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Mitogenome of Coprophanaeus Ensifer and Phylogenetic Analysis of the Scarabaeidae Family (Coleoptera)

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Mitogenome of Coprophanaeus Ensifer and Phylogenetic Analysis of the Scarabaeidae Family (Coleoptera) Genetics and Molecular Biology, 44, 3, e20200417 (2021) Copyright © Sociedade Brasileira de Genética. DOI: https://doi.org/10.1590/1678-4685-GMB-2020-0417 Research Article Evolutionary Genetics Mitogenome of Coprophanaeus ensifer and phylogenetic analysis of the Scarabaeidae family (Coleoptera) Catarine Aragone de Albuquerque Mello1*, Igor Costa Amorim1*, Alexandre Freitas da Silva2, Giuliene Rocha de Medeiros1, Gabriel Luz Wallau2 and Rita de Cássia de Moura1 1Universidade de Pernambuco, Instituto de Ciências Biológicas, Laboratório de Biodiversidade e Genética de Insetos, Recife, PE, Brazil. 2Departamento de Entomologia, Instituto Aggeu Magalhães – FIOCRUZ, Recife, Pernambuco, Brazil. Abstract Several studies about the phylogenetic relationships of the Scarabaeinae subfamily (Coleoptera: Scarabaeidae) have been performed, but some phylogenetic uncertainties persist including the relationship and monophyly of different tribes and some genera. The aim of this study was to characterize the mitogenome of Coprophanaeus ensifer in order to establish its position within the Scarabaeidae family and to contribute to the resolution of some phylogenetic uncertainties. The mitogenome was sequenced on the Illumina HiSeq 4000, assembled using the Mitobim software and annotated in MITOS WebServer. The phylogenetic trees were reconstructed by Bayesian inference. The C. ensifer mitogenome is a molecule of 14,964 bp that contains the number and organization of the genes similar to those of most Coleoptera species. Phylogenetic reconstruction suggests monophyly of the tribe Phanaeini and supports the hypothesis that Coprini is a sister group of Phanaeini. The results also revealed the position of the tribe Oniticellini which is grouped with Onthophagini and Onitini. The geographic distribution of these species that form the most ancestral clade suggests with Scarabaeinae originated in Africa. Keywords: Dung beetle, mitochondrial genome, phylogenomics. Received: November 12, 2020; Accepted: May 02, 2021. Introduction 2002; Bai et al., 2011; Tarasov and Génier, 2015; Tarasov In the order Coleoptera, the family Scarabaeidae is and Dimitrov, 2016 and references therein). Differences in particularly interesting due to its large adaptive radiation, the number of lineages have also been reported for Coprini, as well as being formed by lineages with different feeding with descriptions of two or three lineages (Philips et al., 2004; habits, including phytophagous, saprophagous and copro- Monaghan et al., 2007). necrophagous species (Gunter et al., 2016). The species of The phylogenetic relationships of some Scarabaeinae this family were grouped into 19 subfamilies (Smith, 2009); tribes are also contradictory; for example, the relationships among these, Scarabaeinae are important because these among the Deltochilini, Eurysternini, Onthophagini, Oniticellini, beetles provide ecosystem services such as recycling of Onitini and Sisyphini tribes are frequently altered (Tarasov organic matter, biological control of agricultural pests, and and Génier, 2015). The position of the tribe Phanaeini is also secondary seed dispersal (Nichols et al., 2008). This subfamily uncertain since it formed a sister group with the tribe Eucraniini is characterized by high species diversity, with about 6,200 in molecular studies (Ocampo and Hawks, 2006; Monaghan et species taxonomically grouped into 267 genera and 12 tribes al., 2007) and with the tribe Coprini in morphological studies (Tarasov and Génier, 2015). (Philips et al., 2004). Furthermore, based on morphological Most phylogenetic studies indicate that eight of the 12 analyses, Vaz-de-Mello (2007) showed that Phanaeini also Scarabaeinae tribes are monophyletic (Eucraniini, Eurysternini, formed a cluster with Eucraniini, Onitini, and Onthophagini. Gymnopleurini, Oniticellini, Onitini, Phanaeini, Scarabaeini, In the tribe Phanaeini, phylogenetic uncertainties and Sisyphini) and one is polyphyletic (Deltochilini) (Tarasov have also been described within the genus Coprophanaeus and Génier, 2015). Contradictory results have been described d’Olsoufieff, 1924 (Maldaner et al., 2018). Phylogenetic for the remaining tribes (Ateuchini, Coprini, and Onthophagini), analyses based on molecular markers (mitochondrial COI, COII with morphological and/or molecular analyses suggesting and 16S genes) indicated Coprophanaeus to be paraphyletic, monophyly of these tribes, although they are frequently since the species of this genus form a clade with Diabroctis reported as being paraphyletic or polyphyletic (Villalba et al., mirabilis and Sulcophanaeus faunus (Maldaner et al., 2018). Within the genus