Abstract
Hipposideros larvatus sensu lato constitutes a widespread species complex consisting of morphologically similar forms with a taxonomy that is in need of a revision. Here we present the results of a phylogenetic analysis of members of this species complex based on two mitochondrial (CytB and COI) and seven nuclear (ABHD11, ACOX2, COPS, RAG2, ROGDI2, SORBS2 and THY) genes, and a morphometric analysis. Morphological data, although showing certain diversity, does not allow an accurate delimitation of the taxonomic boundaries and occasionally contradict to genetic grouping. The molecular analyses based on mitochondrial data support the paraphyly of the H. larvatus species complex, with H. armiger recovered nested within. The nuclear data recovered all the lineages of H. larvatus sensu lato forming a monophyletic clade. Within it, apparently four different species-level clades could be revealed in Southeast Asia. One is distributed in northern Myanmar, southern China (including Hainan) and northern Vietnam, and also reaches into central Vietnam along the coast (Cham Islands). The valid name for this taxon must be H. poutensis Allen. The second clade is comprised by populations inhabiting the Malay Peninsula and the Sunda Islands, we identify this taxon as H. larvatus sensu stricto. The third taxon was identified only from southern Myanmar. The fourth taxon is distributed in southern and central Indochina. Its representatives were not related to any of the forms identified in Myanmar, and therefore, its previous identification with H. grandis sounds questionable. Since both the third and fourth taxa cannot now be unambiguously associated with a particular named form, we conventionally designate them as H. cf. grandis 1 and 2.
References
Abramov, A.V. & Kruskop, S.V. (2012) The mammal fauna of Cat Ba Island. Russian Journal of Theriology, 11 (1), 57–72. https://doi.org/10.15298/rusjtheriol.11.1.05
Allen, J.A. (1906) Mammals from the Island of Hainan, China. Bulletin of American Museum of Natural History, 22, 463–491.
Allen, G.M. (1936) Two new races of Indian bats. Records of the Indian Museum, 38, 343–346.
Altekar, G., Dwarkadas, S., Huelsenbeck, J.P. & Ronquist, F. (2004) Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics, 20 (3), 407–415. https://doi.org/10.1093/bioinformatics/btg427
Artyushin, I.V., Bannikova, A.A., Lebedev, V.S. & Kruskop, S.V. (2009) Mitochondrial DNA relationships among North Palaearctic Eptesicus (Vespertilionidae, Chiroptera) and past hybridization between Common Serotine and Northern Bat. Zootaxa, 2262, 40–52. https://doi.org/10.11646/zootaxa.2262.1.2
Çoraman, E., Dundarova, H., Dietz, C. & Mayer, F. (2020) Patterns of mtDNA introgression suggest population replacement in Palaearctic whiskered bat species. Royal Society Open Science, 7 (6), 191805. https://doi.org/10.1098/rsos.191805
Corbet, G.B. & Hill, J.E. (1992) The mammals of the Indomalayan region: a systematic review. Oxford University Press, Oxford, 488 pp.
Douangboubpha, B., Bumrungsri, S., Soisook, P., Satasook, C., Thomas, N.M. & Bates, P.J.J. (2010) A taxonomic review of the Hipposideros bicolor species complex and H. pomona (Chiroptera: Hipposideridae) in Thailand. Acta Chiropterologica, 12, 415–438. https://doi.org/10.3161/150811010X537990
Francis, C.M. (2019) A field guide to the mammals of South-East Asia. 2nd Edition. Bloomsbury Wildlife, London, 416 pp.
