Developmental palaeontology in synapsids: The fossil record of ontogeny in mammals and their closest relatives

Proceedings of the Royal Society B: Biological Sciences

Volumn 277, Issue 1685, 2010, Pages 1139-1147

  Sánchez Villagra, Marcelo R ^a  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

Author keywords

Allometry; Growth; Heterochrony; Modularity; Paleohistology; Skeletochronology

Indexed keywords

ALLOMETRY; DENDROCHRONOLOGY; DEVELOPMENTAL BIOLOGY; EVOLUTIONARILY STABLE STRATEGY; FOSSIL RECORD; GENE EXPRESSION; GROWTH RATE; HISTOLOGY; LIFE HISTORY; LONGEVITY; MAMMAL; PALEONTOLOGY; PHENOTYPE; PHYLOGENETICS; REPTILE; SKELETAL REMAINS;

MALIA; MAMMALIA; PHYLO; SYNAPSIDA;

EID: 77951493470     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.2005     Document Type: Review

References (98)

1. Abdala, F. & Giannini, N. P. 2000 Gomphodont cynodonts of the Chañares Formation: The analysis of an ontogen- etic sequence. J. Vert. Paleontol. 20, 501-506. (doi:10. 1671/0272-4634(2000)020[0501:GCOTCA]2.0.CO;2)
2. Asher, R. J. & Lehmann, T. 2008 Dental eruption in afrotherian mammals. BMC Biol. 6, 14. (doi:10.1186/ 1741-7007-6-14)
3. Asher, R. J. & Olbricht, G. 2009 Dental ontogeny in Macro- scelides proboscideus (Afrotheria) and Erinaceus europaeus (Lipotyphla). J. Mamm. Evol. 16, 99-115. (doi:10. 1007/S10914-009-9105-9112)
4. Bakker, R. T. 1982 Juvenile-adult habitat shift in Permian fossil reptiles and amphibians. Science 217, 53-55. (doi:10.1126/science.217.4554.53)
5. Billet, G., de Muizon, C. & Mamani Quispe, B. 2008 Late Oligocene mesotheriids (Mammalia, Notoungulata) from Salla and Lacayani (Bolivia). Zool. J. Linn. Soc. 152, 153-200.
6. Brinkman, D. 1988 Size-independent criteria for estimating relative age in Ophiacodon and Dimetrodon (Reptilia, Pely- cosauria) from the Admiral and lower Belle Plains formations of west-central Texas. J. Vert. Paleontol. 8, 172-180.
7. Brown, P. et al. 2004 A new small-bodied hominin from the late Pleistocene of Flores, Indonesia. Nature 431, 1055-1061. (doi:10.1038/ nature02999)
8. Bryant, H. N. 1988 Delayed eruption of the deciduous upper canine in the sabretoothed carnivore Barbourofelis lovei (Carnivora, Nimravidae). J. Vert. Paleontol. 8, 295-306.
9. Burke, A. C., Nelson, C. E., Morgan, B. A. & Tabin, C. 1995 Hox genes and the evolution of vertebrate axial mor- phology. Development 212, 333-346.
10. Cartelle, C. & De Iuliis, G. 2006 Eremotherium laurillardi (Lund) (Xenarthra, Megatheriidae), the Panamerican giant ground sloth: taxonomic aspects of the ontogeny of skull and dentition. J. Syst. Palaeontol. 4, 199-209. (doi:10.1017/S1477201905001781)
11. Chinsamy,A.&Hurum,J.H. 2006Bonemicrostructureandgrowthpatternsofearlymammals.ActaPalaeontol.Pol.51, 325-338.(Pubitemid43757409)
12. Cifelli, R. L. & de Muizon, C. 1998 Tooth eruption and replacement pattern in early marsupials. Compt. Rend.l'A- cad. Sci. Sér. II, Sci.Terr. Planèt. 326, 215-220.
13. Clemens, W. A. & Lillegraven, J. A. 1986 New Late Cretac- eous, North American advanced therian mammals that fit neither the marsupial nor eutherian molds. Contrib. Geol. Univ. Wyom. Spec. Pap. 3, 55-85.
14. Croft, D. A. 2007 The middle Miocene (Laventan) Queb- rada Honda fauna, southern Bolivia, and a description of its notoungulates. Palaeontology 50, 277-303. (doi:10. 1111/j.1475-4983.2006.00610.x)
15. Dean, M. C. 2006 Tooth microstructure tracks the pace of human life-history evolution. Proc. R. Soc. B 273, 2799-2808. (doi:10.1098/rspb.2006. 3585)
