If Dung Beetles (Scarabaeidae: Scarabaeinae) Arose in Association with Dinosaurs, Did They Also Suffer a Mass Co-Extinction at the K-Pg Boundary?

Nicole L Gunter,Stephen L Cameron,Adam Slipinksi,Tom A Weir,Ladislav Bocak,Ben J Mans

doi:10.1371/journal.pone.0153570

Abstract

The evolutionary success of beetles and numerous other terrestrial insects is generally attributed to co-radiation with flowering plants but most studies have focused on herbivorous or pollinating insects. Non-herbivores represent a significant proportion of beetle diversity yet potential factors that influence their diversification have been largely unexamined. In the present study, we examine the factors driving diversification within the Scarabaeidae, a speciose beetle family with a range of both herbivorous and non-herbivorous ecologies. In particular, it has been long debated whether the key event in the evolution of dung beetles (Scarabaeidae: Scarabaeinae) was an adaptation to feeding on dinosaur or mammalian dung. Here we present molecular evidence to show that the origin of dung beetles occurred in the middle of the Cretaceous, likely in association with dinosaur dung, but more surprisingly the timing is consistent with the rise of the angiosperms. We hypothesize that the switch in dinosaur diet to incorporate more nutritious and less fibrous angiosperm foliage provided a palatable dung source that ultimately created a new niche for diversification. Given the well-accepted mass extinction of non-avian dinosaurs at the Cretaceous-Paleogene boundary, we examine a potential co-extinction of dung beetles due to the loss of an important evolutionary resource, i.e., dinosaur dung. The biogeography of dung beetles is also examined to explore the previously proposed “out of Africa” hypothesis. Given the inferred age of Scarabaeinae as originating in the Lower Cretaceous, the major radiation of dung feeders prior to the Cenomanian, and the early divergence of both African and Gondwanan lineages, we hypothesise that that faunal exchange between Africa and Gondwanaland occurred during the earliest evolution of the Scarabaeinae. Therefore we propose that both Gondwanan vicariance and dispersal of African lineages is responsible for present day distribution of scarabaeine dung beetles and provide examples.

Highlights

Recent explanations for the extraordinary diversity of insects, both at the species- and higher taxonomic levels, have largely centered on the role of co-diversification with flowering plants [1]
We present the first evidence of the mid-Cretaceous origin, and Upper Cretaceous radiation of dung beetles, the timing of which is consistent with major global events including rise of the angiosperms and continental breakup of Gondwana
We hypothesise that a change in host diet, to incorporate more nutritious and less fibrous angiosperm foliage, provided a palatable dung source for dung beetle feeding creating a new niche for diversification

Summary

Introduction

Recent explanations for the extraordinary diversity of insects, both at the species- and higher taxonomic levels, have largely centered on the role of co-diversification with flowering plants (angiosperms) [1]. The majority of studies in this area, concern taxa with tight ecological associations with plants (i.e. herbivores or pollinators) and to date no model of the influence of angiosperm evolution on non-herbivorous insects has ever been proposed. Even though non-herbivores represent ~40% of beetle genera [2], potential evolutionary drivers have largely gone unexamined (c.f. Hunt et al [8]), but given that many saprophagous and predatory beetles do not have specialist diets (host or prey species) coevolution paradigms cannot be applied [9]

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