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Using three-dimensional geometric morphometric and dental topographic analyses to infer the systematics and paleoecology of fossil treeshrews (Mammalia, Scandentia)

Published online by Cambridge University Press:  03 July 2020

Keegan R. Selig Open the ORCID record for Keegan R. Selig [Opens in a new window] ,
Eric J. Sargis Open the ORCID record for Eric J. Sargis [Opens in a new window] ,
Stephen G.B. Chester Open the ORCID record for Stephen G.B. Chester [Opens in a new window]  and
Mary T. Silcox Open the ORCID record for Mary T. Silcox [Opens in a new window]
Keegan R. Selig
Affiliation:
Department of Anthropology, University of Toronto Scarborough, 1265 Military Trail, Toronto, ONM1C 1A4, Canada ,
Eric J. Sargis
Affiliation:
Department of Anthropology, Yale University, P.O. Box 208277, New Haven, CT06520, USA Divisions of Vertebrate Zoology and Vertebrate Paleontology, Peabody Museum of Natural History, New Haven, CT, USA
Stephen G.B. Chester
Affiliation:
Department of Anthropology and Archaeology, Brooklyn College, City University of New York, Brooklyn, NY11210, USA Department of Anthropology, The Graduate Center, City University of New York, 365 Fifth Avenue, New York, NY10016, USA New York Consortium in Evolutionary Primatology, New York, NY, USA
Mary T. Silcox
Affiliation:
Department of Anthropology, University of Toronto Scarborough, 1265 Military Trail, Toronto, ONM1C 1A4, Canada ,
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Abstract

Treeshrews are small, Indomalayan mammals closely related to primates. Previously, three-dimensional geometric morphometric analyses were used to assess patterns of treeshrew lower second molar morphology, which showed that the positions of molar landmarks covary with intraordinal systematics. Another analysis used dental topographic metrics to test patterns of functional dental morphology and found that molar curvature, complexity, and relief were an effective means for examining patterns of variation in treeshrew dietary ecology. Here, we build on these analyses by adding two fossil taxa, Prodendrogale yunnanica Qiu, 1986 from the Miocene of China and Ptilocercus kylin Li and Ni, 2016 from the Oligocene of China. Our results show that Pr. yunnanica had a dental bauplan more like that of a tupaiid than that of a ptilocercid, but that the extant tupaiids, including Tupaia and Dendrogale, are more similar to one another in this regard than any are to Prodendrogale. This is contrary to our expectations as Prodendrogale is hypothesized to be most closely related to Dendrogale. Ptilocercus kylin, which has been proposed to be the sister taxon of Pt. lowii Gray, 1848, is characterized by dental morphology like that of Pt. lowii in crest and cuspal position but is interpreted to have been more frugivorous. It has been claimed that Ptilocercus has undergone little morphological change through time. Our results suggest that Pt. kylin was more ecologically distinct from Pt. lowii than previously proposed, providing a glimpse into a more complex evolutionary history of the group than had been inferred.

