Evolutionary Biology

, Volume 37, Issue 1, pp 1–18 | Cite as

Morphological Diversity Despite Isometric Scaling of Lever Arms

Research Article
First Online:
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Abstract

In the absence of a substantial functional shift, morphological evolution is usually expected to follow an allometric trajectory, however, studies of tree squirrel jaws have found isometry across most of their size range. This isometry appears to reflect the integration of a small number of lever arm lengths that are critical for generating bite force. To test whether this integration constrains only the ratios of these lengths, or jaw shape in general, we analyzed jaw shapes and a set of lengths comparable to those used in previous studies for 23 species of sciurine tree squirrels (Sciurus, Tamiasciurus and Microsciurus), a lineage that is both functionally uniform and spans a large size range. We found that the measured lengths were highly correlated and isometric with respect to each other, but negatively allometric with respect to jaw size. Shape differences are generally small, but shape diversity was still greater than the diversity of mechanical advantages (input lever lengths scaled by output lever length). In addition, phylogenetic analyses demonstrated that only a minute fraction of shape evolution is correlated with size evolution. This contrast between the diversity of shape and the stability of proportions among a suite of functionally relevant lengths suggests that constraints on those lengths and the associated mechanical parameters have little or no ability to restrict changes in other aspects of jaw form.

Keywords

Allomety Isometry Jaws Squirrels 
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Notes

Acknowledgements

For access to the specimens in their care, we thank the curators and staff at the following institutions: U.S. National Museum of Natural History, University of Michigan Museum of Zoology, and University of California Museum of Vertebrate Zoology.

