A re-assessment of diversity among Philippine gymnures (Mammalia: Erinaceidae: Podogymnura), with a new species from eastern Mindanao

Author:

BALETE DANILO S.ORCID,HEANEY LAWRENCE R.ORCID,RICKART ERIC A.ORCID,QUIDLAT ROSELYN S.ORCID,ROWSEY DAKOTA M.ORCID,OLSON LINK E.ORCID

Abstract

Podogymnura, a Philippine endemic genus of gymnures (“soft-furred hedgehogs”), has been known previously only from the highlands of central Mindanao (P. truei truei and P. t. minima) and from two small islands off the northeast tip of Mindanao (P. aureospinula). Based on a combination of mitochondrial genetic and qualitative and quantitative morphological data, we recognize P. minima, formerly considered a subspecies of P. truei, as a distinct species. We also recognize specimens from two little-studied montane regions of southeastern Mindanao, Mt. Hamiguitan and Mt. Kampalili, as a distinctive new species, P. intermedia n. sp. We estimate that dispersal of a common ancestor from Borneo to Mindanao ca. 1.9 to 3.5 Ma gave rise to Podogymnura, followed by speciation within Mindanao beginning 0.53 to 0.97 Ma. These results further increase the rich diversity of mammals on Mindanao, and underscore the importance of the eastern Mindanao highlands as a likely important but little-studied center of Philippine mammalian diversity.  

Publisher

Magnolia Press

Subject

Animal Science and Zoology,Ecology, Evolution, Behavior and Systematics

Reference2 articles.

1.

