期刊论文详细信息
BMC Evolutionary Biology
Growth in fossil and extant deer and implications for body size and life history evolution
Marcelo R Sánchez-Villagra6  Nigel T Monaghan2  Gertrud E Rössner7  Margaretha AJ Schlingemann1  John de Vos3  Concepcion Azorit4  Adrian M Lister5  Torsten M Scheyer6  Christian Kolb6 
[1]Department of Integrative Zoology, IBL, Leiden University, Sylviusweg 72, RA Leiden, 2300, The Netherlands
[2]National Museum of Ireland-Natural History, Merrion Street, Dublin 2, Ireland
[3]Naturalis Biodiversity Center, Postbus 9517, RA Leiden, 2300, The Netherlands
[4]Department of Animal and Vegetal Biology and Ecology, Faculty of Experimental Sciences, University of Jaén, Jaén 23071, Spain
[5]Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
[6]Paläontologisches Institut und Museum der Universität Zürich, Karl Schmid-Strasse 4, Zürich, CH-8006, Switzerland
[7]Bayerische Staatssammlung für Paläontologie und Geologie, Richard-Wagner-Strasse 10, München, D-80333, Germany
关键词: Skeletal maturity;    Longevity;    Growth rates;    Cementum analysis;    Bone histology;    Megaloceros;    Candiacervus;    Cervidae;    Pleistocene;    Island evolution;   
Others  :  1129196
DOI  :  10.1186/s12862-015-0295-3
 received in 2014-07-22, accepted in 2015-01-27,  发布年份 2015
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【 摘 要 】

Background

Body size variation within clades of mammals is widespread, but the developmental and life-history mechanisms by which this variation is achieved are poorly understood, especially in extinct forms. An illustrative case study is that of the dwarfed morphotypes of Candiacervus from the Pleistocene of Crete versus the giant deer Megaloceros giganteus, both in a clade together with Dama dama among extant species. Histological analyses of long bones and teeth in a phylogenetic context have been shown to provide reliable estimates of growth and life history patterns in extant and extinct mammals.

Results

Similarity of bone tissue types across the eight species examined indicates a comparable mode of growth in deer, with long bones mainly possessing primary plexiform fibrolamellar bone. Low absolute growth rates characterize dwarf Candiacervus sp. II and C. ropalophorus compared to Megaloceros giganteus displaying high rates, whereas Dama dama is characterized by intermediate to low growth rates. The lowest recorded rates are those of the Miocene small stem cervid Procervulus praelucidus. Skeletal maturity estimates indicate late attainment in sampled Candiacervus and Procervulus praelucidus. Tooth cementum analysis of first molars of two senile Megaloceros giganteus specimens revealed ages of 16 and 19 years whereas two old dwarf Candiacervus specimens gave ages of 12 and 18 years.

Conclusions

There is a rich histological record of growth across deer species recorded in long bones and teeth, which can be used to understand ontogenetic patterns within species and phylogenetic ones across species. Growth rates sensu Sander & Tückmantel plotted against the anteroposterior bone diameter as a proxy for body mass indicate three groups: one with high growth rates including Megaloceros, Cervus, Alces, and Dama; an intermediate group with Capreolus and Muntiacus; and a group showing low growth rates, including dwarf Candiacervus and Procervulus. Dwarf Candiacervus, in an allometric context, show an extended lifespan compared to other deer of similar body size such as Mazama which has a maximum longevity of 12 years in the wild. Comparison with other clades of mammals reveals that changes in size and life history in evolution have occurred in parallel, with various modes of skeletal tissue modification.