References

  1. Alfaro, M. E., Bolnick, D. I., & Wainwright, P. C. (2004). Evolutionary dynamics of complex biomechanical systems: An example using the four-bar mechanism. Evolution, 58, 495–503.PubMedGoogle Scholar
  2. Alfaro, M. E., Bolnick, D. I., & Wainwright, P. C. (2005). Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. American Naturalist, 165, E140–E154.CrossRefPubMedGoogle Scholar
  3. Arbogast, B. S., Browne, R. A., & Weigl, P. D. (2001). Evolutionary genetics and Pleistocene biogeography of North American tree squirrels (Tamiasciurus). Journal of Mammalogy, 82, 302–319.CrossRefGoogle Scholar
  4. Ball, S. S., & Roth, V. L. (1995). Jaw muscles of New World squirrels. Journal of Morphology, 224, 265–291.CrossRefPubMedGoogle Scholar
  5. Best, T. L. (1995a). Sciurus colliaei. Mammalian Species, 497, 1–4.Google Scholar
  6. Best, T. L. (1995b). Sciurus variegatoides. Mammalian Species, 500, 1–6.Google Scholar
  7. Best, T. L. (1995c). Sciurus deppei. Mammalian Species, 505, 1–5.Google Scholar
  8. Best, T. L., & Riedel, S. (1995). Sciurus arizonensis. Mammalian Species, 496, 1–5.Google Scholar
  9. Binder, W. J., & Van Valkenburgh, B. (2000). Development of bite strength and feeding behavior in juvenile spotted hyenas (Crocuta crocuta). Journal of Zoology, 252, 273–283.CrossRefGoogle Scholar
  10. Black, C. C. (1963). A review of the North American Tertiary Sciuridae. Bulletin of the Museum of Comparative Zoology, 130, 109–248.Google Scholar
  11. Bramble, D. M. (1978). Origin of the mammalian feeding complex: Models and mechanisms. Paleobiology, 4, 271–301.Google Scholar
  12. Bryant, M. D. (1945). Phylogeny of Nearctic Sciuridae. American Midland Naturalist, 33, 257–390.CrossRefGoogle Scholar
  13. Carraway, L. N., & Verts, B. J. (1994). Relationship of mandibular morphology to relative bite force in some Sorex from western North America. In J. F. Merritt, G. L. Kirkland Jr., & R. K. Rose (Eds.), Advances in the biology of shrews (pp. 201–210). Pittsburgh, PA: Carnegie Museum of Natural History.Google Scholar
  14. Cartmill, M. (1980). Morphology, function, and evolution of the anthropoid postorbital septum. In R. L. Ciochon & A. B. Chiarelli (Eds.), Evolutionary biology of new world monkeys and continental drift (pp. 243–274). NY: Plenum Press.Google Scholar
  15. Davis, D. D. (1955). Masticatory apparatus in the spectacled bear Tremarctos ornatus. Fieldiana: Zoology, 37, 25–46.Google Scholar
  16. Dullemeijer, P. (1958). The mutual structural influence of the elements in a pattern. Archives Neerlandaises de Zoologie, 13 supplement 1, 74–88.Google Scholar
  17. Dumont, E. R., Herrel, A., Medellíin R. A., Vargas-Contreras, J. A., & Santana, S. E. (2009). Journal of Zoology, 279, 329–337.Google Scholar
  18. Eisenberg, J. F., & Wilson, D. E. (1981). Relative brain size and feeding strategies in didelphid marsupials. American Naturalist, 118, 110–126.CrossRefGoogle Scholar
  19. Emry, R. J., & Thorington, R. W., Jr. (1982). Descriptive and comparative osteology of the oldest fossil squirrel Protosciurus Rodentia Sciuridae. Smithsonian Contributions to Paleobiology, 47, 1–34.Google Scholar
  20. Emry, R. J., & Thorington, R. W., Jr. (1984). The tree squirrel Sciurus (Sciuridae, Rodentia) as a living fossil. In N. Eldredge & S. M. Stanley (Eds.), Living fossils (pp. 23–31). New York: Springer.Google Scholar
  21. Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.CrossRefGoogle Scholar
  22. Foote, M. (1993). Contributions of individual taxa to overall morphological disparity. Paleobiology, 19, 403–419.Google Scholar
  23. Gould, S. J. (1975). On the scaling of tooth size in mammals. American Zoologist, 15, 351–362.Google Scholar
  24. Greaves, W. S. (1982). A mechanical limitation on the position of the jaw muscles of mammals: The one-third rule. Journal of Mammalogy, 63, 261–266.CrossRefGoogle Scholar
  25. Greaves, W. S. (2000). Location of the vector of jaw muscle force in mammals. Journal of Morphology, 243, 293–299.CrossRefPubMedGoogle Scholar
  26. Harrison, R. G., Bogdanowicz, S. M., Hoffmann, R. S., Yensen, E., & Sherman, P. W. (2003). Phylogeny and evolutionary history of the ground squirrels (Rodentia: Marmotinae). Journal of Mammalian Evolution, 10, 249–276.CrossRefGoogle Scholar
  27. Herrel, A., O’Reilly, J. C., & Richmond, A. M. (2002). Evolution of bite performance in turtles. Journal of Evolutionary Biology, 15, 1083–1094.CrossRefGoogle Scholar