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Journal of Paleontology , Volume 94 , Issue 6 , November 2020 , pp. 1202 - 1212
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Copyright © 2020, The Paleontological Society

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References

Berthaume, M.A., Winchester, J.M., and Kupczik, K., 2019, Ambient occlusion and PCV (portion de ciel visible): A new dental topographic metric and proxy of morphological wear resistance: PLOS ONE, v. 14, n. e0215436.CrossRefGoogle ScholarPubMed
Bloch, J.I., Silcox, M.T., Boyer, D.M., and Sargis, E.J., 2007, New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates: Proceedings of the National Academy of Sciences, v. 104, p. 1159–1164.CrossRefGoogle ScholarPubMed
Boyer, D.M., 2008, Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals: Journal of Human Evolution, v. 55, p. 1118–1137.CrossRefGoogle ScholarPubMed
Boyer, D.M., Gunnell, G.F., Kaufman, S., and McGeary, T., 2016, MorphoSource–Archiving and sharing 3D digital specimen data: Journal of Paleontology, v. 22, p. 157–181.Google Scholar
Bunn, J.M., Boyer, D.M., Lipman, Y., St. Clair, E.M., Jernvall, J., and Daubechies, I., 2011, Comparing Dirichlet normal surface energy of tooth crowns, a new technique of molar shape quantification for dietary inference, with previous methods in isolation and in combination: American Journal of Physical Anthropology, v. 145, p. 247–261.CrossRefGoogle ScholarPubMed
Butler, P.M., 1972, The problem of insectivore classification, in Joysey, K.A., and Kemp, T.S., eds., Studies in Vertebrate Evolution: Edinburgh, Oliver and Boyd, p. 253–265.Google Scholar
Butler, P.M., 1980, The tupaiid dentition, in Luckett, W.P., ed., Comparative Biology and Evolutionary Relationships of Tree Shrews, Advances in Primatology: New York, Springer, p. 171–204.CrossRefGoogle Scholar
Carlsson, A, 1922, Über die Tupaiidae und ihre Beziehungen zu den Insectivora und den Prosimiae: Acta Zoologica, v. 3, p. 227–270.CrossRefGoogle Scholar
Chester, S.G.B., Bloch, J.I., Boyer, D.M., and Clemens, W.A., 2015, Oldest known euarchontan tarsals and affinities of Paleocene Purgatorius to Primates: Proceedings of the National Academy of Sciences USA, v. 112, p. 1487–1492.CrossRefGoogle ScholarPubMed
Chopra, S.R.K., and Vasishat, R.N., 1979, Sivalik fossil tree shrew from Haritalyangar, India: Nature, v. 281, p. 214–215.CrossRefGoogle Scholar
Chopra, S.R.K., Kaul, S., and Vasishat, R.N., 1979, Miocene tree shrews from the Indian Sivaliks: Nature, v. 281, p. 213–214.CrossRefGoogle Scholar
Clarke, C., Moran, J.A., and Chin, L., 2010, Mutualism between tree shrews and pitcher plants: Plant Signaling & Behavior, v. 5, p. 1187–1189.CrossRefGoogle ScholarPubMed
Cooke, S.B., 2011, Paleodiet of extinct platyrrhines with emphasis on the Caribbean forms: three-dimensional geometric morphometrics of mandibular second molars: The Anatomical Record, v. 294, p. 2073–2091.CrossRefGoogle ScholarPubMed
Dennis, J.C., Ungar, P.S., Teaford, M.F., and Glander, K.E., 2004, Dental topography and molar wear in Alouatta palliata from Costa Rica: American Journal of Physical Anthropology, v. 125, p. 152–161.CrossRefGoogle ScholarPubMed
Dutta, A.K., 1975, Micromammals from Siwaliks: Indian Minerals, v. 29, p. 76–77.Google Scholar
Emmons, L.H., 1991, Frugivory in treeshrews (Tupaia): The American Naturalist, v. 138, p. 642–649.CrossRefGoogle Scholar
Emmons, L.H., 2000, Tupai: A Field Study of Bornean Treeshrews: Berkeley, University of California Press.CrossRefGoogle Scholar
