University of Wollongong Research Online Faculty of Science, Medicine and Health - Papers: part A Faculty of Science, Medicine and Health 1-1-2015 The phylogeny and evolutionary timescale of muscoidea (diptera: brachycera: calyptratae) inferred from mitochondrial genomes Shuangmei Ding China Agricultural University Xuankun Li China Agricultural University Ning Wang China Agricultural University Stephen L. Cameron Queensland University of Technology Meng Mao University of Wollongong, [email protected] See next page for additional authors Follow this and additional works at: https://ro.uow.edu.au/smhpapers Part of the Medicine and Health Sciences Commons, and the Social and Behavioral Sciences Commons Recommended Citation Ding, Shuangmei; Li, Xuankun; Wang, Ning; Cameron, Stephen L.; Mao, Meng; Wang, Yuyu; Xi, Yuqiang; and Yang, Ding, "The phylogeny and evolutionary timescale of muscoidea (diptera: brachycera: calyptratae) inferred from mitochondrial genomes" (2015). Faculty of Science, Medicine and Health - Papers: part A. 3178. https://ro.uow.edu.au/smhpapers/3178 Research Online is the open access institutional repository for the University of Wollongong. For further information contact the UOW Library: [email protected] The phylogeny and evolutionary timescale of muscoidea (diptera: brachycera: calyptratae) inferred from mitochondrial genomes Abstract Muscoidea is a significant dipteran clade that includes house flies (Family Muscidae), latrine flies (F. Fannidae), dung flies (F. Scathophagidae) and root maggot flies (F. Anthomyiidae). It is comprised of approximately 7000 described species. The monophyly of the Muscoidea and the precise relationships of muscoids to the closest superfamily the Oestroidea (blow flies, flesh flies etc)e ar both unresolved. Until now mitochondrial (mt) genomes were available for only two of the four muscoid families precluding a thorough test of phylogenetic relationships using this data source. Here we present the first two mt genomes for the families Fanniidae (Euryomma sp.) (family Fanniidae) and Anthomyiidae (Delia platura (Meigen, 1826)). We also conducted phylogenetic analyses containing of these newly sequenced mt genomes plus 15 other species representative of dipteran diversity to address the internal relationship of Muscoidea and its systematic position. Both maximum-likelihood and Bayesian analyses suggested that Muscoidea was not a monophyletic group with the relationship: (Fanniidae + Muscidae) + ((Anthomyiidae + Scathophagidae) + (Calliphoridae + Sarcophagidae)), supported by the majority of analysed datasets. This also infers that Oestroidea was paraphyletic in the majority of analyses. Divergence time estimation suggested that the earliest split within the Calyptratae, separating (Tachinidae + Oestridae) from the remaining families, occurred in the Early Eocene. The main divergence within the paraphyletic muscoidea grade was between Fanniidae + Muscidae and the lineage ((Anthomyiidae + Scathophagidae) + (Calliphoridae + Sarcophagidae)) which occurred in the Late Eocene. Disciplines Medicine and Health Sciences | Social and Behavioral Sciences Publication Details Ding, S., Li, X., Wang, N., Cameron, S. L., Mao, M., Wang, Y., Xi, Y. & Yang, D. (2015). The phylogeny and evolutionary timescale of muscoidea (diptera: brachycera: calyptratae) inferred from mitochondrial genomes. PLoS One, 10 (7), e0134170-1-e0134170-17. Authors Shuangmei Ding, Xuankun Li, Ning Wang, Stephen L. Cameron, Meng Mao, Yuyu Wang, Yuqiang Xi, and Ding Yang This journal article is available at Research Online: https://ro.uow.edu.au/smhpapers/3178 RESEARCH ARTICLE The Phylogeny and Evolutionary Timescale of Muscoidea (Diptera: Brachycera: Calyptratae) Inferred from Mitochondrial Genomes Shuangmei Ding1☯, Xuankun Li1☯, Ning Wang1,2, Stephen L. Cameron3, Meng Mao4, Yuyu Wang1, Yuqiang Xi1*, Ding Yang1* 1 Department of Entomology, China Agricultural University, Beijing, China, 2 Institute of Grassland Research, Chinese Academy of Agricultural Sciences, Hohhot, China, 3 Earth, Environmental and Biological Sciences School, Science & Engineering Faculty, Queensland University of Technology, Brisbane, Australia, 4 Centre for Medical Bioscience, School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia ☯ These authors contributed equally to this work. * [email protected] (YQX); [email protected] (DY) Abstract OPEN ACCESS Muscoidea is a significant dipteran clade that includes house flies (Family Muscidae), latrine Citation: Ding S, Li X, Wang N, Cameron SL, Mao flies (F. Fannidae), dung flies (F. Scathophagidae) and root maggot flies (F. Anthomyiidae). M, Wang Y, et al. (2015) The Phylogeny and It is comprised of approximately 7000 described species. The monophyly of the Muscoidea