  28. Herrel, A., Podos, J., Huber, S. K., & Hendry, A. P. (2005). Bite performance and morphology in a population of Darwin’s finches: Implications for the evolution of bite shape. Functional Ecology, 19, 43–48.CrossRefGoogle Scholar
  29. Herron, M. D., Castoe, T. A., & Parkinson, C. L. (2004). Sciurid phylogeny and paraphyly of Holarctic ground squirrels (Spermophilus). Molecular Phylogenetics and Evolution, 31, 1015–1030.CrossRefPubMedGoogle Scholar
  30. Hoffmeister, R. G., & Hoffmeister, D. F. (1991). The hyoid of North American squirrels, Sciuridae, with remarks on associated musculature. Anales del Instituto de Biologica, Universidad Nacional Autónoma de México, Serie Zoología, 62, 219–234.Google Scholar
  31. Huxley, J. S. (1932). Problems of relative growth. Baltimore, MD: Johns Hopkins Univ. Press.Google Scholar
  32. Lemen, C. A. (1980). Relationship between relative brain size and climbing ability in Peromyscus. Journal of Mammalogy, 61, 360–364.CrossRefGoogle Scholar
  33. Lemen, C. A. (2008). A simple morphological predictor of bite force in rodents. Journal of Zoology, 275, 418–422.CrossRefGoogle Scholar
  34. Marcus, L. F., Corti, M., Loy A., Naylor, G., & Slice, D. E. (Eds.). (1996). Advances in morphometrics. In Proceedings of the 1993 NATO advanced studies instititute on morphometrics in Il Ciocco, Italy. Plenum Press.Google Scholar
  35. Marroig, G., & Cheverud, J. M. (2005). Size as a line of least evolutionary resistance: Diet and adaptive morphological radiation in New World monkeys. Evolution, 59, 1128–1142.PubMedGoogle Scholar
  36. McGrath, G. (1987). Relationships of Nearctic tree squirrels of the genus Sciurus. Ph.D. dissertation, University of Kansas, Lawrence, 101 pp.Google Scholar
  37. Mercer, J. M., & Roth, V. L. (2003). The effects of Cenozoic global change on squirrel phylogeny. Science, 299, 1568–1572.CrossRefPubMedGoogle Scholar
  38. Moore, J. C. (1959). Relationships among the living squirrels of the Sciurinae. Bulletin of the American Museum of Natural History, 118, 157–206.Google Scholar
  39. Nitikman, L. Z. (1985). Sciurus granatensis. Mammalian Species, 246, 1–8.CrossRefGoogle Scholar
  40. Oshida, T., & Masuda, R. (2000). Phylogeny and zoogeography of six squirrel species for the genus Sciurus (Mammalia, Rodentia), inferred from cytochrome b gene sequences. Zoological Science, 17, 405–409.PubMedGoogle Scholar
  41. Radinsky, L. B. (1982). Evolution of skull shape in carnivores. 3. The origin and early radiation of the modern carnivore families. Paleobiology, 8, 177–195.Google Scholar
  42. Radinsky, L. B. (1985). Approaches in evolutionary morphology: A search for patterns. Annual Review of Ecology and Systematics, 16, 1–14.CrossRefGoogle Scholar
  43. Roth, V. L. (1996). Cranial integration in the Sciuridae. American Zoologist, 36, 14–23.Google Scholar
  44. 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, 703–719.CrossRefPubMedGoogle Scholar
  45. Strauss, R. E. (1985). Evolutionary allometry and variation in body form in the South American catfish genus Corydoras (Callichthyidae). Systematic Zoology, 34, 381–396.CrossRefGoogle Scholar
  46. Sweet, S. S. (1980). Allometric inference in morphology. American Zoologist, 20, 643–652.Google Scholar
  47. Thorington, R. W., Jr., & R. S. Hoffmann. (2005). Family Sciuridae. In D. E. Wilson & D. M. Reeder (Eds.), Mammal species of the world (pp. 754–818). Washington, DC: Smithsonian Institution Press.Google Scholar
  48. Thorington, R. W., Jr., & Darrow, K. (1996). Jaw muscles of Old World squirrels. Journal of Morphology, 230, 145–165.CrossRefPubMedGoogle Scholar
  49. Turnbull, W. D. (1970). Mammalian masticatory apparatus. Fieldiana: Geology, 18, 149–356.Google Scholar
  50. Velhagen, W. A., & Roth, V. L. (1997). Scaling of the mandible in squirrels. Journal of Morphology, 232, 107–132.CrossRefPubMedGoogle Scholar
  51. Villalobos, F., & Cervantes-Reza, F. (2007). Phylogenetic relationships of Mesoamerican species of the genus Sciurus (Rodentia : Sciuridae). Zootaxa, 1525, 31–40.Google Scholar
  52. Werdelin, L. (1989). Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology, 15, 387–401.Google Scholar
  53. Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. New York: Elsevier.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Kresge Hearing Research Institute and Museum of ZoologyUniversity of MichiganAnn ArborUSA
  2. 2.Museum of PaleontologyUniversity of MichiganAnn ArborUSA

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