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Coleoptera: Scarabaeidae) and Adaptations to Coprophagous Habits Ming Bai1*†, Sha Li1,2†, Yuanyuan Lu1,2, Haidong Yang1, Yijie Tong1 and Xingke Yang1*

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Coleoptera: Scarabaeidae) and Adaptations to Coprophagous Habits Ming Bai1*†, Sha Li1,2†, Yuanyuan Lu1,2, Haidong Yang1, Yijie Tong1 and Xingke Yang1* Bai et al. Frontiers in Zoology (2015) 12:30 DOI 10.1186/s12983-015-0123-z RESEARCH Open Access Mandible evolution in the Scarabaeinae (Coleoptera: Scarabaeidae) and adaptations to coprophagous habits Ming Bai1*†, Sha Li1,2†, Yuanyuan Lu1,2, Haidong Yang1, Yijie Tong1 and Xingke Yang1* Abstract Introduction: The astonishing spectrum of scarabaeine lifestyles makes them an attractive group for studies in entomology and evolutionary biology. As a result of adaptions to specific food substrates and textures, the mouthparts of dung beetles, particularly the mandible, have undergone considerable evolutionary changes and differ distinctly from the presumptive ancestral conditions of the Coleoptera and Polyphaga. The possible functions of dung beetle mouthparts and the evolution of dung feeding have been controversial for decades. Results: In this study, 187 scarabs representing all tribes of the Scarabaeinae and the major lineages within the Scarabaeoidea, along with three major feeding types within the Scarabaeoidea (omnivory, phytophagy and coprophagy), were studied. Based on geometric morphometric and three-dimensional (3D) reconstruction approaches, morphological differences in mandibles among the three feeding types were identified. The ancestral forms of the mandible within the Scarabaeinae were reconstructed and compared with those of modern species. The most recent common ancestor of theScarabaeinaefedonsoftmaterials,and the ancestor of the Scarabaeinae and the Aphodiinae was in an evolutionary transition between processing more solid and softer substrates. Conclusions: Coprophagy originated from omnivorous ancestors that were very likely saprophagous. Furthermore, phytophagy may also have originated from omnivory. In addition, our study addresses the integration and modularity of geometric morphometric data in a phylogenetic context. Keywords: Coprophagy, Dung beetle, Mouthparts, 3D, Geometric morphometric Introduction that is considered highly desirable and nutritious to po- Decomposers use deceased organisms and non-living or- tential dung colonizers. A typical dung community con- ganic compounds as their food source. By breaking sists of dung feeders or predators, many of which are down dead material, they provide nutrients that are cru- beetles. These groups include species of the scarabaeoid cial to the environment and essential for the survival of Scarabaeinae, Aphodiinae, Geotrupidae, and Hybosori- other organisms. Many species of bacteria, fungi and dae, and the hydrophiloid Sphaeridiinae, which use dung protists, the primary decomposers, are unable to ingest as a food substrate, but also include predaceous beetles discrete masses of matter, but instead absorb and belonging to the Staphylinidae or Histeridae. The true metabolize resources on a molecular scale. Insect de- dung beetles belong to a single taxonomic entity and composers, such as dung beetles, burying beetles, fly clade, the scarabaeid subfamily Scarabaeinae, which con- maggots, and others generally consume larger quantities sists of nearly 6000 described species grouped into 240 of organic matter [1]. Vertebrate dung is a special niche genera [2]. The very broad spectrum of scarabaeine life- styles, including elaborate nesting behaviors and special- * Correspondence: [email protected]; [email protected] ized food preferences, has long fascinated insect †Equal contributors researchers [3, 4]. 1Key Laboratory of Zoological Systematics and Evolution, Institute of Adult and larval dung beetles are primarily copropha- Zoology, Chinese Academy of Sciences, Box 92Beichen West RoadChaoyang District, Beijing 100101, People’s Republic Of China gous. However, their feeding habits are not limited to Full list of author information is available at the end of the article this substrate. Many species are known to specialize on © 2015 Bai et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Bai et al. Frontiers in Zoology (2015) 12:30 Page 2 of 10 carrion, the fruiting bodies of basidiomycote fungi, squeezed by the molar lobes while the superfluous liquid freshly dead millipedes [5, 6], rotting fruit and leaves, or was drawn away from the pharynx through filtration the debris of attine leaf-cutter ants. There are even spe- channels. The compacted material formed from com- cies that are predators of millipedes [7], reproductive