Article pp.134-139 du Vol.26 n°3-4 (2014)

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NOTE /NOTE

Longitudinal studies of craniofacial growth in Primates: a short review of radiographic studies

Études longitudinales de la croissance crânio-faciale chez les Primates : une courte revue des études radiographiques

S. Prat

Received: 27 October 2013; Accepted: 3 March 2014

AbstractGrowth studies on human and nonhuman primates contribute to a range of research topics such as somatic growth and the establishment of charts for growth and skeletal maturity, and therefore provide a valuable evolutionary perspective. Longitudinal studies, especially long-term ones, provide the most accurate data to assess the factors that influence growth and development, and to construct growth velocity curves. In this note, we present the main long-term longitudinal radiographic studies of craniofacial growth in human and nonhuman primates. Such studies are extremely rare as they are costly and difficult to implement, especially when ethical and health constraints arise due to the use of X- ray radiographs.

KeywordsLongitudinal · Growth · Craniofacial · Primates · Radiographs

RésuméLes études portant sur la croissance des primates humains et non humains sont utilisées dans différents domaines de recherche tels que la croissance somatique, l’établissement de chartes de croissance et de maturation squelettique ou dans une perspective évolutive. Les études longitudinales, et en particulier celles entreprises sur une longue durée, apparaissent comme les plus pertinentes pour reconstruire les courbes de vitesse de croissance et évaluer les facteurs qui influencent la croissance et le développe- ment. Dans cette note, les principales études radiographiques longitudinales portant sur la croissance crânio-faciale des primates humains et non humains sont présentées. Ces études sont très rares car coûteuses et difficiles à mettre en place en particulier pour des raisons éthiques et sanitaires lorsque des radiographies sont effectuées.

Mots clésLongitudinal · Croissance · Crânio-facial · Primates · Radiographie

Introduction

Growth and development studies involving human and nonhuman primates contribute to a range of challenging topics that include somatic growth, production of growth norms and standards, body size, dental development and craniofacial growth. The latter topic is often used in a phylogenetic perspective to better understand hominin growth patterns and also to compare cranial ontogenetic trajectories. This note is a short review of the literature concerning longitudinal studies on human and nonhuman primates and ongoing studies on craniofacial growth, with a particular focus on radiographic data.

Longitudinal databases (i.e. repeated observations of the same individual over a period of time) are particularly useful sources for understanding growth processes [1]. There are at least three types of longitudinal research design protocols:

long-term, short-term, and mixed. In the latter, certain individuals are sampled repeatedly at different points in their lives, and others only once [2], specimens are distributed across age categories and then serially observed over a given period [3]. Long-term longitudinal observations provide the best datasets for constructing growth velocity curves, and also for investigating factors that influence growth and development.

The majority of longitudinal studies focus on: a) changes in body size and stature during the development of individuals; b) identification of “growth spurts”; and c) growth rates during childhood. The first longitudinal human growth study was made by the Comte de Montbeillard between 1759 and 1777 on his own son, when he took periodic measurements (stature and weight) of his son’s body [4].

S. Prat (*)

UPR 2147, Dynamique de l’Evolution Humaine, 44, rue de l’Amiral Mouchez, 75014 Paris e-mail : [email protected]

DOI 10.1007/s13219-014-0101-6

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Over a century later, the introduction of radiographic cephalometry by Broadbent in 1931 [5] provided a means to overcome the difficulties of locating skeletal landmarks on the body surface of individuals. The subsequent development of techniques for the management of orthodontic treat- ments provided large datasets of serial head X-rays and thus contributed greatly to the understanding of postnatal skull growth patterns.“Even so, there are few longitudinal studies extending throughout the growth period - these would require, after all, the cooperation of subjects and investiga- tors over a period of some 20 years”([6] p. 16)”.

Radiographic techniques are less easily applicable to nonhuman primates. As a consequence, most of our knowledge on patterns of facial growth and ontogeny in nonhuman primates has come from cross-sectional craniometric studies of animals shot in the wild (e.g. [7]).

Short review on longitudinal studies of human growth

A short review of the literature on the main longitudinal studies on human growth is presented in Table 1, with some examples of subsequent work. These studies often focus on stature, skeletal maturity and/or orthodontics. To complete the dataset in Table 1, see [8] for a list of European and North American growth studies that do not involve radiographic methods.

