Heterochrony and post-natal growth in mammals - an examination of growth plates in limbs

Journal of Evolutionary Biology

Volumn 27, Issue 1, 2014, Pages 98-115

  Geiger, M ^a   Forasiepi, A M ^b   Koyabu, D ^c   Sanchez Villagra M R ^a  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Growth plate closure; Heterochrony; Limbs; Mammals

Indexed keywords

BIOLOGICAL DEVELOPMENT; BONE; DIACHRONISM; GROWTH RATE; HABITAT STRUCTURE; LIMB; MAMMAL; PHYLOGENETICS;

EUTHERIA; MAMMALIA; METATHERIA; MONOTREMATA;

ANIMAL; COMPARATIVE STUDY; GROWTH PLATE; GROWTH, DEVELOPMENT AND AGING; LIMB; LOCOMOTION; MAMMAL;

ANIMALS; EXTREMITIES; GROWTH PLATE; LOCOMOTION; MAMMALS;

EID: 84891631238     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12279     Document Type: Article

References (88)

1. Anders, U., von Koenigswald, W., Ruf, I. & Smith, B.H. 2011. Generalized individual dental age stages for fossil and extant placental mammals. Paläontol. Z. 85: 321-339.
2. Arkin, A.M. & Katz, J.F. 1956. The effects of pressure on epiphyseal growth - the mechanism of plasticity of growing bone. J. Bone Joint Surg. Am. 38: 1056-1076.
3. Asher, R.J. 2007. A web-database of mammalian morphology and a reanalysis of placental phylogeny. BMC Evol. Biol. 7: 108.
4. Asher, R.J. & Helgen, K.M. 2010. Nomenclature and placental mammal phylogeny. BMC Evol. Biol. 10: 102.
5. Asher, R.J., Bennett, N. & Lehmann, T. 2009. The new framework for understanding placental mammal evolution. BioEssays 31: 853-864.
6. Benjamini, Y. & Hochberg, Y. 1995. Controlling the False Discovery Rate - a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57: 289-300.
7. Bennett, C.V. & Goswami, A. 2013. Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biol. 11: 52.
8. Blanga-Kanfi, S., Miranda, H., Penn, O., Pupko, T., DeBry, R.W. & Huchon, D. 2009. Rodent phylogeny revised: analysis of six nuclear genes from all major rodent clades. BMC Evol. Biol. 9: 71.
9. Breburda, E., Wirth, T., Leiser, R. & Griss, P. 2001. The influence of intermittent external dynamic pressure and tension forces on the healing of an epiphyseal fracture. Arch. Orthop. Traum. Surg. 121: 443-449.
10. Bull, G. & Payne, S. 1982. Tooth eruption and epiphysial fusion in pigs and wild boar. In: Aging and Sexing Animal Bones from Archaeological Sites (B. Wislon, C. Grigson, S. Payne, eds), pp. 55-71. British Archaeological Reports, Oxford.
11. Carter, D.R. & Wong, M. 1988. The role of mechanical loading histories in the development of diarthrodial joints. J. Orthop. Res. 6: 804-816.
12. Carter, D.R., Wong, M. & Orr, T.E. 1991. Musculoskeletal ontogeny, phylogeny, and functional adaptation. J. Biomech. 24: 3-16.
13. Carter, D.R., Mikić, B. & Padian, K. 1998. Epigenetic mechanical factors in the evolution of long bone epiphyses. Zool. J. Linn. Soc. 123: 163-178.
14. Cheverud, J.M. 1981. Epiphyseal union and dental eruption in Macaca mulatta. Am. J. Phys. Anthropol. 56: 157-167.
15. Ciancio, M.R., Castro, M.C., Galliari, F.C., Carlini, A.A. & Asher, R.J. 2012. Evolutionary implications of dental eruption in Dasypus (Xenarthra). J. Mamm. Evol. 19: 1-8.
16. Curran-Everett, D. 2000. Multiple comparisons: philosophies and illustrations. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279: R1-R8.
17. Dawson, A.B. 1925. The age order of epiphyseal union in the long bones of the albino rat. Anat. Rec. 31: 1-17.
18. Dawson, A.B. 1934. Additional evidence of the failure of epiphyseal union in the skeleton of the rat studies on wild and captive gray Norway rats. Anat. Rec. 60: 501-511.
19. Dawson, A.B. 1935. The sequence of epiphyseal union in the skeleton of the mouse with special reference to the phenomenon of 'lapsed' union. Anat. Rec. 63: 93-99.