【 授权许可】

   
2015 Kolb et al.; licensee BioMed Central.

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【 参考文献 】
  • [1]Foster JB: Evolution of mammals on islands. Nature 1964, 202:234-5.
  • [2]Lomolino MV: Body size of mammals on islands: the island rule reexamined. Am. Nat. 1985, 125:310-6.
  • [3]Lomolino MV, van der Geer AA, Lyras GA, Palombo MR, Sax DF, Rozzi R: Of mice and mammoths: generality and antiquity of the island rule. J Biogeogr 2013, 40:1427-39.
  • [4]Lister AM: Rapid dwarfing of red deer on jersey in the last interglacial. Nature 1989, 342:539-42.
  • [5]van der Geer A, Lyras G, de Vos J, Dermitzakis M: Evolution of Island Mammals. Adaptation and Extinction of Placental Mammals on Islands. Sussex, Wiley-Blackwell; 2010.
  • [6]Quintana J, Köhler M, Moyà-Solà S. Nuragulus rex, gen. et sp. nov., an endemic insular giant rabbit from the Miocene of Minorca (Balearic Islands). J Vertebr Paleontol. 2011;31(2):231–40.
  • [7]Palkovacs EP: Explaining adaptive shifts in body size on islands: a life history approach. Oikos 2003, 103:37-44.
  • [8]Lomolino MV, Sax DF, Palombo MR, van der Geer A: Of mice and mammoths: evaluations of causal explanations for body size evolution in insular mammals. J Biogeogr 2012, 39:842-54.
  • [9]Raia P, Meiri S: The island rule in large mammals: paleontology meets ecology. Evolution 2006, 60:1731-42.
  • [10]Sander PM, Andrassy P: Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: what do they tell us about dinosaur physiology? Palaeontogr Abt A 2006, 277:143-59.
  • [11]Sander PM, Christian A, Clauss M, Fechner R, Gee CT, Griebeler E-M, et al.: Biology of the sauropod dinosaurs: the evolution of gigantism. Biol Rev 2011, 86(1):117-55.
  • [12]Erickson GM, Curry Rogers K, Yerby SA: Dinosaurian growth patterns and rapid avian growth rates. Nature 2001, 412:429-33.
  • [13]Erickson GM, Makovicky PJ, Currie PJ, Norell MA, Yerby SA, Brochu CA: Gigantism and comparative life history parameters of tyrannosaurid dinosaurs. Nature 2004, 430:772-5.
  • [14]Chinsamy-Turan A (ed.): Forerunners of Mammals:Rradiation, Histology, Biology. Indiana: Indiana University Press;2012.
  • [15]Huttenlocker AK, Botha-Brink J: Bone microstructure and the evolution of growth patterns in Permo-Triassic therocephalians (Amniota, Therapsida) of South Africa. PeerJ 2014, 2:e325.
  • [16]de Vos J: The endemic Pleistocene deer of Crete. P K Ned Akad B 1979, 82(1):59-90.
  • [17]de Vos J: The Endemic Pleistocene Deer of Crete. North-Holland Publishing Company, Amsterdam; 1984.
  • [18]Vislobokova IA: Giant deer: origin, evolution, role in the biosphere. Paleontol J 2012, 46(7):643-775.
  • [19]Vislobokova IA: Morphology, taxonomy, and phylogeny of megacerines (Megacerini, Cervidae, Artiodactyla). Palaeontol J 2013, 47(8):833-950.
  • [20]Lister AM, Edwards CJ, Nock DAW, Bunce M, van Pijlen IA, Bradley DG, et al.: The phylogenetic position of the 'giant deer' Megaloceros giganteus. Nature 2005, 438(7069):850-3.
  • [21]Sickenberg O: Eine Säugetierfauna des tieferen Biharium aus dem Becken von Megalopolis (Peloponnes, Griechenland). Annales Géologiques des Pays Helléniques 1975, 27:25-73.
  • [22]Gould GC, MacFadden BJ: Gigantism, dwarfism, and Cope’s rule: “Nothing in evolution makes sense without a phylogeny”. B Am Mus Nat Hist 2004, 285:219-37.
  • [23]de Vos J: Pleistocene deer fauna in Crete: its adaptive radiation and extinction. Tropics 2000, 10(1):125-34.
  • [24]de Vos J, Van der Geer A: Major patterns and processes in biodiversity: taxonomic diversity on islands explained in terms of sympatric speciation. In World Islands in Prehistory, International Insular Investigations, V Deia International Conference of Prehistory. Edited by WW H, EJ A. British Archaeological Reports International Series, Oxford; 2002:395-405.
  • [25]Chritz KL, Dyke GJ, Zazzo A, Lister AM, Monaghan NT, Sigwart JD: Palaeobiology of an extinct Ice Age mammal: Stable isotope and cementum analysis of giant deer teeth. Palaeogeogr Palaeocl 2009, 282(1–4):133-44.
