Abstract
Protomiltogramma Townsend is the largest and most diverse genus of miltogrammine flesh flies in Australia. However, no comprehensive taxonomic work had been completed on the Australian members of this genus in almost a century. This study presents the first taxonomic revision of all Australian species of Protomiltogramma (Sarcophagidae: Miltogramminae), completed using an integrative approach combining molecular and morphological data. Eight new species endemic to Australia are described: P. dalbiensis sp. n., P. grandis sp. n., P. incana sp. n., P. kapnos sp. n., P. nigrisensa sp. n., P. popularis sp. n., P. rubra sp. n. and P. subtilis sp. n. In addition, P. australis Malloch, 1930 is synonymised with P. cincta Townsend, 1916, syn. n. and P. mallochi Verves, 1987 is synonymised with P. laticeps Malloch, 1930, syn. n. Molecular phylogenetics is used to place the Australian Protomiltogramma among the miltogrammine genera of the world.
References
Aljanabi, S.M. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25, 4692–4693. https://doi.org/10.1093/nar/25.22.4692
Baker, G.L. & Pigott, R. (1983) Parasitism of the Australian plague locust Chortoicetes terminifera (Walker) (Orthoptera: Acrididae) by Prionyx saevus (Smith) (Hymenoptera: Sphecidae). Australian Entomology Magazine, 10, 67–74.
Baranov, N. (1938) Neue indo-australische Tachinidae. Bulletin of Entomological Research, 29, 405–414. https://doi.org/10.1017/S0007485300026304
Buenaventura, E., Szpila, K., Cassel, B.K., Wiegmann, B.M. & Pape, T. (2020) Anchored hybrid enrichment challenges the traditional classification of flesh flies (Diptera: Sarcophagidae). Systematic Entomology, 45, 281–301. https://doi.org/10.1111/syen.12395
Butterworth, N.J., Byrne, P.G. & Wallman, J.F. (2019) The blow fly waltz: field and laboratory observations of novel and complex dipteran courtship behavior. Journal of Insect Behavior, 32, 109–119. https://doi.org/10.1007/s10905-019-09720-1
Cumming, J.M. & Wood, D.M. (2017) 3. Adult morphology and terminology. In: Kirk-Spriggs, A.H. & Sinclair, B.J. (Eds.), Manual of Afrotropical Diptera. Vol. 1. Introductory Chapters and Keys to Diptera Families. Suricata 4. South African National Biodiversity Institute, Pretoria, pp. 89–133.
Daniels, G. (1977) A note on the behaviour of Protomiltogramma Townsend (Diptera: Sarcophagidae). Australian Entomology Magazine, 4, 6.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
Fan, Z.-D. (Ed.) (1992) Key to the Common Flies of China. Second edition. Shanghai Institute of Entomology, Academia Sinica, Shanghai, 992 pp. [in Chinese with English subtitle, preface and English descriptions of all new taxa.]