Balete, D.S., Quidlat, R.S. & Ibañez, J.C. (2006) The non-volant small mammals of Mt. Hamiguitan, Eastern Mindanao, Philippines. Banwa,3, 65–80.
Balete, D.S., Heaney, L.R., Rickart, E.A., Quidlat, R.S. & Ibanez, J.C. (2008) A new species of Batomys (Muridae: Murinae) from eastern Mindanao Island, Philippines. Proceedings of the Biological Society of Washington, 121, 411–428. https://doi.org/10.2988/07-47.1
Bannikova, A.A., Lebedev, V.S., Abramov, A.V. & Rozhnov, V.V. (2014) Contrasting evolutionary history of hedgehogs and gymnures (Mammalia: Erinaceomorpha) as inferred from multigene study. Biological Journal of the Linnean Society, 112, 499–519. https://doi.org/10.1111/bij.12299
Bouckaert, R.R. et al. (2014). BEAST 2: A software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10, 1–7.
Brown, J.C. (1971) The description of mammals. 1. The external characters of the head. Mammal Review, 1, 151–168. https://doi.org/10.1111/j.1365-2907.1972.tb00333.x
Brown, J.C. & Yalden, D.W. (1973) The description of mammals. 2. Limbs and locomotion of terrestrial mammals. Mammal Review, 3, 107–134. https://doi.org/10.1111/j.1365-2907.1973.tb00178.x
Corbet, G.B. & Hill, J.E. (1992) Mammals of the Indo-Malayan region: systematic review. Oxford: Oxford University Press. 488 pp.
den Tex, R-J., Thorington, R.W. Jr., Maldonado, J.E. & Leonard, J.A. (2010) Speciation dynamics in the SE Asian tropics: Putting a time perspective on the phylogeny and biogeography of Sundaland tree squirrels, Sundasciurus. Molecular Phylogenetics and Evolution, 55, 711–720. https://doi.org/10.1016/j.ympev.2009.12.023
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
Esselstyn, J.A., Timm, R.M. & R.M. Brown. (2009) Do geological or climatic processes drive speciation in dynamic archipelagos? The tempo and mode of diversification in Southeast Asia shrews. Evolution, 63, 2595–2610. https://doi.org/10.1111/j.1558-5646.2009.00743.x
Fernando, E.S., Suh, M.H., Lee, J. & Lee, D.K. (2008) Forest formations of the Philippines. Seoul: GeoBook Publishing Co.
Frost, D.R., Wozencraft, W.C. & Hoffmann, R.S. (1991) Phylogenetic relationships of hedgehogs and gymnures (Mammalia: Insectivora: Erinaceidae). Smithsonian Contributions to Zoology, 518, 1–69. https://doi.org/10.5479/si.00810282.518
Gunderson, A.M., Lanier, H.C. & Olson, L.E. (2012) Limited phylogeographic structure and genetic variation in Alaska’s arctic and alpine endemic, the Alaska marmot. Journal of Mammalogy, 93, 66–75. https://doi.org/10.1644/10-MAMM-A-380.1
Hall, R. (1998) The plate tectonics of Cenozoic SE Asia and the distribution of land and sea. In Biogeography and geological evolution of SE Asia. R. Hall & J. D. Holloway (Ed.), Leiden, Backhuys Publishers, pp. 99–131.
Hall, R. (2013) The palaeogeography of Sundaland and Wallacea since the Late Jurassic. Journal of Limnology, 72, 1–17. https://doi.org/10.4081/jlimnol.2013.s2.e1
He, K., Chen, J., Gould, G.C., Yamaguchi, N., Ai, H., Wang, Y., Zhang, Y. & Jiang, X. (2012) An estimation of Erinaceidae phylogeny: a combined analysis approach. PLoS ONE, 7, 1–14. https://doi.org/10.1371/journal.pone.0039304
Heaney, L.R. (1986) Biogeography of mammals in Southeast Asia: estimates of rates of colonization, extinction, and speciation. Biological Journal of the Linnean Society, 28, 127–165. https://doi.org/10.1111/j.1095-8312.1986.tb01752.x
Heaney, L.R. & Rabor, D.S. (1982) An annotated checklist of the mammals of Dinagat and Siargao islands, Philippines. Occasional Papers of the Museum of Zoology, University of Michigan, 699, 1–30.
Heaney, L.R. & Morgan, G.S. (1982) A new species of gynmure, Podogymnura, (Mammalia: Erinaceidae) from Dinagat Island, Philippines. Proceedings of the Biological Society of Washington, 95, 13–26.
Heaney, L.R., Balete, D.S., Duya, M.R.M., Duya, M.V., Jansa, S.A., Steppan, S.J. & Rickart, E.A. (2016a). Doubling diversity: a cautionary tale of previously unsuspected mammalian diversity on a tropical oceanic island. Frontiers of Biogeography, 8.2, e29667, pp. 1–19. https://doi.org/10.21425/F58229667
Heaney, L.R., Balete, D.S. & Rickart, E.A.  (2016b) The Mammals of Luzon Island: Biogeography and Natural History of a Philippine Fauna.  Johns Hopkins University Press, Baltimore. 287 pp.
Heaney, L.R., Balete, D.S., Dolar, L., Alcala, A.C., Dans, A., Gonzales, P.C., Ingle, N.R., Lepiten, M., Oliver, W., Ong, P., Rickart, E.A., Tabaranza, B.R. Jr. & Utzurrum, R. C. B. (1998) A synopsis of the mammalian fauna of the Philippine Islands. Fieldiana: Zoology, New Series, 88, 1–61.
Heaney, L.R., Dolar, M.L., Balete, D.S., Esselstyn, J.A., Rickart, E.A. & Sedlock, J.L. (2010) Synopsis of Philippine Mammals. Field Museum website, http://www.fieldmuseum.org/philippine_mammals/
Heaney, L.R., Tabaranza, B.R. Jr., Rickart, E.A., Balete, D.S. & Ingle, N.R. (2006) The mammals of Mt. Kitanglad Nature Park, Mindanao, Philippines. Fieldiana: Zoology (New Series), 112, 1–63. https://doi.org/10.3158/0015-0754(2006)186[1:TMOMKN]2.0.CO;2
Hoogstraal, H. (1951) Philippine zoological expedition, 1946–1947. Narrative and itinerary. Fieldiana: Zoology, 33, 1–33.
