Skip to main content

The Evolution and Paleobiogeography of Flying Squirrels (Sciuridae, Pteromyini) in Response to Global Environmental Change

Abstract

Flying squirrels are strictly arboreal squirrels adopting a special gliding form of locomotion. This group of animals has a long history that has mirrored the vicissitude of forests. The discrepancy in the distribution between fossils and extant species indicates a mysterious evolution history requiring further exploration. This study compiles the worldwide fossils of Pteromyini to the species level in order to reproduce the spatiotemporal distribution pattern of flying squirrels and deduce the ancestral distribution according to dispersal-vicariance analysis of a phylogeny of the extant species. In addition, we reconstruct the paleoenvironmental background and find that flying squirrels probably originated in the Oligocene–Miocene transition from Europe and immediately dispersed to Asia and North America. Influenced by glaciation, CO2 reduction, geologic movements and the Paratethys retreat, the Northern Hemisphere underwent climate deterioration and grassland expansion during the late Miocene, and thus the diversity of Pteromyini dramatically decreased. The uplift of the Tibet Plateau in addition to the strengthened Asian monsoons intensified the aridity in central Asia, but brought sufficient water to the densely forested regions of South and Southeast Asia. These forests are likely both refugia and diversification center for flying squirrels during glacial periods in the Quarternary. The subsequent connection and separation events among these heterogeneous habitats has probably been a driving force in the speciation of flying squirrels. Based on this work, we predict a bleak future for the flying squirrels, one which is closely associated with the fate of forests in Asia.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Achard, F., Eva, H. D., Stibig, H. J., Mayaux, P., Gallego, J., Richards, T., et al. (2002). Determination of deforestation rates of the world’s humid tropical forests. Science, 297(5583), 999–1002.

    PubMed  CAS  Article  Google Scholar 

  2. Aldana Carrasco, E. J. (1992). Los esciuropteros del Mioceno de la cuenca del Valles-Penedes (Cataluna, Espana). Geogaceta, 11, 114–116.

    Google Scholar 

  3. Ali, S. S., Yu, Y., Pfosser, M., & Wetschnig, W. (2012). Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies). Annals of Botany, 109(1), 95–107.

    PubMed  Article  Google Scholar 

  4. An, Z. S., Kutzbach, J. E., Prell, W. L., & Porter, S. C. (2001). Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature, 411(6833), 62–66.

    CAS  Article  Google Scholar 

  5. Arbogast, B. S. (2007). A brief history of the New World flying squirrels: phylogeny, biogeography, and conservation genetics. Journal of Mammalogy, 88(4), 840–849.

    Article  Google Scholar 

  6. Axelrod, D. I. (1985). Rise of the Grassland Biome, Central North-America. Botanical Review, 51(2), 163–201.

    Article  Google Scholar 

  7. Baranova, G. I. (1976). On the records of Phoopetaurista moldaviensis Baranova et Konkova, 1974 (Rodentia, Pteromyidae) in the Middle Pliocene deposits of the USSR. Trudy Zoologicheskogo Instituta, Akademiya Nauk SSSR, 66, 98–100.

    Google Scholar 

  8. Baranova, G. I. & Konkova, N. I. (1974). A new species of flying squirrel from the genus Pliopetaurista Kretzoi 1962 (Rodentia Pteromyidae) in Middle Pliocene fauna of Moldavia. In B. A. Trofimov (Eds.), Mammals of the late Caenozoic of the south-west USSR (pp. 91–98). Shtiintza, Kishinev.

  9. Barnosky, A. D. (1986). Arikareean, Hemingfordian, and Barstovian mammals from the Miocene Colter Formation, Jackson Hole, Teton County, Wyoming. Bulletin of Carnegie Museum of Natural History, 26, 1–69.

  10. Bigelow, N. H., Brubaker, L. B., Edwards, M. E., Harrison, S. P., Prentice, I. C., Anderson, P. M., et al. (2003). Climate change and Arctic ecosystems: 1. Vegetation changes north of 55°N between the last glacial maximum, mid-Holocene, and present. Journal of Geophysical Research-Atmospheres, 108(D19), 8170. doi:10.1029/2002JD002558.

  11. Black, C. C. (1966). Tertiary Sciuridae (Mammalia: Rodentia) from Bavaria. Mitteilungen der Bayerischen Staatssammlung fuer Palaeontologie und Historische Geologie, 6, 51–63.

