Life-history correlates of enamel microstructure in cebidae (platyrrhini, primates)

Anatomical Record

Volumn 294, Issue 12, 2011, Pages 2193-2206

  Hogg, Russell T ^a   Walker, Robert S ^b  

^a FLORIDA GULF COAST UNIVERSITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Cebidae; Enamel growth; Foraging independence; Life history; Maternal investment; Risk aversion

Indexed keywords

AGE; ANIMAL TISSUE; ARTICLE; AVERSION; BIRTH RATE; BODY MASS; BRAIN; CATARRHINI; CEBIDAE; DENTISTRY; ECOLOGY; ENAMEL; EVOLUTIONARY ADAPTATION; FAMILY PLANNING; FEMALE; FORAGING; LIFE HISTORY; NONHUMAN; ONTOGENY; PHYLOGENY; PRIORITY JOURNAL; RISK; WEANING;

AGE FACTORS; ANIMALS; CEBIDAE; DENTAL ENAMEL; FEMALE; MALE; SPECIES SPECIFICITY; TOOTH;

CEBIDAE; LEMURIDAE; PLATYRRHINI; PRIMATES; SIMIIFORMES;

EID: 81255198343     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21503     Document Type: Article

References (98)

1. Beynon AD, Clayton CB, Ramirez Rozzi FV, Reid DJ. 1998. Radiographic and histological methodologies in estimating the chronology of crown development in modern humans and great apes: a review, with some applications for studies on juvenile hominids. J Human Evol 35: 351-370.
2. Beynon AD, Dean MC. 1987. Crown-formation time of a fossil hominid premolar tooth. Arch Oral Biol 32: 773-780.
3. Beynon AD, Dean MC, Reid DJ. 1991. Histological study on the chronology of the developing dentition in gorilla and orangutan. Am J Phys Anthropol 86: 189-203.
4. Beynon AD, Wood BA. 1986. Variations in enamel thickness and structure in East African hominids. Am J Phys Anthropol 70: 177-195.
5. Boughner JC, Dean MC. 2004. Does space in the jaw influence the timing of molar crown initiation? A model using baboons (Papio anubis) and great apes (Pan troglodytes, Pan paniscus). J Human Evol 46: 253-275.
6. Boyde A. 1989. Enamel. In: Oksche A, Vollrath L, editors. Handbook of microscopic anatomy, Vol. V/6: Teeth. Berlin: Springer-Verlag. p 309-473.
7. Bromage TG, Dean MC. 1985. Re-evaluation of the age at death of immature fossil hominids. Nature 317: 525-527.
8. Bromage TG, LaCruz R, Hogg R, Goldman H, McFarlin SC, Warshaw J, Dirks W, Perez Ochoa A, Smolyar I, Enlow DH, Boyde A. 2009. Lamellar bone reconciles enamel rhythms, body size, and organismal life history. Calcif Tissue Int 84: 388-404.
9. Bromage TG, Schrenk F, Zonneveld FW. 1995. Paleoanthropology of the Malawi Rift: an early hominid mandible from Chiwondo Beds, Northern Malawi. J Hum Evol 28: 71-108.
10. Byrne RW. 1995. Primate cognition: comparing problems and skills. Am J Primatol 37: 127-141.
11. Catlett KK, Schwartz GT, Godfrey LR, Jungers WL. 2010. "Life history space": a multivariate analysis of life history variation in extant and extinct Malagasy lemurs. Am J Phys Anthropol 142: 391-404.
12. Charnov EL, Berrigan D. 1993. Why do female primates have such long lifespans and so few babies? or life in the slow lane. Evol Anthropol 1: 191-194.
13. Cuvier G. 1817. La Règne Animal, Distribué d'Après son Organization, Tome I. Paris: Deterville.
14. Dean MC. 1998. A comparative study of cross striation spacings in cuspal enamel and of four methods of estimating the time taken to grow molar cuspal enamel in Pan, Pongo, and Homo. J Hum Evol 35: 449-462.
15. Dean MC. 2000. Progress in understanding hominoid dental development. J Anat 197: 77-101.
16. Dean MC. 2009. Extension rates and growth in tooth height of modern human and fossil hominin canines and molars. In: Koppe T, Meyer G, Alt KW, editors. Comparative dental morphology. Basel: Karger. p 68-73.
17. Dean MC, Beynon AD. 1991. Histological reconstruction of crown formation times and initial root formation times in a modern human child. Am J Phys Anthropol 86: 215-228.
18. Dean MC, Shellis RP. 1998. Observations on stria morphology in the lateral enamel of Pongo, Hylobates, and Proconsul teeth. J Hum Evol 35: 401-410.
19. Dean MC, Vesey P. 2008. Preliminary observations on increasing root length during the eruptive phase of tooth development in modern humans and great apes. J Hum Evol 54: 258-271.