Evolutionary Timescale of Muscoidea (Diptera: and the precise relationships of muscoids to the closest superfamily the Oestroidea (blow Brachycera: Calyptratae) Inferred from Mitochondrial flies, flesh flies etc) are both unresolved. Until now mitochondrial (mt) genomes were avail- Genomes. PLoS ONE 10(7): e0134170. doi:10.1371/ journal.pone.0134170 able for only two of the four muscoid families precluding a thorough test of phylogenetic rela- tionships using this data source. Here we present the first two mt genomes for the families Editor: Bi-Song Yue, Sichuan University, CHINA Fanniidae (Euryomma sp.) (family Fanniidae) and Anthomyiidae (Delia platura (Meigen, Received: March 12, 2015 1826)). We also conducted phylogenetic analyses containing of these newly sequenced mt Accepted: July 6, 2015 genomes plus 15 other species representative of dipteran diversity to address the internal Published: July 30, 2015 relationship of Muscoidea and its systematic position. Both maximum-likelihood and Bayes- Copyright: © 2015 Ding et al. This is an open ian analyses suggested that Muscoidea was not a monophyletic group with the relationship: access article distributed under the terms of the (Fanniidae + Muscidae) + ((Anthomyiidae + Scathophagidae) + (Calliphoridae + Sarcopha- Creative Commons Attribution License, which permits gidae)), supported by the majority of analysed datasets. This also infers that Oestroidea unrestricted use, distribution, and reproduction in any was paraphyletic in the majority of analyses. Divergence time estimation suggested that the medium, provided the original author and source are credited. earliest split within the Calyptratae, separating (Tachinidae + Oestridae) from the remaining families, occurred in the Early Eocene. The main divergence within the paraphyletic muscoi- Data Availability Statement: All data are available from the Genbank database (accession numuber dea grade was between Fanniidae + Muscidae and the lineage ((Anthomyiidae + Scatho- KP01268 and KP01269). phagidae) + (Calliphoridae + Sarcophagidae)) which occurred in the Late Eocene. Funding: DY was funded by the National Natural Science Foundation of China (31320103902) and the National "Twelfth Five-Year" Plan for Science and Technology Support (2012BAD19B00). SLC was funded by an Australian Research Council Future Introduction Fellowship (FT120100746) The funders had no role in study design, data collection and analysis, decision Muscoidea, with approximately 7000 described species, is nearly 5% of the known species- to publish, or preparation of the manuscript. level diversity of the Diptera, the true flies [1], and includes the following four families: PLOS ONE | DOI:10.1371/journal.pone.0134170 July 30, 2015 1/17 The Phylogeny of Muscoidea Based on Mt Genomes Competing Interests: The authors have declared Scathophagidae, Anthomyiidae, Fanniidae and Muscidae. Most muscoid flies are sapropha- that no competing interests exist. gous, coprophagous or necrophagous as larvae, but some species are parasitic, predatory or phytophagous. Besides these ‘positive’ roles in the ecosystem, some species such as houseflies carry various pathogenic microorganisms (e.g. Escherichia coli, Shigella spp., Salmonella spp.) [2]. Although muscoid flies have economic and medical importance, with high ecological signif- icance, their phylogenetic relationships are still controversial. Numerous phylogenetic studies have been carried out with morphological and molecular data to reconstruct relationships either within Muscoidea or more broadly across the Calyptratae [1, 3–5]. McAlpine (1989) recovered Muscoidea as a monophyletic group based on a combination of morphological char- acter states [3], while Michelsen (1991) pointed out that Muscoidea was considered as ‘‘the Calyptratae less the Hippoboscoidea and Oestroidea” [6]. Based on four mitochondrial and four nuclear genes from 127 exemplar species of Muscoidea, Kutty et al. (2008) found that Muscoidea was paraphyletic, with the clade (Anthomyiidae + Scathophagidae) sister to a monophyletic Oestroidea. This set of relationships was subsequently also found by Kutty et al. (2010) and Wiegmann et al. (2011) in molecular analyses utilizing different taxon and gene combinations from thosed used in Kutty et al. (2008). On the other hand, in the most compre- hensive morphological phylogenetic analysis of flies ever conducted, Lambkin et al. (2013) recovered the clade Scathophagidae + (Anthomyiidae + (Muscidae + Oestroidea)) [7]; Fannii- dae was not included in this analysis. The evolutionary age of the Muscoidea has also never been directly assessed by phylogenetic means. Wiegmann et al. (2003) [8] suggested that the Calyptratae (represented by a muscid) diverged from the acalyptrates