20. Fabre, P.H., Hautier, L., Dimitrov, D. & Douzery, E.J.P. 2012. A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol. Biol. 12: 88.
21. Farnum, C.E. 2007. Postnatal growth of fins and limbs through endochondral ossification. In: Fins into Limbs: Evolution, Development, and Transformation (B.K. Hall, ed.), pp. 118-151. University of Chicago Press, Chicago, IL and London.
22. Field, A.P. 2005. Kendall's coefficient of concordance. In: Encyclopedia of Statistics in Behavioral Science, vol. 2 (B.S. Everitt, D.C. Howell, eds), pp. 1010-1011. Chichester, Wiley VCH.
23. Germain, D. & Laurin, M. 2009. Evolution of ossification sequences in salamanders and urodele origins assessed through event-pairing and new methods. Evol. Dev. 11: 170-190.
24. Haines, R.W. 1942. The evolution of epiphyses and of endochondral bone. Biol. Rev. 17: 267-292.
25. Hall, B.K. 2005. Bones and Cartilage: Developmental and Evolutionary Skeletal Biology. Elsevier Academic Press, Amsterdam.
26. Hallström, B.M., Schneider, A., Zoller, S. & Janke, A. 2011. A genomic approach to examine the complex evolution of laurasiatherian mammals. PLoS ONE 6: e28199.
27. Harrison, L.B. & Larsson, H.C. 2008. Estimating evolution of temporal sequence changes: a practical approach to inferring ancestral developmental sequences and sequence heterochrony. Syst. Biol. 57: 378-387.
28. Hofer, H., Schultz, A.H. & Starck, D. 1956. Primatologia: Handbuch der Primatenkunde - Handbook of primatology - Manuel de primatologie. S. Karger, Basel.
29. Hurum, J.H. & Kielan-Jaworowska, Z. 2008. Postcranial skeleton of a Cretaceous multituberculate mammal Catopsbaatar. Acta Palaeontol. Pol. 53: 545-566.
30. Jeffery, J.E., Bininda-Emonds, O.R.P., Coates, M.I. & Richardson, M.K. 2005. A new technique for identifying sequence heterochrony. Syst. Biol. 54: 230-240.
31. Jenkins, F.A. Jr & Schaff, C.R. 1988. The Early Cretaceous mammal Gobiconodon (Mammalia, Triconodonta) from the Cloverly Formation in Montana. J. Vertebr. Paleontol. 8: 1-24.
32. Ji, Q., Luo, Z.X. & Ji, S.A. 1999. A Chinese triconodont mammal and mosaic evolution of the mammalian skeleton. Nature 398: 326-330.
33. Kendall, M.G. 1955. Rank Correlation Methods, 2nd edn. Griffin, London.
34. Kielan-Jaworowska, Z. & Gambaryan, P.P. 1994. Postcranial Anatomy and Habits of Asian Multituberculate Mammals. Scandinavian University Press, Oslo.
35. King, S.J., Godfrey, L.R. & Simons, E.L. 2001. Adaptive and phylogenetic significance of ontogenetic sequences in Archaeolemur, subfossil lemur from Madagascar. J. Hum. Evol. 41: 545-576.
36. Koch, W. 1935. The age order of epiphyseal union in the skeleton of the European bison (Bos bonasus L.). Anat. Rec. 61: 371-376.
37. Koyabu, D., Endo, H., Mitgutsch, C., Suwa, G., Catania, K.C., Zollikofer, C.P.E. et al. 2011. Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals. EvoDevo 2: 1-19.
38. Krebs, B. 1991. Das Skelett von Henkelotherium guimarotae gen. et sp. nov. (Eupantotheria, Mammalia) aus dem Oberen Jura von Portugal. Berliner geowiss. Abh, 133: 1-110.
39. Laurin, M. & Germain, D. 2011. Developmental characters in phylogenetic inference and their absolute timing information. Syst. Biol. 60: 630-644.
40. Li, G. & Luo, Z.-X. 2006. A Cretaceous symmetrodont therian with some monotreme-like postcranial features. Nature 439: 195-200.
41. Lowrance, E.W. 1949. Variability and growth of the opossum skeleton. J. Morphol. 85: 569-593.
42. Luo, Z.-X. & Ji, Q. 2005. New study on dental and skeletal features of the Cretaceous "symmetrodontan" mammal Zhangheotherium. J. Mamm. Evol. 12: 337-357.
43. Luo, Z.-X., Chen, P., Li, G. & Chen, M. 2007. A new eutriconodont mammal and evolutionary development in early mammals. Nature 446: 288-293.
44. Maddison, W.P. & Maddison, D.R. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. http://mesquiteproject.org.