20. DiBitetti MS, Janson CH. 2000. When will the stork arrive? Patterns of birth seasonality in neotropical primates. Am J Primatol 50: 109-130.
21. Dirks W. 1998. Histological reconstruction of dental development and age at death in a juvenile gibbon (Hylobates lar). J Hum Evol 35: 411-425.
22. Dirks W. 2003. Effect of diet on dental development in four species of catarrhine primates. Am J Primatol 61: 29-40.
23. Dirks W, Anemone RL, Holroyd PA, Reid DJ, Walton P. 2009. Phylogeny, life history, and the timing of molar crown formation in two archaic ungulates, Meniscotherium and Phenacodus (Mammalia, 'Condylarthra'). In: Koppe T, Meyer G, Alt KW, editors. Comparative dental morphology. Basel: Karger. p 3-8.
24. Dirks W, Bowman JE. 2007. Life history theory and dental development in four species of catarrhine primates. J Hum Evol 53: 309-320.
25. Dirks W, Bromage TG, Agenbroad L. 2010. The timing of molar lamellae formation in Mammuthus columbi and Palaeoloxodon cypriotes from dental histology. Fifth International Conference on Mammoths and their Relatives. Quart Hors-série 3: 35-36.
26. Dirks W, Reid DJ, Jolly CJ, Phillips-Conroy JE, Brett FL. 2002. Out of the mouths of baboons: stress, life history, and dental development in the Awash National Park hybrid zone, Ethiopia. Am J Phys Anthropol 118: 239-252.
27. Dunbar RM. 1992. Neocortex size as a constraint on group size in primates. J Hum Evol 22: 469-494.
28. Dunbar RM. 1995. Neocortex size and group size in primates: a test of the hypothesis. J Hum Evol 28: 287-296.
29. Ford SM, Davis LC. 1992. Systematics and body size: implications for feeding adaptations in New World monkeys. Am J Phys Anthropol 88: 415-468.
30. Fragaszy DM, Bard K. 1997. Comparison of development and life history in Pan and Cebus. Int J Primatol 18: 683-701.
31. Fragaszy DM, Boinski S. 1995. Patterns of individual diet choice and efficiency of foraging in capuchin monkeys (Cebus olivaceus). J Comp Psychol 109: 339-348.
32. Fragaszy DM, Visalberghi E, Fedigan LM. 2004. The complete capuchin: the biology of the genus Cebus. Cambridge: Cambridge University Press.
33. Fragaszy DM, Visalberghi E, Robinson JG. 1990. Variability and adaptability in the genus Cebus. Folia Primatol 54: 114-118.
34. Garber PA, Leigh SR. 1997. Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care. Folia Primatol 68: 1-22.
35. Gibson KR. 1986. Cognition, brain size and the extraction of embedded food resources. In: Else J, Lee PC, editors. Primate ontogeny, cogntion and social behavior. Cambridge: Cambridge University Press. p 93-104.
36. Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. 2001. Teeth, brains, and primate life histories. Am J Physical Anthropol 114: 192-214.
37. Godfrey LR, Samonds KE, Jungers WL, Sutherland MR. 2003. Dental development and primate life histories. In: Kappeler PM, Pereira ME, editors. Primate life histories and socioecology. Chicago: University of Chicago Press. p 177-203.
38. Godfrey LR, Samonds KE, Jungers WL, Sutherland MR, Irwin MT. 2004. Ontogenetic correlates of diet in Malagasy lemurs. Am J Physical Anthropol 123: 250-276.
39. Godfrey LR, Samonds KE, Wright PC, King SJ. 2005. Schultz's unruly rule: dental developmental sequences and schedules in small-bodied, folivorous lemurs. Folia Primatol 76: 77-99.
40. Godfrey LR, Schwartz GT, Samonds KE, Jungers WL, Catlett KK. 2006. The secrets of lemur teeth. Evol Anthropol 15: 142-154.
41. Hartwig WC. 1996. Perinatal life history traits in New World monkeys. Am J Primatol 40: 99-130.
42. Harvey PH, Clutton-Brock TH. 1985. Life history variation in primates. Evolution 39: 559-581.
43. Harvey PH, Martin RD, Clutton-Brock TH. 1987. Life histories in comparative perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 181-196.
44. Hladik, A, Hladik CM. 1969. Rapports trophiques entre végétation et primates dans la forêt de Barro Colorado (Panama). Terre Vie 1: 25-117.
45. Hogg RT. 2010. Dental Microstructure and Growth in the Cebid Primates. Ph.D. Dissertation, City University of New York.