16. Delfino, M. & Sánchez-Villagra, M. R. In press. A survey of the rock record of reptilian ontogeny. Sem. Cell Dev. Biol. (doi:10.1016/j. semcdb.2009.11.007)
17. de Ricqlès, A. 1972 Recherches paléohistologiques sur les os longs des Tétrapodes. III, Titanosuchiens Dinocéphales et Dicynodontes. Ann. Paléontol. (Vertébrés) 58, 17-60.
18. Donoghue, P. C. J. 2005 Saving the stem-group: a contradic- tion in terms. Paleobiology 31, 553-558.
19. Fisher, D. C. 2001 Season of death, growth rates, and life history of North American mammoths. In Proc. Int. Conf. Mammoth Site Studies (ed. D. West). University of Kansas Publications in Anthropology, 22, pp. 121-135.
20. Fox, D. L. & Fisher, D. C. 2001 Stable isotope ecology of a late Miocene population of Gomphotherium (Mammalia, Proboscidea) from Port of Entry Pit, Oklahoma: diet, climate and diagenesis. PALAIOS 16, 279-293.
21. Galis, F., van Dooren, T. J. M., Feuth, H., Ruinard, S., Witkam, A., Steigenga, M. J., Metz, J. A. J. & Wijnaendts, L. C. D. 2006 Extreme selection against homeotic transformations of cervical vertebrae in humans. Evolution 60, 2643-2654.
22. Gerber, S., Eble, G. J. & Neige, P. 2008 Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity. Evolution 62, 1450-1457. (doi:10.1111/j.1558-56462008.00370.x)
23. Gilbert, S. F & Epel, D. 2008 Ecological developmental biology. Sunderland, MA: Sinauer Associates.
24. Gingerich, P. D. et al. 2009 New protocetid whale from the middle Eocene of Pakistan. PLoS ONE 4, e4366. (doi:10.1371/joumal.pone.0004366)
25. Godfrey, L. R. & Sutherland, M. R. 1995 Flawed inference: why size-based tests of heterochronic processes do not work. J. Theor. Biol. 172, 43-61. (doi:10.1006/jtbi.l995. 0004)
26. Godfrey, L. R., Samonds, K. E., Wright, P. C. & King, S. J. 2005 Schultz's unruly rule: dental developmental sequences and schedules in smallbodied, folivorous lemurs. Folia Primatol. 76, 77-99. (doi:10.1159/ 000083615)
27. Gostling, N. J., Donoghue, P. C. J. & Bengtson, S. 2007 The earliest fossil embryos begin to mature. Evol. Dev. 9, 206-207.
28. Goswami, A. 2006 Cranial modularity shifts during mamma- lian evolution. Am. Nat. 168, 270-280. (doi:10.1086/ 505758)
29. Gould, S. J. 1977 Ontogeny and phylogeny. Cambridge, MA: Belknap Press.
30. Gruber, G. & Micklich, N. 2007 Messel-treasures of the Eocene. Darmstadt, Germany: Hessisches Landesmuseum.
31. Guenther, M. F. 2009 Influence of sequence heterochrony on hadrosaurid dinosaur postcranial development. Anat. Rec. 292, 1427-1441. (doi:10.1002/ar.20988)
32. Guthrie, R. D. 2003 Rapid body size decline in Alaskan Pleistocene horses before extinction. Nature 426, 169-171. (doi:10.1038/nature02098)
33. Hafner, J. C. & Hafner, M. S. 1988 Heterochrony in rodents. In Heterochrony in evolution: a multidisciplinary approach (ed. M. L. McKinney), pp. 217-235. New York, NY: Plenum Press.
34. Hall, B. K. 2005 Bones and cartilage. Amsterdam, The Netherlands: Elsevier Academic.
35. Hersch, A. H. 1934 Evolutionary relative growth in titanotheres. Am. Nat. 68, 537-561.
36. Hopson, J. A. & Rougier, G. W. 1993 Braincase structure in the oldest known skull of a therian mammal: implications for mammalian systematics and cranial evolution. Am. J. Sci. 293A, 268-299.
37. Jacob, T. et al. 2006 Pygmoid Australomelanesian Homo sapiens skeletal remains from Liang Bua, Flores. Proc. Natl; Acad. Sci. USA 103, 13421-13426. (doi:10.1073/ pnas.0605563103)
38. Kaiser, T. M. & Brinkmann, G. 2006 Measuring dental wear equilibriums. Palaeogeogr., Palaeoclim., Palaeoecol. 239, 221-240. (doi:10.1016/j.palaeo.2006.01.013)
