Zoomorphology

, Volume 124, Issue 4, pp 189–203

Post-natal ontogeny of the mandible and ventral cranium in Marmota species (Rodentia, Sciuridae): allometry and phylogeny

Original Article

Abstract

Post-natal ontogenetic variation of the marmot mandible and ventral cranium is investigated in two species of the subgenus Petromarmota (M. caligata, M. flaviventris) and four species of the subgenus Marmota (M. caudata, M. himalayana, M. marmota, M. monax). Relationships between size and shape are analysed using geometric morphometric techniques. Sexual dimorphism is negligible, allometry explains the main changes in shape during growth, and males and females manifest similar allometric trajectories. Anatomical regions affected by size-related shape variation are similar in different species, but allometric trajectories are divergent. The largest modifications of the mandible and ventral cranium occur in regions directly involved in the mechanics of mastication. Relative to other anatomical regions, the size of areas of muscle insertion increases, while the size of sense organs, nerves and teeth generally decreases. Epigenetic factors, developmental constraints and size variation were found to be the major contributors in producing the observed allometric patterns. A phylogenetic signal was not evident in the comparison of allometric trajectories, but traits that allow discrimination of the Palaearctic marmots from the Nearctic species of Petromarmota are present early in development and are conserved during post-natal ontogeny.

Keywords

Mandible/ventral cranium Sexual dimorphism Allometric trajectories Masticatory muscles/epigenetics/constraints Phylogenetic signal 