Evans, A.R., 2013, Shape descriptors as ecometrics in dental ecology: Hystrix, v. 24, p. 133–140.Google Scholar
Evans, A.R., Wilson, G.P., Fortelius, M., and Jernvall, J., 2007, High-level similarity of dentitions in carnivorans and rodents: Nature, v. 445, p. 78–81.CrossRefGoogle ScholarPubMed
Godfrey, L.R., Winchester, J.M., King, S.J., Boyer, D.M., and Jernvall, J., 2012, Dental topography indicates ecological contraction of lemur communities: American Journal of Physical Anthropology, v. 148, p. 215–227.CrossRefGoogle ScholarPubMed
Gray, J.E., 1848, Description of a new genus of insectivorous Mammalia, or Talpidae, from Borneo: Proceedings of the Zoological Society of London, p. 23–24.Google Scholar
Günther, A., 1876, Remarks on some Indian and more especially Bornean mammals: Proceedings of the Zoological Society of London, v. 1876, p. 424–428.Google Scholar
Guy, F., Gouvard, F., Boistel, R., Euriat, A., and Lazzari, V., 2013, Prospective in (primate) dental analysis through tooth 3D topographical quantification: PLOS ONE, v. 8, n. e66142.CrossRefGoogle ScholarPubMed
Guy, F., Lazzari, V., Gilissen, E., and Thiery, G., 2015, To what extent is primate second molar enamel occlusal morphology shaped by the enamel–dentine junction?: PLOS ONE, v. 10, n. e0138802.CrossRefGoogle ScholarPubMed
Hammer, Ø., Harper, D.A.T., and Ryan, P.D., 2001, PAST: paleontological statistics software package for education and data analysis: Palaeontologia Electronica, v. 4, p. 1–9.Google Scholar
Horsfield, T., 1824, Zoological Researches in Java and the Neighboring Islands: London, Kingbury, Parbury & Allen.Google Scholar
Jacobs, L.L., 1980, Siwalik fossil tree shrews, in Luckett, W.P., ed., Comparative Biology and Evolutionary Relationships of Tree Shrews, Advances in Primatology: New York, Springer, p. 205–216.CrossRefGoogle Scholar
Kvartalnov, P.V., 2009, Ecology and behavior of the slender-tailed tree-shrew (Dendrogale murina, Scandentia): Zoologicheskii Zhurnal, v. 88, p. 1387–1395.Google Scholar
Langham, N.P.E., 1982, The ecology of the common tree shrew, Tupaia glis in peninsular Malaysia: Journal of Zoology, v. 197, p. 323–344.CrossRefGoogle Scholar
Langham, N.P.E., 1983, Distribution and ecology of small mammals in three rain forest localities of Peninsula Malaysia with particular references to Kedah Peak: Biotropica, v. 15, p. 199–206.CrossRefGoogle Scholar
Le Gros Clark, W.E., 1924, On the brain of the tree shrew (Tupaia minor): Proceedings of the Zoological Society of London, v. 1924, p. 1053–1074.Google Scholar
Le Gros Clark, W.E., 1925, On the skull of Tupaia: Proceedings of the Zoological Society of London, v. 95, p. 559–567.CrossRefGoogle Scholar
Li, Q., and Ni, X., 2016, An early Oligocene fossil demonstrates treeshrews are slowly evolving “living fossils”: Scientific Reports, v. 6, n. 18627.CrossRefGoogle Scholar
López-Torres, S., Selig, K.R., Prufrock, K.A., Lin, D., and Silcox, M.T., 2018, Dental topographic analysis of paromomyid (Plesiadapiformes, Primates) cheek teeth: more than 15 million years of changing surfaces and shifting ecologies: Historical Biology, v. 30, p. 76–88.CrossRefGoogle Scholar
McKenna, M.C., 1966, Paleontology and the origin of the primates: Folia Primatologica, v. 4, p. 1–25.CrossRefGoogle ScholarPubMed
Luckett, W.P., 1980, The suggested evolutionary relationships and classification of tree shrews, in Luckett, W.P., ed., Comparative Biology and Evolutionary Relationships of Tree Shrews, Advances in Primatology: New York, Springer, p. 3–31.CrossRefGoogle Scholar