45. Martin, T. 2005. Postcranial anatomy of Haldanodon exspectatus (Mammalia, Docodonta) from the Late Jurassic (Kimmeridgian) of Portugal and its bearing for mammalian evolution. Zool. J. Linn. Soc. 145: 219-248.
46. Meng, J., Hu, Y., Wang, Y., Wang, X. & Li, C. 2006. A Mesozoic gliding mammal from northeastern China. Nature 444: 889-893.
47. Meredith, R.W., Janečka, J.E., Gatesy, J., Ryder, O.A., Fisher, C.A., Teeling, E.C. et al. 2011. Impacts of the Cretaceous terrestrial revolution and KPg extinction on mammal diversification. Science 334: 521-524.
48. Meslin, C., Mugnier, S., Callebaut, I., Laurin, M., Pascal, G., Poupon, A. et al. 2012. Evolution of genes involved in gamete interaction: evidence for positive selection, duplications and losses in vertebrates. PLoS ONE 7: e44548.
49. Midford, P.E., Garland, T. Jr & Maddison, W.P. 2011. PDAP Package of Mesquite. Version 1.16. http://mesquiteproject.org/pdap_mesquite/.
50. Miller, W., Drautz, D.I., Janečka, J.E., Lesk, A.M., Ratan, A., Tomsho, L.P. et al. 2009. The mitochondrial genome sequence of the Tasmanian tiger (Thylacinus cynocephalus). Genome Res. 19: 213-220.
51. Mullender, M.G., Huiskes, R., Versleyen, H. & Buma, P. 1996. Osteocyte density and histomorphometric parameters in cancellous bone of the proximal femur in five mammalian species. J. Orthop. Res. 14: 972-979.
52. Murphy, W.J., Pringle, T.H., Crider, T.A., Springer, M.S. & Miller, W. 2007. Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res. 17: 413-421.
53. van Nievelt, A.F.H. & Smith, K.K. 2005. To replace or not to replace: the significance of reduced functional tooth replacement in marsupial and placental mammals. Paleobiology 31: 324-346.
54. Nilsson, O. & Baron, J. 2004. Fundamental limits on longitudinal bone growth: growth plate senescence and epiphyseal fusion. Trends Endocrinol. Metab. 15: 370-374.
55. Nishihara, H., Maruyama, S. & Okada, N. 2009. Retroposon analysis and recent geological data suggest near-simultaneous divergence of the three superorders of mammals. Proc. Natl. Acad. Sci. USA 106: 5235-5240.
56. Nowak, R.M. 1999. Walker's Mammals of the World, 6th edn. Johns Hopkins University Press, Baltimore, MD.
57. O'Leary, M.A., Bloch, J.I., Flynn, J.J., Gaudin, T.J., Giallombardo, A., Giannini, N.P. et al. 2013. The placental mammal ancestor and the post-K-Pg radiation of placentals. Science 339: 662-667.
58. Parfitt, A.M. 2002. Misconceptions (1): epiphyseal fusion causes cessation of growth. Bone 30: 337-339.
59. Parsons, F.G. 1904. Observations on traction epiphyses. J. Anat. Physiol. 38: 248-258.
60. Perelman, P., Johnson, W.E., Roos, C., Seuánez, H.N., Horvath, J.E., Moreira, M.A.M. et al. 2011. A molecular phylogeny of living primates. PLoS Genet. 7: e1001342.
61. Polly, D.P. 2007. Limbs in mammalian evolution. In: Fins into Limbs: Evolution, Development, and Transformation (B.K. Hall, ed.), pp. 245-268. University of Chicago Press, Chicago, IL and London.
62. Porter, R.W. 1978. The effect of tension across a growing epiphysis. J. Bone Joint Surg. Br. 60: 252-255.
63. Prasad, A.B., Allard, M.W., Program, N.C.S. & Green, E.D. 2008. Confirming the phylogeny of mammals by use of large comparative sequence data sets. Mol. Biol. Evol. 25: 1795-1808.
64. Raff, R.A. & Wray, G.A. 1989. Heterochrony - developmental mechanisms and evolutionary results. J. Evol. Biol. 2: 409-434.
65. dos Reis, M., Inoue, J., Hasegawa, M., Asher, R.J., Donoghue, P.C.J. & Yang, Z.H. 2012. Phylogenomic datasets provide both precision and accuracy in estimating the timescale of placental mammal phylogeny. Proc. R. Soc. Biol. Sci. Ser. B 279: 3491-3500.
66. Richardson, M.K., Gobes, S.M., van Leeuwen, A.C., Polman, J.A., Pieau, C. & Sánchez-Villagra, M.R. 2009. Heterochrony in limb evolution: developmental mechanisms and natural selection. J. Exp. Biol. 312: 639-664.