References

  1. Adams DC, Slice DE, Rohlf FJ (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. It J Zool 71:5–16CrossRefGoogle Scholar
  2. Armitage KB (1999) Evolution of sociality in marmots. J Mammal 80:1–10CrossRefGoogle Scholar
  3. Armitage KB (2000) The evolution, ecology, and systematics of marmots. Oecologia Montana 9:1–18Google Scholar
  4. Arnold W (1990) The evolution of marmot sociality: I. Why disperse late? Behav Ecol Sociobiol 27:229–237Google Scholar
  5. Atchley WR, Cowley DE, Vogl C, McLellan T (1992) Evolutionary divergence, shape change, and genetic correlation structure in the rodent mandible. Syst Biol 41:196–221CrossRefGoogle Scholar
  6. Ball SS., Roth VL (1995) Jaw muscle of New World squirrels. J Morphol 224:265–291CrossRefPubMedGoogle Scholar
  7. Barash DP (1974) The evolution of marmot society: a general theory. Science 185:415–420PubMedCrossRefGoogle Scholar
  8. Barash DP (1989) Marmots Social behavior and ecology. Stanford Univ Press, Palo Alto, p 360Google Scholar
  9. Bibikov DI (1999) Marmots of the world. In: KB Armitage (ed), http://www.cons-dev.org/marm/MARM/PUBNET/Theses/Bibikov/bibtex/bibikov.html
  10. Blumstein DT, Armitage KB (1998) Life history consequences of social complexity: a comparative study of ground-dwelling sciurids. Behav Ecol 9:8–19CrossRefGoogle Scholar
  11. Blumstein DT, Armitage KB (1999) Cooperative breeding in marmots. Oikos 84:369–382CrossRefGoogle Scholar
  12. Cardini A (2003) The geometry of marmot (Rodentia, Sciuridae) mandible: phylogeny and patterns of morphological evolution. Syst Biol 52:186–205PubMedCrossRefGoogle Scholar
  13. Cardini A. (2004) Evolution of marmots (Rodentia, Sciuridae): combining information on labial and lingual sides of the mandible. Acta Theriol 49:301–318Google Scholar
  14. Cardini A., O’Higgins P (2004) Patterns of morphological evolution in Marmota (Rodentia, Sciuridae): geometric morphometrics of the cranium in the context of marmot phylogeny, ecology and conservation. Biol J Linn Soc 82:385–407CrossRefGoogle Scholar
  15. Cardini A, Tongiorgi P (2003) Yellow-bellied marmots ‘in the shape space’: sexual dimorphism, growth and allometry of the mandible. Zoomorphol 122:11–23Google Scholar
  16. Cardini A, Hoffmann RS, Thorington Jr RW. Morphological evolution in marmots (Rodentia, Sciuridae): size and shape of the dorsal and lateral surfaces of the cranium. J Zool Syst Evol Res, in pressGoogle Scholar
  17. Dryden IL., Mardia KV (1998) Statistical shape analysis. Wiley, New York, p 347Google Scholar
  18. Emerson SB, Bramble DM (1993) Scaling, allometry and skull design. In: Hanken J, Hall BK (eds) The skull, vol 3, Functional and evolutionary mechanisms. The University of Chicago Press, Chicago, pp385–421Google Scholar
  19. Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev Cambridge Philosoph Soc 41:587–640CrossRefGoogle Scholar
  20. Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, CambridgeGoogle Scholar
  21. Hafner DJ (1984) Evolutionary relationships of the Nearctic Sciuridae. In: Murie JO, Michener GR (eds) The biology of ground-dwelling squirrels. University of Nebraska Press, Lincoln, pp 3–23Google Scholar
  22. Herring SW (1993) Formation of the vertebrate face: epigenetic and functional influences. Am Zool 33:472–483Google Scholar
  23. Herron DM, Castoe TA, Parkinson CL (2004) Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus). Molec Phylog Evol 31:1015–1030CrossRefGoogle Scholar
  24. Hoffmann RS, Koeppl JW, Nadler CF (1979) The relationships of the amphiberigian marmots (Mammalia, Sciuridae). Occas Pap Mus nat Hist Univ Kans 83:1–56Google Scholar
  25. Huxley JS (1924). Constant differential growth-ratios and their significance. Nature 114:895–896CrossRefGoogle Scholar
  26. Huxley JS (1932a). Problems of relative growth. Methuen, London. Reprinted 1993, Johns Hopkins University Press, BaltimoreGoogle Scholar
  27. Huxley JS (1932b) Problems of relative growth. Methuen, London. Reprinted 1972: Dover Publications, New YorkGoogle Scholar
  28. Kendall DG (1984) Shape manifolds, Procrustean metrics and complex projective spaces. Bull London Math Soc 16:81–121CrossRefGoogle Scholar
  29. Klingenberg CP (1998). Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73:79–123CrossRefPubMedGoogle Scholar
  30. Laghenbach GE, Van Eijden TMGJ (2001) Mammalian feeding motor patterns. Amer Zool 41:1338–1351CrossRefGoogle Scholar
  31. Larson PM (2004) Chondrocranial morphology and ontogenetic allometry in larval Bufo americanus (Anura, Bufonidae). Zoomorphol 123:95–106CrossRefGoogle Scholar
  32. Lightfoot PS, German RZ (1998) The effect of muscular dystrophy on craniofacial growth in mice: a study of heterochrony and ontogenetic allometry. J Morphol 1998Google Scholar