    Google Scholar 

  12. Black, C. C., & Kowalski, K. (1974). The Pliocene and Pleistocene Sciuridae (Mammalia, Rodentia) from Poland. Acta Zoologica Cracoviensia, 19(19), 461–485.

    Google Scholar 

  13. Bouwens, P., & de Bruijn, H. (1986). The flying squirrels Hylopetes and Petinomys and their fossil record. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen Series B Physical Sciences, 89(2), 113–123.

    Google Scholar 

  14. Bruch, A. A., Uhl, D., & Mosbrugger, V. (2007). Miocene climate in Europe—Patterns and evolution—A first synthesis of NECLIME. Palaeogeography, Palaeoclimatology, Palaeoecology, 253(1–2), 1–7.

    Article  Google Scholar 

  15. Bulot, C. (1980). Decouverte de nouveaux rongeurs dans le gisement d’Estrepouy (Gers). Bulletin du Museum National d’Histoire Naturelle Section C Sciences de la Terre Paleontologie Geologie Mineralogie, 2(4), 397–406.

    Google Scholar 

  16. Bulot, C. (1981). Le Chene de Navere: nouveau gisement de mammiferes du Miocene gersois. Bulletin de la Societe d’Histoire Naturelle de Toulouse, 117(1–4), 133–145.

    Google Scholar 

  17. Casanovas-Vilar, I., Angelone, C., Alba, D. M., Moya-Sola, S., Koehler, M., & Galindo, J. (2010). Rodents and lagomorphs from the Middle Miocene hominoid-bearing site of Barranc de Can Vila 1 (els Hostalets de Pierola, Catalonia, Spain). Neues Jahrbuch für Geologie und Paläontologie Abhandlungen, 257(3), 297–315.

    Article  Google Scholar 

  18. Chaimanee, Y., & Jaeger, J. J. (2000). A new flying squirrel Belomys thamkaewi n. sp. (Mammalia: Rodentia) from the Pleistocene of West Thailand and its biogeography. Mammalia, 64(3), 307–318.

    Article  Google Scholar 

  19. Cuenca, B. G. & Canudo, J. I. (1992). Los Sciuridae (Rodentia, Mammalia) del Oligoceno inferior de Montalban y Olalla (Teruel, Espana). Discusion sobre el origen de los esciuridos. Boletin de la Real Sociedad Espanola de Historia Natural Seccion Geologica, 87 (1–4), 155–169.

  20. Curran, L. M., Trigg, S. N., McDonald, A. K., Astiani, D., Hardiono, Y. M., Siregar, P., et al. (2004). Lowland forest loss in protected areas of Indonesian Borneo. Science, 303(5660), 1000–1003.

    PubMed  CAS  Article  Google Scholar 

  21. Daams, R. (1977). Aragonian Sciuroptera (Sciuridae, Rodentia, Mammalia) from Spain. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen - Series B: Palaeontology, Geology, Physics and Chemistry, 80(5), 356–359.

    Google Scholar 

  22. Dahlmann, T. (2001). The micromammals from the Lower Pliocene locality of Woelfersheim/Wetterau (Mammalia: Lipotyphla, Chiroptera, Rodentia). Die Kleinsaeuger der unter-pliozaenen Fundstelle Woelfersheim in der Wetterau (Mammalia: Lipotyphla, Chiroptera, Rodentia). Courier Forschungsinstitut Senckenberg, 227, 1–129.

    Google Scholar 

  23. Danner-Hock, G. (1970). Die Wirbeltierfauna aus dem Alt-Pliozan (O-Pannon) vom Eichkogel bei Modling (NO.). 3. Rodentia. Annalen des Naturhistorischen Museums in Wien A Mineralogie Petrologie Geologie Palaeontologie Archaeozoologie Anthropologie Praehistorie, 74, 597–605.

    Google Scholar 

  24. Daxner-Hock, G. (1975). Taxonomische probleme um das Genus Miopetaurista Kretzoi, 1962 (Fam. Sciuridae). Palaeontologische Z, 49 (1-2), 75-77.

    Google Scholar 

  25. Daxner-Hoeck, G. (2004). Flying squirrels (Pteromyinae, Mammalia) from the Upper Miocene of Austria. Annalen des Naturhistorischen Museums in Wien A Mineralogie Petrologie Geologie Palaeontologie Archaeozoologie Anthropologie Praehistorie, 106A, 387–423.