39. Kangas, A. T., Evans, A. R., Thesleff, I. & Jernvall, J. 2004 Nonindependence of mammalian dental characters. Nature 432, 211-214. (doi:10.1038/nature02927)
40. Kavanagh, K. D., Evans, A. R. & Jernvall, J. 2007 Predicting evolutionary patterns of mammalian teeth from develop- ment. Nature 449, 427-433. (doi:10.1038/nature06153) (Pubitemid 47509546)
41. Kelley, J. 2002 Life history evolution in Miocene and extant apes. In Human evolution through developmental change (eds N. Minugh-Purvis & K. J. McNamara), pp. 223-248.Baltimore, MD: Johns Hopkins University Press.
42. Kemp, T S. 2005 The origin and evolution of mammals. Oxford, UK: Oxford University Press.
43. Kemp, T. S. 2007 The origin of higher taxa: macroevolution- ary processes, and the case of the mammals. Acta Zool. (Stockholm) 88, 3-22. (doi:10.1111/j.1463-6395.2007. 00248.x)
44. Kielan-Jaworowska, Z., Cifelli, R. L. & Luo, X. 2004 Mam- mals from the age of dinosaurs. Origins, evolution and structure. New York, NY: Columbia University Press.
45. King, S. J., Arrigo-Nelson, S. J., Pochron, S. T, Semprebon, G. M., Godfrey, L. R., Wright, P. C. & Jernvall, J. 2005 Dental senescence in a long-lived primate links infant survival to rainfall. Proc. Natl Acad. Sci. USA 102, 16 579-16 583. (doi:10.1073/pnas.0508377102)
46. Klingenberg, C. P. 1998 Heterochrony and allometry: The analysis of evolutionary change in ontogeny. Biol. Rev. 73, 79-123. (doi:10.1017/ S000632319800512X)
47. Klingenberg, C. P. 2008 Morphological integration and developmental modularity. Ann. Rev. Ecol. Syst. 39, 115-132.
48. Köhler, M. & Moyà-Solà, S. 2004 Reduction of brain and sense organs in the fossil insular bovid Myotragus. Brain Behav. Evol 63, 125-140. (Pubitemid 38316504)
49. Lawling, A. M. & Polly, P. D. 2010 Geometric morpho- metries: recent applications to the study of evolution and development. J. Zool. 280, 1-7. (doi:10.1111/ j.1469-7998.2009.00620.x)
50. Laws, R. M. 1952 A new method of age determination for mammals. Nature 169, 972-973. (doi:10.1038/ 169972b0)
51. Lieberman, D. E. 2009 Paleoanthropology: Homo fioresiensis from head to toe. Nature 459, 41-42. (doi:10.1038/ 459041a)
52. Lister, A. M. 1990 Critical reappraisal of the middle Pleisto- cene deer species 'Cervus' elaphoides Kahlke. Quaternaire 3-4, 175-192.
53. Lomolino, M. V. 2005 Body size evolution in insular ver- tebrates: generality of the island rule. J. Biogeogr. 32, 1683-1699. (doi:10.1111/j.l365- 2699.2005.01314.x)
54. Luo, Z.-X., Kielan-Jaworowska, Z. & Cifelli, R. L. 2004 Evolution of dental replacement in mammals. Bull. Carnegie Mus. Nat. Hist. 36, 159-175. (doi:10.2992/ 0145-9058(2004)36[159:EODRIM]2.0.CO;2)
55. MacPhee, R. D. E. 1987 Basicranial morphology and onto- geny of the extinct giant lemur Megaladapis. Am. J. Phys. Anthropol. 74, 333-355. (doi:10.1002/ajpa. 1330740307)
56. Macrini, T. 2002 Quantitative comparison of ontogenetic and phylogenetic character changes in the synapsid mandible and auditory region. J. Mammal Evol. 9, 185-208. (doi:10.1023/A:1022667116022)
57. Maier,W1999Ontheevolutionarybiologyofearlymam-mals: withmethodologicalremarksontheinteractionbetweenontogeneticadaptationandphylog enetictrans-formation.Zool.Anzeiger.238,55-74.(Pubitemid129514352)
58. Marshall, P. M. & Butler, P. M. 1966 Molar cusp develop- ment in the bat, Hipposideros beatus, with reference to the ontogenetic basis of occlusion. Arch. Oral Biol. 11, 949-965. (doi:10.1016/0003-9969(66)90197-X)
