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Phylogenetics of the keratin-feeding beetle family Trogidae (Coleoptera: Scarabaeoidea) By Werner Petrus Strümpher A THESIS SUBMITTED FOR THE DEGREE OF DOCTOR OF PHILOSOPHY at RHODES UNIVERSITY Grahamstown December 2015 Omorgus (Omorgus) gigas (Harold, 1872) Photograph by: W.P. Strümpher Summary Trogidae constitute a monophyletic and biologically unique family within the Scarabaeoidea, being the only keratinophagous group in its superfamily. Traditionally, the family has been divided into three distinctive genera, Omorgus Erichson, Polynoncus Burmeister, and Trox Fabricius. Although the taxonomy of the group is relatively well studied, recently changes to the existing classification have been proposed without the family as currently constituted being subjected to phylogenetic analyses. In this study I present the first molecular phylogeny for this cosmopolitan family, based on three partially sequenced gene regions: 16SrRNA, 18S rRNA and 28S rRNA domain 2. Analyses resolved relationships between and within genera and subgenera that are largely congruent with existing taxonomic hypotheses based on morphology. I recovered four well-supported radiations: Polynoncus, Omorgus, Holarctic Trox and Afrotropical Phoberus. One of the more surprising results was the monophyly of Phoberus. Based on the evidence, I propose reinstating the genus Phoberus to accommodate all Afrotropical (including Madagascan endemic) species. The results re-emphasise the validity of Scholtz‟s (1986a) classification system for the genus Omorgus and its subgenera and provide evidence of an African origin for Madagascan trogids. Divergence analysis was able to date the major events for the origin of extant lineages of Trogidae. The subsequent diversification of the major lineages is largely attributed to Pangaean and Gondwanan vicariance events in the Mid-Jurassic and early Late Cretaceous, respectively. The separation of the landmasses resulted in the evolution of four distinct groups: Omorgus, Polynoncus, Trox and Phoberus. The monophyletic subgenus Phoberus MacLeay is of particular interest; about one- third (14 of 40) of the species in the Afrotropical region have lost the ability to fly. To gain insights into the evolution of flightlessness in this clade, phylogenetic relationships among species were inferred using molecular sequence data. Four partial sequences of four genes (COI, 16S, 18S and 28S domain 2) were obtained for 27 species, covering all of the recognised species-groups. Estimated times of divergence were based on published mutation rates for COI. The results recovered eight monophyletic lineages, supporting the morphology-based subdivisions of the 1 genus. Flightlessness evolved at least five times within the subgenus. There is no strong support for the re-acquisition of functional wings once they are lost. Diversification, and the present relictual distributions, in African Phoberus can be linked to climatic and geological events associated with the Miocene and Pliocene Climate Optimum in southern Africa. The evolution of flightlessness in Phoberus is consistent with the habitat stability hypothesis. All flightless species occupy refugial areas with relatively long-term environmental stability. Phoberus is a promising model group for studying evolutionary trends relating to flightlessness, speciation and biogeography. Flightlessness is a counterintuitive evolutionary development, given the many advantages of flight. To interpret the diversification in the flightless Phoberus capensis Scholtz, the phylogenetic relationships among several populations of P. capensis are investigated. Phylogenetic relationships among populations were inferred using molecular sequence data that suggested three distinct evolutionary lineages, which was also supported by morphological characters. Divergence time estimates suggest a Pliocene-Pleistocene diversification. Based on these results, it is suggested that P. capensis experienced climatically-driven allopatric speciation with sheltered Afrotemperate forests and high mountain peaks serving as important refugia in response to climatic exacerbations. The P. capensis complex thus represents a speciation process in which flight-restricted populations evolved in close allopatry, possibly as recently as the Pleistocene. Two of the three divergent and geographically distinct lineages are described as novel species. This study represents the most recent comprehensive work on the Trogidae. On the basis of this study, it is proposed that taxonomic changes to the generic classification of the family be made. Trogidae are formally divided into two subfamilies, Omorginae and Troginae. The subgenus Phoberus is restored to genus rank to include all the Afrotropical species, and Afromorgus is confirmed at subgeneric rank. The genus Madagatrox is synonymised with Phoberus. 2 Table of contents Summary……………………………………………………….....……….……….……... 1 Table of contents……………………..……………………...…………………….……... 3 Preface………..…………………………………………………...………………....….... 5 Acknowledgements……………………………………………..……………...….……... 6 Declaration................................................................................................................ 7 Chapter 1: Overview of the biology, taxonomy and biogeography of the Trogidae (Coleoptera: Scarabaeoidea)……………………..………….................... 8 Overview………………...…..……………….....………….…….….……….…………. 8 Keratin-feeding specialisation................……………………….….…….…………... 9 Systematics...…….……….………………...................................................………. 13 Taxonomic history..........................................................………..…….….....……... 13 Current classification.............................................….......………..……….……...... 17 Geographic distribution of genera and subgenera.............................................… 17 Evolution and fossil record..................................................................................... 22 Molecules and phylogeny...................................................................................... 22 The scope and aim of the study...….…………….……………………….………….. 23 References……………………………………………………………………..……...... 24 Chapter 2: Phylogeny of the family Trogidae (Coleoptera: Scarabaeoidea) inferred from mitochondrial and nuclear ribosomal DNA sequence data........ 35 Abstract…………………...…………………………………………………..…..…….. 35 Introduction……………………………………………………….……………….....…. 36 Materials & Methods…………………………….………….……………………......... 39 Results…………...………………………………………………………………....…... 44 Discussion…………………………………………………………….……………….... 51 Acknowledgements……………………………...……………………………………... 58 References……………...…………………………………………….………...…….... 58 Supporting information……………………………………………….…………….….. 68 3 Chapter 3: Evolution of flightlessness in the Afrotropical Trox (Phoberus) (Coleoptera: Trogidae)........................................................................................... 86 Abstract……………………………………………………………………….….….…... 86 Introduction…………………………………………………………………….….….…. 86 Materials & Methods……………………………………………………....…......…..... 92 Results……………………………………………………...……………………….…... 103 Discussion……………………………………………………………………………..... 114 Acknowledgements……………………………………………………………........…. 120 References…………………………………………………………………………….... 120 Supporting information……………………………………………………………..….. 129 Chapter 4: Allopatric speciation in the flightless Phoberus capensis (Coleoptera: Trogidae) group, with description of two new species................. 139 Abstract……………………………………………….………………….….…….…….. 139 Introduction............................................................................................................ 139 Materials & Methods.............................................................................................. 142 Results................................................................................................................... 146 Discussion............................................................................................................. 152 Systematics........................................................................................................... 154 Acknowledgements………………………………………………......………….......… 161 References............................................................................................................ 161 Supporting information........................................................................................... 169 Chapter 5: Overview and revision of the extant genera and subgenera of Trogidae (Coleoptera: Scarabaeoidea)………….................................................. 178 Abstract.................................................................................................................. 178 Introduction............................................................................................................ 178 Taxonomy.............................................................................................................. 191 References............................................................................................................ 205 Appendix 1............................................................................................................. 213 Appendix 2............................................................................................................. 218 Chapter 6: General conclusion.............................................................................. 222 4 Preface This thesis comprises six chapters. The first and last chapters provide a
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