The burden of motherhood: Gliding locomotion in mammals influences maternal reproductive investment

Journal of Mammalogy

Volumn 89, Issue 3, 2008, Pages 617-625

  Fokidis, H Bobby ^a   Risch, Thomas S ^b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARKANSAS STATE UNIVERSITY   (United States)

Author keywords

Flying squirrel; Glider; K selection; Life history; Marsupial; Phylogeny; Reproduction; Supertree

Indexed keywords

BODY MASS; COMPARATIVE STUDY; GLIDING; LIFE HISTORY TRAIT; MARSUPIAL; METABOLISM; MORPHOLOGY; MORTALITY; NATURAL SELECTION; PARENTAL INVESTMENT; PHYLOGENY; PREGNANCY; REPRODUCTIVE PRODUCTIVITY; WING;

ANIMALIA; MAMMALIA; METATHERIA; PTEROMYINI; SCIURIDAE;

EID: 45249124714     PISSN: 00222372     EISSN: None     Source Type: Journal    
DOI: 10.1644/07-MAMM-A-116R1.1     Document Type: Article

References (90)

1. ADKINS, R. M., A. H. WALTON, AND R. L. HONEYCUTT. 2003. Higher-level systematics of rodents and divergence time estimates based on two congruent nuclear genes. Molecular Phylogenetics and Evolution 26:409-420.
2. ALLEN, G. M. 1940. The mammals of China and Mongolia, part II. Natural history of central Asia. Vol. XI. Central Asiatic Expeditions, American Museum of Natural History, New York.
3. ARNASON, U., ET AL. 2002. Mammalian mitogenomic relationships and the root of the eutherian tree. Proceedings of the National Academy of Sciences 99:8151-8156.
4. AUSTAD, S. N., AND K. E. FISCHER. 1991. Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. Journal of Gerontology 46:47-53.
5. BARCLAY, R. M. R., ET AL. 2004. Variation in the reproductive rate of bats. Canadian Journal of Zoology 82:688-693.
6. BININDA-EMONDS, O. R. P., J. L. GITTLEMAN, AND A. PURVIS. 1999. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biological Reviews 74:143-175.
7. BININDA-EMONDS, O. R. P., ET AL. 2003. Supertrees are a necessary not-so-evil: a comment on Gatesy et al. Systematic Biology 52: 724-729.
8. BLACKBURN, D. G., AND H. E. EVANS. 1986. Why are there no viviparous birds? American Naturalist 128:165-190.
9. CARDILLO, M., O. R. P. BININDA-EMONDS, E. BOAKES, AND A. PURVIS. 2004. A species-level phylogenetic supertree of marsupials. Journal of Zoology (London) 264:11-31.
10. CARRAWAY, L. N., AND B. J. VERTS. 1994. Sciurus griseus. Mammalian Species 474:1-7.
11. CORBET, G. B., AND J. E. HILL. 1992. The mammals of the Indomalayan region. Oxford University Press, Oxford, United Kingdom.
12. DAVENPORT, J. 2003. Allometric constraints on stability and maximum size in flying fish: implications for their evolution. Journal of Fish Biology 62:455-463.
13. DIAL, R., B. BLOODWORTH, A. LEE, P. BOYNE, AND J. HEYS. 2004. The distribution of free space and its relation to canopy composition at six forest sites. Forest Science 50:312-325.
14. DOLAN, P. G., AND D. C. CARTER. 1977. Glaucomys volans. Mammalian Species 78:1-6.
15. EMMONS, L. H., AND A. H. GENTRY. 1983. Tropical forest structure and the distribution of gliding and prehensile-tailed vertebrates. American Naturalist 121:513-524.
16. FELSENSTEIN, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
17. FLEMING, M. R., AND H. FREY. 1984. Aspects of the natural history of feathertail gliders (Acrobates pygmaeus) in Victoria. Pp. 403-408 in Possums and gliders (A. P. Smith and I. D. Hume, eds.). Surrey Beatty and Sons, Sydney, Australia.
18. FOKIDIS, H. B., T. S. RISCH, AND T. C. GLENN. 2007. Reproductive and resource benefits to large female body size in a mammal exhibiting female-biased sexual size dimorphism. Animal Behaviour 73:479-488.
19. GOLDINGAY, R. L. 1992. The socioecology of the yellow-bellied glider, Petaurus australis, in a coastal forest. Australian Journal of Zoology 40:267-278.
