Skip to main content

Advertisement

SpringerLink
Log in

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

  • Original Article
  • Published:
Zoomorphology Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig 3
Fig 4
Fig 5
Fig 6

Similar content being viewed by others

References

  • Adams DC, Slice DE, Rohlf FJ (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. It J Zool 71:5–16

    Article  Google Scholar 

  • Armitage KB (1999) Evolution of sociality in marmots. J Mammal 80:1–10

    Article  Google Scholar 

  • Armitage KB (2000) The evolution, ecology, and systematics of marmots. Oecologia Montana 9:1–18

    Google Scholar 

  • Arnold W (1990) The evolution of marmot sociality: I. Why disperse late? Behav Ecol Sociobiol 27:229–237

    Google Scholar 

  • Atchley WR, Cowley DE, Vogl C, McLellan T (1992) Evolutionary divergence, shape change, and genetic correlation structure in the rodent mandible. Syst Biol 41:196–221

    Article  Google Scholar 

  • Ball SS., Roth VL (1995) Jaw muscle of New World squirrels. J Morphol 224:265–291

    Article  PubMed  CAS  Google Scholar 

  • Barash DP (1974) The evolution of marmot society: a general theory. Science 185:415–420

    Article  PubMed  Google Scholar 

  • Barash DP (1989) Marmots Social behavior and ecology. Stanford Univ Press, Palo Alto, p 360

    Google Scholar 

  • Bibikov DI (1999) Marmots of the world. In: KB Armitage (ed), http://www.cons-dev.org/marm/MARM/PUBNET/Theses/Bibikov/bibtex/bibikov.html

  • Blumstein DT, Armitage KB (1998) Life history consequences of social complexity: a comparative study of ground-dwelling sciurids. Behav Ecol 9:8–19

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1999) Cooperative breeding in marmots. Oikos 84:369–382

    Article  Google Scholar 

  • Cardini A (2003) The geometry of marmot (Rodentia, Sciuridae) mandible: phylogeny and patterns of morphological evolution. Syst Biol 52:186–205

    Article  PubMed  Google Scholar 

  • Cardini A. (2004) Evolution of marmots (Rodentia, Sciuridae): combining information on labial and lingual sides of the mandible. Acta Theriol 49:301–318

    Google Scholar 

  • 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 82:385–407

    Article  Google Scholar 

  • Cardini A, Tongiorgi P (2003) Yellow-bellied marmots ‘in the shape space’: sexual dimorphism, growth and allometry of the mandible. Zoomorphol 122:11–23

    Google Scholar 

  • 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 press

  • Dryden IL., Mardia KV (1998) Statistical shape analysis. Wiley, New York, p 347

    Google Scholar 

  • 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, pp385–421

  • Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev Cambridge Philosoph Soc 41:587–640

    Article  CAS  Google Scholar 

  • Gould SJ (2002) The structure of evolutionary theory. Harvard University Press, Cambridge

    Google Scholar 

  • 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 3–23

    Google Scholar 

  • Herring SW (1993) Formation of the vertebrate face: epigenetic and functional influences. Am Zool 33:472–483

    Google Scholar 

  • Herron DM, Castoe TA, Parkinson CL (2004) Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus). Molec Phylog Evol 31:1015–1030

    Article  CAS  Google Scholar 

  • Hoffmann RS, Koeppl JW, Nadler CF (1979) The relationships of the amphiberigian marmots (Mammalia, Sciuridae). Occas Pap Mus nat Hist Univ Kans 83:1–56

    Google Scholar 

  • Huxley JS (1924). Constant differential growth-ratios and their significance. Nature 114:895–896

    Article  Google Scholar 

  • Huxley JS (1932a). Problems of relative growth. Methuen, London. Reprinted 1993, Johns Hopkins University Press, Baltimore

  • Huxley JS (1932b) Problems of relative growth. Methuen, London. Reprinted 1972: Dover Publications, New York

  • Kendall DG (1984) Shape manifolds, Procrustean metrics and complex projective spaces. Bull London Math Soc 16:81–121

    Article  Google Scholar 

  • Klingenberg CP (1998). Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 73:79–123

    Article  PubMed  CAS  Google Scholar 

  • Laghenbach GE, Van Eijden TMGJ (2001) Mammalian feeding motor patterns. Amer Zool 41:1338–1351

    Article  Google Scholar 

  • Larson PM (2004) Chondrocranial morphology and ontogenetic allometry in larval Bufo americanus (Anura, Bufonidae). Zoomorphol 123:95–106