59. Maxwell, E. E. & Caldwell, M. W. 2003 First record of live birth in Cretaceous ichthyosaurs: closing an 80 million year gap. Proc. R. Soc. Lond. B 270(Suppl. 1), S104-S107. (doi:10.1098/rsbl.2003.0029)
60. McKinney, M. L. & Schoch, R. 1985 Titanothere allometry, heterochrony, and biomechanics: revising an evolution- ary classic. Evolution 39, 1352-1363. (doi:10.2307/ 2408791)
61. McNamara, K. J. 1997 Shapes of time. Baltimore, MD: John Hopkins University Press.
62. Millien, V. & Damuth, J. 2004 Climate change and size evol- ution in an island rodent species: new perspectives on the island rule. Evolution 58, 1353-1360.
63. Müller, J., Scheyer, T. M., Head, J. J., Barrett, P., Werneburg, I., Ericson, P. G. P., Pol, D. & Sánchez-Villagra, M. R. In press. Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes. Proc. Natl Acad. Sci. USA.
64. Needham, J. 1933 On the dissociability of the fundamental processes in ontogenesis. Biol. Rev. 8, 180-223. (doi:10. 1111/j.l469-185X.1933.tb01153.x)
65. Olson, E. C. & Miller, R. L. 1958 Morphological integration. Chicago, IL: University of Chicago Press.
66. Parrington, F R. 1971 On the Upper Triassic mammals. Phil. Trans. R. Soc. Lond. B 261, 231-272. (doi:10. 1098/rstb. 1971.0055)
67. Polly, P. D. 2007 Development with a bite. Nature 449, 413-415. (doi:10.1038/449413a)
68. Porto, A., de Oliveira, F B., Shirai, L. T., De Conto, V. & Marroig, G. 2008 The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol. Biol. 36, 118-135. (doi:10.1007/ S11692-008-9038-9043)
69. Radinsky, L. 1984 Ontogeny and phylogeny in horse skull evolution. Evolution 38, 1-15. (doi:10.2307/2408541)
70. Raff, R. A. 1996 The shape of life. Chicago, IL: University of Chicago Press.
71. Raff, R. A. 2007 Written in stone: fossils, genes and evo- devo. Nat. Genet. 8, 911-920.
72. Raff, E. C., Villinski, J. A., Turner, F R., Donahue, P. C. & Raff, R. A. 2006 Experimental taphonomy: feasibility of fossil embryos. Proc. Natl Acad. Sci. USA 103, 5846-5851. (doi:10.1073/pnas.0601536103)
73. Ray, S., Bandyopadhyay, S. & Deblina Bhawal, D. 2009 Growth patterns as deduced from bone microstructure of some selected neotherapsids with special emphasis on dicynodonts: phylogenetic implications. Palaeoworld 18, 53-66. (doi:10.1016/j.palwor.2008.09.001)
74. Renvoisé, E., Evans, A. R., Jebrane, A., Labruère, C., Laffont, R. & Montuire, S. 2009 Evolution of mammal tooth patterns: new insights from a developmental predic- tion model. Evolution 63, 1327-1340. (doi:10.1111/ j.1558-5646.2009.00639.x)
75. Richtsmeier, J. T. 2003 Growth. In Keywords and concepts in evolutionary developmental biology (eds B. K. Hall & W. M. Olson), pp. 161-169. Cambridge, MA: Harvard University Press.
76. Roth, V. L. 1984 How elephants grow: heterochrony and the calibration of developmental stages in some living and fossil species. J. Vert. Paleo. 4, 126-145.
77. Roth, V. L. 1992 Inferences from allometry and fossils: dwarfing of elephants on islands. Oxf. Surv. Evol. Biol. 8, 259-288.
78. Rowe,T1996Coevolutionofthemammalianmiddleearandneocortex.Science273, 651-654.(doi:10.1126/science.273.5275.651)(Pubitemid26262119)
79. Schwartz, G. T., Samonds, K. E., Godfrey, L. R., Jungers, W. L. & Simons, E. L. 2002 Dental microstructure and life history in subfbssil Malagasy lemurs. Proc. Natl Acad. Sci. USA 99, 6124-6129. (doi:10.1073/pnas.092685099)
80. Sears, K. E., Behringer, R. R., Rasweiler, J. J. & Niswander, L. A. 2006 Development of bat flight: morphologic and molecular evolution of bat wing digits. Proc. Natl Acad. Sci. USA 103, 6581-6586. (doi:10.1073/pnas. 0509716103)