    Google Scholar 

  26. Daxner-Hoeck, G. (2010). Sciuridae, Gliridae and Eomyidae (Rodentia, Mammalia) from the Middle Miocene of St. Stefan in the Gratkorn Basin (Styria, Austria). Annalen des Naturhistorischen Museums in Wien A Mineralogie Petrologie Geologie Palaeontologie Archaeozoologie Anthropologie Praehistorie, 112, 507–535.

    Google Scholar 

  27. de Bruijn, H. (1998). Vertebrates from the Early Miocene lignite deposits of the opencast mine Oberdorf (Western Styrian Basin, Austria): 6. Rodentia 1. (Mammalia). Annalen des Naturhistorischen Museums in Wien A Mineralogie Petrologie Geologie Palaeontologie Archaeozoologie Anthropologie Praehistorie, 99A, 99–137.

    Google Scholar 

  28. de Bruijn, H. (1999). Superfamily Sciuroidea. In G. E. Rossner & K. Heissig (Eds.), The Miocene land mammals of Europe (pp. 271–280). Munchen: Verlag Dr. Friedrich Pfeil.

    Google Scholar 

  29. de Bruijn, H., & Unay, E. (1989). Petauristinae (Mammalia, Rodentia) from the Oligocene of Spain, Belgium, and Turkish Thrace. Natural History Museum of Los Angeles County Science Series, 33(supplement), 139–145.

    Google Scholar 

  30. de Bruijn, H., van der Meulen, A. J. & Katsikatsos, G. (1980). The mammals from the Lower Miocene of Aliveri (Island of Evia, Greece). Part 1. The Sciuridae. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen Series B Physical Sciences, 83(3), 241–261.

  31. Dehm, R. (1950). Die Nagetiere aus dem Mittel-Miocan (Burdigal um) von Wintershof - West bie Eichstatt in Bayern. Abhandlungen Neues Jahrbuch für Geologie und Paläontologie, 91(B), 321–428.

  32. Dehm, R. (1962). Altpleistocane Sauger von Schernfeld bei Eichst&tt in Bayern. Mitteilungen der Bayerischen Staatssammlung fuer Palaeontologie und Historische Geologie, 2, 17–61.

    Google Scholar 

  33. Edwards, E. J., Osborne, C. P., Stromberg, C. A., Smith, S. A., Bond, W. J., Christin, P. A., et al. (2010). The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science, 328(5978), 587–591.

    PubMed  CAS  Article  Google Scholar 

  34. Emry, R. J., & Korth, W. W. (2007). A new genus of squirrel (Rodentia, Sciuridae) from the mid-Cenozoic of North America. Journal of Vertebrate Paleontology, 27(3), 693–698.

    Article  Google Scholar 

  35. Engesser, B. (1979). Relationships of some insectivores and rodents from the Miocene of North America and Europe. Bulletin of Carnegie Museum of Natural History, 14(supplement), 1–68.

    Google Scholar 

  36. Fedorov, V. B., Fredga, K., & Jarrell, G. H. (1999). Mitochondrial DNA variation and the evolutionary history of chromosome races of collared lemmings (Dicrostonyx) in the Eurasian Arctic. Journal of Evolutionary Biology, 12(1), 134–145.

    Article  Google Scholar 

  37. Flower, B. P., & Kennett, J. P. (1994). The middle Miocene climatic transition—East Antarctic ice-sheet development, deep-ocean circulation and global carbon cycling. Palaeogeography, Palaeoclimatology, Palaeoecology, 108(3–4), 537–555.

    Article  Google Scholar 

  38. Garcia-Alix, A., Minwer-Barakat, R., Martin-Suarez, E., & Freudenthal, M. (2007). New data on Mio-Pliocene Sciuridae (Rodentia, Mammalia) from southern Spain. Comptes Rendus Palevol, 6(4), 269–279.

    Article  Google Scholar 

  39. Guo, Z. T., Peng, S. Z., Hao, Q. Z., Biscaye, P. E., An, Z. S., & Liu, T. S. (2004). Late Miocene-Pliocene development of Asian aridification as recorded in the Red-Earth Formation in northern China. Global and Planetary Change, 41(3–4), 135–145.

    Article  Google Scholar 

  40. Haffer, J. (1969). Speciation in Amazonian forest birds. Science, 165(3889), 131–137.

    PubMed  CAS  Article  Google Scholar 

  41. Haq, B. U., & Al-Qahtani, A. M. (2005). Phanerozoic cycles of sea-level change on the Arabian Platform. Geoarabia, 10(2), 127–160.

