Sains Malaysiana 51(10)(2022):
3125-3141
http://doi.org/10.17576/jsm-2022-5110-01
Phylogenetic
Relationships and Morphological Variation of Gymnures (Galericidae: Hylomys) from Genting Highlands,
Pahang, Malaysia
(Hubungan Filogenetik dan Variasi Morfologi Tikus Babi (Galericidae: Hylomys) daripada Tanah
Tinggi Genting, Pahang, Malaysia)
MUHAMMAD
FARHAN ABD WAHAB1, MASAHARU MOTOKAWA2, FAISAL ALI
ANWARALI KHAN3, DHARINI PATHMANATHAN4 & HASMAHZAITI
OMAR1,5,*
1Institute of Biological
Sciences, Faculty of Science, Universiti Malaya,
50603 Kuala Lumpur, Federal Territory, Malaysia
2The Kyoto
University Museum, Kyoto University, Kyoto 606-8501, Japan
3Faculty of Resource Science
and Technology, Universiti Malaysia Sarawak, 94300
Kota Samarahan, Sarawak, Malaysia
4Institute of Mathematical
Sciences, Faculty of Science, Universiti Malaya,
50603 Kuala Lumpur, Federal Territory, Malaysia
5Museum of Zoology (Block F14),
Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia
Diserahkan: 11 Februari 2022/Diterima: 2 Jun 2022
Abstract
Gymnures from the
genus Hylomys are widely distributed across Sundaland and the Indochinese region. However, the
relationships among its members in Peninsular Malaysia especially from Genting
Highlands are still lacking. This study aims to examine the morphology and
genetically analyse of the Hylomys specimens collected from the new isolated population of Genting Highlands,
Pahang, Malaysia. Morphometric analyses showed that morphological variation
exists among the Hylomys lineage. The external
morphology and the skull measurements of the taxa studied coincide with those
of Hylomys maxi from Peninsular
Malaysia and Sumatra based on descriptive statistics and principal component
analysis (PCA). The differences within the Hylomys taxa are also evident in the phylogenetic tree and K2P genetic distances
analyses inferred from cyt b. Hylomys samples from Genting Highlands formed a
clade with H. maxi from Cameron Highlands and Fraser’s Hill, Peninsular
Malaysia and Sumatra. However, they were separated from Hylomys parvus(Sumatra), Hylomys suillus (Java) and Hylomys dorsalis (Borneo). Relatively, low genetic distances were detected
among the studied taxa with other H. maxi (<6% K2P distance) while
high genetic distances were observed when compared to other Hylomys taxa (>18.0% K2P distance). Based on these facts, we confirm that the gymnures
from Genting Highlands belong to a valid species, Hylomys maxi along with other Peninsular Malaysia samples based on genetics and
morphological data which probably originated from Sumatra a long time ago.
Keywords: Biogeography; Eulipotyphyla; genetic relationships; morphology;
Peninsular Malaysia
Abstrak
Tikus
babi daripada genus Hylomys mempunyai taburan yang luas di Sundaland dan
Indochina. Walau bagaimanapun, kajian mengenai hubungan antara kumpulan tikus
babi di Semenanjung Malaysia terutamanya dari Tanah Tinggi Genting masih
kurang dijalankan. Penyelidikan ini bertujuan untuk mengkaji morfologi dan
menganalisis secara genetik spesimen Hylomys yang dikumpul daripada
populasi baru Tanah Tinggi Genting, Pahang, Malaysia. Analisis morfometrik
mendedahkan bahawa variasi morfologi wujud dalam kalangan Hylomys.
Morfologi luaran dan ukuran tengkorak takson yang dikaji bertepatan dengan Hylomys
maxi dari Semenanjung Malaysia dan Sumatera berdasarkan statistik
deskriptif dan analisis komponen utama (PCA). Perbezaan dalam takson Hylomys juga jelas pada pokok filogenetik dan analisis jarak genetik K2P berdasarkan
urutan gen cyt b. Sampel Hylomys dari Tanah Tinggi Genting
membentuk klad dengan H. maxi dari Tanah Tinggi Cameron dan Bukit
Fraser, Semenanjung Malaysia dan Sumatera. Walau bagaimanapun, mereka
dipisahkan daripada Hylomys parvus (Sumatera), Hylomys suillus (Jawa) dan Hylomys dorsalis (Borneo). Secara relatifnya, jarak genetik
yang rendah dikesan dalam kalangan takson yang dikaji dengan H. maxi lain
(<6% jarak K2P) manakala jarak genetik yang tinggi diperhatikan jika
dibandingkan dengan takson Hylomys yang lain (>18.0% jarak K2P).