20. GOLDINGAY, R. L. 2000. Gliding mammals of the world: diversity and ecological requirements. Pp. 9-44 in Biology of gliding mammals (R. L. Goldingay and J. Scheibe, eds.). Filander-Verlag, Fürth, Germany.
21. GOLDINGAY, R. L., AND R. P. KAVANAGH. 1993. Socioecology of the yellow-bellied glider (Petaurus australis) at Waratah Creek, N.S.W. Australian Journal of Zoology 38:327-341.
22. GRENYER, R., AND A. PURVIS. 2003. A composite species-level phylogeny of the 'Insectivora' (Mammalia: order Lipotyphla Haeckel, 1866). Journal of Zoology (London) 260:245-257.
23. GUILLEMETTE, M., AND J. F. OUELLET. 2005. Temporary flightlessness as a potential cost of reproduction in pre-laying common eiders Somateria mollissima. Ibis 147:301-306.
24. HARVEY, P. H., AND M. D. PAGEL. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford, United Kingdom.
25. HAYSSEN, V., AND T. H. KUNZ. 1996. Allometry of litter mass in bats: maternal size, wing morphology, and phylogeny. Journal of Mammalogy 77:476-490.
26. HAYSSEN, V., A. TIENHOVEN, AND A. TIENHOVEN. 1993. Asdell's patterns of mammalian reproduction. Cornell University Press, Ithaca, New York.
27. HENRY, S. R. 1984. Social organization of the greater glider (Petauroides volans) in Victoria. Pp. 221-228 in Possums and gliders (A. P. Smith and I. D. Hume, eds.). Surrey Beatty and Sons, Sydney, Australia.
28. HOLMES, D. J., AND S. N. AUSTAD. 1994. Fly now, die later: life-history correlates of gliding and flying in mammals. Journal of Mammalogy 75:224-226.
29. HUCHON, D., ET AL. 2002. Rodent phylogeny and a timescale for the evolution of Glires: evidence from an extensive taxon sampling using three nuclear genes. Molecular Biology and Evolution 19:1053-1065.
30. JACKSON, S. M. 2000. Glide angle in the genus Petaurus and a review of gliding in mammals. Mammal Review 30:9-30.
31. JONES, K. E., AND A. MACLARNON. 2001. Bat life histories: testing models of mammalian life-history evolution. Evolutionary Ecology Research 3:465-476.
32. KENNEDY, M., AND R. D. M. PAGE. 2002. Seabird supertrees: combining partial estimates of procellariiform phylogeny. Auk 119:88-108.
33. KINGDON, J. 1997. The Kingdon field guide to African mammals. Academic Press, London, United Kingdom.
34. LANDRY, S. O. 1999. A proposal for a new classification and nomenclature for the Glires (Lagomorpha and Rodentia). Mitteilungen aus dem Museum für Naturkunde in Berlin - Zoologische Reihe 75:283-316.
35. LEKAGUL, B., AND J. A. MCNEELY. 1977. Mammals of Thailand. Kurusapha Ladprao Press, Bangkok, Thailand.
36. MCGUIRE, J. A., AND R. DUDLEY. 2005. The cost of living large: comparative gliding performance in flying lizards (Agamidae: Draco). American Naturalist 166:93-106.
37. MCLEAN, J., AND J. SPEAKMAN. 2000. Morphological changes during postnatal growth and reproduction in the brown long-eared bat Plecotus auritus: implications for wing loading and predicted flight performance. Journal of Natural History 34:773-791.
38. MENG, J., Y. HU, Y. WANG, X. WANG, AND C. LI. 2006. A Mesozoic gliding mammal from northeastern China. Nature 444:889-893.
39. MERCER, J. M., AND V. L. ROTH. 2003. The effects of Cenozoic global change on squirrel phylogeny. Science 299:1568-1572.
40. MONTGELARD, C., S. BENTZ, C. TIRARD, O. VERNEAU, AND F. M. CATZEFLIS. 2002. Molecular systematics of Sciurognathi (Rodentia): the mitochondrial cytochrome b and 12S rRNA genes support the Anomaluroidea (Pedetidae and Anomaluridae). Molecular Phylogenetics and Evolution 22:220-233.
41. MUELLER, H. C., AND K. MEYER. 1985. Evolution of reversed sexual dimorphism in size: a comparative analysis of the Falconiformes of the western Palearctic. Current Ornithology 2:65-101.
