Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2020-06-08
Page range: 1–54
Abstract views: 128
PDF downloaded: 4

Taxonomy and evolution of asymmetric male genitalia in the subgenus
Ashima Chen (Diptera: Drosophilidae: Phortica Schiner), with descriptions
of seven new species

Hokkaido University Museum, Hokkaido University, Sapporo 060-0810, Japan
Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand
Systematic & Cytogenetic Laboratory, Department of Zoology and Biotechnology, HNB Garhwal University, Srinagar-Garhwal, 246174, Uttarakhand, India.
Systematic & Cytogenetic Laboratory, Department of Zoology and Biotechnology, HNB Garhwal University, Srinagar-Garhwal, 246174, Uttarakhand, India.
Zoology Division (Museum Zoologicum Bogoriense), Research Center for Biology-LIPI, Jl. Raya Jakarta-Bogor Km. 46, Cibinong 16911, West Java, Indonesia.
Department of Biological Sciences, Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan
Diptera Ancestral state reconstruction Antisymmetry Directional asymmetry Lachryphagy Male genitalia Morphology Phylogeny Species complex Species group Species subgroup Synapomorphy Terminology


The taxonomy of the subgenus Ashima of the genus Phortica is revised. A cladistic analysis of 66 morphological characters is conducted, covering 35 species (28 known and 7 new species: Phortica efragmentata sp. nov., P. andreagigoni sp. nov., P. watabei sp. nov., P. halimunensis sp. nov., P. akutsui sp. nov., P. kerinciensis sp. nov., and P. takehiroi sp. nov.) which correspond to 71.4% of 49 total spp. of Ashima. The resulting cladogram shows that the studied species are separated into several clades/subclades/cluster each highly supported with specific synapomorphies. Those clades/subclades/cluster are newly defined as the following species groups, subgroups or complex: the afoliolata, foliiseta, nigrifoliiseta and angulata species groups; the foliiseta, tanabei, nigrifoliiseta and glabra species subgroups; and the foliiseta species complex. The subgenus Ashima is peculiar in having the asymmetric male genitalia as the ground plan and showing the antisymmetry (i.e. intraspecific mirror-image variation) in some species but the directional asymmetry (i.e. side-fixed asymmetry) in others. The evolution of genital asymmetry in this subgenus is estimated by mapping the states (symmetry, directional asymmetry and antisymmetry) of bilateral structures of male genitalia on the cladogram. This ancestral state reconstruction estimates that the directional asymmetry of male genitalia has evolved at the ancestor of this subgenus and then changed to the antisymmetric state independently in two lineages, the angulata + nigrifoliiseta species groups and the foliiseta species complex. In this study, a standardized terminology recently proposed for the male terminalia of Drosophila melanogaster is extendedly adopted to describe the morphology of male terminalia in the subgenus Ashima, one group of the subfamily Steganinae.



  1. Acurio, A.E., Rhebergen, F.T., Paulus, S., Courtier-Orgogozo, V. & Lang, M. (2019) Repeated evolution of asymmetric genitalia and right-sided mating behavior in the Drosophila nannoptera species group. BMC Evolutionary Biology, 19, 109.

    An, K.Y., Cao, H.L., Wang, X.L. & Chen, H.W. (2015) The subgenus Ashima (Diptera, Drosophildae, Phortica) from China, with DNA barcoding and descriptions of three new species. Systematics and Biodiversity, 13, 42–51.

    Ashburner, M. (1981) Entomophagous and other bizarre Drosophilidae. In: Ashburner, M., Carson, H.L. & Thompson Jr., J.N. (Eds.), The Genetics and Biology of Drosophila. Vol. 3a. Academic Press Inc., London, pp. 395−429.

    Bächli, G. (1971) Leucophenga und Paraleucophenga (Diptera Brachycera), Fam. Drosophilidae. Exploration du Parc National de l'Upemba. Mission G. F. de Witte, Fasc. 71, 192 pp., 39 pls.

    Bächli, G. & Vilela, C.R. (2002) Six new species of Drosophila (Diptera, Drosophilidae) from Parque Nacional Henri Pittier, Venezuela. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 75, 223–243.