    Article  Google Scholar 

  • Lightfoot PS, German RZ (1998) The effect of muscular dystrophy on craniofacial growth in mice: a study of heterochrony and ontogenetic allometry. J Morphol 1998

  • Marcus LF, Hingst-Zaher E, Zaher H (2000) Application of landmark morphometrics to skulls representing the orders of living mammals. Hystrix 11:27–48

    Google Scholar 

  • Mercer JM, Roth VL (2003) The effects of Cenozoic global change on squirrel phylogeny. Science 299:1568–1572

    Article  PubMed  CAS  Google Scholar 

  • Miller JP, German RZ (1999) Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr 129:2061–2069

    PubMed  CAS  Google Scholar 

  • Monteiro LR (1999) Multivariate regression models and geometric morphometrics: the search for causal factors in the analysis of shape. Syst Biol 48:192–199

    Article  PubMed  CAS  Google Scholar 

  • Mosimann JE (1970) Size allometry: size and shape variables with characterizations of the lognormal and generalized amma distributions. J Am Stat Assoc 65:930–945

    Article  Google Scholar 

  • 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 438–545

  • 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 163–185

    Google Scholar 

  • 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 

  • Polly PD (2003) Paleophylogeography: the tempo of geographic differentiation in marmots (Marmota). J Mammal 84:278–294

    Article  Google Scholar 

  • Ponce de Leon MS, Zollikofer CPE (2001) Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412:534–538

    Article  PubMed  Google Scholar 

  • Rohlf FJ (1999) Shape statistics: Procrustes superimpositions and tangent spaces. J Class 16:197–223

    Article  Google Scholar 

  • Rohlf FJ (2002) NTSYS-pc, version 2.11n. Exeter Software, Setauket, New York

  • Rohlf FJ (2003) Bias and error in estimates of mean shape in morphometrics. J Hum Evol 44:665–683

    Article  PubMed  Google Scholar 

  • Rohlf FJ (2004) Tps Series. Department of Ecology and Evolution, State University of New York, Stony Brook. http://life.bio.sunysb.edu/morph/

  • Rohlf FJ, Corti M (2000) Use of two-block partial least squares to study covariation in shape. Syst Biol 49:740–753

    Article  PubMed  CAS  Google Scholar 

  • Rohlf FJ, Loy A, Corti M (1996) Morphometric analysis of Old World Talpidae (Mammalia, Insectivora) using partial-warp scores. Syst Biol 45:344–362

    Article  Google Scholar 

  • Roth VL (1996) Cranial integration in the Sciuridae. Am Zool 36:14–23

    Google Scholar 

  • Slice D (1999) Morpheus (beta version). Department of Ecology and Evolution, State University of New York, Stony Brook, New York

    Google Scholar 

  • Slice D (2001) Landmark coordinates aligned by Procrustes analysis do not lie in Kendall’s shape space. Syst Biol 50:141–149

    Article  PubMed  CAS  Google Scholar 

  • SPSS for Windows (1999) SPSS Inc., versions 9.0.1, 10.0.6. SPSS Inc., Chicago

  • Statistica for Windows (1993) StatSoft Inc., version 4.5. StatSoft Inc., Tulsa

  • 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 48:715–734

    Article  PubMed  CAS  Google Scholar 

  • Swiderski DL (2003) Separating size from allometry: analysis of lower jaw morphology in the fox squirrel, Sciurus niger. J Mammal 84:861–876

    Article  Google Scholar 

  • Thorington RW, Darrow K (1996) Jaw muscles of Old World squirrels. J Morphol 230:145–165

    Article  PubMed  Google Scholar 

  • Van Vuren D, Salsbury CM (1992) The relation between premolar wear and age in yellow-bellied marmots, Marmota flaviventris. Can Field-Nat 106:134–136

    Google Scholar 

  • Velhagen WA, Roth VL (1997) Scaling the mandible in squirrels. J Morphol 232:107–132

    Article  PubMed  CAS  Google Scholar 

  • 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 44:1568–1587

    Article  Google Scholar 

  • Zelditch ML, Sheets HD, Fink WD (2000) Spatiotemporal reorganization of growth rates in the evolution of ontogeny. Evolution 54:1363–1371