Hutterer, R. (2005) Order Erinaceomorpha. In Wilson, D.E. & D.M. Reeder (Eds.), Mammal Species of the World. Johns Hopkins University Press, 2, 142 pp.
Irwin, D.M., Kocher, T.D. & Wilson, A.C. (1991) Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution, 32, 128–144. https://doi.org/10.1007/BF02515385
Kocher, T.D., Thomas, W.K., Meyer, A., Edwards, S.V., Pääbo, S., Villablanca, F.X. & Wilson, A.C. (1989) Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proceedings of the National Academy of Sciences, USA, 86, 6196–6200. https://doi.org/10.1073/pnas.86.16.6196
Jansa, S.A., Barker, F.K. & Heaney, L.R. (2006) The pattern and timing of diversification of Philippine endemic rodents: Evidence from mitochondrial and nuclear gene sequences. Systematic Biology, 55, 73–88. https://doi.org/10.1080/10635150500431254
Lanfear, R., Calcott; B., Ho, S.Y.W. & Guindon, S. (2012) PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–1701. https://doi.org/10.1093/molbev/mss020
Lanier, H.C. & Olson, L.E. (2009) Inferring divergence times within pikas (Ochotona) using mtDNA and relaxed molecular dating techniques. Molecular Phylogenetics and Evolution, 53, 1–12. https://doi.org/10.1016/j.ympev.2009.05.035
Lopatin, A.V. (2006) Early Paleogene insectivore mammals of Asia and establishment of the major groups of Insectivora. Paleontological Journal, 40, S205–S240. https://doi.org/10.1134/S0031030106090012
Mearns, E.A. (1905) Descriptions of new genera and species of mammals from the Philippine Islands. Proceedings of the United States National Museum, 28, 425–460. https://doi.org/10.5479/si.00963801.1402.425
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop, GCE 2010. https://doi.org/10.1109/GCE.2010.5676129
Ostende, L.W. (2001) A revised generic classification of the Galericini (Insectivora, Mammalia) with some remarks on their paleobiogeography and phylogeny. Geobios, 34, 681–695. https://doi.org/10.1016/S0016-6995(01)80029-2
Poduschka, V.W. & Poduschka, C. (1985) Beitrage zur Kenntnis der Gattung Podogymnura Mearns 1905 (Insectivora: Echinosoricinae). Zeitschrift fur Saugetierkunde, 50, 1–21.
Rambaut, A., Drummond, A.J. & Suchard, M.A. (2013) Tracer MCMC Analysis Package. <http://beast.bio.ed.ac.uk>.
Rickart, E.A. (2003) Chromosomes of Philippine mammals (Insectivora, Dermoptera, Primates, Rodentia, Carnivora). Proceedings of the Biological Society of Washington, 116, 473–487.
Roberts T.E., Lanier, H.C., Sargis, E.J. & Olson, L.E. (2011) Molecular phylogeny of treeshrews (Mammalia: Scandentia) and the timescale of diversification in Southeast Asia. Molecular Phylogenetics and Evolution, 60, 358–372. https://doi.org/10.1016/j.ympev.2011.04.021
Rowe, K.C., Achmadi, A.S., Fabre, P-H., Schenk, J.J., Steppan, S. J. & Esselstyn, J.A. (2019) Oceanic islands of Wallacea as a source for dispersal and diversification of murine rodents. Journal of Biogeography, 46, 2752–2768. https://doi.org/10.1111/jbi.13720
Rowsey, D.M., Duya, M.R.M., Ibañez, J.C., Jansa, S.A., Rickart, E.A. & Heaney, L.R. (2022) A new genus and species of shrew-like mouse (Rodentia: Muridae) from a new center of endemism in eastern Mindanao, Philippines. Journal of Mammalogy, 103. https://doi.org/10.1093/jmammal/gyac057.
Sajona, F.G., Bellon, H., Maury, R.C., Pubellier, M., Quebral, R.D., Cotten, J., Bayon, F.E., Pagados, E. & Pamatian, P. (1997) Tertiary and Quaternary magmatism in Mindanao and Leyte (Philippines): geochronology, geochemistry and tectonic setting. Journal of Asian Earth Sciences, 2–3, 121–153. https://doi.org/10.1016/S1367-9120(97)00002-3
Sanborn, C.C. (1952) Philippine zoological expedition, 1946 – 1947: Mammals. Fieldiana: Zoology, 33, 1–158.
Sanborn, C.C. (1953) Mammals from Mindanao, Philippine Islands collected by the Danish Philippine Expedition, 1951–1952. Videnskabelige Meddelelser Dansk Naturhistorisk Forening, 115, 283–288.
Springer, M.S. & Douzery, E. (1996) Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. Journal of Molecular Evolution, 43, 357–373. https://doi.org/10.1007/BF02339010
SPSS, Inc. (2000) SYSTAT 10. SPSS, Inc., Chicago, IL.
Stamatakis, A., Hoover, P. & Rougemont, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology, 57, 758–771. https://doi.org/10.1080/10635150802429642
Steppan, S., Zawadski, C. & Heaney, L.R. (2003) Molecular phylogeny of the endemic Philippine rodent Apomys (Muridae) and the dynamics of diversification in an oceanic archipelago. Biological Journal of the Linnean Society, 80, 699–715. https://doi.org/10.1111/j.1095-8312.2003.00274.x
Szalay, F.S. (1969) Mixodectidae, Microsyopidae, and the insectivore-primate transition. Bulletin of the American Museum of Natural History, 140, 193–330.
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526.
Yumul, G.P. Jr., Dimalanta, C.B., Maglambayan, V.B. & Marquez, E.J. (2008) Tectonic setting of a composite terrane: A review of the Philippine island arc system. Geosciences Journal, 1, 7–17. https://doi.org/10.1007/s12303-008-0002-0

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