Coprophanaeus, taxonomic uncertainty also exists regarding C. (Megaphanaeus) ensifer (Maldaner et al., Send correspondence to Rita de Cássia de Moura. Universidade de 2018). Individuals of this species exhibit a large variation in Pernambuco, Brasil, Laboratório de Biodiversidade e Genética de size, color and geographic distribution, suggesting the presence Insetos, Instituto de Ciências Biológicas, Rua Arnóbio Marques, 310, 50.100-130 Recife, PE, Brazil. E-mail: [email protected]. of cryptic species (Maldaner et al., 2019). Considering the phylogenetic and taxonomic uncertainties, *These authors contributed equally to this article. more robust analyses (using larger datasets) of Scarabaeinae 2 Mello et al. tribes, genera and species are necessary (Tarasov and Dimitrov, sequence was uploaded to the MITOS WebServer for gene 2016). In view of the absence of recombination and exclusively annotation of the C. (M.) ensifer mitogenome using the genetic maternal inheritance in animals, mitochondrial DNA is used code 05 - invertebrate. for phylogeographic inferences (Boore and Brown, 1998), resolution of taxonomic uncertainties, and phylogenetic Phylogenetic analysis reconstructions (Vilstrup et al., 2011). Specific mitochondrial The phylogenetic trees were reconstructed using two genes (Baca et al., 2017; Nolasco-Soto et al., 2017; Villastrigo datasets: 1) complete nucleotide sequence of the mitogenome, et al., 2019), or the complete mitogenome can be used in except for the control region; 2) concatenated amino acid such studies, conferring greater robustness to the analysis by sequence of protein-coding genes of the mitogenome. In addition providing a larger set of molecular data (Yuan et al., 2016; to the mtDNA of C. (M.) ensifer, we used the Scarabaeidae Nie et al., 2018). Based on the mitogenome, phylogenetic mitogenomes available at NCBI until September, 2019. These uncertainties were resolved in different taxonomic groups, mitogenomes included species of Scarabaeinae (32 spp.), including the beetle family Chrysomelidae (Nie et al., 2018). Melolonthinae (6 spp.), Rutelinae (3 spp.), Cetoniinae (3 spp.), The present study aimed to characterize the mitochondrial Aphodiinae (3 spp.), and Dinastinae (1 spp.). Additionally, DNA of C. (M.) ensifer and to investigate the phylogenetic three species of the family Lucanidae were included as relationships within the family Scarabaeidae. In addition, this outgroups (Prosopocoilus gracilis, Odontolabis cuvera study provides molecular markers that can be used to test fallaciosa, Dynodorcus curvidens hopei), since this family specific taxonomic hypothesis such as assessing the presence is considered sister group to Scarabaeidae, according to of cryptic species in C. (M.) ensifer. molecular and morphological evidence (Grebennikov and Scholtz, 2004; Timmermans et al., 2016; Yang et al., 2018). Material and Methods These sequences were retrieved from the National Center for Biotechnology Information database (NCBI). The accession Collection of the biological sample numbers are listed in Table S1. The resulting sequences were Coprophanaeus (M.) ensifer (Germar, 1821) specimens aligned using MAFFT and then treated with Gblock 0.91b were collected in Aldeia, Camaragibe (8º1’18” S; 34º58’52” using default parameters (Castresana, 2000). W), Pernambuco, Brazil, with pitfall traps baited with rotten For phylogenetic analysis, the GTR G+I and MtREV meat. This collection was authorized by IBAMA/SISBIO G+I+F substitution models were used for nucleotide and protein through the permanent license of zoological material of the sequences, respectively. These models were selected based on class Insecta (16278 – 1). The specimens were identified at Akaike’s information criterion (AIC) using jModelTest v. 2.1.4 the Laboratory of Biodiversity and Insect Genetics (LGBI), (Darriba et al., 2012) and ProtTest v. 3.4.2 (Abascal et al., University of Pernambuco (UPE), using the identification key 2005). The trees were reconstructed by Bayesian inference on of the genus Coprophanaeus (Edmonds and Zídek, 2010) and the CIPRES Science Gateway webserver using the following by comparison with other specimens of the Entomological MCMC parameters: Number of generations of 10 million, Collection of the University of Pernambuco (CEUPE), sampling every 1,000 generations, four Markov chains, and Laboratory of Biodiversity and Genetics of Insects (LBGI), burn-in of 20%. The tree was visualized and edited using Institute of Biological Sciences, University of Pernambuco, Figtree v. 1.4.3 (Rambaut, 2016). Pernambuco, Brazil (curator: Rita de Cássia de Moura). In addition, the identification was confirmed by the taxonomist Results and Discussion Fernando Silva (UFPA). The specimens were sacrificed and stored in 100% alcohol until the time of DNA extraction. Characterization of the mitogenome Only one specimen was used for this study. The analysis
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