Abstract
Closely related species often exhibit similar niches and reproductive interactions. As competition for shared resources, reproductive interference, and hybridization may exclude one or the other species, the coexistence of closely related species is one of the main research topics in ecology and evolution. Drosophila biauraria and D. triauraria are closely related species with a broad sympatric distribution in Japan. To understand the mechanism underlying their coexistence, we investigated their habitat-use pattern, seasonal occurrence, and the frequency at which they were collected together in Sugadaira Montane (Nagano Prefecture), where grasslands, young forests, and mature forests are present. Slight differences in habitat-use pattern and seasonal occurrence were found between D. biauraria and D. triauraria. However, both species were sometimes collected together. Especially, D. triauraria females were collected together with heterospecific males, suggesting that D. triauraria females may be at risk of reproductive interference and hybridization. Female mate preference for conspecific males was expected to play an important role in reducing their reproductive interaction; however, abnormal genital structures in a few males found in this study suggest the possibility of their hybridization.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andrade CAC, Hatadani LM, Klaczko LB (2005) Phenotypic plasticity of the aedeagus of Drosophila mediopunctata: effect of the temperature. J Therm Biol 30:518–523. https://doi.org/10.1016/j.jtherbio.2005.05.011
Bock IR, Wheeler MR (1972) The Drosophila melanogaster species group. Univ Texas Publs 7213:1–102
Friberg M, Leimar O, Wiklund C (2013) Heterospecific courtship, minority effects and niche separation between cryptic butterfly species. J Evol Biol 26:971–979. https://doi.org/10.1111/jeb.12106
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282. https://doi.org/10.1086/590510
Hardin G (1960) The competitive exclusion principle. Science 131:1292–1297. https://doi.org/10.1126/science.131.3409.1292
Ives AR (1988) Aggregation and the coexistence of competitors. Ann Zool Fennici 25:75–88
Kim BK, Watanabe TK, Kitagawa O (1989) Evolutionary genetics of the Drosophila montium subgroup. I. Reproductive isolations and the phylogeny. Jpn J Genet 64:177–190. https://doi.org/10.1266/jjg.64.177
Kimura MT (1983) A new species of the Drosophila auraria complex, D. subauraria, from northern Japan (Diptera, Drosophilidae). Kontyu 51:593–595
Kimura MT (1987) Habitat differentiation and speciation in the Drosophila auraria species-complex (Diptera, Drosophilidae). Kontyu 55:429–436
Kimura MT (1988) Interspecific and geographic variation of diapause intensity and seasonal adaptation in the Drosophila auraria species complex (Diptera: Drosophilidae). Funct Ecol 2:177–183. https://doi.org/10.2307/2389693
Kurokawa H (1956) Comparative studies on some characteristics of three races of Drosophila auraria. Annot Zool Jpn 29:225–233
Kurokawa H (1959) Experiments on sexual isolation between races A and B of Drosophila auraria. Annot Zool Jpn 32:220–224
Kurokawa H (1960) Sexual isolation among the three races, A, B, and C of Drosophila auraria. Jpn J Genet 35:161–166. https://doi.org/10.1266/jjg.35.161
Kurokawa H (1963) Population Genetics on Three Races of Drosophila auraria Peng II. Sexual isolation among strains within race C. Jpn J Genet 38:1–5. https://doi.org/10.1266/jjg.38.1
Kurokawa H (1967a) Variation in male genitalia of Drosophila auraria collected in nature. Annot Zool Jpn 40:154–160
Kurokawa H (1967b) Population genetics on three races of Drosophila auraria Peng III. Geographical and ecological distribution of the races, A, B, and C, with special regard to its speciation. Jpn J Genet 42:109–119. https://doi.org/10.1266/jjg.42.109
Kyogoku D, Kokko H (2020) Species coexist more easily if reinforcement is based on habitat preferences than on species recognition. J Anim Ecol 89:2605–2616. https://doi.org/10.1111/1365-2656.13321
Kyogoku D, Wheatcroft D (2020) Heterospecific mating interactions as an interface between ecology and evolution. J Evol Biol 33:1330–1344. https://doi.org/10.1111/jeb.13687
Leisch F, Kostyshack MS, LazyData TRUE (2019) Package ‘bootstrap.’ Diabete 14:1
Lenth RV, Buerkner P, Herve M, Love J, Miguez F, Riebl H, Singmann H (2021) emmeans: Estimated marginal means, aka least-Squares means. version 1.7.0. https://CRAN.R-project.org/package=emmeans. Accessed 22 Oct 2021
Losos JB (2008) Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecol Lett 11:995–1003. https://doi.org/10.1111/j.1461-0248.2008.01229.x
Mayr E (1963) Animal species and evolution. Belknap Press, Cambridge
Minami N (1979) Niche analysis of three closely related species of the genus Drosophila. J Fac Sci Hokaido Univ 22:33–41
Noriyuki S, Osawa N, Nishida T (2012) Asymmetric reproductive interference between specialist and generalist predatory ladybirds. J Anim Ecol 81:1077–1085. https://doi.org/10.1111/j.1365-2656.2012.01984.x