81. Sears, K. E., Goswami, A., Flynn, J. J. & Niswander, L. A. 2007 The correlated evolution of Runx2 tandem repeats, transcriptional activity and facial length in Carnivora. Evol. Dev. 9, 555-565. (Pubitemid 350045753)
82. Shea, B. T 1985 Bivariate and multivariate growth allome- try: statistical and biological considerations. J. Zool. 206, 367-390.
83. Smith, B. H. 1986 Dental development in Australopithecus and early Homo. Natures, 327-330. (doi:10.1038/323327a0)
84. Smith, B. H. 2000 'Schultz's Rule' and the evolution of tooth emergence and replacement in primates and ungu- lates. In Development, function, and evolution of teeth (eds M. F Teaford, M. M. Smith & M. W. J. Ferguson), pp. 212-227. Cambridge, UK: Cambridge University Press.
85. Smith, K. K. 2001 Heterochrony revisited: The evolution of developmental sequences. Biol. J. Linn. Soc. 73, 169-186. (doi:10.1111/j.1095-8312.2001. tb01355.x)
86. Sondaar, P. Y. 1977 Insularity and its effect on mammal evolution. In Major patterns in vertebrate evolution (eds M. K. Hecht, P. C. Goody & B. M. Hecht), pp. 671-707. New York, NY: Plenum.
87. Stallibrass, S. 1982 The use of cement layers for absolute ageing of mammalian teeth: a selective review of the litera- ture, with suggestions for further studies and alternative applications. In Ageing and sexing animal bones from arche- ological sites (eds B. Wilson, C. Grigson & S. Payne), pp. 109-126. BAR British Series 109.
88. Thewissen, J. G. M. & McLellan, W. A. 2009 Maiacetus: dis- placed fetus or last meal? PLOS One (Commentary 01 May 2009).
89. van Nievelt, A. F. H. & Smith, K. K. 2005 To replace or not to replace: The significance of reduced tooth replacement in marsupial and placental mammals. Paleobiology 31, 324-346. (doi:10.1666/0094-8373(2005) 031[0324:TRONTR] 2.0.CO;2)
90. Vrba, E. S. 2004 Ecology, evolution, and development: perspectives from the fossil record. In Environment, develop- ment, and evolution (eds B. K. Hall, R. D. Pearson & G. B. Muller), pp. 85-105. Cambridge, MA: MIT Press.
91. Vrba, E. S. 2005 Mass turnover and heterochrony events in response to physical change. Paleobiology 31, 157-174. (doi:10.1666/0094-8373(2005)031[0157: MTAHEI]2.0. CO;2)
92. Vucetich, M. G., Deschamps, C. M., Olivares, A. I. & Dozo, M. T. 2005 Capybaras, size, shape, and time. Acta Palaeontol. Pol. 50, 259-272.
93. Wagner, G. P. 2007 The current state and the future of devel- opmental evolution. In From embryology to evo-devo. A history of developmental evolution (eds M. D. Laubichler & J. Maienschein), pp. 525-546. Cambridge, MA: MIT Press.
94. Werdelin, L. 1987 Jaw geometry and molar morphology in marsupial carnivores: analysis of a constraint and its macroevolutionary consequences. Paleobiology 13, 342-350.
95. Weston, E. M. 2003 Evolution of ontogeny in the hippopota- mus skull: using allometry to dissect developmental change. Biol. J. Linn. Soc. 80, 625-638. (doi:10.1111/j. 1095-8312.2003.00263.x)
96. Weston, E. M. & Lister, A. M. 2009 Insular dwarfism in hippos and a model for brain size reduction in Homo flor- esiensis. Nature 459, 86-88. (doi:10.1038/nature07922)
97. Wilson, L. A. B. & Sánchez-Villagra, M. R. 2009 Hetero- chrony and patterns of cranial suture closure in hystricognath rodents. J. Anat. 214, 339-354. (doi:10. 1111/j.1469-7580.2008.01031.x)
98. Wilson, L. A. B. Sf Sánchez-Villagra, M. R. 2010 Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents. Proc. R. Soc. B 277, 1227-1234. (doi:10.1098/rspb.2009.1958)