    Google Scholar 

  42. Haq, B. U., Hardenbol, J., & Vail, P. R. (1987). Chronology of fluctuating sea levels since the Triassic. Science, 235(4793), 1156–1167.

    PubMed  CAS  Article  Google Scholar 

  43. Haynes, S., Jaarola, M., & Searle, J. B. (2003). Phylogeography of the common vole (Microtus arvalis) with particular emphasis on the colonization of the Orkney archipelago. Molecular Ecology, 12(4), 951–956.

    PubMed  CAS  Article  Google Scholar 

  44. Heissig, K. (1979). Die fruhesten Flughornchen und primitive Ailuravinae (Rodentia, Mamm.) aus dem suddeutschen Oligozan. Mitteilungen der Bayerischen Staatssammlung fuer Palaeontologie und Historische Geologie, 19, 139–169.

    Google Scholar 

  45. Hir, J., & Venczel, M. (2005). New Middle Miocene vertebrate localities from Subpiatra (Bihor district, Romania). Acta Palaeontologica Romaniae, 5, 211–221.

    Google Scholar 

  46. Ho, C. K., Qi, G. Q., & Chang, C. H. (1997). A preliminary study of Late Pleistocene carnivore fossils from the Penghu Channel, Taiwan. Annual of Taiwan Museum, 40, 195–224.

    Google Scholar 

  47. Huang, W., Si, X., Hou, Y., Miller-Antonio, S., & Schepartz, L. A. (1995). Excavations at Panxian Dadong, Guizhou Province. Southern China. Current Anthropology, 36(5), 844–846.

    Article  Google Scholar 

  48. Huchon, D., Chevret, P., Jordan, U., Kilpatrick, C. W., Ranwez, V., Jenkins, P. D., et al. (2007). Multiple molecular evidences for a living mammalian fossil. Proceedings of the National academy of Sciences of the United States of America, 104(18), 7495–7499.

    PubMed  CAS  Article  Google Scholar 

  49. Huelsenbeck, J. P., Ronquist, F., Nielsen, R., & Bollback, J. P. (2001). Evolution—Bayesian inference of phylogeny and its impact on evolutionary biology. Science, 294(5550), 2310–2314.

    PubMed  CAS  Article  Google Scholar 

  50. IUCN. (2011). IUCN red list of threatened species. Version 2011.1. http://www.iucnredlist.org. Downloaded on 10 October 2011.

  51. Jaarola, M., & Searle, J. B. (2002). Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology, 11(12), 2613–2621.

    PubMed  CAS  Article  Google Scholar 

  52. Jin, C., Dong, W., Liu, J. Y., Wei, G. B., Xu, Q. Q., Zheng, J. J., et al. (2000). A preliminary study of the early Pleistocene deposits and the mammalian fauna from the Renzi Cave, Fancheng, Anhui, China. Acta Anthropologica Sinica, 19(supplement), 235–245.

    Google Scholar 

  53. Jin, C. Z., Kawamura, Y., & Taruno, H. (1999). Pliocene and Early Pleistocene insectivore and rodent faunas from Dajushan, Qipanshan and Haimao in north China and the reconstruction of the faunal succession from the Late Miocene to Middle Pleistocene. Journal of Geosciences. Osaka City University, 42, 1–19.

    Google Scholar 

  54. Kadlecova, E. (2003). A preliminary report of Paracitellus eminens Dehm, 1950 (Aplodontidae, Ailuravinae, Rodentia, Mammalia) from the Early Miocene of NW Bohemia. Acta Universitatis Carolinae Geologica, 47(1–4), 63–66.

    Google Scholar 

  55. Keeley, J. E., & Rundel, P. W. (2005). Fire and the Miocene expansion of C(4) grasslands. Ecology Letters, 8(7), 683–690.

    Article  Google Scholar 

  56. Kitazoe, K., Kishino, H., Waddell, P. J., Nakajima, N., Okabayashi, T., Watabe, T., et al. (2007). Robust time estimation reconciles views of the antiquity of placental mammals. PLoS One, 2(4), 1–11.

    Article  Google Scholar 

  57. Koenigswald, W. V. (1973). Husarenhof 4, eine alt-bis mittelpleistozane Kleinsaugerfauna aus Wurttemberg nit Petaurla. Neues Jb Geol Paleont Abh, 143(1), 23–38.