46. Janson CH, Boinksi S. 1992. Morphological and behavioral adaptations for foraging in generalist primates: the case of the cebines. Am J Phys Anthropol 88: 483-498.
47. Janson CH, van Schaik C. 1993. Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA, editors. Juvenile primates: Life history, development and behavior. New York: Oxford University Press. p 57-76.
48. Jerison HJ. 1973. Evolution of the brain and intelligence. New York: Academic Press.
49. Joffe TH. 1997. Social pressures have selected for an extended juvenile period in primates. J Hum Evol 32: 593-605.
50. Jordana X, Kohler M. 2010. Enamel microstructure in the fossil bovid Myotragus balearicus (Majorca, Spain): implications for life-history evolution of dwarf mammals in insular ecosystems. Paleogeog, Paleoclimatol, Paleoecol 300: 59-66.
51. Kinzey WG. 1997. Part 2: Synopsis of New World primates. In: Kinzey WG, editor. New World primates: ecology, evolution, and behavior. Edison, NJ: Aldine Transaction. p 169-324.
52. Kirk EC. 2006. Visual influences on primate encephalization. J Hum Evol 51: 76-90.
53. Lee PC. 1999. Comparative ecology of postnatal growth and weaning among haplorhine primates. In: Lee PC, editor. Comparative primate socioecology. Cambridge: Cambridge University Press. p 111-139.
54. Leigh SR. 1994. Ontogenetic correlates of diet in anthropoid primates. Am J Phys Anthropol 94: 499-522.
55. Leigh SR, Bernstein RM. 2006. Ontogeny, life history, and maternal reproductive strategies in baboons. In: Swedell L, Leigh SR, editors. Reproduction and fitness in baboons. New York: Springer. p 225-256.
56. Lindenfors P. 2002. Sexually antagonistic selection on primate size. J Evol Biol 15: 595-607.
57. Macho G. 2001. Primate molar crown formation times and life history evolution revisited. Am J Primatol 55: 189-201.
58. Martin RD. 1990. Primate origins and evolution: a phylogenetic reconstruction. Princeton: Princeton University Press.
59. Milton K. 1980. The foraging strategy of howler monkeys: a study in primate economics. New York: Columbia University Press.
60. Nicolson NA. 1987. Infants, mothers, and other females. In: Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker T, editors. Primate societies. Chicago: University of Chicago Press. p 330-342.
61. Osterholtz M, Walter L, Roos C. 2009. Retropositional events consolidate the branching order among New World monkey genera. Mol Phylog Evol 50: 507-513.
62. Pagel M. 1997. Inferring evolutionary processes from phylogenies. Zool Scripta 26: 331-348.
63. Pagel M. 1999. Inferring the historical patterns of biological evolution. Nature 401: 877-884.
64. Pereira ME, Leigh SR. 2003. Modes of primate development. In: Kappeler PM, Pereira E, editors. Primate life histories and socioecology. Chicago: University of Chicago Press. p 149-176.
65. Ray D. 2007. SINEs of progress: mobile element applications to molecular ecology. Mol Ecol 16: 19-33.
66. Ray D, Xing J, Hedges D, Hall M, Laborde M, Anders B, White B, Stoilova N, Fowlkes J, Landry K, Chemnick L, Ryder O, Batzer MA. 2005. Alu insertion loci and platyrrhine primate phylogeny. Mol Phylog Evol 35: 117-126.
67. Reid DJ, Beynon AD, Ramirez-Rozzi FV. 1998a. Histological reconstruction of dental development in four individuals from a medieval site in Picardie, France. J Hum Evol 35: 463-477.
68. Reid DJ, Schwartz GT, Dean MC, Chandresakera MS. 1998b. A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes. J Hum Evol 35: 427-448.
69. Risnes S. 1986. Enamel apposition rates and prism periodicity in human teeth. Scand J Dent Res 94: 394-404.
70. Risnes S. 1998. Growth tracks in dental enamel. J Hum Evol 35: 331-350.
71. Rosenberger AL. 1984. Fossil New World monkeys dispute the molecular clock. J Hum Evol 13: 737-742.
72. Rosenberger AL. 1992. Evolution of feeding niches in New World monkeys. Am J Physical Anthropol 88: 525-562.
73. Rosenberger AL, Setoguchi T, Shigehara N. 1990. The fossil record of callitrichine primates. J Hum Evol 19: 209-236.