Hedtke, S.M., Townsend, T.M. & Hillis, D.M. (2006) Resolution of phylogenetic conflict in large data sets by increased taxon sampling. Systematic Biology, 55, 522–529. https://doi.org/10.1080/10635150600697358
Johnston, N.P., Wallman, J.F., Dowton, M., Szpila, K. & Pape, T. (2020d) Taxonomic revision of Australian Amobia Robineau-Desvoidy, 1830 (Sarcophagidae: Miltogramminae): integrating morphology and genetics finds a new species and tackles old problems. European Journal of Taxonomy, 722, 75–96. https://doi.org/10.5852/ejt.2020.722.1135
Johnston, N.P., Wallman, J.F. & Pape, T. (2019) First record of Miltogramminae from New Caledonia: A new species of Protomiltogramma (Diptera: Sarcophagidae). Zootaxa, 4612 (4), 595–599. https://doi.org/10.11646/zootaxa.4612.4.12
Johnston, N.P., Wallman, J.F. & Pape, T. (2020c) Integrative Taxonomy of Australian Metopia (Sarcophagidae: Miltogramminae) Reveals a New Species and Challenges Traditional Phylogeny. Insect Systematics and Diversity, 4, 1–16. https://doi.org/10.1093/isd/ixaa016
Johnston, N.P., Wallman, J.F., Pape, T. & Whitmore, D. (2020a) Macronychia (Diptera: Sarcophagidae) goes cosmopolitan: description and molecular delineation of the first Australian species. Austral Entomology, 59, 292–301. https://doi.org/10.1111/aen.12447
Johnston, N.P., Wallman, J.F, Szpila, K. & Pape, T. (2020b) An enigma no more: An integrated taxonomic revision of Aenigmetopia Malloch reveals novel phylogenetic placement and four new species (Diptera: Sarcophagidae: Miltogramminae). Invertebrate Systematics, 34, 519–534. https://doi.org/10.1071/IS19051
Kimura, M. (1980) A Simple Method for Estimating Evolutionary Rates of Base Substitutions through Comparative Studies of Nucleotide Sequences. Journal of Molecular Evolution, 16, 111–120. https://doi.org/10.1007/BF01731581
Kurahashi, H. & Chaiwong, T. (2007) Two new species of Protomiltogramma from Thailand (Diptera, Sarcophagidae). Japanese Journal of Systematic Entomology, 13, 173–178.
Kurahashi, H. & Leh, M.U. (2008) Two new species of Protomiltogramma from Malaysia (Diptera, Sarcophagidae). Japanese Journal of Systematic Entomology, 14, 1–6.
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773. https://doi.org/10.1093/molbev/msw260
Leaché, A.D., Banbury, B.L., Linkem, C.W. & De Oca, A.N.M. (2016) Phylogenomics of a rapid radiation: Is chromosomal evolution linked to increased diversification in North American spiny lizards (Genus Sceloporus)? BMC Evolutionary Biology, 16, 63. https://doi.org/10.1186/s12862-016-0628-x
Malloch, J.R. (1930) Notes on Australian Diptera. XXV. Proceedings of the Linnean Society of New South Wales, 55, 429–450.
Meiklejohn, K.A., Dowton, M., Pape, T. & Wallman, J.F. (2013a) A key to the Australian Sarcophagidae (Diptera) with special emphasis on Sarcophaga (sensu lato). Zootaxa, 3680 (1), 148–189. https://doi.org/10.11646/zootaxa.3680.1.11
Meiklejohn, K.A., Wallman, J.F. & Dowton, M. (2011) DNA-based identification of forensically important Australian Sarcophagidae (Diptera). International Journal of Legal Medicine, 125, 27–32. https://doi.org/10.1007/s00414-009-0395-y
Meiklejohn, K.A., Wallman, J.F., Pape, T., Cameron, S.L. & Dowton, M. (2013b) Utility of COI, CAD and morphological data for resolving relationships within the genus Sarcophaga (sensu lato) (Diptera: Sarcophagidae): A preliminary study. Molecular Phylogenetics and Evolution, 69, 133–141. https://doi.org/10.1016/j.ympev.2013.04.034
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), New Orleans, 2010, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
Nandi, B.C. (2002) Diptera Sarcophagidae. Zoological Survey of India, Calcutta, 608 pp.
Pape, T. (1996) Catalogue of the Sarcophagidae of the world (Insecta: Diptera). Memoirs on Entomology, International, 8, 1–557.
Pape, T. (1998) 3.52 Family Sarcophagidae. In: Papp, L. & Darvas, B. (Eds.), Contributions to a Manual of Palaearctic Diptera. Science Herald, Budapest, pp. 649–678.