Berdasarkan fakta ini, kami mengesahkan bahawa tikus babi daripada Tanah Tinggi
Genting tergolong dalam spesies yang sah, Hylomys maxi bersama sampel
Semenanjung Malaysia yang lain berdasarkan data genetik dan morfologi yang
mungkin berasal dari Sumatera pada satu masa dahulu.
Kata kunci: Biogeografi; Eulipotyphyla; hubungan genetik;
morfologi; Semenanjung Malaysia
RUJUKAN
Akaike, H. 1974.
A new look at statistical model identification. IEEE Trans. Automat. Control 19: 716-723.
Arai,
S, Mori, T., Yoshida, H. & Shiraishi, S. 1985. A
note on the Japanese Water Shrew, Chimarrogale himalayica platycephala,
from Kyushu. Journal of the Mammalogical Society of Japan 10: 193-203.
Arnason, U., Adegoke, J.A., Gullberg,
A., Harley, E.H., Janke, A. & Kullberg, M. 2008. Mitogenomic relationship
of placental mammals and molecular estimates of their divergences. Gene 421: 37-51.
Avise, J.C., Arnold, J., Ball, R.M., Bermingham,
E., Lamb, T., Neigell, J.E., Reebl,
C.A. & Saunders, N.C. 1987. Intraspecific Phylogeography:
The mitochondrial DNA bridge between population genetics and systematics. Ann.
Rev. Ecol. Syst. 18: 489-522.
Bannikova, A.A., Lebedev, V.S., Abramov, A.V. & Rozhnov, V.V. 2014. Contrasting evolutionary history of
Hedgehogs and Gymnures (Mammalia: Erinceomorpha) as
inferred from a multigene study. Biological Journal of the Linnean Society 112: 499-519.
https://doi.org/10.1111/bij.12299
Batin, Z., Nor, S.M. & Ahmad, M.Y. 2002. Influence of
elevational habitat changes on non-volant small mammal species distribution and
diversity on Mount Nuang, Hulu Langat, Selangor,
Malaysia. Asian Network for Scientific Information. Pakistan Journal of
Biological Sciences 5(8): 819-824.
Bird, M.I.,
Taylor, D. & Hunt, C. 2005. Paleoenvironments of Insular Southeast Asia
during the Last Glacial Period: A Savannah Corridor in Sundaland? Quat. Sci. Rav. 24: 2228-2242.
Blainville,
H.M.D. de. 1838. Recherches sur l’anciennete des Mammiferes insectivores a la surface de la terre; precedes de l’histoire de
la science a ce sujet, des principes de leur classification
et de leur distribution geographique actuelle. Comptes Rendus Hebdomadaires de
Seances de l’Academie des Sciences 6: 738-744.
Bradley, R.D.
& Baker, R.J. 2001. A test of the genetic species concept: Cytochrome b sequences and mammals. Journal of Mammalogy 82: 960-973.
Cavendish, M.
2007. Malaysia, Singapore, Brunei and The Philippines. World and Its Peoples: Eastern and Southern Asia 9: 1583.
Chasen, F.N. 1940. A handlist of Malaysian mammals: A
systematic list of the mammals of the Malay Peninsula, Sumatra, Borneo, and
Java, including the adjacent small islands. Bulletin of the Raffles Museum Singapore 15: 1-209.
Corbet,
G.B. 1988. The Family Erinaceidae: A synthesis of Its
Taxonomy, Phylogeny, Ecology and Zoogeography. Mammal Review 18:
117-172.
Corbet,
G.B. & Hill, J.E. 1992. The Mammals of the Indomalayan Region: A Systematic Review. Oxford: Oxford University Press.
Darriba, D., Taboada, G.L., Doallo,
R. & Posada, D. 2012. jModelTest 2: More models,
new heuristics and parallel computing. Nature Methods 9: 772.
Dubey, S., Salamin, N., Ohdachi, S.D. &
Vogel, P. 2007. Molecular phylogenetics of shrews (Mammalia: Soricidae) reveal timing of transcontinental colonizations. Molecular Phylogenetics Evolution 44(1): 126-137.
Engesser, B. & Jiang, J. 2011. Odontological and craniological comparisons of the recent hedgehogs Neotetracus with Hylomys and Neohylomys (Erinaceidae, Insectivora,
Mammalia). Vertebrata Palasiatica 49: 406-422.