    Bächli, G., Vilela, C.R., Andersson Escher, S. & Saura, A. (2004) The Drosophilidae (Diptera) of Fennoscandia and Denmark. Fauna Entomologica Scandinavica. Vol. 39. Brill, Leiden, 362 pp.

    Bänziger, H., Boongird, S., Sukumalanand, P. & Bänziger, S. (2009) Bees (Hymenoptera: Apidae) that drink human tears. Journal of the Kansas Entomological Society, 82, 135–150.

    Beuk, P.L.T. & Máca, J. (1995) Amiota collini, a new European species of Amiota sensu stricto (Diptera, Drosophilidae). Dipterists Digest, Series 2, 2, 8–12.

    Bhaibulaya, M., Prasertsilpa, S. & Vajrasthira, S. (1970) Thelazia callipaeda Railliet and Henry, 1910, in man and dog in Thailand. The American Journal of Tropical Medicine and Hygiene, 19, 476–479.

    Cao, H.L., Wang, X.L., Gao, J.J., Prigent, S.R., Watabe, H., Zhang, Y.P. & Chen, H.W. (2011) Phylogeny of the African and Asian Phortica (Drosophilidae) deduced from nuclear and mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 61, 677–685.

    Chatterjee, R.N., Chatterjee, P., Kuthe, S., Acharyya-Ari, M. & Chatterjee, R. (2015) Intersex (ix) mutations of Drosophila melanogaster cause nonrandom cell death in genital disc and can induce tumours in genitals in response to decapentaplegic (dppdisk) mutations. Journal of Genetics, 94, 207‒220.

    Chen, H.W. & Aotsuka, T. (2004) A survey of the genus Stegana Meigen from southern Japan (Diptera, Drosophilidae), with descriptions of three new species. Journal of Natural History, 38, 2779‒2788.

    Chen, H.W., Gao, J.J. & Wen, S.Y. (2005a) Species diversity of the genus Phortica Schiner in Yunnan, China, with descriptions of nine new species (Diptera, Drosophildae [sic]). Journal of Natural History, 39, 3951‒3978.

    Chen, H.W. & Máca, J. (2012) Ten new species of the genus Phortica from the Afrotropical and Oriental regions (Diptera: Drosophilidae). Zootaxa, 3478 (1), 493–509.

    Chen, H.W. & Toda, M.J. (1998) Amiota (Phortica) omega species-complex, with descriptions of two new species from southern China (Diptera: Drosophilidae). Entomological Science, 1, 403–407.

    Chen, H.W. & Toda, M.J. (2001) A revision of the Asian and European species in the subgenus Amiota Loew (Diptera, Drosophilidae) and the establishment of species-groups based on phylogenetic analysis. Journal of Natural History, 35, 1517‒1563.

    Chen, H.W., Toda, M.J. & Gao, J.J. (2005b) The Phortica (s. str.) foliiseta species-complex (Diptera, Drosophilidae) from China and its adjacent countries. Acta Zootaxonomica Sinica, 30, 419‒429.

    Chen, H.W., Toda, M.J., Lakim, M.B. & Mohamed, M.B. (2007) The Phortica sensu stricto (Insecta: Diptera, Drosophilidae) from Malaysia. The Raffles Bulletin of Zoology, 55, 23‒41.

    Chen, H.W. & Wang, B.C. (2004) Stegana (Oxyphortica) nigripennis species-group, with descriptions of four new species from Southeast Asia (Insecta: Diptera: Drosophilidae). The Raffles Bulletin of Zoology, 52, 29‒36.

    Chen, H.W., Watabe, H.-A., Gao, J.J., Takamori, H., Zhang, Y.P. & Aotsuka, T. (2005c) Species diversity of the subgenus Amiota (s. str.) Loew, 1862 (Diptera, Drosophilidae) in southern China. Journal of Natural History, 39, 265–310.

    Chen, H.Z. & Toda, M.J. (1994) A new species of Paraleucophenga (Diptera: Drosophilidae) from China. Entomotaxonomia, 16, 71–74.