Oguma Y, Kurokawa H, Akai S, Tamaki H, Kajita J (1987a) Interspecific differences in some courtship behavioral properties among the four species belonging to the Drosophila auraria complex. Zool Sci 4:889–896
Oguma Y, Kurokawa H, Tachibana N (1987b) Sexual isolation among four sibling species of Drosophila auraria species complex. Bull Sugadaira Montane Res Ctr Univ Tsukuba 8:133–139 (in Japanese with English summary)
Oguma Y, Kurokawa H, Takamori H, Murayama Y, Katayama N (1987c) Collection survey of Drosophiliid flies in Sugadaira Montane Research Center, University of Tsukuba. Bull Sugadaira Montane Res Ctr Univ Tsukuba 8:49–55 (in Japanese with English summary)
Ohsaki N, Ohata M, Sato Y, Rausher MD (2020) Host plant choice determined by reproductive interference between closely related butterflies. Am Nat 196:512–523. https://doi.org/10.1086/710211
Okada T (1954) Comparative morphology of the Drosophilid flies. I Kontyu 22:26–49
Okada T (1979) Furoku (Appendix) 1–5. In: Moriwaki D (ed) Syojobae no Iden Jisshu (practical training of Drosophila genetics). Baifukan, Tokyo, pp 164–191 (in Japanese)
Onuma M, Kamimura Y, Sawamura K (2022) Genital coupling and copulatory wounding in the Drosophila auraria species complex (Diptera: Drosophilidae). Biol J Linn Soc 135:195–207. https://doi.org/10.1093/biolinnean/blab134
Peluffo AE, Hamdani M, Vargas-Valderrama A, David JR, Mallard F, Graner F, Courtier-Orgogozo V (2021) A morphological trait involved in reproductive isolation between Drosophila sister species is sensitive to temperature. Ecol Evol 11:7492–7506. https://doi.org/10.1002/ece3.7580
R Core Team (2020) R: A language and environment for statistical computing. https://www.r-project.org/. Accessed 25 Nov 2021
Sevenster JG (1996) Aggregation and coexistence. I. Theory and Analysis. J Anim Ecol 65:297–307. https://doi.org/10.2307/5876
Shuker DM, Burdfield-Steel ER (2017) Reproductive interference in insects. Ecol Entomol 42:65–75. https://doi.org/10.1111/een.12450
Soto IM, Carreira VP, Fanara JJ, Hasson E (2007) Evolution of male genitalia: environmental and genetic factors affect genital morphology in two Drosophila sibling species and their hybrids. BMC Evol Biol 7:77. https://doi.org/10.1186/1471-2148-7-77
Takada H (1954) Two types of D. auraria, with special regard to the difference in distribution by altitude. Jpn J Genet 29:109–113. https://doi.org/10.1266/JJG.29.109
Toda MJ (1973) Seasonal activity and microdistribution of Drosophilid fies in Misumai in Sapporo. J Fac Sci, Hokaido Univ 18:532–550
Toda MJ (1977) Two new “retainer” bait traps. Drosophila Inf Ser 52:180
Tomaru M, Oguma Y (1994) Differences in courtship song in the species of the Drosophila auraria complex. Anim Behav 47:133–140. https://doi.org/10.1006/anbe.1994.1015
Tomaru M, Matsubayashi H, Oguma Y (1995) Heterospecific inter-pulse intervals of courtship song elicit female rejection in Drosophila biauraria. Anim Behav 50:905–914. https://doi.org/10.1016/0003-3472(95)80093-X
Tomaru M, Matsubayashi H, Oguma Y (1998) Effects of courtship song in interspecific crosses among the species of the Drosophila auraria complex (Diptera: Drosophilidae). J Insect Behav 11:383–398. https://doi.org/10.1023/A:1020954731063
Watada M, Matsumoto M, Kondo M, Kimura MT (2011) Taxonomic study of the Drosophila auraria species complex (Diptera: Drosophilidae) with description of a new species. Entomol Sci 14:392–398. https://doi.org/10.1111/j.1479-8298.2011.00461.x
Wiklund C, Fagerström T (1977) Wy do maled emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia 31(2):153–158
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softe 27:1–25. https://doi.org/10.1863/jss.v027.i08
Acknowledgements
We thank Mr. Koji Nagaoka for helping with the fly collection. We thank Drs. Masahito T. Kimura and Masanori J. Toda at Hokkaido University, Dr. Masayoshi Watada at Ehime University, and the National Institute of Genetics Meeting, “Identification workshop for diversity study in Drosophila, Japan” organized by the National BioResource Project for introducing to identify species. This study was financially partly supported by the COE for Education of Forest and Grassland Biodiversity and Natural History Science in Sugadaira Kogen Research Center, University of Tsukuba (FY 2013-2017 MEXT Joint Usage Education Centers by the Minister of Education, Culture, Sports, Science and Technology) and by the Support for Pioneering Research Initiated by the Next Generation from the Japan Science and Technology Agency (JPMJSP2124 to MO).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Onuma, M., Sato, Y. & Sawamura, K. Habitat and seasonal occurrence differ among closely related species of the Drosophila auraria species complex (Diptera: Drosophilidae). Appl Entomol Zool 58, 35–44 (2023). https://doi.org/10.1007/s13355-022-00801-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13355-022-00801-w