42. MUNEMASA, M., M. NIKAIDO, S. DONNELLAN, C. C. AUSTIN, N. OKADA, AND M. HASEGAWA. 2006. Phylogenetic analysis of diprotodontian marsupials based on complete mitochondrial genomes. Genes and Genetic Systems 81:181-191.
43. MUUL, I., AND L. B. LIAT. 1974. Reproductive frequency in Malaysian flying squirrels Hylopetes and Pteromyscus. Journal of Mammalogy 55:393-400.
44. MUUL, I., AND L. B. LIAT. 1978. Comparative morphology, food habits, and ecology of some Malaysian arboreal rodents. Pp. 361-368 in The ecology of arboreal foliovores (G. G. Montgomery, ed.). Smithsonian Institution Press, Washington, D.C.
45. MYERS, P. 1978. Sexual dimorphism in size of vespertilionid bats. American Naturalist 112:701-711.
46. NIXON, K. C. 1999. The Parsimony Ratchet, a new method for rapid parsimony analysis. Cladistics 15:407-414.
47. NOVACEK, M. J. 1989. Higher mammalian phylogeny: the morphological-molecular synthesis. Pp. 421-435 in Nobel symposium: hierarchy of life (B. Fernholm, K. Bremer, and H. Jomvall, eds.). Elsevier, Amsterdam, The Netherlands.
48. NOWAK, R. M. 1999. Walker's mammals of the world. 6th ed. Johns Hopkins University Press, Baltimore, Maryland.
49. OLSSON, M., R. SHINE, AND E. BAK-O LSSON. 2000. Locomotor impairment of gravid lizards: is the burden physical or physiological? Journal of Evolutionary Biology 13:263-268.
50. OSHIDA, T., ET AL. 2004. Phylogenetic position of the small Kashmir flying squirrel Hylopetes (Eoglaucomys) fimbriatus, in the subfamily Pteromyinae. Canadian Journal of Zoology 82:1336-1342.
51. PAGE, R. D. M. 1996. TreeView: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12:357-358.
52. PARKER, S. P. 1990. Grzimek's encyclopaedia of mammals. McGraw-Hill, New York.
53. PAYNE, J., C. M. FRANCIS, AND K. PHILLIPPS. 1994. A field guide to the mammals of Borneo. Sabah Society and World Wildlife Fund Malaysia, Kuala Lumpur, Malaysia.
54. PROMISLOW, D. E. L., AND P. H. HARVEY. 1990. Living fast and dying young: a comparative analysis of life history variation among mammals. Journal of Zoology (London) 220:417-437.
55. PURVIS, A., AND A. RAMBAUT. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Computer Applications in the Biosciences 11:247-251.
56. QUIN, D. G. 1995. Population ecology of the squirrel glider (Petaurus norfolcensis) and the sugar glider (P. breviceps) (Marsupiala: Petauridae) at Limeburners Creek, on the central north coast of New South Wales. Wildlife Research 22:471-505.
57. RAYNER, J. M. V. 1981. Flight adaptations in vertebrates. Symposia of the Zoological Society of London 48:137-172.
58. READ, A. F., AND P. H. HARVEY. 1989. Life history differences among the eutherian radiations. Journal of Zoology (London) 219:329-353.
59. ROBINS, J. H., J. S. SCHEIBE, AND K. LAVES. 2000. Sexual size dimorphism and allometry in southern flying squirrels, Glaucomys volans. Pp. 229-248 in Biology of gliding mammals (R. L. Goldingay and J. Scheibe, eds.). Filander-Verlag, Fürth, Germany.
60. RISCH, T. S., F. S. DOBSON, AND J. O. MURIE. 1995. Is mean litter size the most productive? A test in Columbian ground squirrels. Ecology 76:1643-1654.
61. RISCH, T. S., G. R. MICHENER, AND F. S. DOBSON. 2007. Variation in litter size: a test of hypotheses in Richardson's ground squirrels. Ecology 88:306-314.
62. ROFF, D. A. 2002. Life history evolution. Sinauer Associates, Inc., Publishers, Sunderland, Maryland.
63. SCHMITZ, J., M. OHME, B. SURYOBROTO, AND H. ZISCHLER. 2002. The colugo (Cynocephalus variegatus Dermoptera): the primates' gliding sister? Molecular Biology and Evolution 19:2308-2312.
64. SHINE, R. 1988. Constraints on reproductive investment: a comparison between aquatic and terrestrial snakes. Evolution 42:17-27.