    Cheng, Y., Gao, J.J. & Chen, H.W. (2009) Stegana ornatipes species group from the Oriental Region (Diptera: Drosophilidae). Zootaxa, 2216 (1), 37–48.

    Cheng, Y., Gao, J.J., Watabe, H. & Chen, H.W. (2008) Revision of the genus Phortica Schiner 1862 in China (Diptera: Drosophilidae). Zoological Studies, 47, 614‒632.

    Cumming, J.M. & Wood, D.M. (2017) 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. South African National Biodiversity Institute, Pretoria, pp. 89–133.

    Duda, O. (1923) Die orientalischen und australischen Drosophiliden-Arten (Dipteren) des Ungarischen National-Museums zu Budapest. Annales Historico-Naturales Musei Nationalis Hungarici, 20, 24‒59.

    Fallén, C.F. (1823) Geomyzides Sveciae. Berlingianis, Lundae (Lund), 8 pp.

    Fartyal, R.S., Sati, P.C., Pradhan, S., Kandpal, M.C., Toda, M.J., Chatterjee, R.N., Singh, B.K. & Bhardwai, A. (2017) A review of the genus Lordiphosa Basden in India, with descriptions of four new species from the Himalayan region (Diptera, Drosophilidae). ZooKeys, 688, 49–79.

    Ferris, G.F. (1950) External morphology of the adult. In: Demerec, M. (Ed.) Biology of Drosophila. Cold Spring Harbor Laboratory Press, New York, NY, pp. 368–419.

    Gigon, A., Langenauer, R., Meier, C. & Nievergelt, B. (2000) Blue Lists of threatened species with stabilized or increasing abundance: A new instrument for conservation. Conservation Biology, 14, 402–413.

    Gong, L., Zhu, L. & Chen, H.W. (2018) Six new species of the subgenera Alloparadisa and Ashima (Diptera: Drosophilidae: Phortica) from Yunnan, China, with DNA barcoding information. Annales de la Société entomologique de France, New Series, 54, 434–446.

    Gottschalk, M.S., Martins, M.B., Praxedes, C.L.B. & de Mederros, H.F. (2012) A new Amazonian species from the Drosophila annulimana species group (Diptera, Drosophilidae). Revista Brasileira de Entomologia, 56, 431–435.

    Grimaldi, D.A. (1986) The Chymomyza aldrichii species-group (Diptera: Drosophilidae): relationships, new Neotropical species, and the evolution of some sexual traits. Journal of the New York Entomological Society, 94, 342‒371.

    Grimaldi, D.A. (1990) A phylogenetic, revised classification of genera in the Drosophilidae (Diptera). Bulletin of the American Museum of Natural History, 197, 1‒139.

    Grimaldi, D.A. (1993) Amber fossil Drosophilidae (Diptera), Part II: Review of the genus Hyalistata, new status (Steganinae). American Museum Novitates, 3084, 1‒15.

    Grimaldi, D.A. (2018) Hirtodrosophila of North America (Diptera: Drosophilidae). Bulletin of the American Museum of Natural History, 421, 1‒75.

    Hu, Y.G. & Toda, M.J. (2001) Polyphyly of Lordiphosa and its relationships in Drosophilinae (Diptera: Drosophilidae). Systematic Entomology, 26, 15–31.

    Hu, Y.G., Toda, M.J. & Watabe, H.-A. (1999) A revision of the Lordiphosa tenuicauda species-group, with descriptions of eight new species from China (Diptera: Drosophilidae). Entomological Science, 2, 105–119.

    Huber, B.A. (2010) Mating positions and the evolution of asymmetric insect genitalia. Genetica, 138, 19–25.

    Huber, B.A., Sinclair, B.J. & Schmitt, M. (2007) The evolution of asymmetric genitalia in spiders and insects. Biological Reviews, 82, 647–698.

    Hunter, A.S. (1988) High altitude flower-breeding Drosophila (Diptera: Drosophilidae). Pan-Pacific Entomologist, 64, 299–312.