Luckett, W.P., and Jacobs, L.L., 1980, Proposed fossil tree shrew genus Palaeotupaia: Nature, v. 288, p. 104–104.CrossRefGoogle Scholar
Lyon, M.W., 1913, Treeshrews: an Account of the Mammalian family Tupaiidae: Proceedings of the United States National Museum, v. 45, p. 1–188.CrossRefGoogle Scholar
Matschie, P., 1898, Über Säugethiere von den Philippinen: Sitz-Ber. Ges. Nat. Freunde, Berlin, v. 1898, p. 38–43.Google Scholar
Mein, P., and Ginsburg, L., 1997, Les mammifères du gisement miocène inférieur de Li Mae Long, Thailande: Systématique, biostratigraphie et paléoenvironnement: Geodiversitas, v. 9, p. 783–844.Google Scholar
M'Kirera, F., and Ungar, P.S., 2003, Occlusal relief changes with molar wear in Pan troglodytes troglodytes and Gorilla gorilla gorilla: American Journal of Primatology, v. 60, p. 31–41.CrossRefGoogle Scholar
Napier, J.R., and Napier, P.H., 1967, A Handbook of Living Primates: London, Academic Press.Google Scholar
Ni, X., and Qiu, Z., 2002, The micromammalian fauna from the Leilao, Yuanmou hominoid locality: implications for biochronology and paleoecology: Journal of Human Evolution, v. 42, p. 535–546.Google Scholar
Ni, X., and Qiu, Z., 2012, Tupaiine tree shrews (Scandentia, Mammalia) from the Yuanmou Lufengpithecus locality of Yunnan, China: Swiss Journal of Palaeontology, v. 131, p. 51–60.CrossRefGoogle Scholar
Ni, X., Gebo, D.L., Dagosto, M., Meng, J., Tafforeau, P., Flynn, J.J., and Beard, K.C., 2013, The oldest known primate skeleton and early haplorhine evolution: Nature, v. 498, p. 60–64.CrossRefGoogle ScholarPubMed
O'Leary, M.A., et al. , 2013, The placental mammal ancestor and the post-K-Pg radiation of placentals: Science, v. 339, p. 662–667.CrossRefGoogle ScholarPubMed
Olson, L.E., Sargis, E.J., and Martin, R.D., 2004, Phylogenetic relationships among treeshrews (Scandentia): a review and critique of the morphological evidence: Journal of Mammalian Evolution, v. 11, p. 49–71.CrossRefGoogle Scholar
Pampush, J.D., Winchester, J.M., Morse, P.E., Vining, A.Q., Boyer, D.M., and Kay, R.F., 2016a, Introducing molaR: a new R package for quantitative topographic analysis of teeth (and other topographic surfaces): Journal of Mammalian Evolution, v. 23, p. 397–412.CrossRefGoogle Scholar
Pampush, J.D., Spradley, J.P., Morse, P.E., Harrington, A.R., Allen, K.L., Boyer, D.M., and Kay, R.F., 2016b, Wear and its effects on dental topography measures in howling monkeys (Alouatta palliata): American Journal of Physical Anthropology, v. 161, p. 705–721.CrossRefGoogle Scholar
Prufrock, K.A., Boyer, D.M., and Silcox, M.T., 2016a, The first major primate extinction: an evaluation of paleoecological dynamics of North American stem primates using a homology free measure of tooth shape: American Journal of Physical Anthropology, v. 159, p. 683–697.CrossRefGoogle Scholar
Prufrock, K.A., López-Torres, S., Silcox, M.T., and Boyer, D.M., 2016b, Surfaces and spaces: troubleshooting the study of dietary niche space overlap between North American stem primates and rodents: Surface Topography: Metrology and Properties, v. 4, n. 024005.Google Scholar
Qiu, Z.D., 1986, Fossil tupaiid from the hominoid locality of Lufeng, Yunnan: Vertebrata PalAsiatica, v. 24, p. 308.Google Scholar
Raffles, T.S., 1821, Descriptive catalogue of a zoological collection, made on account of the honourable East India 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 of those countries: Transactions of the Linnean Society of London, v. 13, p. 239–274.CrossRefGoogle Scholar