The longitudinal growth studies of the 1930s and 40s were conducted for two main reasons: to see how children grow, and to establish norms or standards for size, skeletal development and maturity. In Europe, the most important longitudinal studies, in terms of duration and the number of individuals involved, are the Harpenden Growth Study directed by Tanner (1948-1971) (e.g. [9,10]) the Zurich Lon- gitudinal Study (1954-) (e.g. [11,12]) and the studies directed by Sempé (1953-1975) (e.g. [13-15]). In North America, the growth standards from the Brush Foundation, the Denver Growth Study and the Fels Longitudinal Studies have many implications for clinical medicine, nutritional surveys, body composition and dentofacial growth studies, and for the identification of postnatal ossification centres [16]. Some of these studies (e.g. the Fels Longitudinal Study) led to the creation of skeletal maturity and pediatric growth charts [0-3 years] in the United States [17], or were used in human evolutionary studies, such as Moorrees’s dental development chart [18].

Some of these longitudinal studies built up cephalometric radiography databases, initially to quantify orthodontic malocclusion. The use of these databases in human craniofacial growth studies has been recently developed, especially those from two long-term human longitudinal studies: the Denver Growth Study and the Fels Longitudinal Study, which is the

longest ongoing longitudinal study in the world. The Den- ver Growth Study has been employed in several fields (see Table 1). The cephalometric radiographs have been used in ontogenetic perspectives (cranial base angulation [19], vocal-tract shape [20], facial dimorphism [21], dissociation of size and shape of basicranial elements during ontogeny [22]), and in evolutionary perspectives (e.g. role of the sphenoid bone during human evolution [23]). The Fels Longitu- dinal Study started in 1924 and is still being added to. The lateral cranial radiograph protocol began in 1931 but ended in 1982. This study produced the last long-term radiographic database on humans in the world. More than 380 research articles [24,25], including some with anthropological and human evolutionary perspectives [26], have been produced.

Short review on longitudinal studies of growth in nonhuman primates

Knowledge on nonhuman primate growth and development is crucial to understand various aspects of human evolution, and especially to model the evolution of human growth. How- ever, there are few nonhuman growth studies, and far fewer than human-based studies. They are often cross-sectional or mixed-longitudinal analyses, especially for the great apes, because of the difficulties involved in conducting experimental procedures. These studies often concern the growth of limb segments [38], skeletal maturity (ossification [39]), scoring of dental development or tooth emergence (e.g. [40-46]), or evolutionary perspectives (e.g. facial retraction [47]).

The largest radiographic database on chimpanzees [46]

was produced with a mixed-longitudinal sample of 33Pan troglodytesthat were used in experimental studies on anterior maxillo-facial growth mechanisms (e.g. [48-49]). Con- cerning macaques, the main long-term longitudinal craniofacial growth studies were conducted by Sirianniet al. (e.g.

[50-54]) on 34 male and 23 female pigtailed macaque monkeys(Macaca nemestrina). Before these studies, the growth of juvenileM. nemestrinamandibles was documented only in cross-sectional or short-term longitudinal studies (for a literature review see [3]). Concerning baboons (genus Papio), despite the fact that they are important animals for modelling many aspects of human biology [2], only a limited amount of longitudinal data is available. Ontogenetic studies are often based on cross-sectional data on individuals shot in the wild [55,56]. The main long-term longitudinal study focusing on craniofacial growth was conducted by Swindler et al. on 16 olive baboons (Papio anubis) from 3 months to 3 years of age [50]. But, as noted by Leigh in 2006, “far better data are needed to understand the mechanics of these [Author’s Note: ontogenetic] processes, especially longitu- dinally collected data from animals of precisely known age or chronological ages”([7] p. 81).