    Google Scholar 

  58. Koprowski, J. L., & Nandini, R. (2008). Global hotspots and knowledge gaps for tree and flying squirrels. Current Science (Bangalore), 95(7), 851–856.

    Google Scholar 

  59. Korth, W. W. (1994). The Tertiary record of rodents in North America. Topics in Geobiology, 12, 1–319.

    Google Scholar 

  60. Korth, W. W. (2009). Mammals from the blue ash local fauna (Late Oligocene), South Dakota. Rodentia, part 3: family Sciuridae. Paludicola, 7(2), 47–60.

    Google Scholar 

  61. Kretzoi, M. (1959). Insectivoren, Nagetiere und Lagomorphen der jungstpliozanen Fauna von Csarnota im Villanyer Gebirga (Sudungarn). Vertebrata Hungarica, 1, 237–246.

    Google Scholar 

  62. Kretzoi, M. (1962). Fauna und faunenhorizont von Csarnota. Jahresbericht der Ungarischen Geologischen Anstalt, 1959, 297–396.

    Google Scholar 

  63. Kretzoi, M. (1965). Die Nager und Lagomorphen von Voigtstedt in Thuringen und ihre chronologische Aussage. Paläontologische Abhandlungen. Abteilung A. Paläozoologie., 2, 585–661.

    Google Scholar 

  64. Laub, R. S. (2009). New data on holocene fossil mammal occurrences at the hiscock site and its environs, western New York state. Bulletin of the Buffalo Society of Natural Sciences, 38, 33–42.

    Google Scholar 

  65. Liu, W., Wu, X. Z., Pei, S. W., Wu, X. J., & Norton, C. J. (2010). Huanglong Cave: A late Pleistocene human fossil site in Hubei Province, China. Quaternary International, 211(1–2), 29–41.

    Article  Google Scholar 

  66. Mai, D. H., & Walther, H. (1991). Die oligozänen und untermiozänen Floren NW-Sachsens und des Bitterfelder Raumes. Abhandlungen des Staatlichen Museums für Mineralogie und Geologie zu Dresden, 38, 1–230.

    Google Scholar 

  67. Marincovich, L., & Gladenkov, A. Y. (1999). Evidence for an early opening of the Bering Strait. Nature, 397(6715), 149–151.

    CAS  Article  Google Scholar 

  68. Markovic, Z. (2008). Rodents of Middle Miocene localities of Lazarevac village and Bele Vode (Central Serbia). Bulletin of the Natural History Museum in Belgrade, 1, 79–98.

    Google Scholar 

  69. Martin, R. A. (1974). Fossil mammals from the Coleman 2A fauna, Sumter County. In S. D. Webb (Eds.), Pleistocene mammals of Florida (pp. 35–99). Gainesville: University Presses of Florida.

  70. McKenna, M. C. & Bell, S. K. (1997). Book classification of mammals: above the species level. New York & Chichester, West Sussex: Columbia University Press.

  71. Mein, P. (1970a). Les sciuropteres (Mammalia, Rodentia) Neogenes d’Europe Occidentale. Geobios, Lyon, 3(3), 7–77.

    Article  Google Scholar 

  72. Mein, P. (1970b). Les sciuropteres (Mammalia, Rodentia) Neogenes d’Europe Occidentale. Geobios, 3(3), 7–77.

    Article  Google Scholar 

  73. Mein, P. (1992). Taxonomy. In: B. Bassano, P. Durio, U. Gallo Orsi, & E. Macchi, (Eds.), First international symposium on Alpine Marmot (Marmota marmota) and on genus Marmota. Proceedings: Saint Vincent, AostaItaly, October 2830, 1991 (pp. 6–12). Torino.: Dipartimento di Produzioni Animali, Epidemiologia ed Ecologia.

  74. Mein, P., & Adrover, H. R. (1977). Yacimiento de El Arquillo 3, en Teruel, Espana. (Nota preliminar). Acta Geologica Hispanica, 12(1–3), 46–48.

    Google Scholar 

  75. Mein, P., & Ginsburg, L. (2002). Sur l’âge relatif des différents karstiques miocènes de La Grive-Saint-Alban (Isère). Cahiers scientifiques, Muséum d’Histoire naturelle, 2, 7–47.

    Google Scholar 

  76. Menouret, B., & Mein, P. (2008). The Upper Miocene vertebrates of Soblay (Ain, France). Documents des Laboratoires de Geologie Lyon, 165, 1–97.