74. Rosenberger AL, Strier KB. 1989. Adaptive radiation of the ateline primates. J Hum Evol 18: 717-750.
75. Rosenberger AL, Tejedor M, Cooke SB, Pekar S. 2009. Platyrrhine ecophylogenetics in space and time. In: Garber P, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB, editors. South American primates: comparative perspectives in the study of behavior, ecology, and conservation. New York: Springer. p 69-116.
76. Ross C. 1991. Life history patterns of New World monkeys. Int J Primatol 12: 481-502.
77. Ross C, Jones KE. 1999. Socioecology and the evolution of primate reproductive rates. In: Lee PC, editor. Comparative primate socioecology. Cambridge: Cambridge University Press. p 73-110.
78. Schneider H, Canavez FC, Sampaio I, Moreira, MAM, Tagliaro C, Seuanez HN. 2001. Can molecular data place each neotropical monkey in its own branch? Chromosoma 109: 515-523.
79. Schultz AH. 1935. Eruption and decay of the permanent teeth in primates. Am J Phys Anthropol 19: 489-581.
80. Schultz AH. 1960. Age changes in the skulls and teeth of the Central American monkeys Alouatta, Cebus, and Ateles. Proc Zool Soc Lond 133: 337-399.
81. Schwartz GT, Dean MC. 2001. Ontogeny of canine dimorphism in extant hominoids. Am J Phys Anthropol 115: 259-288.
82. Schwartz GT, Godfrey LR, Mahoney P. 2007. Inferring primate growth, development, and life history from dental microstructure: the case of the extinct giant Malagasy lemur, Megaladapis. In: Bailey SE, Hublin JJ, editors. Dental perspectives on human evolution: state of the art research in dental paleoanthropology. Dordrecht: Springer. p 147-162.
83. Schwartz GT, Mahoney P, Godfrey LR, Cuozzo FP, Jungers WL, Randria GFN. 2005. Dental development in Megaladapis edwardsi (Primates, Lemuriformes): implications for understanding life history variation in subfossil lemurs. J Hum Evol 49: 702-721.
84. Schwartz GT, Samonds KE, Godfrey LR, Jungers WL, Simons EL. 2002. Dental microstructure and life history in subfossil Malagasy lemurs. Proc Natl Acad Sci USA 99: 6124-6129.
85. Shellis RP. 1984. Variations in growth of the enamel crown in human teeth and a possible relationship between growth and enamel structure. Archs Oral Biol 29: 697-705.
86. Shellis RP. 1998. Utilization of periodic markings in enamel to obtain information on tooth growth. J Human Evol 35: 387-400.
87. Smith BH. 1989. Dental development as a measure of life history in primates. Evolution 43: 683-88.
88. Smith BH. 2000. 'Schultz's rule' and the evolution of tooth emergence and replacement patterns in primates and ungulates. In: Teaford MF, Smith MM, Ferguson MWJ, editors. Development, function and evolution of teeth. Cambridge: Cambridge University Press. p 212-227.
89. Smith BH, Crummett TL, Brandt KL. 1994. Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories. Ybk Phys Anthropol 37: 177-231.
90. Smith TM, Martin LB, Reid DJ, de Bonis L, Koufos GD. 2004. An examination of dental development in Graecopithecus freybergi (=Ouranopithecus macedoniensis). J Hum Evol 46: 551-577.
91. Smith TM, Tafforeau P, Reid DJ, Grun R, Eggins S, Boutakiout M, Hublin J. 2007. Earliest evidence of modern human life history in North African early Homo sapiens. Proc Natl Acad Sci USA 104: 6128-6133.
92. Strier KB. 1992. Atelinae adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88: 515-524.
93. Tejedor MF, Tauber AA, Rosenberger AL, Swisher CC, Palcios ME. 2006. New primate genus from the Miocene of Argentina. Proc Natl Acad Sci USA 103: 5437-5441.
94. Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man. London: Heinemann. p 136-179.
95. Trivers RL. 1974. Parent-offspring conflict. Int Comp Biol 14: 249-264.
96. Visalberghi E. 1987. Acquisition of nut-cracking behaviour by 2 capuchin monkeys (Cebus apella). Folia Primatol 49: 168-181.
97. Visalberghi E, McGrew WC. 1997. Cebus meets Pan. Int J Primatol 18: 677-681.
98. Wilbur H, Tinkle D, Collins J. 1974. Environmental certainty, trophic level, and resource availability in life history evolution. Am Nat 108: 805-817.