Francis, C.M., Borisenko, A.V., Ivanova, N.V., Eger, J.L., Lim, B.K., Guillén-Servent, A., Kruskop, S.V., Mackie, I. & Hebert, P.D.N. (2010) The Role of DNA Barcodes in Understanding and Conservation of Mammal Diversity in Southeast Asia. PLoS ONE, 5 (9), e12575. https://doi.org/10.1371/journal.pone.0012575
Hill, J.E. (1963) A revision of the genus Hipposideros. Bulletin of British Museum (Natural Histtory), Zoology, 1963, 11, 1–129. https://doi.org/10.5962/bhl.part.4716
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Hughes, A.C., Satasook, C., Bates, P.J.J., Bumrungsri, S. & Jones, G. (2011) Explaining the causes of the zoogeographic transition around the Isthmus of Kra: using bats as a case study. Journal of Biogeography, 38, 2362–2372. https://doi.org/10.1111/j.1365-2699.2011.02568.x
Igea, J., Juste, J. & Castresana, J. (2010) Novel intron markers to study the phylogeny of closely related mammalian species. BMC Evolutionary Biology, 10, 369. https://doi.org/10.1186/1471-2148-10-369
Ivanova, N.V., Clare, E.L. & Borisenko, A.V. (2012) DNA barcoding in mammals. In: Kress, W.J. & Erickson, D.L. (Eds.), DNA Barcodes: Methods and Protocols. Methods in Molecular Biology. Vol. 858. Humana Press, New Jersey, pp. 153–182. https://doi.org/10.1007/978-1-61779-591-6_8
Katoh, T. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
Kitchener, D.J. & Maryanto, I. (1993) Taxonomic reappraisal of the Hipposideros larvatus species complex (Chiroptera: Hipposideridae) in the Greater and Lesser Sunda Islands, Indonesia. Records of the Western Australian Museum, 16, 119–173.
Koopman, K.F. (1994) Chiroptera: Systematics. Handbook of Zoology. Vol. VIII. Mammalia. Part 60. Walter de Gruyter, New York, New York, 217 pp.
Kruskop, S.V. (2015) Dull and bright: cryptic diversity within the “Hipposideros larvatus” species group in Indochina (Chiroptera, Hipposideridae). Lynx, Praha, New Series, 46, 29–42.
Kruskop, S.V. (2013) Bats of Vietnam. Checklist and an identification manual, 2nd ed., revised and supplemented. KMK Ltd., Moscow, 300 pp.
Kruskop, S.V. (2014) The bacula of some bat species from Indo-China: rhinolophoids (Chiroptera: Rhinolophidae, Hipposideridae). Plecotus et al., 17, 3–17.
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 (3), 772–773. https://doi.org/10.1093/molbev/msw260
Lim, V.-C., Ramli, R., Bhassu, S. & Wilson, J.-J. (2017) A checklist of the bats of Peninsular Malaysia and progress towards a DNA barcode reference library. PLoS ONE, 12 (7), e0179555. https://doi.org/10.1371/journal.pone.0179555
Matthee, C.A., Burzlaff, J.D., Taylor, J.F. & Davis, S.K. (2001) Mining the mammalian genome for artiodactyl systematics. Systematic Biology, 50, 1–24. https://doi.org/10.1080/106351501300317987
Medway, L. (1969) The wild mammals of Malaya and offshore islands including Singapore. Oxford University Press, Kuala Lumpur, Singapore and London, xix + 127 pp.
Meng, X., Liu T., Zhang, L., Jin, L., Sun, K. & Feng, J. (2021) Effects of colonization, geography and environment on genetic divergence in the intermediate leaf-nosed bat, Hipposideros larvatus. Animals, 11, 733. https://doi.org/10.3390/ani11030733
Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., von Haeseler, A. & Lanfear R. (2020) IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
Monadjem, A., Soisook, P., Thong, V.D. & Kingston, T. (2019) Family Hipposideridae (Old World Leaf-nosed Bats). In: Wilson, D.E. & Mittermeier, R.A. (Eds.), Handbook of the Mammals of the World. Vol. 9. Lynx Edictions, Barcelona, pp. 210–259.