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Special thanks to P. Tongiorgi, Università di Modena e Reggio Emilia; E. Capanna and M. Corti, University of Roma ‘La Sapienza’; V. Peracino, then Parco Nazionale del Gran Paradiso, Torino; R. Ramousse, University of Lyon 1; K. B. Armitage, University of Kansas, Lawrence; S. Elton, University of Hull; R. Z. German, University of Cincinnati; L. Spezia, Museo di Storia Naturale di Milano; F. J. Rohlf, State University of New York; C. P.Klingenberg, University of Manchester; Kornelius Kupczik, University College London; M. L. Zelditch, University of Michigan, Ann Arbor; Charles Oxnard, University of Western Australia. Many other colleagues and friends contributed to our work. Thanks to: I. V. Rymalov, Russian Academy of Science, Moscow; H. Seidler and K. Schaefer, University of Vienna; S. Herring, University of Washington; P. Jenkins, and the mammal section staff of the British Museum of Natural History, London; L. Gordon and the other mammal curators of the National Museum of Natural History, Washington; M. Podestà, Museo Civico di Storia Naturale, Milano; A. O. Averianov, G. I. Baranova, K. Tsytsulina and the other very friendly colleagues of the Zoological Institutes of the Russian Academy of Sciences, St. Petersburg; and Dino Scaravelli, formerly Museo di Storia Naturale, Cesena. The manuscript was greatly improved thanks to helpful comments by M. Collyer, Iowa State Univrsity at Ames, L. R. Monteiro, Universidade Estadual do Norte Fluminense, Rio de Janeiro, and an anonymous referee.

This work was supported by grants from Italian Ministero dell’Università e della Ricerca Scientifica e Tecnologica (Progetto Giovani Ricercatori Università di Modena e Reggio Emilia), and Accademia Nazionale dei Lincei (borse Lincei — Royal Society) to A. Cardini.

Author information

Authors and Affiliations

  1. Hull York Medical School, The University of York, Heslington, York, YO10 5DD, UK

    Andrea Cardini

  2. Hull York Medical School and Department of Biology, The University of York, YO10 5DD, Heslington, York, UK

    Paul O’Higgins

  3. The University of Hull, Cottingham Road, HU6 7RX, Hull, UK

    Andrea Cardini

Authors
  1. Andrea Cardini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul O’Higgins
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrea Cardini.

Appendix

Appendix

Abbreviations

USNM, National Museum of Natural History (Washington, USA); BMNHL, British Museum of Natural History (London, UK); ZIN, Zoological Institutes of the Russian Academy of Sciences (St. Petersburg, Russia); PNGP, National Park Gran Paradiso (Torino, Italy); SC, collection of Dino Scaravelli; DBA UMR, Department of Animal Biology, University of Modena and Reggio Emilia.

M. caligata

USNM 42636, 42638, 42793, 48580, 53595, 66696, 66697, 66698, 68716, 72222, 72223, 72225, 72226, 72227, 72235, 74995, 74996, 74998, 76233, 81913, 88005, 88006, 90132, 90134, 96206, 96207, 96533, 97952, 97953, 98154, 101296, 101298, 101300, 114833, 127594, 135161, 135163, 137319, 146449, 170741, 174501, 174502, 174503, 202533, 202790, 221012, 226148, 226719, 230108, 233212, 235255, 235257, 235258, 271698, 271699, 271701; only mandible: BMNHL 593.a or 45.7.4.9, 593.c (or 62.12.12.7), USNM 67073; only skull: BMNHL 1398.b, 2.3.7.5, USNM 66695, 67076, 101299, 170682, 210830, 256660.

M. caudate

BNHML, 10.12.2.25, 5.10.8.2, 69.493, 76.3.9.3, 8.10.3.16, 8.7.6.27, 88.3.20.25, 9.4.3.112, 92.1.1.7, USNM 35497, 35498, 35500, 62112, 62114, 62116, 62117, 62118, 173377, 173380, 173381, 173382, 173383, 173384, 298212, 327143, 353196, 353197, 353199; only mandible: BMNHL 1937.6.12.7, 77.11.23.3, 91.5.16.2, 97.10.3.54, USNM 35499, 62115, 353200; only skull: BMNHL 89.3.9.7 (or 1963a), 9.4.3.111, ZIN 22535, 27912, 2805 or 15318, 29355, 32666, 40549, 40551, 40553, 40555, 51537, USNM 62113, 62119, 173376, 173378, 173385, 173386, 353198.