    Google Scholar 

  77. Mercer, J. H. (1983). Cenozoic Glaciation in the Southern-Hemisphere. Annual Review of Earth and Planetary Sciences, 11, 99–132.

    CAS  Article  Google Scholar 

  78. Mercer, J. M., & Roth, V. L. (2003). The effects of Cenozoic global change on squirrel phylogeny. Science, 299(5612), 1568–1572.

    PubMed  CAS  Article  Google Scholar 

  79. Meredith, R. W., Hekkala, E. R., Amato, G., & Gatesy, J. (2011). A phylogenetic hypothesis for Crocodylus (Crocodylia) based on mitochondrial DNA: Evidence for a trans-Atlantic voyage from Africa to the New World. Molecular Phylogenetics and Evolution, 60(1), 183–191.

    PubMed  Article  Google Scholar 

  80. Nadachowski, A., Miroslaw-Grabowska, J., David, A., Tomek, T., Garapich, A., Pascaru, V., et al. (2006). Faunal assemblages and biostratigraphy of several Pliocene sites from Moldova. Courier Forschungsinstitut Senckenberg, 256, 249–259.

    Google Scholar 

  81. Nicoara, I. (2011). Upper turolian sciuroidea (rodentia, mammalia) from the republic of moldova. Acta Palaeontologica Romaniae, 7, 257–265.

    Google Scholar 

  82. Nowak, R. M. (1999). Book Walker’s mammals of the world. Baltimore & London: Johns Hopkins University Press.

    Google Scholar 

  83. Nylander, J. A. A., Olsson, U., Alstrom, P., & Sanmartin, I. (2008). Accounting for phylogenetic uncertainty in biogeography: A Bayesian approach to dispersal-vicariance analysis of the thrushes (Aves: Turdus). Systematic Biology, 57(2), 257–268.

    PubMed  Article  Google Scholar 

  84. Oshida, T., Abramov, A., Yanagawa, H., & Masuda, R. (2005). Phylogeography of the Russian flying squirrel (Pteromys volans): implication of refugia theory in arboreal small mammal of Eurasia. Molecular Ecology, 14(4), 1191–1196.

    PubMed  CAS  Article  Google Scholar 

  85. Oshida, T., Lin, L.-K., Yanagawa, H., Endo, H., & Masuda, R. (2000). Phylogenetic relationships among six flying squirrel genera, inferred from mitochondrial cytochrome b gene sequences. Zoological Science, 17(4), 485–489.

    CAS  Google Scholar 

  86. Otto-Bliesner, B. L., Brady, E. C., Clauzet, G., Tomas, R., Levis, S., & Kothavala, Z. (2006). Last glacial maximum and Holocene climate in CCSM3. Journal of Climate, 19(11), 2526–2544.

    Article  Google Scholar 

  87. Popov, V. V. (2004). Pliocene small mammals (Mammalia, Lipotyphla, Chiroptera, Lagomorpha, Rodentia) from Muselievo (North Bulgaria). Geodiversitas, 26(3), 403–491.

    Google Scholar 

  88. Pratt, A. E., & Morgan, G. S. (1989). New sciurid (Mammalia: Rodentia) from the Early Miocene Thomas Farm Local Fauna. Florida. Journal of Vertebrate Paleontology, 9(1), 89–100.

    Article  Google Scholar 

  89. Qiu, Z. D. (1991). The Neogene mammalian faunas of Ertemte and Harr Obo in Inner Mongolia (Nei Mongol), China—8. Sciuridae (Rodentia). Senckenbergiana Lethaea, 71(3–4), 223–255.

    Google Scholar 

  90. Qiu, Z. D. (2002). Sciurids from the Late Miocene Lufeng hominoid locality, Yunnan. Vertebrata Palasiatica, 40(3), 177–193.

    Google Scholar 

  91. Qiu, Z. D., & Liu, Y. P. (1986). The Aragonian vertebrate fauna of Xiacaowan, Jiangsu—5. Sciuridae (Rodentia, Mammalia). Vertebrata Palasiatica, 24(3), 195–209.

    Google Scholar 

  92. Ray, N. & Adams, J. M. (2001). A GIS-based vegetation map of the world at the last glacial maximum (25,000–15,000 BP). Internet Archaeology (http://intarch.ac.uk/journal/issue11/rayadams_toc.html), 11.