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Table1Mainlong-termlongitudinalgrowthstudiesonhumans,usingX-Rayradiographs;inbold,X-raycraniofacialradiographicstudies(X-Ray:X-Rayradiographs/Princi- palesétudesradiographiqueslongitudinalesàlongtermeportantsurlacroissancehumaine,engraslesbasesdedonnéesradiographiquescrâniennes(X-Ray:radiographies àRayonsX). NameSampleStudyPeriodMethodMainobjectivesReferences[e.g.] OxfordChildHealth Survey 650children[2-5years[1944-64Anthropometry X-Ray(hand,wrist) Effectsofenvironmentonphysical development.Growth(stature) Skeletalmaturity

[27] HarpendenGrowth Study

Atleast170children Every3monthsthroughout theiradolescentgrowthspurts 1948-1971Anthropometry X-Ray Growth(stature,lengthoflowerlimb, bi-iliacdiameter)

[9,10,28] LondonLongitudinal Studies224children[0-20]years Every3monthsthefirstyear, annuallythereafteruntilage20

1949-69Anthropometry X-RayMeasurement(biceps,triceps, subscapular,suprailiac),skin-fold thicknessmeasurements

[29] Paris558new-born,every6months1953-1975Anthropometry X-Ray(hand,wrist andelbow)

Growth(weight,stature,head circumference) Skeletalmaturity(hand,wristandelbow)

[13-15] TheBroadbent- Bolton-Brush GrowthStudy,

2,800participantsinbothstudiesBrush:1926-1942 Broadbent-Bolton: 1929-1959 200,000X-Ray (headandthemajorjoints ofthebody)

Skeletalmaturity[30,31] DenverGrowth Study

334participantsatthebeginning 2,4,6months,andafterevery 6monthsuptomid-adolescence

1927-1967Anthropometry Electrocardiography Bloodanalysis Interviews X-Ray(hand-wrist,upper andlowerlimbs,head) Growth,skin-foldthicknesses,health history,nutritionalintake Skeletalmaturity Upperandlowerlimbgrowth Craniofacialgrowth

[19-23,32-36] FelsLongitudinal Study

3,000participants(250families, threegenerations)including 1,200serialparticipants. 1,3,6,9and12monthsofage;twice ayearuntilage18andthenbiennially

1929-stillcontinueAnthropometry:1929- DualenergyX-Ray Absorptiometry:1990- Interviews:health andbehaviourdata:1929- Physicalactivity:1988- X-Ray(hand-wrist, head):1931-1982 Growth(weight,stature..) Bodycompositionandbonedensity, subcutaneoustissuemeasurements Skeletalmaturity Healthknowledge(e.g.effectofsmoking onthefetus,obesity),preventionofrisk factorsforcardiovasculardisease Craniofacialgrowth

Morethan380publications [24-26] MichiganGrowth study721individuals1953-19703,266X-Ray(head)OrthodonticsstudiesclassII malocclusion2majoratlas Cephalometricstandards (n=84individuals)[37] Dentalcastmeasurements (n=208individuals), 66publishedpapers

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To complete the previous studies, we are conducting a long-term longitudinal study on 35 olive baboons (Papio anubis) at the CNRS Primatology Station (UPS 846, Guy Dubreuil, Romain Lacoste, Valérie Moulin) at Rousset- sur-Arc (France), which is one of the largest breeding and housing centres for nonhuman primates in Europe. Lateral cranial radiographs of each individual are taken every 3 months from the age of 3 months to 2 years, and every 6 months until their skeletal maturity is complete, with longitudinal follow-up spanning the years from 2007 to 2015 [59]. More than five hundred lateral cranial radiographs have already been made. Another long-term longitudinal study concerning anthropometric and radiographic explorations of the locomotor system is in progress with the same sample population (dir. Gilles Berillon). Together, they make up a project that is providing unique data on growth in olive baboons and a unique radiographic atlas. Since there are no

craniofacial growth standards for olive baboons in the literature, the availability of these standards will be of great value to researchers interested in primate growth. Furthermore, because the chronological age of each individual is known, the longitudinal craniofacial radiographic data is used to establish a dental maturity chart, which can be compared to postcranial skeletal maturation.

Conclusion

Understanding the evolution of human growth requires comparative analyses of other primates in order to show which ontogenetic changes are peculiar to humans and which are common to different primates (e.g. [3,60,61]).

For this reason, the generaPan,Gorilla,Pongo, Papioand Macacaare often used as model in human evolution because

Table 2 Main longitudinal craniofacial growth and dental studies (tooth emergence and development) on nonhuman primates; in bold, long-term longitudinal X-Ray radiographic studies (X-Ray: X-Ray radiographs) / Principales études longitudinales portant sur la croissance crânio-faciale et l’éruption et de développement dentaire des primates non-humains, en gras les études radiographiques longitudinales à long terme (X-Ray: Radiographies à Rayons X).