Esselstyn, J.A.,
Timm, R.M. & Brown, R.M. 2009. Do geological or climatic processes drive
speciation in dynamic archipelagos? The tempo and mode of diversification
in Southeast Asian shrews. Evolution 63: 2595-2610.
Felsenstein, J. 1985. Confidence limits on phylogenies: An
approach using the bootstrap. Evolution 39: 783-791.
Fischer,
G. 1814. Zoognosia. Tabulis Synopticis Illustrata. 3.
Moscow: Nicolai Sergeidis Vsevolozsky.
Frost,
D.R., Wozencraff, W.C. & Hoffmann, R.S. 1991. Phylogenetic
relationships of Hedgehogs and Gymnures (Mammalia: Insectivora: Erinaceidae). Smithsonian Contributions to Zoology 518: 1-69.
Gorog, A.J., Sinaga,
M.H. & Engstrom, M.D. 2004. Vicariance or dispersal? Historical
biogeography of three Sunda Shelf murine rodents (Maxomys surifer, Leopoldomys sabanus and Maxomys whiteheadi). Biological Journal of the Linnean Society 81:
91-109.
He,
K., Chen, J-H., Gould, G.C., Yamaguchi, N., Ai, H-S., Wang, Y-X., Zhang, Y-P.
& Jiang, X-L. 2012. An estimation of Erinaceidae Phylogeny: A combined analysis approach. PLoS ONE 7(6): e39304. https://doi:10.1371/journal.pone.003930
Heaney, L.R.,
Walsh, J.S. & Peterson, A.T. 2005. The roles of geological history and
colonization abilities in genetic differentiation between mammalian populations
in the Philippine archipelago. Journal of Biogeography 32: 229-247.
Hewitt, G.M.
2000. The genetic legacy of the quaternary ice ages. Nature 405:
907-913.
Huelsenbeck, J.P. & Ronquist,
F.R. 2001. MrBayes: Bayesian inference of phylogenetic
trees. Bioinformatics 17: 754-755.
Hutterer, R. 2005. Order Soricomorpha.
In Mammal Species of the World: A Taxonomic and Geographic Reference. 3rd ed., edited by Wilson, D.E. & Reeder, D.M. Baltimore: Johns Hopkins
University Press. pp. 220-311.
Jenkins,
P.D. & Robinson, M.F. 2002. Another variation on the Gymnure Theme:
Description of a new species of Hylomys (Lipotyphyla, Erinaceidae, Galericinae). Bulletin National History Museum London (Zoology) 68(1): 1-11.
Khoo,
T.T. & Tan, B.K. 1983. Geological evolution of Peninsular Malaysia. Workshop
on Stratigraphic Correlation of Thailand and Malaysia. pp. 253-290.
Kimura,
M. 1980. A simple method for estimating evolutionary rate of base substitutions
through comparative studies of nucleotide sequences. Molecular and Evolution
Journal 16: 111-120.
Kloss,
C.B. 1916. On a collection of mammals from Siam. Journal of the Natural
History Society of Siam 2: 1-36.
Kumar, S., Stecher, G., Li, M., Knyaz, C.
& Tamura, K. 2018. Mega X: Molecular evolutionary genetics analysis across
computing platforms. Molecular Biology 35: 1547-1549.
Langham, N. 1983.
Distribution and ecology of small mammals in Three Rain Forest Localities of
Peninsula Malaysia with particular references to Kedah Peak. The Association
for Tropical Biology and Conservation. Biotropica 15: 199-206.
Lim,
B.L., Lim, K.K.P. & Yong, H.S. 1999. The terrestrial mammals of Pulau Tioman, Peninsular
Malaysia, with a catalogue of specimens at the Raffles Museum, National
University of Singapore. The Raffles Bulletin of Zoology 6: 101-123.
McKenna,
M.C. & Bell, S.K. 1997. Classification of Mammals Above the Species
Level. New York: Columbia University Press. 1(12): 1-631.
Medway,
L. 1983. The Wild Mammals of Malaya (Peninsular Malaysia) and Singapore. 2nd
edition. Kuala Lumpur: Oxford University Press.
Müller,
S. 1840. Over de Zoogdieren van den Indischen Archipel. pp. 1-8
[1839], pp. 9-57+6 unnumbered pp. [1840], in Verhandelingen over de Natuurlijke Geschiedenis der Nederlandsche overzeesche bezittingen, door de Leden der Natuurkundige Commissie in Indiö en andere Schrijvers (C.J. Temminck, ed.). [V. 3] Zoology [1839-1845]. J. Luchtmans en C. C. van der Hoek.