  93. Raymo, M. E., & Ruddiman, W. F. (1992). Tectonic forcing of late Cenozoic climate. Nature, 359(6391), 117–122.

    CAS  Article  Google Scholar 

  94. Ronquist, F. (1997). Dispersal-vicariance analysis: A new approach to the quantification of historical biogeography. Systematic Biology, 46(1), 195–203.

    Article  Google Scholar 

  95. Ruez, D. R., Jr. (2001). Early Irvingtonian (latest Pliocene) rodents from Inglis 1C, Citrus County, Florida. Journal of Vertebrate Paleontology, 21(1), 153–171.

    Article  Google Scholar 

  96. Shevyreva, N. S., & Baranova, G. I. (2003). Sciuromorpha (Rodentia) from the Miocene of Zaissan Depression, eastern Kazakhstan. Russian Journal of Theriology, 2(1), 9–13.

    Google Scholar 

  97. Shushpanov, K. I., & Lungu, A. N. (1993). New dates about Sciuridaeu [Sciuridae] Pteromyidae (Rodentia) of Late Neogene of Moldova. Buletinul Academiei de Stiinte a Republicii Moldova Stiinte Biologice si Chimice, 3(33–37), 74.

    Google Scholar 

  98. Sinitsa, M. V. (2011). Pliopetaurista (Mammalia, Rodentia) from the Neogene of Ukraine. Vestnik Zoologii, 45(1), 19–33.

    Google Scholar 

  99. Skwara, T. (1986). A new ‘flying squirrel’ (Rodentia: Sciuridae) from the Early Miocene of southwestern Saskatchewan. Journal of Vertebrate Paleontology, 6(3), 290–294.

    Article  Google Scholar 

  100. Steppan, S. J., Storz, B. L., & Hoffmann, R. S. (2004). Nuclear DNA phylogeny of the squirrels (Mammalia: Rodentia) and the evolution of arboreality from c-myc and RAG1. Molecular Phylogenetics and Evolution, 30(3), 703–719.

    PubMed  CAS  Article  Google Scholar 

  101. Storch, G., Engesser, B., & Wuttke, M. (1996). Oldest fossil record of gliding in rodents. Nature, 379(6564), 439–441.

    CAS  Article  Google Scholar 

  102. Sun, J. M., Zhang, Z. Q., & Zhang, L. Y. (2009). New evidence on the age of the Taklimakan Desert. Geol, 37(2), 159–162.

    Article  Google Scholar 

  103. Terzea, E. (1980). Deux micromammiferes du pliocene de Roumanie. Travaux de l’Institut de Speologie “Emile Racovitza”, 19, 191–201.

  104. Thorington, R. W. (1984). Flying squirrels are monophyletic. Science, 225(4666), 1048–1050.

    PubMed  Article  Google Scholar 

  105. Thorington, R. W., Darrow, K., & Anderson, C. G. (1998). Wing tip anatomy and aerodynamics in flying squirrels. Journal of Mammalogy, 79(1), 245–250.

    Article  Google Scholar 

  106. Thorington, R. W., & Heaney, L. R. (1981). Body proportions and gliding adaptations of flying squirrels (Petauristinae). Journal of Mammalogy, 62(1), 101–114.

    Article  Google Scholar 

  107. Thorington, R. W., & Hoffmann, R. S. (2005). Family Sciuridae. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world: A taxonomic and geographic reference (3rd ed., pp. 754–818). Baltimore: Johns Hopkins University Press.

    Google Scholar 

  108. Thorington, R. W., Schennum, C. E., Pappas, L. A., & Pitassy, D. (2005). The difficulties of identifying flying squirrels (Sciuridae: Pteromyini) in the fossil record. Journal of Vertebrate Paleontology, 25(4), 950–961.

    Article  Google Scholar 

  109. Tong, H. W. (2007). Aeretes melanopterus (Pteromyinae, Rodentia) from Tianyuan Cave near Zhoukoudian (Choukoutien) in China. Geobios (Villeurbanne), 40(2), 219–230.

    Article  Google Scholar 

  110. Tong, H. W., Zhang, S. Q., Li, Q., & Xu, Z. J. (2008). Late Pleistocene mammalian fossils from the Xitaiping Cave, Shidu, Beijing. Vertebrata Palasiatica, 46(1), 51–70.