Species Sample (individuals) Methods Main objectives References

Pan troglodytes 16

irregular intervals [birth to 13 years]

Mixed-longitudinal 99 lateral head X-Ray

Dental development [43]

P. troglodytes 16 Mixed-longitudinal

Dental examinations 473 teeth

Dental emergence [41]

P. troglodytes 58 [1 month -10 years]

Irregular intervals

Mixed-longitudinal Intra-oral examinations

Dental emergence [44]

P. troglodytes 33 [3 months-5 years]

irregular intervals

Mixed-longitudinal 299 lateral head X-Ray

Dental development [46]

P. troglodytes 33 [3 months-5 years] Mixed-longitudinal Anterior maxillo-facial growth mechanisms

[48]

Macaca nemestrina

32 [1-7 years[ Mixed-longitudinal X-Ray

Cranial base growth [51]

M. nemestrina 57 [8 months-9 years] X-Ray Mandible growth [53]

M. nemestrina 38 [3 months-3 years] X-Ray Craniofacial growth [50]

M. nemestrina 38 [3 months-3 years] Cephalometry, dental and palatal casts

Palatal growth [57]

M. mulatta 50 [birth-7 years] Cephalometry, body measurements, observations

Eruption of the deciduous teeth, physical growth

[40,58]

Papio anubis 16 [3 months-3 years]

every 3 months

X-Ray Craniofacial growth [50]

P. anubis 16 [3 months-3 years] Cephalometry, dental and palatal casts

Palatal growth [57]

P. anubis 35 [6 months-8 years]

every 2 months until 2 years old,

every 6 months after

X-Ray Craniofacial growth [59]

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of their close phylogenetic relationships withHomo sapiens and their general craniofacial similarities with hominins [19]. Since nonhuman primate life history, compared to humans, displays faster post-natal maturation rates, longitudinal craniofacial follow-up of nonhuman primates (with radiographic data in particular) can rapidly provide useful information on individual variability and sexual dimorphism in terms of growth rate, identification of pubertal growth, evaluation of the degree to which skeletal morphologies grow independently and analyses of the effects of size and shape (allometry), which are among the keys to a better understanding of our evolutionary history (e.g. [62,63]).

However, this short review of the literature has highlighted the scarcity of long-term craniofacial radiographic monitor- ing (four studies performed on human and four on nonhuman primates (Macaca nemestrina and Papio anubis) (Tables 1 and 2). Indeed, there is considerable reluctance towards undertaking or financing longitudinal studies. There- fore, longitudinal data are difficult to obtain nowadays, because of the length of time required to ensure that a viable number of individuals remains involved during the whole period of study, and for ethical reasons (in particular when X-Ray radiographs are used). Moreover, long-term longitudinal studies on nonhuman primates mean working with the same cohort over many years as well as ongoing sedation of the animals, which is not possible in the field. They are therefore conducted within Primate Research Institutes, which are also a scare resource around the world.

AcknowledgementsI would like to thank Gilles Berillon and Guillaume Daver for the organization of the Symposium on“Primates non-humains : bilan des recherches et perspectives anthropobiologiques”, 1838^es Journées de la Société d’Anthropologie de Paris; the reviewers for their comments;

Jason Lewis and Caroline Phillips for improving the English text.

References

1. Kodlin D, Thompson DJ (1958) An appraisal of the longitudinal approach to studies in growth and development. Monographs of the Society for research in child development 23(1):1–47 2. Coelho AM (1985) Baboon dimorphism: growth of weight,

length and adiposity from birth to 8 years of age. In: Watts ES (ed) Nonhuman primate models for human growth and development. Alan R Liss Inc, New York, pp 125-59

3. Sirianni J, Swindler DR (1979) A review of postnatal craniofacial growth in Old World monkeys and apes. Yearbook of Phys Anthrop 22:80–104

4. Scammon RE (1927) The first seriatim study of human growth.

Am J Phys Anthrop 10:329–36

5. Broadbent BH (1931) A new X-ray technique and its application to orthodontia. The introduction of cephalometric radiography.