Roberts, T.E., Sargis, E.J., and Olson, L.E., 2009, Networks, trees, and treeshrews: assessing support and identifying conflict with multiple loci and a problematic root: Systematic Biology, v. 58, p. 257–270.CrossRefGoogle Scholar
Roberts, T.E., Lanier, H.C., Sargis, E.J., and Olson, L.E., 2011, Molecular phylogeny of treeshrews (Mammalia: Scandentia) and the timescale of diversification in Southeast Asia: Molecular Phylogenetics and Evolution, v. 60, p. 358–372.CrossRefGoogle ScholarPubMed
Saban, R., 1963, Contribution à l'étude de 1’os temporal des Primates: Description chez l'homme et les Prosimiens; Anatomie comparée et phylogénie: Mémoires du Muséum National d'Histoire Naturelle, v. 29, p. l–377.Google Scholar
Sargis, E.J., 2001, A preliminary qualitative analysis of the axial skeleton of tupaiids (Mammalia, Scandentia): functional morphology and phylogenetic implications: Journal of Zoology, v. 253, p. 473–483.CrossRefGoogle Scholar
Sargis, E.J., 2002, The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae): an analysis of primatomorphan and volitantian characters: Journal of Mammalian Evolution, v. 9, p. 137–160.CrossRefGoogle Scholar
Sargis, E.J., 2004, New views on tree shrews: the role of tupaiids in primate supraordinal relationships: Evolutionary Anthropology, v. 13, p. 56–66.CrossRefGoogle Scholar
Sargis, E.J., 2007, The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae) and its implications for primate supraordinal relationships, in Ravosa, M. J., and Dagosto, M., eds., Primate Origins: Adaptations and Evolution: New York, Springer, p. 51–82.CrossRefGoogle Scholar
Sargis, E.J., Woodman, N., Reese, A.T., and Olson, L.E., 2013a, Using hand proportions to test taxonomic boundaries within the Tupaia glis species complex (Scandentia, Tupaiidae): Journal of Mammalogy, v. 94, p. 183–201.CrossRefGoogle Scholar
Sargis, E.J., Woodman, N., Morningstar, N.C., Reese, A.T., and Olson, L.E., 2013b, Morphological distinctiveness of Javan Tupaia hypochrysa (Scandentia, Tupaiidae): Journal of Mammalogy, v. 94, p. 938–947.CrossRefGoogle Scholar
Sargis, E.J., Campbell, K.K., and Olson, L.E., 2014a, Taxonomic boundaries and craniometric variation in the treeshrews (Scandentia, Tupaiidae) from the Palawan Faunal Region: Journal of Mammalian Evolution, v. 21, p. 111–123.CrossRefGoogle Scholar
Sargis, E.J., Woodman, N., Morningstar, N.C., Reese, A.T., and Olson, L.E., 2014b, Island history affects faunal composition: the treeshrews (Mammalia: Scandentia: Tupaiidae) from the Mentawai and Batu Islands, Indonesia: Biological Journal of the Linnean Society, v. 111, p. 290–304.CrossRefGoogle Scholar
Sargis, E.J., Woodman, N., Morningstar, N.C., Bell, T.N., and Olson, L.E., 2017, Skeletal variation and taxonomic boundaries among mainland and island populations of the common treeshrew (Mammalia: Scandentia: Tupaiidae): Biological Journal of the Linnean Society, v. 120, p. 286–312.Google Scholar
Schlegel, H., 1857, Handleiding to De Beoefening Der Dierkunde: Koninklijke Akademie, Zee-En Landmagt, Leiden, v. 1, p. 58–59.Google Scholar
Schlegel, H., and Müller, S., 1843, Over de op de oostindische eilanden levende soorten van het geslacht: Hylogalea Verh Nat Gesch Nederl Overz Bezitt, v. 1843, p. 159–168.Google Scholar
Selig, K.R., Sargis, E.J., and Silcox, M.T., 2019a, Three-dimensional geometric morphometric analysis of treeshrew (Scandentia) lower molars: insight into dental variation and systematics: The Anatomical Record, v. 302, p. 1154–1168.Google Scholar