    Kamimura, Y. (2014) Pre- and postcopulatory sexual selection and the evolution of sexually dimorphic traits in earwigs (Dermaptera). Entomological Science, 17, 139–166.

    Kamimura, Y. & Polak, M. (2011) Does surgical manipulation of Drosophila intromittent organs affect insemination success? Proceedings of the Royal Society B, 278, 815‒816.

    Kopp, A.V. & True, J.R. (2002) Evolution of male sexual characters in the oriental Drosophila melanogaster species group. Evolution & Development, 4, 278–291.

    Kozlov, D.P. (1962) The life cycle of nematode Thelazia callipaeda parasitic in the eye of man and carnivores. Doklady Akademy Nauk SSSR, 142, 732‒733. [in Russian; not seen, mentioned in Otranto et al. 2005]

    Lang, M. & Orgogozo, V. (2012) Distinct copulation positions in Drosophila pachea males with symmetric or asymmetric external genitalia. Contributions to Zoology, 81, 87‒94.

    Máca, J. (1977) Revision of Palaearctic species of Amiota subg. Phortica (Diptera, Drosophilidae). Acta Entomologica Bohemoslovaca, 74, 115‒130.

    Máca, J. (1980) European species of the subgenus Amiota s. str. (Diptera, Drosophilidae). Acta Entomologica Bohemoslovaca, 77, 328‒346.

    Máca, J. (2003) Taxonomic notes on the genera previously classified in the genus Amiota Loew (Diptera: Drosophilidae, Steganinae). Acta Universitatis Carolinae Biologica, 47, 247‒274.

    Máca, J. & Lin, F.J. (1993a) The Drosophilidae of Taiwan: Genera Amiota (excluding subgenus Phortica) and Leucophenga (Nankangomyia subg. nov.). Bulletin of the Institute of Zoology, Academia Sinica, 32, 1‒11.

    Máca, J. & Lin, F.J. (1993b) The Drosophilidae of Taiwan: Genus Amiota, subgenus Phortica. Bulletin of the Institute of Zoology, Academia Sinica, 32, 171‒183.

    Máca, J. & Otranto, D. (2014) Drosophilidae feeding on animals and the inherent mystery of their parasitism. Parasites & Vectors, 7, 516.

    McAlpine, J.F. (1968) An annotated key to drosophilid genera with bare or micropubescent aristae and a revision of Paracacoxenus (Diptera: Drosophilidae). Canadian Entomologist, 100, 514‒532.

    McAlpine, J.F. (1981) Morphology and terminology: adults. In: MaAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J., Vockeroth, J.R. & Wood, D.M. (Eds.), Manual of Nearctic Diptera. Vol. 1. Biosystematics Research Institute, Ottawa, pp. 9–63.

    Okada, T. (1956) Systematic Study of Drosophilidae and Allied Families of Japan. Gihodo, Tokyo, 183 pp.

    Okada, T. (1971) A revision and taxometric analysis of the genus Amiota Loew of Japan and adjacent countries (Diptera, Drosophilidae). Kontyû, 39, 82‒98.

    Okada, T. (1976) Subdivision of the genus Chymomyza Czeryny (Diptera, Drosophilidae), with description of three new species. Kontyû, 44, 496‒511.

    Okada, T. (1981) The genus Chymomyza Czeryny (Diptera, Drosophilidae) from New Guinea, Bismarck Archipelago and Southeast Asia, with an ecological note. Kontyû, 49, 166‒177.

    Otranto, D., Cantacessi, C., Testini, G. & Lia, R.P. (2006) Phortica variegata as an intermediate host of Thelazia callipaeda under natural conditions: Evidence for pathogen transmission by a male arthropod vector. International Journal for Parasitology, 36, 1167‒1173.

    Otranto, D., Lia, R.P., Cantacessi, C., Testini, G., Troccoli,A., Shen, J.L. & Wang, Z.X. (2005) Nematode biology and larval development of Thelazia callipaeda (Spirurida, Thelaziidae) in the drosophilid intermediate host in Europe and China. Parasitology, 131, 847‒855.