    Google Scholar 

  111. Turner, A. (2001). Hominoid evolution and climatic change in Europe volume 1. The evolution of neogene terrestrial ecosystems in Europe. Journal of Human Evolution, 40(2), 159–160.

    Article  Google Scholar 

  112. Venczel, M., Hir, J., Huza, R. R., Popa, E., & Golban, D. (2005). A new Middle Miocene vertebrate fauna from Subpiatra (Bihor County, Romania). Nymphaea, 32, 23–38.

    Google Scholar 

  113. Werner, J. (1994). Beitrage zur Biostratigraphie der Unteren Susswasser-Molasse Suddeutschlands - Rodentia und Lagomorpha (Mammalia) aus den Fundstellen der Ulmer Gegend. Stuttgarter Beitraege zur Naturkunde Serie B (Geologie und Palaeontologie), 200, 1–263.

    Google Scholar 

  114. Wing, S. L. (1998). Tertiary vegetation of North America as a context for mammalian evolution. In: C. M. Janis & K. M. Scott & L. L. Jacobs (Eds.), Evolution of tertiary mammals of north America. Volume 1: terrestrial carnivores, ungulates, and ungulatelike mammals (pp. 37–65). Cambridge, New York & Melbourne: Cambridge University Press.

  115. Young, C. C. (1934). On the Insectivora, Cheiroptera, Bodentia and Primates, other than Sinanthropus, from locality at Choukoutien. Palaeontologia Sinica, C8, 1–160.

    Google Scholar 

  116. Young, C. C. (1947). Notes on a Pleistocene microfauna from Loping, Kiangsi. Bulletin of the Geological Society of China, 27, 163–170.

    Google Scholar 

  117. Yu, Y., Harris, A. J., & He, X. (2010). S-DIVA (statistical dispersal-vicariance analysis): A tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution, 56(2), 848–850.

    PubMed  Article  Google Scholar 

  118. Yu, Y., Harris, A. J. & He, X. J. (2011). RASP (reconstruct ancestral state in phylogenies) 2.0 beta. Available at http://mnh.scu.edu.cn/soft/blog/RASP.

  119. Yu, F., Pang, J., Kilpatrick, C. W., McGuire, P. M., Wang, Y., Lu, S., et al. (2006). Phylogeny and biogeography of the Petaurista philippensis complex (Rodentia: Sciuridae), inter- and intraspecific relationships inferred from molecular and morphometric analysis. Molecular Phylogenetics and Evolution, 38(3), 755–766.

    PubMed  CAS  Article  Google Scholar 

  120. Zachos, J., Pagani, M., Sloan, L., Thomas, E., & Billups, K. (2001). Trends, rhythms, and aberrations in global climate 65 Ma to present. Science, 292(5517), 686–693.

    PubMed  CAS  Article  Google Scholar 

  121. Zhang, Z. Q. (2006). Chinese Late Neogene land mammal community and the environmental changes of East Asia. Vertebrata Palasiatica, 44(2), 133–142.

    Google Scholar 

  122. Zhang, Z. S., Wang, H. J., Guo, Z. T., & Jiang, D. B. (2007). Impacts of tectonic changes on the reorganization of the Cenozoic paleoclimatic patterns in China. Earth and Planetary Science Letters, 257(3–4), 622–634.

    CAS  Google Scholar 

  123. Zheng, S. H. (1993). Quaternary rodents of Sichuan-Guizhou area, China. Beijing: Science Press.

    Google Scholar 

Download references

Acknowledgments

We deeply appreciate the contributors to the Paleobiology database and Genbank for making information publicly available. We appreciate Dr. Douglas Chesters for his help in language. We thank editors and anonymous reviewers for their constructive suggestions in improvement of this manuscript. Our research is supported by grants from the Natural Science Foundation of China (No: 31101629, 31172065, J0930004 and 30970332) and a grant (Y229YX5105) from the Key Laboratory of Zoological Systematics and Evolution of the Chinese Academy of Sciences.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Qisen Yang.

Appendix

Appendix

See Table 2.

Table 2 Fossil records of flying squirrels

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lu, X., Ge, D., Xia, L. et al. The Evolution and Paleobiogeography of Flying Squirrels (Sciuridae, Pteromyini) in Response to Global Environmental Change. Evol Biol 40, 117–132 (2013). https://doi.org/10.1007/s11692-012-9191-6

Download citation

Keywords

  • Sciuridae
  • Pteromyini
  • Evolution
  • Paleobiogeography
  • Dispersal-vicariance analysis