Selig, K.R., Sargis, E.J., and Silcox, M.T., 2019b, The frugivorous insectivores? Functional morphological analysis of molar topography for inferring diet in extant treeshrews (Scandentia): Journal of Mammalogy, v. 100, p. 1901–1917.Google Scholar
Selig, K.R., López-Torres, S., Sargis, E.J., and Silcox, M.T., 2019c, First 3D dental topographic analysis of the enamel–dentine junction in non-primate euarchontans: contribution of the enamel-dentine junction to molar morphology: Journal of Mammalian Evolution, v. 26, p. 587–598.CrossRefGoogle Scholar
Silcox, M.T., Bloch, J.I., Boyer, D.M., Chester, S.G.B., López-Torres, S., 2017, The evolutionary radiation of plesiadapiforms: Evolutionary Anthropology, v. 26, p. 74–94.CrossRefGoogle ScholarPubMed
Spradley, J.P., Pampush, J.D., Morse, P.E., and Kay, R.F., 2017, Smooth operator: the effects of different 3D mesh retriangulation protocols on the computation of Dirichlet normal energy: American Journal of Physical Anthropology, v. 163, p. 94–109.CrossRefGoogle ScholarPubMed
Steele, D.G., 1973, Dental variability in the tree shrews (Tupaiidae), in Zingeser, M.R. ed., Craniofacial Biology of Primates: Symposium of the IVth International Congress of Primatology: Basel, Karger, p. 154–179.Google Scholar
Thomas, O., 1892, On some new Mammalia from the East Indian Archipelago: Annals and Magazine of Natural History, v. 9, p. 240–254.CrossRefGoogle Scholar
Thomas, O., 1893, Description of a new Bornean Tupaia: Annals and Magazine of Natural History, v. 12, p. 53–54.CrossRefGoogle Scholar
Thomas, O., 1894, On the Palawan representative of Tupaia ferruginea: Annals and Magazine of Natural History, v. 13, p. 367.CrossRefGoogle Scholar
Timmins, R.J., Duckworth, J.W., Robson, C.R., and Walston, J.L., 2003, Distribution, status and ecology of the mainland slender-tailed treeshrew Dendrogale murina: Mammal Review, v. 33, p. 272–283.CrossRefGoogle Scholar
Tong, Y., 1988, Fossil tree shrews from the Eocene Hetaoyuan Formation of Xichuan, Henan: Vertebrata PalAsiatica, v. 26, p. 214–220.Google Scholar
Ungar, P.S., and M'Kirera, F., 2003, A solution to the worn tooth conundrum in primate functional anatomy: Proceedings of the National Academy of Sciences, v. 100, p. 3874–3877.CrossRefGoogle ScholarPubMed
Ungar, P.S., Healy, C., Karme, A., Teaford, M., and Fortelius, M., 2016, Dental topography and diets of platyrrhine primates: Historical Biology, v. 30, p. 64–75.CrossRefGoogle Scholar
Van Valen, L., 1965, Treeshrews, primates, and fossils: Evolution, v. 19, p. 137–151.CrossRefGoogle Scholar
Visualization Sciences Group, 2009, Avizo: Burlington, Mercury Computer systems.Google Scholar
Wagner, J.A., 1841, Schreber's Säugthiere, Supplementband, 2: Abtheilung, v. 21841, p. 37–44, 553.Google Scholar
Wiens, F., Zitzmann, A., Lachance, M.-A., Yegles, M., Pragst, F., Wurst, F.M., von Holst, D., Guan, S.L., and Spanagel, R., 2008, Chronic intake of fermented floral nectar by wild treeshrews: Proceedings of the National Academy of Sciences, v. 105, p. 10426–10431.CrossRefGoogle ScholarPubMed
Winchester, J.M., 2016a, Molar topographic shape as a system for inferring functional morphology and developmental patterning in extant cercopithecoid primates [Ph.D. dissertation]: New York, Stony Brook University, 606 p.Google Scholar
Winchester, J.M., 2016b, MorphoTester: an open source application for morphological topographic analysis: PLOS ONE v. 11, n. e0147649.Google Scholar