65. SHINE, R. 2003. Effects of pregnancy on locomotor performance: an experimental study on lizards. Oecologia 136:450-456.
66. SHINE, R., S. KEOGH, P. DOUGHTY, AND H. GIRAGOSSYAN. 1998. Costs of reproduction and the evolution of sexual dimorphism in a 'flying lizard' Draco melanopogon (Agamidae). Journal of Zoology (London) 246:203-213.
67. SMITH, M. J. 1973. Petaurus breviceps. Mammalian Species 30:1-5.
68. STAFFORD, B. J., R. W. THORINGTON, JR., AND T. KAWAMICHI. 2002. Gliding behavior of Japanese giant flying squirrels (Petaurista leucogenys). Journal of Mammalogy 83:553-562.
69. STAPP, P. 1992. Energetic influences on the life history of Glaucomys volans. Journal of Mammalogy 73:914-920.
70. STAPP, P. 1994. Can predation explain life-history strategies in mammalian gliders? Journal of Mammalogy 75:227-228.
71. STEPPAN, S. J., B. L. STORZ, AND R. S. HOFFMANN. 2004. Nuclear DNA phylogeny of the squirrels (Mammalia: Rodentia) and the evolution of arboreality from c-myc and RAG1. Molecular Phylogenetics and Evolution 30:703-719.
72. STONER, C. J., O. R. P. BININDA-EMONDS, AND T. CARO. 2003. The adaptive significance of colouration in lagomorphs. Biological Journal of the Linnean Society 79:309-328.
73. STORCH, G., B. ENGESSER, AND M. WUTTKE. 1996. Oldest fossil record of gliding in rodents. Nature 379:439-441.
74. SUCKLING, G. C. 1984. Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Australian Wildlife Research 11:49-78.
75. SWOFFORD, D. L. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts.
76. TATE, G. H. H. 1945. Notes on the squirrel-like and mouse-like possums (Marsupiala). American Museum Novitates 1305:1-12.
77. THOMAS, A. L. R., AND G. K. TAYLOR. 2001. Animal flight dynamics I. Stability in gliding flight. Journal of Theoretical Biology 212: 399-424.
78. THORINGTON, R. W., JR., K. DARROW, AND C. G. ANDERSON. 1998. Wing tip anatomy and aerodynamics in flying squirrels. Journal of Mammalogy 79:245-250.
79. THORINGTON, R. W., JR., AND L. R. HEANEY. 1981. Body proportions and gliding adaptations of flying squirrels (Petauristinae). Journal of Mammalogy 62:101-114.
80. THORINGTON, R. W., JR., D. PITASSY, AND S. A. JANSA. 2002. Phylogenies of flying squirrels (Pteromyinae). Journal of Mammalian Evolution 9:99-135.
81. THORINGTON, R. W., JR., C. E. SCHENNUM, L. A. PAPPAS, AND D. PITASSY. 2005. The difficulties of identifying flying squirrels (Sciuridae: Pteromyini) in the fossil record. Journal of Vertebrate Paleontology 25:950-961.
82. THORLEY, J. L., AND R. D. M. PAGE. 2000. RadCon: phylogenetic tree comparison and consensus. Bioinformatics 16:486-487.
83. TYNDALE-BISCOE, C. H., AND M. B. RENFREE. 1987. Reproductive physiology of marsupials. Cambridge University Press, Cambridge, United Kingdom.
84. VAUGHAN, T. A., J. M. RYAN, AND N. J. CAPZAPLEWSKI. 2000. Mammalogy. Saunders College Publishing, Orlando, Florida.
85. WARD, S. J. 1990. Life-history of the feathertail glider, Acrobates pygmaeus, (Acrobatidae: Marsupiala) in south-eastern Australia. Australian Journal of Zoology 38:503-517.
86. WELLS-GOSLING, N., AND L. R. HEANEY. 1984. Glaucomys sabrinus. Mammalian Species 229:1-8.
87. WESTERN, D., AND J. SSEMAKULA. 1982. Life history patterns in birds and mammals and their evolutionary interpretation. Oecologia 54:281-290.
88. WILSON, D. E., AND D. M. REEDER. 2005. Mammal species of the world: a taxonomic and geographic reference. 3rd ed. Johns Hopkins University Press, Baltimore, Maryland.
89. WISCHUSEN, E. W., N. R. INGLE, AND M. E. RICHMOND. 1992. Observations on the reproductive behaviour and social behaviour of the Philippine flying lemur (Cynocephalus volans). Malayan Nature Journal 46:65-71.
90. YU, F., 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 38:755-766.