    Palmer, A.R. (1996) From symmetry to asymmetry: phylogenetic patterns of asymmetry variation in animals and their evolutionary significance. Proceedings of the National Academy of Sciences of the United States of America, 93, 14279–14286.

    Peñafiel-Vinueza, A.D. & Rafael, V. (2018) Five new species of Drosophila guarani group from the Andes of southern Ecuador (Diptera, Drosophilidae). ZooKeys, 781, 141–163.

    Pitnick, S. & Heed, W.B. (1994) New species of cactus-breeding Drosophila (Diptera: Drosophilidae) in the nannoptera species group. Annals of the Entomological Society of America, 87, 307–310.

    Prigent, S. & Chen, H.W. (2008) A survey of the genus Phortica Schiner from Kenya, Africa (Diptera, Drosophilidae). Zootaxa, 1773 (1), 18–30.

    Rice, G., David, J.R., Kamimura, Y., Masly, J.P., Mcgregor, A.P., Nagy, O., Noselli, S., Nunes, M.D.S., O’Grady, P., Sánchez-Herrero, E., Siegal, M.L., Toda, M.J., Rebeiz, M., Courtier-Orgogozo, V. & Yassin, A. (2019) A standardized nomenclature and atlas of the male terminalia of Drosophila melanogaster. Fly, 13, 51–64.

    Saìnchez, L., Casares, F., Gorfinkiel, N. & Guerrero, I. (1997) The genital disc of Drosophila melanogaster. II. Role of the genes hedgehog, decapentaplegic and wingless. Development Genes and Evolution, 207, 229–241.

    Schaffner, F. (2008) Recherches en entomologie vétérinaire et médicale à l’Institut de parasitologie de Zürich. Deux sujets d’actualité: Phortica spp. et Ver oriental, Culicoides spp. et Langue bleue du mouton. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 81, 120.

    Schiner, I.R. (1862) Vorläufiger Commentar zum dipterologischen Theile der "Fauna Austriaca", mit einer näheren Begründung der in derselben aufgenommenen neuen Dipteren-Gattungen. V. [part]. Wiener Entomologische Monatschrift, 6, 428‒436.

    Senior-White, R.A. (1921) New Ceylon Diptera. Spolia Zeylanica, 11, 381‒396.

    Shen, J.L., Gasser, R.B., Chu, D., Wang, Z.X., Yuan, X., Cantacessi, C. & Otranto, D. (2006) Human thelaziosis – a neglected parasitic disease of the eye. Journal of Parasitology, 92, 872‒875.

    Sidorenko, V.S. (1998) New data on Asian drosophilid flies (Diptera, Drosophilidae). Part 3. Far Eastern Entomologist, 56, 1‒8.

    Sinclair, B.J. (2000) Morphology and terminology of Diptera male terminalia. In: Papp, L. & Darvas, B. (Eds.), Contributions to a Manual of Palaearctic Diptera. Vol. 1. Science Herald, Budapest, pp. 53‒74.

    Swofford, D.L. (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MA. Available from: (accessed 9 December 2019)

    Toda, M.J. (1983) Two species of the subgenus Lordiphosa Basden of the genus Drosophila (Diptera, Drosophilidae) from Japan. Kontyû, 51, 468-473.

    Toda, M.J. (2019) DrosWLD-Species: Taxonomic Information Database for World Species of Drosophilidae. Available from: (accessed 11 January 2020)

    Toda, M.J. & Peng, T.X. (1990) Eight new species of the subgenus Phortica (Diptera: Drosophilidae, Amiota) from Guangdong Province, southern China. Entomotaxonomia, 12, 41‒55.

    Toda, M.J., Sidorenko, V.S., Watabe, H.-A., Kholin, S.K. & Vinokurov, N.N. (1996) A revision of the Drosophilidae (Diptera) in East Siberia and Russian Far East: Taxonomy and biogeography. Zoological Science, 13, 455‒477.