67. Roach, H.I., Mehta, G., Oreffo, R.O.C., Clarke, N.M.P. & Cooper, C. 2003. Temporal analysis of rat growth plates: cessation of growth with age despite presence of a physis. J. Histochem. Cytochem. 51: 373-383.
68. Rougier, G.W. 1993. Vincelestes neuquenianus Bonaparte (Mammalia, Theria), un primitivo mammífero del Cretácico Inferior de la Cuenca Neuquina. Ph.D. Thesis, Universidad Nacional de Buenos Aires, Buenos Aires.
69. Samuels, J.X. & Van Valkenburgh, B. 2008. Skeletal indicators of locomotor adaptations in living and extinct rodents. J. Morphol. 269: 1387-1411.
70. Sánchez-Villagra, M.R. 2002. Comparative patterns of postcranial ontogeny in therian mammals: an analysis of relative timing of ossification events. J. Exp. Zool. 294: 264-273.
71. Sánchez-Villagra, M.R. 2013. Why are there fewer marsupials than placentals? On the relevance of geography and physiology in mammalian diversity and disparity evolutionary patterns. J. Mamm. Evol. 20: 279-290.
72. Schmid, E. 1972. Atlas of Animal Bones - For Prehistorians, Archaeologists and Quaternary Geologists; Knochenatlas - Für Prähistoriker, Archäologen und Qartärgeologen. Elsevier Publishing Company, Amsterdam.
73. Sears, K.E. 2004. Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58: 2353-2370.
74. Sears, K.E. 2009. Differences in the timing of prechondrogenic limb development in mammals: the marsupial-placental dichotomy resolved. Evolution 63: 2193-2200.
75. Sears, K.E., Doroba, C.K., Cao, X., Xie, D. & Zhong, S. 2012. Molecular determinants of marsupial limb integration and constraint. In: From Clone to Bone: The Synergy of Morphological and Molecular Tools in Palaeobiology (R.J. Asher & J. Müller, eds), pp. 257-278. Cambridge studies in morphology and molecules. Cambridge University Press, Cambridge.
76. Serrano, E., Sarasa, M., Pérez, J.M. & Gállego, L. 2011. Patterns of epiphyseal fusion in the appendicular skeleton of the Iberian wild goat Capra pyrenaica, and comparisons with other Artiodactyla. Mamm. Biol. 76: 97-100.
77. Shea, B.T. 1993. Bone growth and primate evolution. In: Bone, Vol. 7, Bone Growth - B (B.K. Hall, ed.), pp. 133-157. CRC Press, Boca Raton, FL.
78. Shigehara, N. 1980. Epiphyseal union, tooth eruption, and sexual maturation in the common tree shrew, with special reference to its systematic problem. Primates 21: 1-19.
79. Stevenson, P.H. 1924. Age order of epiphyseal union in man. Am. J. Phys. Anthropol. 7: 53-93.
80. Tappen, N.C. & Severson, A. 1971. Sequence of eruption of permanent teeth and epiphyseal union in New World monkeys. Folia Primatol. 15: 293-312.
81. Todd, T.W. 1930a. The anatomical features of epiphysial union. Child Dev. 1: 186-194.
82. Todd, T.W. 1930b. Comparative youth: the physical aspect. Child Dev. 1: 79-89.
83. Todd, T.W. & Todd, A.W. 1938. The epiphysial union pattern of the ungulates with a note on Sirenia. Am. J. Anat. 63: 1-36.
84. Walter, L.R. 1985. The formation of secondary centers of ossification in kannemeyeriid dicynodonts. J. Paleontol. 59: 1486-1488.
85. Washburn, S.L. 1946. The sequence of epiphysial union in the opossum. Anat. Rec. 95: 353-363.
86. Weisbecker, V., Goswami, A., Wroe, S. & Sánchez-Villagra, M.R. 2008. Ossification heterochrony in the therian postcranial skeleton and the marsupial-placental dichotomy. Evolution 62: 2027-2041.
87. Wilson, D.E. & Reeder, D.M. 2005. Mammal Species of the World. A Taxonomic and Geographic Reference, 3rd edn. Johns Hopkins University Press, Baltimore, Maryland.
88. Zhou, X.M., Xu, S.X., Xu, J.X., Chen, B.Y., Zhou, K.Y. & Yang, G. 2012. Phylogenomic analysis resolves the interordinal relationships and rapid diversification of the laurasiatherian mammals. Syst. Biol. 61: 150-164.