Nor,
S.M. 2001. Elevational diversity patterns of small mammals on Mount Kinabalu,
Sabah, Malaysia. Global Ecology and Biogeography 10(1): 41-62.
https://doi.10.1046/j.1466-822x.2001.00231.x
Ohdachi, S., Dokuchaev, N.E.,
Hasegawa, M. & Masuda, R. 2001. Intraspecific phylogeny and geographic
variation of six species of Northeastern Asiatic Sorex Species based on the mitochondrial cytochrome b sequences. Molecular Ecology 10: 2199-2213.
Omar,
H., Hashim, R., Bhassu, S. & Ruedi,
M. 2013. Morphological and genetic relationships of the Crocidura monticola species complex (Soricidae: Crocidurinae) in Sundaland. Mammalian Biology 78: 446-454.
Pomel, A. 1848. Etudes sur les Carnassiers Insectivores (Extrait). Seconde Partie. Classification des Insectivores. Archives
des Sciences Physiques et Naturelles 9: 244-251.
Raes, N., Cannon, C.H., Hijmans,
R.J., Piessens, T., Saw, L.G., Welzen,
P.C.V. & Slik, J.W.F. 2014. Historical
distribution of Sundaland’s Dipterocarp Rainforests
at Quaternary Glacial Maxima. Proceedings of the National Academy of
Sciences of the United States of America 111: 16790-1679.
Raffles, T.S.
1822. “1821”. Descriptive catalogue of a zoological collection, made on account
of the honorable East Indian Company, in the Island of Sumatra and Its
Vicinity, under the Direction of Sir Thomas Stamford Raffles,
Lieutenant-Governor of Fort Marlborough, with additional notices illustrative
of the natural history. Transactions of the Linnaean Society of London 13(1): 239-274.
Robinson,
H.C. & Kloss, C.B. 1916. Preliminary diagnoses of some new species and
subspecies of mammals and birds obtained in Korinchi,
West Sumatra, Feb-June 1914. Journal of the Straits Branch of the Royal
Asiatic Society 73: 269-278.
Ruedi, M. & Fumagalli, L.
1996. Genetic structure of Gymnures (Genus Hylomys; Erinaceidae) on Continental Islands of Southeast
Asia: Historic effects of fragmentation. Journal of Zoological Systematics
and Evolutionary Research 34: 153-162.
Ruedi, M., Chapuisat, M. &
Iskandar, D. 1994. Taxonomic status of Hylomys parvus and Hylomys suillus (Insectivota: Erinaceidae): Biochemical and morphological analyses. Journal
of Mammalogy 75(4): 965-978.
Shaw,
T-H. & Wong, S. (Wang Sung). 1959. A new insectivores from Hainan. [In
Chinese; English summary]. Acta Zoologica Sinica 11: 422-425.
Smith,
A.T., Yan, X., Hoffman, R., Lunde, D., MacKinnon, J., Wilson, D.E. & Wozencraft, W.C. 2008. A Guide to the Mammals of China.
Princeton: Princeton University Press.
Sody, H.J.V. 1933. Ten new mammals from the Dutch East
Indies. Annals and Magazine of Natural History 10: 430-442.
Thomas,
O. 1925. The Spedan Lewis South American Exploration.
I. On mammals from Southern Bolivia. Annals and Magazine of Natural History 9 15(89): 575-582.
Thomas,
O. 1888. On a Collection of Mammals Obtained by Emin Pasha in Equatorial Africa and Presented by Him to the Natural History Museum. Proceedings
of the Zoological Society of London 1888: 3-17.
Trouessart, E.L. 1909. Neotetracus sinensis, a new insectivore of the family Erinaceidae. Annals and Magazine of Natural History 8 4: 389-391.
Waddell,
P.J., Cao, Y., Hauf, J. & Hasegawa, M. 1999. Using
novel phylogenetic methods to evaluate mammalian mtDNA,
including amino acid-invariant sites-logdet plus site
stripping to detect internal conflicts in the data, with special
reference to the positions of Hedgehog, Armadillo and Elephant. Systematic
Biology 48: 31-53.
Wilson,
D.E. & Mittermeier, R.A. 2018. Handbook of the Mammals of the World 8.
Insectivores, Sloth and Colugos. Lynx Edicions,
Barcelona.
* Pengarang untuk surat-menyurat; email: zaiti_1978@um.edu.my
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