  • [26]Gould SJ: Positive allometry in antlers of the "Irish Elk", Megaloceros giganteus. Nature 1973, 244:375-6.
  • [27]Woodman PC, McCarthy M, Monaghan NT: The Irish Quaternary fauna project. Quaternary Sci Rev 1997, 16:129-59.
  • [28]Hughes S, Hayden TJ, Douady CJ, Tougard C, Germonpré M, Stuart A, et al.: Molecular phylogeny of the extinct giant deer, Megaloceros giganteus. Mol Phylogenet Evol 2006, 40:285-91.
  • [29]Rössner GE: Odontologische und schädelanatomische Untersuchungen an Procervulus (Cervidae, Mammalia). Münchner Geowissenschaftliche Abhandlungen (A) 1995, 29:1-128.
  • [30]McElligott AG, Mattiangeli V, Mattiello S, Verga M, Reynolds CA, Hayden TJ: Fighting tactics of fallow bucks (Dama dama, Cervidae): Reducing the risks of serious conflict. Ethology 1998, 104:789-803.
  • [31]Habermehl K-H: Altersbestimmung bei Wild- und Pelztieren - Möglichkeiten und Methoden - Ein praktischer Leitfaden für Jäger, Biologen und Tierärzte. Hamburg, Berlin, Verlag Paul Parey; 1985.
  • [32]Pei K: Post-natal growth of the Formosan Reeves' Muntjac Muntiacus reevesi micrurus. Zool Stud 1996, 35:111-7.
  • [33]Palombo MR, Köhler M, Moya-Sola S, Giovinazzo C: Brain versus body mass in endemic ruminant artiodactyls: a case studied of Myotragus balearicus and smallest Candiacervus species from Mediterranean Islands. Quatern Int 2008, 182:160-83.
  • [34]Gilbert C, Ropique A, Hassanin A: Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): Systematics, morphology, and biogeography. Mol Phylogenet Evol 2006, 40:101-17.
  • [35]Hassanin A, Delsuc F, Ropiquet A, Hammer C, van Vuuren BJ, Matthee C, et al.: Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. C R Biol 2012, 335:32-50.
  • [36]Stearns SC: The Evolution of Life Histories. Oxford University Press, Oxford; 1992.
  • [37]Garcia-Martinez R, Marin-Moratalla N, Jordana X, Köhler M: The ontogeny of bone growth in two species of dormice: reconstructing life history traits. C R Palevol 2011, 10(5–6):489-98.
  • [38]Chinsamy-Turan A. Microstructure of bones and teeth of nonmammalian therapsids. In Forerunners of Mammals: Radiation, Histology, Biology. Edited by Chinsamy-Turan A. Indiana: Indiana University Press; 2012;65–88.
  • [39]Marin-Moratalla N, Jordana X, Köhler M: Bone histology as an approach to providing data on certain key life history traits in mammals: implications for conservation biology. Mamm Biol 2013, 78:422-9.
  • [40]Castanet J, Croci S, Aujard F, Perret M, Cubo J, de Margerie E: Lines of arrested growth in bone and age estimation in a small primate: Microcebus murinus. J Zool 2004, 263:31-9.
  • [41]Köhler M, Marín-Moratalla N, Jordana X, Aanes R: Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 2012, 487:358-61.
  • [42]Woodward HN, Padian K, Lee AH. Skeletochronology. In Histology of Fossil Tetrapods - Advancing Methods, Analysis and Interpretation. Edited by Padian K, Lamm E-T. Berkeley, Los Angeles, London: University of California Press; 2013: 195–215.
  • [43]Klevezal GA: Recording Structures of Mammals. Determination of Age and Reconstruction of Life History. Rotterdam/Brookfield, A.A.Balkema; 1996.
  • [44]Azorit C, Munoz-Cobo J, Hervas J, Analla M: Aging through growth marks in teeth of Spanish red deer. Wildl Soc Bull 2004, 32(3):702-10.
  • [45]Azorit C, Analla M, Hervas J, Carrasco R, Munoz-Cobo J: Growth marks observation: preferential techniques and teeth for ageing of Spanish red deer (Cervus elaphus hispanicus). Anat Histol Embryol-J Vet Med Ser C 2002, 31(5):303-7.
  • [46]Köhler M, Moyà-Solà S: Physiological and life history strategies of a fossil large mammal in a resource-limited environment. P Natl Acad Sci USA 2009, 106(48):20354-8.
  • [47]Calder WA: Size, Function, and Life History. Harvard University Press, Cambridge, Massachusetts, London; 1984.
  • [48]Case TJ: On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q Rev Biol 1978, 53(3):243-82.
  • [49]Schmidt-Nielsen K: Scaling: Why is Animal Size so Important?. Cambridge University Press, Cambridge & New York; 1984.