pressed small particles was then ingested. ants, and termites. All of these food substrates are more Oneproposedevolutionaryscenarioisthatadult or less soft and contain significant moisture. As a result Scarabaeoidea shifted from harder and drier sub- of adaptions to food texture, the mouthparts of dung strates (i.e., detritus) to a softer and moister diet beetles have deviated considerably from the basic struc- (dung) [3]. Although there are some discrepancies in ture of the Coleoptera. In general, the major compo- the detailed evidence presented [4], it is generally nents of the Scarabaeinae mouthparts tend to be agreed that dung beetles likely evolved from a membranous and hairy (Fig. 1). The most variable elem- detritus-feeding ancestor, a hypothesis that is based ent shows greatly weakened mandibular incisor lobes on qualitative observations [14]. To date, quantitative that are poorly adapted for the cutting of hard food. In analyses, including an approach using geometric mor- addition, fine but robust ridged molar areas with a con- phometrics, have been lacking [15–17]. To test this vex surface fitting tightly into the opposing concave sur- scenario and to reconstruct the evolution of the char- face are present in these mandibles [3, 4]. The acter system, we selected the mandible, the most de- morphology of the other mouthparts is not significantly rived mouthpart component, from 187 species different from the basic structure of the Coleoptera, ex- representing all major lineages of the Scarabaeoidea, cept that the labrum-epipharynx is membranous and with comprehensive sampling from the Scarabaeinae, hairy, the maxillae is lacking a hook or tooth on the laci- for this study (Additional file 1: Table S1). Three nia and there are strong paraglossae and very weak glos- feeding types (omnivory, phytophagy and coprophagy) sae in the labium. The membranous and hairy elements were evaluated, and only the Scarabaeinae (true dung remove large fragments from the food and scoop liquid beetles) were treated as coprophagous (see Materials components into the oral cavity [8]. and methods for details). The mandibles associated The possible functions of the dung beetle mouthparts with the three feeding types were initially compared have been a subject of controversy for decades (Fig. 1). based on two-dimensional (2D) and 3D morphological It was presumed that the molar lobes crush large parti- observations. The morphological variations of the cles into much finer ones that are then imbibed [3]. mandible of studied species were then analyzed using However, trituration of dung particles was not confirmed geometric morphometrics. The ancestral form of the in a serial experiment by Holter [9–13]. Moreover, Hol- mandible for the studied species was reconstructed. ter [9] assumed that the food was collected by the maxil- Last, based on the obtained results, the evolution of lary palps, that the large particles were brushed out by the mandibles, which play a crucial role in feeding filtration setae on the mouthparts (primarily the maxillae behavior, was inferred, and coprophagous adaptations and labium), and that the remaining paste was then were discussed. Our study also addresses the Fig. 1 Mouthparts of coprophagous and phytophagous scarabs. Mandible (a, e); maxillary (b, f); epipharynx (c, g); labium (d, h). Coprophagous scarabs (a–d) represented by a: Synapsis yunnanus, b: Heliocopris dominus, c: Onthophagus (Palaeonthophagus) gibbulus, and d: Paracopris punctulatus. Phytophagous scarabs (e–h) represented by Mimela passerinii mediana. One curve (=50 landmarks) was selected from the mandible (a) for the geometric morphometric analysis Bai et al. Frontiers in Zoology (2015) 12:30 Page 3 of 10 integration and modularity of geometric morphomet- of the Scarabaeoidea for the phylogenetic and morpho- ric data in a phylogenetic context. metric analyses [20–22]. Micro-CT scanning and three-dimensional reconstruction Materials and methods The mandibles from three specimens representing Taxa examined three feeding types were scanned with an X-radia 400 This study is based on exemplars of 187 species, most of at the Institute of Zoology, Chinese Academy of Sci- which are housed at the Institute of Zoology, Chinese ences (beam strength: 60KV, absorption contrast). Academy of Sciences, and additional photographs of Micro-computed tomography (micro-CT) images were mandibles of species from the literature (Additional file 1: used for the 3D reconstructions. Based on the obtained Table S1). The specimens were examined and dissected image stacks, the structures of the specimens were re- using a LEICA MZ 12.5 dissecting microscope. Ethical constructed
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