The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals

Abstract

Extant terrestrial biodiversity arguably is driven by the evolutionary success of angiosperm plants, but the evolutionary mechanisms and timescales of angiosperm-dependent radiations remain poorly understood. The Scarabaeoidea is a diverse lineage of predominantly plant-and dung-feeding beetles.Here, we present a phylogenetic analysis of Scarabaeoidea based on four DNA markers for a taxonomically comprehensive set of specimens and link it to recently described fossil evidence. The phylogeny strongly supports multiple origins of coprophagy, phytophagy and anthophagy. The ingroupbased fossil calibration of the tree widely confirmed a Jurassic origin of the Scarabaeoidea crown group. The crown groups of phytophagous lineages began to radiate first (Pleurostict scarabs: 108 Ma; Glaphyridae between 101 Ma), followed by the later diversification of coprophagous lineages (crown-group age Scarabaeinae: 76 Ma; Aphodiinae: 50 Ma). Pollen feeding arose even later, at maximally 62 Ma in the oldest anthophagous lineage. The clear time lag between the origins of herbivores and coprophages suggests an evolutionary path driven by the angiosperms that first favoured the herbivore fauna (mammals and insects) followed by the secondary radiation of the dung feeders. This finding makes it less likely that extant dung beetle lineages initially fed on dinosaur excrements, as often hypothesized.

The first scarabaeid beetle (Coleoptera, Scarabaeidae, Melolonthinae) described from the Mesozoic (Late-Cretaceous) of Africa

“…These taxa include Lichniini, removed from the Glaphyridae (Hawkins, 2006), and subfamilies of the Scarabaeidae; Aclopinae, Allidiostomatinae, Euchirinae, Orphninae and Pachypodinae. The paraphyletic grade of the Melolonthinae is also supported by recent studies (Ahrens et al 2014;McKenna et al 2015). Given the uncertainties of the current phylogeny, the Orapa specimen is placed as Melolonthinae incertae sedis.…”

“…A fungivorous (Scholtz and Chown 1996) or saprophagous (Cambefort 1991) diet, the suggested ancestral diets of adult scarabaeoidea, could be possible. However, estimates of the origin of the pleurostict crown group suggest that phytophagy emerged between 109 and 128 Ma (Ahrens et al 2014) which gives some support to the proposal that the adult beetle may have fed on living plants. That the paleoenvironment of the inner crater was likely dominated by angiosperms (Bamford 1990) does at least indicate that a proportion of its sustenance, either through adult feeding or larval feeding on plant roots, humus or rotting wood, was likely derived from angiosperms, particularly if the specimen was an inhabitant of the crater environment.…”

“…The Orapa specimen's relationship to angiosperm radiation is equally unclear although its existence prior to the apparent large radiation of pleurostict scarabs in the Tertiary may suggest that even the dominance of angiosperms, approximately 60% of species during the Turonian (Lidgard and Crane 1990), was not yet sufficient to drive a major radiation in the pleurosticts. Ahrens et al (2014) suggest that this later radiation was the result of a large propagation in available niches brought about by increased angiosperm productivity and synergistic and self-propagating changes in litter and microbial conditions over wide biogeographical regions. This in turn corresponded with enrichment in pleurostict endosymbiotic gut microflora.…”

“…According to estimated divergence times given by Ahrens et al (2014), the Orapa specimen existed early in the radiation of the pleurostict scarabaeids and before the divergence of many of the extant melolonthine tribes and the subfamilies of the 'Higher Scarabaeidae' (Rutelinae, Dynastinae and Cetoniinae). The age of the Orapa specimen and its apparent basal positon in what is a very diverse and still poorly understood phylogeny (Jameson and Ratcliffe 2000), limits what can be inferred regarding its relationship to extent taxa.…”

“…Cyclocephalini) or may exhibit intra-specific variation. From the existing fossil record and divergence time estimates (Ahrens et al 2014;Krell 2006), the Dynastinae are thought to have diverged from the Rutelinae during the Palaeogene. On the balance of available evidence the placement of the specimen within the Dynastinae is thought unlikely.…”