Murray, S.W., Campell, P., Kingston, T., Zubaid, A., Francis, C.M. & Kunz, T.H. (2012) Molecular phylogeny of hipposiderid bats from Southeast Asia and evidence of cryptic diversity. Molecular Phyliogenetics and Evolution, 62, 597–611. https://doi.org/10.1016/j.ympev.2011.10.021
Nesi, N., Nakouné, E., Cruaud, C. & Hassanin, A. (2011) DNA barcoding of African fruit bats (Mammalia, Pteropodidae). The mitochondrial genome does not provide a reliable discrimination between Epomophorus gambianus and Micropteropus pusillus. Comptes Rendus Biologies, 334, 544–554. https://doi.org/10.1016/j.crvi.2011.05.003
Ragan, M.A. (1992a) Phylogenetic inference based on matrix representation of trees. Molecular Phyliogenetics and Evolution, 1 (1), 53–58. https://doi.org/10.1016/1055-7903(92)90035-F
Ragan, M.A. (1992b) Matrix representation in reconstructing phylogenetic relationships among the eukaryotes. Biosystems, 28 (1-3), 47–55. https://doi.org/10.1016/0303-2647(92)90007-L
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19 (12), 1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual. 2nd Edition. Cold Spring Harbor laboratory press, New York, New York, 1546 pp.
Simmons, N.B. (2005) Order Chiroptera. In: Wilson, D.E. & Reeder D.M. (Eds.), Mammal Species of the World. A Taxonomic and Geographic Reference. Third Edition. Volume 1. Johns Hopkins University Press, Baltimore, Maryland, pp. 312–529.
Tate, G.H.H. (1941) A review of the genus Hipposideros with special reference to Indo-Australian species. Bulletin of American Museum of Natural History, 78, 353–393.
Thabah, A., Rossiter, S.J., Kingston, T., Zhang, S., Parsons, S., Mya, K.M., Akbar, Z. & Jones, G. (2006) Genetic divergence and echolocation call frequency in cryptic species of Hipposideros larvatus s.l. (Chiroptera: Hipposideridae) from the Indo-Malayan region. Biological Journal of Linnean Society, 88, 119–130. https://doi.org/10.1111/j.1095-8312.2006.00602.x
Thong, V.D., Puechmaille, S.J., Denzinger, A., Bates, P., Dietz, C., Csorba, G., Soisook, P., Teeling, E.C., Matsumura, S., Furey, N. & Schnitzler, H.-U. (2012) Systematics of the Hipposideros turpis complex and a description of a new subspecies from Vietnam. Mammal Review, 42, 166–192. https://doi.org/10.1111/j.1365-2907.2011.00202.x
Topál, G. (1975) Bacula of some Old World leaf-nosed bats (Rhinolophidae and Hipposideridae, Chiroptera: Mammalia). Vertebrata Hungarica, 16, 21–53.
Topál, G. (1993) Taxonomic status of the Hipposideros larvatus alongensis Bourret, 1942 and occurrence of Hipposideros turpis Bangs, 1904 in Vietnam (Mammalia, Chiroptera). Acta Zoologica Hungarica, 39, 267–288.
Vallo, P., Benda, P., Červený, J. & Koubek, P. (2012) Conflicting mitochondrial and nuclear paraphyly in small-sized West African house bats (Vespertilionidae). Zoologica Scripta, 42 (1), 1–12. https://doi.org/10.1111/j.1463-6409.2012.00563.x
Yusefovich, A.P., Artyushin, I.V., Raspopova, A.A., Bannikova, A.A. & Kruskop, S.V. (2020) An attempt to reconstruct the phylogeny of the Hipposideros leaf-nosed bats based on nuclear gene markers. Doklady Biological Science, 493, 136–140. https://doi.org/10.1134/S0012496620040109
Yuzefovich, A.P., Artyushin, I.V. & Kruskop, S.V. (2021) Not the cryptic species: Diversity of Hipposideros gentilis (Chiroptera: Hipposideridae) in Indochina. Diversity, 13 (5), 218. https://doi.org/10.3390/d13050218
Zubaid, A. & Davidson, G.W.H. (1987) A comparative study of the baculum in Peninsular Malaysian hipposiderines. Mammalia, 51, 139–144. https://doi.org/10.1515/mamm.1987.51.1.139