  33. Marcus LF, Hingst-Zaher E, Zaher H (2000) Application of landmark morphometrics to skulls representing the orders of living mammals. Hystrix 11:27–48Google Scholar
  34. Mercer JM, Roth VL (2003) The effects of Cenozoic global change on squirrel phylogeny. Science 299:1568–1572CrossRefPubMedGoogle Scholar
  35. Miller JP, German RZ (1999) Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr 129:2061–2069PubMedGoogle Scholar
  36. Monteiro LR (1999) Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol 48:192–199CrossRefPubMedGoogle Scholar
  37. Mosimann JE (1970) Size allometry: size and shape variables with characterizations of the lognormal and generalized amma distributions. J Am Stat Assoc 65:930–945CrossRefGoogle Scholar
  38. Novacek MJ (1993) Patterns of diversity in mammalian skull. In: Hanken J, Hall BK (eds) The skull, vol 2, Functional and evolutionary mechanisms. The University of Chicago Press, Chicago, pp 438–545Google Scholar
  39. O’Higgins P (2000) Quantitative approaches to the study of the craniofacial growth and evolution: advances in morphometric techniques. In: O'Higgins P, Cohn M (eds) Development, growth and evolution. Linnean Society of London, London, pp 163–185Google Scholar
  40. O’Higgins P, Jones N (1999) Morphologika. Tools for shape analysis. Univerisity College, London. http://www.york.ac.uk/res/jme/resources.htm Google Scholar
  41. Polly PD (2003) Paleophylogeography: the tempo of geographic differentiation in marmots (Marmota). J Mammal 84:278–294CrossRefGoogle Scholar
  42. Ponce de Leon MS, Zollikofer CPE (2001) Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412:534–538CrossRefPubMedGoogle Scholar
  43. Rohlf FJ (1999) Shape statistics: Procrustes superimpositions and tangent spaces. J Class 16:197–223CrossRefGoogle Scholar
  44. Rohlf FJ (2002) NTSYS-pc, version 2.11n. Exeter Software, Setauket, New YorkGoogle Scholar
  45. Rohlf FJ (2003) Bias and error in estimates of mean shape in morphometrics. J Hum Evol 44:665–683CrossRefPubMedGoogle Scholar
  46. Rohlf FJ (2004) Tps Series. Department of Ecology and Evolution, State University of New York, Stony Brook. http://life.bio.sunysb.edu/morph/
  47. Rohlf FJ, Corti M (2000) Use of two-block partial least squares to study covariation in shape. Syst Biol 49:740–753CrossRefPubMedGoogle Scholar
  48. Rohlf FJ, Loy A, Corti M (1996) Morphometric analysis of Old World Talpidae (Mammalia, Insectivora) using partial-warp scores. Syst Biol 45:344–362CrossRefGoogle Scholar
  49. Roth VL (1996) Cranial integration in the Sciuridae. Am Zool 36:14–23Google Scholar
  50. Slice D (1999) Morpheus (beta version). Department of Ecology and Evolution, State University of New York, Stony Brook, New YorkGoogle Scholar
  51. Slice D (2001) Landmark coordinates aligned by Procrustes analysis do not lie in Kendall’s shape space. Syst Biol 50:141–149PubMedCrossRefGoogle Scholar
  52. SPSS for Windows (1999) SPSS Inc., versions 9.0.1, 10.0.6. SPSS Inc., ChicagoGoogle Scholar
  53. Statistica for Windows (1993) StatSoft Inc., version 4.5. StatSoft Inc., TulsaGoogle Scholar
  54. Steppan SC, Akhverdyan MR, Lyapunova EA, Fraser DG, Vorontsov NN, Hoffmann RS, Braun MJ (1999) Molecular phylogeny of the marmots (Rodentia, Sciuridae): tests of evolutionary and biogeographic hypotheses. Syst Biol 48:715–734CrossRefPubMedGoogle Scholar
  55. Swiderski DL (2003) Separating size from allometry: analysis of lower jaw morphology in the fox squirrel, Sciurus niger. J Mammal 84:861–876CrossRefGoogle Scholar
  56. Thorington RW, Darrow K (1996) Jaw muscles of Old World squirrels. J Morphol 230:145–165CrossRefPubMedGoogle Scholar
  57. Van Vuren D, Salsbury CM (1992) The relation between premolar wear and age in yellow-bellied marmots, Marmota flaviventris. Can Field-Nat 106:134–136Google Scholar
  58. Velhagen WA, Roth VL (1997) Scaling the mandible in squirrels. J Morphol 232:107–132CrossRefPubMedGoogle Scholar
  59. Voss RS, Marcus LF, Escalante P (1990) Morphological evolution in muroid rodents I. Conservative patterns of craniometric covariance and their ontogenetic basis in the neotropical genus Zygodontomys. Evolution 44:1568–1587CrossRefGoogle Scholar
  60. Zelditch ML, Sheets HD, Fink WD (2000) Spatiotemporal reorganization of growth rates in the evolution of ontogeny. Evolution 54:1363–1371PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Hull York Medical SchoolThe University of YorkHeslington, YorkUK
  2. 2.Hull York Medical School and Department of BiologyThe University of YorkHeslington, YorkUK
  3. 3.The University of HullHullUK

Personalised recommendations