelicerate and other cohabitants that consumed trunk tissues of the early conifer Ningxiaites specialis. The multiple examples of wood boring networks consisted of: (i) presence of an entry tunnel through bark, (ii) mother gallery built from evacuated cambium, (iii) placement of up to 11 eggs in a lateral niche series, (iv) emergence of multi-instar, parallel-oriented larval tunnels through cambium, wood and bark, and (v) the separate exit of larvae through tunnels. This wood-boring system became ecologically convergent with Early Cretaceous bark-beetle borings 120 million later. These data indicate that the most diverse lineage of organisms, Polyphaga, got its ecological and evolutionary start in Permian conifers in association with tritrophic nutritional dependence on wood and cellulytic fungi. These beetles exploited a primitive form of agriculture convergent with bark beetles that required subsociality. The conditions for subsociality―shelter in the same microenvironment, group living and cooperation, division of labor and colony defense―all were satisfied by the wood-boring network. The demise of this unique wood-boring association at the end of the Permian and its re-evolution 120 million years later by bark beetles is a spectacular example in the behavioral and ecological convergence in the fossil insect record.