    Tsacas, L. & Okada, T. (1983) On the Oriental and New Guinean species of the genus Amiota Loew originally described by Duda as Phortica foliiseta, with descriptions of three new species (Diptera, Drosophilidae). Kontyû, 51, 228‒237.

    Vaz, S.C., Vilela, C.R. & Carvalho, A.B. (2018) Two new species of Drosophila (Diptera, Drosophilidae) associated with inflorescences of Goeppertia monophylla (Marantaceae) in the city of São Paulo, state of São Paulo, Brazil. Revista Brasileira de Entomologia, 62, 159–168.

    Vilela, C.R. (1984) Occurrence of the Drosophila flavopilosa species group (Diptera, Drosophilidae) in the State of Sao Paulo (Brazil) with description of one new species. Revista Brasileira de Zoologia, 2, 63–69.

    Vilela, C.R. & Bächli, G. (1990) Taxonomic studies on Neotropical species of seven genera of Drosophilidae (Diptera). Mitteilungen der Schweizerischen Entomologischen Gesellschaft, Supplement 63, 1–332.

    Vilela, C.R. & Bächli, G. (2004) Revisions of the Drosophila macroptera and D. rubrifrons species groups, with description of a new Neotropical group (Diptera, Drosophilidae). Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 77, 1‒68.

    Vilela, C.R., Bächli, G. & Stensmyr, M.C. (2008) Redescription of Drosophila endobranchia (Diptera, Drosophilidae), an aberrant member of the canalinea species group. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 81, 199‒208.

    Vilela, C.R. & Pereira, M.A.Q.R. (1992) Breeding sites of Neotropical Drosophilidae (Diptera). I. Living flowers of Cestrum schlechtendalii (Solanaceae). Revista Brasileira de Entomologia, 36, 475−482.

    Vincent, B.J., Rice, G.R., Wong, G.M., Glassford, W.J., Downs, K.I., Shastay, J.L., Charles-Obi1, K., Natarajan, M., Gogo, M., Zeitlinger, J. & Rebeiz, M. (2019) An atlas of transcription factors expressed in male pupal terminalia of Drosophila melanogaster. G3: Genes|Genomes|Genetics, 9, 3961.

    Wang, Z.X., Wang, K.C. & Chen, Q. (2002) Experimental studies on the susceptibility of Thelazia callipaeda to Amiota okadai in three provinces of China. Chinese Journal of Zoonoses, 18, 61−63.

    Watabe, H.-A. & Lin, F.J. (1992) Discovery of the male of Chymomyza atrimana (Diptera, Drosophilidae). Japanese Journal of Entomology, 60, 869−870.

    Watrous, L.E. & Wheeler, Q.D. (1981) The outgroup comparison method of character analysis. Systematic Zoology, 30, 1−11.

    Wheeler, M.R. (1952) XI. The Drosophilidae of the Nearctic region, exclusive of the genus Drosophila. The University of Texas Publication, 5204, 162‒218.

    Zhang, W.X. & Liang, X.C. (1992) Seven new species of the subgenus Lordiphosa of Drosophila. Acta Zootaxonomica Sinica, 17, 473–482. [in Chinese, with English summary]

    Zhang, W.X. & Shi, L. (1997) Subgenus Phortica of genus Amiota in Hengduan Mountains region, China, with descriptions of three new species. Zoological Research, Kunming, 18, 367‒375. [in Chinese, with English summary]

    Zhang, W.X. & Toda, M.J. (1992) A new species-subgroup of the Drosophila immigrans species-group (Diptera, Drosophilidae), with description of two new species from China and revision of taxonomic terminology. Japanese Journal of Entomology, 60, 839‒850.

    Zhao, F., Gao, J.J. & Chen, H.W. (2009) Taxonomy and molecular phylogeny of the Asian Paraleucophenga Hendel (Diptera, Drosophilidae). Zoological Journal of the Linnean Society, 155, 615–629.

    Zhu, L., Qin, T. & Chen, H.W. (2017) Three new species of the subgenus Ashima (Diptera, Drosophilidae, Phortica) from south-western China, with DNA barcoding information. Journal of Natural History, 51, 71–82.