  • [50]Stein K, Sander M: Histological core drilling: a less destrcutive method for studying bone histology. In Methods in Fossil Preparation: Proceedings of the First Annual Fossil Preparation and Collections Symposium. Petrified Forest National Park, Petrified Forest; 2009:69-80.
  • [51]Sander PM, Tückmantel C: Bone lamina thickness, bone apposition rates, and age estimates in sauropod humeri and femora. Palaeontol Z 2003, 77(1):161-72.
  • [52]Hammer Ø, Harper DAT, Ryan PD. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 2001;4(1): 9. http://palaeoelectronica.org/2001_1/past/issue1_01.htm
  • [53]Ponton F, Elzanowski A, Castanet J, Chinsamy-Turan A, Margerie E, de Ricqlès A, et al.: Variation of the outer circumferential layer in the limb bones of birds. Acta Ornithol 2004, 39(2):21-4.
  • [54]Horner JR, Ricqlès AJD, Padian K: Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 1999, 25:295-304.
  • [55]van der Geer A, de Vos J, Lyras G, Dermitzakis M: New data on the Pleistocene Cretan deer Candiacervus sp. II (Cervinae, Mammalia). Cour Forsch Senck 2006, 256:131-7.
  • [56]Stein K, Prondvai E. Rethinking the nature of fibrolamellar bone: an integrative biological revision of sauropod plexiform bone formation. Biol Rev. 2013;1–24
  • [57]Francillon-Vieillot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire JY, et al. Microstructure and mineralization of vertebrate skeletal tissues. In Skeletal Biomineralization: Patterns, Processes and Evolutionary Trends. Edited by Carter JG. New York: Van Nostrand Reinhold; 1990: 471–530.
  • [58]Enlow DH, Brown SO: A comparative histological study of fossil and recent bone tissues. Part III. Tex J Sci 1958, 10:187-230.
  • [59]Horner JR, Padian K: Age and growth dynamics of Tyrannosaurus rex. P Roy Soc Lond B Bio 2004, 271:1875-80.
  • [60]de Ricqlès A, Meunier FJ, Castanet J, Francillon-Vieillot H. Comparative microstructure of bone. In Bone Volume 3: Bone Matrix and Bone Specific Products. Edited by Hall BK. Boca Raton: CRC Press; 1991;1–78.
  • [61]van der Geer A, Dermitzakis M, de Vos J: Relative growth of the metapodials in a juvenile island deer: Candiacervus (Mammalia, Cervidae) from the Pleistocene of Crete. Hell J Geosc 2006, 41:119-25.
  • [62]van der Geer A, Lyras GA, MacPhee RDE, Lomolino MV, Drinia H: Mortality in a predator-free insular environment: the dwarf deer of Crete. Am Mus Novit 2014, 3807:1-26.
  • [63]Tacutu R, Craig T, Budovsky A, Wuttke D, Lehmann G, Taranukha D, et al.: Human ageing genomic resources: integrated databases and tools for the biology and genetics of ageing. Nucleic Acids Res 2013, 41(D1):D1027-33.
  • [64]Huttenlocker AK, Woodward HN, Hall BK. The biology of bone. In Histology of Fossil Tetrapods - Advancing Methods, Analysis and Interpretation. Edited by Padian K, Lamm E-T. Berkeley, Los Angeles, London: University of California Press; 2013: 13–34.
  • [65]Austad SN, Fischer KE: Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. J Gerontol 1991, 46(2):B47-53.
  • [66]McNab B: Resource use and the survival of land and freshwater vertebrates on oceanic islands. Am Nat 1994, 144:643-60.
  • [67]McNab BK: Minimizing energy expenditure facilitates vertebrate persistence on oceanic islands. Ecol Lett 2002, 5:693-704.
  • [68]McNab BK: Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 2010, 164:13-23.
  • [69]Aaris-Sorensen K, Liljegren R: Late Pleistocene remains of giant deer (Megaloceros giganteus Blumenbach) in Scandinavia: chronology and environment. Boreas 2004, 33:61-73.
  • [70]Stearns SC: Life history evolution: successes, limitations, and prospects. Naturwissenschaften 2000, 87:476-86.
  • [71]Curtin AJ, Macdowell AA, Schaible EG, Roth L: Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation X-ray microtomography. J Vertebr Paleontol 2012, 32(4):939-55.
  • [72]Raia P, Barbera C, Conte M: The fast life of a dwarfed giant. Evol Ecol 2003, 17(3):293-312.
  • [73]O'Leary, MA; Kaufman SG. MorphoBank 3.0: Web application for morphological phylogenetics and taxonomy. 2012; http://www.morphobank.org.
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