Pape, T. & Szpila, K. (2012) Taxonomy and nomenclature of Eremasiomyia macularis and Miltogramma maroccana (Diptera: Sarcophagidae: Miltogramminae). The Canadian Entomologist, 144, 169–181. https://doi.org/10.4039/tce.2012.14
Philippe, H., Zhou, Y., Brinkmann, H., Rodrigue, N. & Delsuc, F. (2005) Heterotachy and long-branch attraction in phylogenetics. BMC Evolutionary Biology, 5, 50. https://doi.org/10.1186/1471-2148-5-50
Piwczyński, M., Pape, T., Deja-Sikora, E., Sikora, M., Akbarzadeh, K. & Szpila, K. (2017) Molecular phylogeny of Miltogramminae (Diptera: Sarcophagidae): implications for classification, systematics and evolution of larval feeding strategies. Molecular Phylogenetics and Evolution, 116, 49–60. https://doi.org/10.1016/j.ympev.2017.07.001
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21, 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
Rohdendorf, B.B. (1967) The directions of historical development of Sarcophagidae (Diptera). Trudy Paleontologicheskogo Instituta Akademii Nauk SSSR, 116, 1–92.
Spofford, M.G. & Kurczewski, F.E. (1985) Courtship and Mating Behavior of Phrosinella aurifacies Downes (Diptera: Sarcophagidae: Miltogramminae). Proceedings of the Entomological Society of Washington, 87, 273–282.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Szpila, K., Walczak, K., Johnston, N.P., Pape, T. & Wallman, J.F. (2021). First instar larvae of endemic Australian Miltogramminae (Diptera: Sarcophagidae). Scientific Reports, 11, 1–12. https://doi.org/10.1038/s41598-020-80139-x
Townsend, C.H.T. (1916) New genera and species of Australian Muscoidea. The Canadian Entomologist, 48, 151–160. https://doi.org/10.4039/Ent48151-5.
Verves, Yu. G. (1979) Review of species of the Miltogrammatinae (Diptera, Sarcophagidae) of Sri Lanka. Entomologicheskoe Obozrenie, 58, 905–919.
Verves, Yu. G. (1987) Sarcophagidae (Diptera), Collected by V.F. Zaitev and G.M. Dlusskij in Australia and Oceania. Entomologicheskoe Obozrenie, 66, 653–668.
Verves, Yu. G. (1989) The phylogenetic systematics of the Miltogramminae flies (Diptera, Sarcophagidae) of the World. Japanese Journal of Medical Science and Biology, 42, 111–126. https://doi.org/10.7883/yoken1952.42.111
Verves, Yu. G. & Khrokalo, L. (2020) Review of subtribe Pterellina Rohdendorf, 1967 (Diptera: Sarcophagidae) of Middle East with descriptions of twelve new species. Annales de la Société Entomologique de France, 56, 235–265. https://doi.org/10.1080/00379271.2020.1743755
White, T.E., Vogel-Ghibely, N. & Butterworth, N.J. (2019) Flies exploit predictable perspectives and backgrounds to enhance iridescent signal salience and mating success. The American Naturalist, 2019, 707584. https://doi.org/10.1086/707584
Whitfield, J.B. & Lockhart, P.J. (2007) Deciphering ancient rapid radiations. Trends in Ecology and Evolution, 22, 258–265. https://doi.org/10.1016/j.tree.2007.01.012
Winkler, I.S., Blaschke, J.D., Davis, D.J., Stireman, J.O. III, O’Hara, J.E., Cerretti, P. & Moulton, J.K. (2015) Explosive radiation or uninformative genes? Origin and early diversification of tachinid flies (Diptera: Tachinidae). Molecular Phylogenetics and Evolution, 88, 38–54. https://doi.org/10.1016/j.ympev.2015.03.021
Young, A.D., Lemmon, A.R., Skevington, J.H., Mengual, X., Ståhls, G., Reemer, M., Jordaens, K., Kelso, S., Lemmon, E.M., Hauser, M., De Meyer, M., Misof, B. & Wiegmann, B.M. (2016) Anchored enrichment dataset for true flies (order Diptera) reveals insights into the phylogeny of flower flies (family Syrphidae). BMC Evolutionary Biology, 16, 1–13. https://doi.org/10.1186/s12862-016-0714-0