M. flaviventris

BMNHL 40.823, USNM 23951, 25523, 25524, 25527, 30143, 41419, 41914, 42080, 42112, 42122, 42368, 65920, 74057, 74373, 79365, 80360, 88243, 89312, 93688, 93689, 93690, 93708, 99759, 99760, 100532, 100533, 108792, 128750, 128753, 128754, 133505, 139082, 147183, 156923, 157828, 158033, 158500, 158980, 168477, 168799, 168883, 168884, 170148, 177297, 180918, 186520, 191366, 191367, 191369, 204891, 208268, 211232, 212471, 221896, 221898, 228271, 228273, 229842, 233382, 234960, 242645, 243663, 243664, 243665, 244551, 244552, 274340, 291192, 575170; only mandible: USNM 72565, 89311; only skull: USNM 41198, 41345, 42858, 42859, 93709, 94343, 168494, 202937, 215215, 498417.

M. himalayana

BMNHL 11.2.1.94, 11.2.1.95, 12.3.18.2, 22.9.1.82, 22.9.1.83, 22.9.1.85, 23.9.1.38, 23.9.1.40, 23.9.1.41, 36.4.12.6, 5.12.5.2, 5.12.5.3, 8.2.29.1, 8.7.6.30, 96.11.4.2, 96.11.4.9, USNM 62121, 62122, 84099, 84100, 84101, 84102, 84104, 102576, 144038, 144039, 144040, 144041, 144042, 144043, 198638, 240674, 240675, 240676, 240677, 255960, 259438, 259439, 573031, 573032, 573033, 573035, 573036, 573037, 576183, 576184; only mandible: BMNHL 11.10.3.5, 25.10.2.4, 26.10.12.1, 8.7.6.20, 91.10.7.98, 99.3.1.13, USNM 198637, 255959, 255961, 255962; only skull: BMNHL 23.9.1.39, 92.1.1.4, USNM 84103, 255958, 255963, 395249, 573034.

M. marmota

BMNHL 1087.a, 19.7.7.2363, 19.7.7.2859, 2.8.4.30, 2.8.4.31, 2.8.4.32, 2.8.4.33, 59.9.6.36 (or 1087.c), 7.1.1.131, 7.1.1.195, 7.4.19.1, 8.8.10.145, 8.8.10.63, 8.8.10.65, USNM 14336, 115219, 115220, 115221, 115222, MSNM Ma 4532, 6085, 6103, DBA UMR three specimens not in catalogue, SC 160, 173, 178, 182, 159(II), 175(I); only mandible: BMNHL 1087.b, 55.12.24.124, MSNM Ma 4501, 4799, 6084, 6104, PNGP 1 specimen not in catalogue, SC 6, 12, 15, 17, 32, 39, 40, 45, 158, 161, 164, 165, 166, 167, 168, 171, 149, 159(I), 21B, 25B, 26B, 29B, 2B (A1/2), 34B, 35B, 36B, 38B, A1/1 or B41, A7; only skull: BMNHL 8.8.10.64, PNGP 2 specimens not in catalogue, USNM 153386, DBA UMR 2 specimens not in catalogue, SC 175(II).

M. monax

BMNHL 19.7.7.2552, 1989.337, 1991.119, 36.11.6.30, 36.11.6.31, 36.11.6.34, 36.11.6.35, 592.b, 592.c, 592.d (or 51.8.16.19, 592.e, 6.1.6.6, MSNM Ma 4550, USNM 23033, 25184, 35361, 43560, 53920, 67692, 67693, 68717, 71074, 72186, 72187, 77142, 77143, 77924, 78354, 78355, 78356, 78357, 78358, 96140, 96574, 101295, 174594, 177740, 186521, 191345, 202785, 203532, 227255, 227256, 228929, 233345, 234703, 236424, 242724, 243073, 243949, 244482, 247013, 259345, 283359, 291554, 291786, 291787, 337132, 347745, 347746, 347752, 396279, 564087; only mandible: BMNHL 592.a (or 43.9.14.9), 36.11.6.32, USNM 243607, 293895; only skull: USNM 58695, 78360, 81901, 170740, 202786, 207198, 228524, 233348, 245442, 249883, 564086.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cardini, A., O’Higgins, P. Post-natal ontogeny of the mandible and ventral cranium in Marmota species (Rodentia, Sciuridae): allometry and phylogeny. Zoomorphology 124, 189–203 (2005). https://doi.org/10.1007/s00435-005-0008-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00435-005-0008-3

Keywords

Search

Navigation