Skip to main content
Log in

Morphological Diversity Despite Isometric Scaling of Lever Arms

  • Research Article
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ball, S. S., & Roth, V. L. (1995). Jaw muscles of New World squirrels. Journal of Morphology, 224, 265–291.

    Article  CAS  PubMed  Google Scholar 

  • Best, T. L. (1995a). Sciurus colliaei. Mammalian Species, 497, 1–4.

    Google Scholar 

  • Best, T. L. (1995b). Sciurus variegatoides. Mammalian Species, 500, 1–6.

    Google Scholar 

  • Best, T. L. (1995c). Sciurus deppei. Mammalian Species, 505, 1–5.

    Google Scholar 

  • Best, T. L., & Riedel, S. (1995). Sciurus arizonensis. Mammalian Species, 496, 1–5.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Black, C. C. (1963). A review of the North American Tertiary Sciuridae. Bulletin of the Museum of Comparative Zoology, 130, 109–248.

    Google Scholar 

  • Bramble, D. M. (1978). Origin of the mammalian feeding complex: Models and mechanisms. Paleobiology, 4, 271–301.

    Google Scholar 

  • Bryant, M. D. (1945). Phylogeny of Nearctic Sciuridae. American Midland Naturalist, 33, 257–390.

    Article  Google Scholar 

  • 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 

  • 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 

  • Davis, D. D. (1955). Masticatory apparatus in the spectacled bear Tremarctos ornatus. Fieldiana: Zoology, 37, 25–46.

    Google Scholar 

  • Dullemeijer, P. (1958). The mutual structural influence of the elements in a pattern. Archives Neerlandaises de Zoologie, 13 supplement 1, 74–88.

    Google Scholar 

  • Dumont, E. R., Herrel, A., Medellíin R. A., Vargas-Contreras, J. A., & Santana, S. E. (2009). Journal of Zoology, 279, 329–337.

    Google Scholar 

  • Eisenberg, J. F., & Wilson, D. E. (1981). Relative brain size and feeding strategies in didelphid marsupials. American Naturalist, 118, 110–126.

    Article  Google Scholar 

  • 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 

  • 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 

  • Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.

    Article  Google Scholar 

  • Foote, M. (1993). Contributions of individual taxa to overall morphological disparity. Paleobiology, 19, 403–419.

    Google Scholar 

  • Gould, S. J. (1975). On the scaling of tooth size in mammals. American Zoologist, 15, 351–362.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Greaves, W. S. (2000). Location of the vector of jaw muscle force in mammals. Journal of Morphology, 243, 293–299.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Herrel, A., O’Reilly, J. C., & Richmond, A. M. (2002). Evolution of bite performance in turtles. Journal of Evolutionary Biology, 15, 1083–1094.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Huxley, J. S. (1932). Problems of relative growth. Baltimore, MD: Johns Hopkins Univ. Press.

    Google Scholar 

  • Lemen, C. A. (1980). Relationship between relative brain size and climbing ability in Peromyscus. Journal of Mammalogy, 61, 360–364.

    Article  Google Scholar 

  • Lemen, C. A. (2008). A simple morphological predictor of bite force in rodents. Journal of Zoology, 275, 418–422.

    Article  Google Scholar 

  • 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.

  • 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.

    PubMed  Google Scholar 

  • McGrath, G. (1987). Relationships of Nearctic tree squirrels of the genus Sciurus. Ph.D. dissertation, University of Kansas, Lawrence, 101 pp.

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

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Nitikman, L. Z. (1985). Sciurus granatensis. Mammalian Species, 246, 1–8.

    Article  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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 

  • Radinsky, L. B. (1985). Approaches in evolutionary morphology: A search for patterns. Annual Review of Ecology and Systematics, 16, 1–14.

    Article  Google Scholar 

  • Roth, V. L. (1996). Cranial integration in the Sciuridae. American Zoologist, 36, 14–23.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Strauss, R. E. (1985). Evolutionary allometry and variation in body form in the South American catfish genus Corydoras (Callichthyidae). Systematic Zoology, 34, 381–396.

    Article  Google Scholar 

  • Sweet, S. S. (1980). Allometric inference in morphology. American Zoologist, 20, 643–652.

    Google Scholar 

  • 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.

  • Thorington, R. W., Jr., & Darrow, K. (1996). Jaw muscles of Old World squirrels. Journal of Morphology, 230, 145–165.

    Article  PubMed  Google Scholar 

  • Turnbull, W. D. (1970). Mammalian masticatory apparatus. Fieldiana: Geology, 18, 149–356.

    Google Scholar 

  • Velhagen, W. A., & Roth, V. L. (1997). Scaling of the mandible in squirrels. Journal of Morphology, 232, 107–132.

    Article  CAS  PubMed  Google Scholar 

  • Villalobos, F., & Cervantes-Reza, F. (2007). Phylogenetic relationships of Mesoamerican species of the genus Sciurus (Rodentia : Sciuridae). Zootaxa, 1525, 31–40.

    Google Scholar 

  • Werdelin, L. (1989). Constraint and adaptation in the bone-cracking canid Osteoborus (Mammalia: Canidae). Paleobiology, 15, 387–401.

    Google Scholar 

  • Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. New York: Elsevier.

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Donald L. Swiderski.

Appendix

Appendix

Table 7 List of taxa and museum specimen numbers
Table 8 Average lever arm lengths (cm) for each species

Rights and permissions

Reprints and permissions

About this article

Cite this article

Swiderski, D.L., Zelditch, M.L. Morphological Diversity Despite Isometric Scaling of Lever Arms. Evol Biol 37, 1–18 (2010). https://doi.org/10.1007/s11692-010-9081-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-010-9081-8

Keywords

Navigation