Angle Orthod 1:45–66

6. Moore WJ, Lavelle CLB (1974) Growth of the facial skeleton in the hominoidea. Academic press, London, 236 p

7. Leigh SR (2006) Cranial ontogeny of Papio Baboons (Papio hamadryas). Am J Phys Anthrop 130:71–84

8. Ulijaszek SJ, Johnston FE, Preece MA (1998) The Cambridge Encyclopedia of Human Growth and Development. Cambridge University Press, Cambridge, 509 p

9. Marubini LF, Resele JM, Tanner JM, et al (1972) The Fit of Gompertz and Logistic Curves to Longitudinal Data during Ado- lescence on Height, Sitting Height and Biacromial Diameter in Boys and Girls of the Harpenden Growth Study. Hum Biol 44 (3):511–23

10. Tanner JM, Whitehouse RH, Marubini E, et al (1976) The adolescent growth spurt of boys and girls of the Harpenden Growth Study. Ann Hum Biol 3(2):109–26

11. Prader A, Largo RH, Molinari L, et al (1989) Physical growth of Swiss children from birth to 20 years of age; First Zurich longitudinal study of growth and development. Helv Paediatr Acta Suppl 52:1–125

12. Jenni OG, Caflisch J, Molinari L, et al (2007) Sleep duration from age 1 to 10 years: variability and stabiliy in comparison with growth. Pediatrics 120(4):e769–76

13. Sempé P, Sempé M (1971) Croissance et Maturation osseuse.

Analyse auxologique et radiologique, Théraplix, Paris, 103 p 14. Sempé M, Pavia C (1979) ATLAS de la maturation squelet-

tique du poignet, de la main et du coude, S.I.M.E.P., Lyon- Villeurbanne, 239 p

15. Sempé M, Pavia C, Bouchard M (2001) Auxologie et maturation squelettique. Biom Hum Anthropol, XIX (1-2):1–8

16. Garn SM (1981) The growth of growth. Am J Phys Anthrop 56:521–30

17. Roche AF, Chumlea WC, Thissen D (1988) Assessing the skeletal maturity of the hand-wrist: FELS method, Charles C. Thomas, Springfield, 339 p

18. Moorrees CFA (1959) The dentition of the growing child: a longitudinal study of dental development between 3 and 18 years of age, Harvard University Press, Cambridge, 245 p

19. Lieberman DE, McCarthy RC (1999) The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions. J Hum Evol 36:487–517

20. Lieberman DE, McCarthy RC, Hiiemae KM, et al (2001) Ontog- eny of postnatal hyoid and larynx descent in humans. Arch Oral Biol 46:117–28

21. Bulygina E, Mitteroecker P, Aiello L (2006) Ontogeny of facial dimorphism and patterns of individual development within one human population. Am J Phys Anthrop 131:432–43

22. Bastir M, Rosas A, O’Higgins P (2006) Craniofacial levels and the morphological maturation of the human skull. J Anat 209:637–54

23. Lieberman DE (1998) Sphenoid shortening and the evolution of modern human cranial shape. Nature 393:158–62

24. Roche AF (1992) Growth, maturation and body composition:

The Fels Longitudinal Study 1929-1991, Cambridge University Press, Cambridge, 282 p

25. Roche AF, Sun S (2003) Human growth Assesment and Interpre- tation, Cambridge University Press, Cambridge, 311 p

26. Sherwood RJ, Duren DL, Demerath EW, et al (2008) Quantita- tive genetics of modern human cranial variation. J Hum Evol 54:909–14

27. Hewitt D, Westropp CK, Acheso RM (1955) Oxford child health survey effect of childish aliments on skeletal development. Brit J Prev Soc Med 9:179–86

28. Marshall WA (1974) Interrelationships of skeletal maturation, sexual development and somatic growth in man. Ann Hum Biol 1:29–40

(6)

29. Tanner, JM, Hughes PCR, Whitehouse RH (1981) Radiographi- cally determined widths of bone, muscle and fat in the upper arm and calf from age 3 to 18 years. Ann Hum Biol 8:495–517 30. Broadbent BH Sr, Broadbent BH Jr, Golden WH (1975) Bolton

Standards of Dentofacial Developmental Growth, Mosby, St Louis, 166 p

31. Dean D, Hans MG, Bookstein FL, et al (2000) Three- dimensional Bolton-Brush Growth study landmark data:ontogeny and sexual dimorphism of the Bolton Standards Cohort. Cleft Palate Craniofac J 37:145–56

32. Ruff C (2003) Growth in bone strength, body size, and muscle size in a juvenile longitudinal sample. Bone 33:317–29 33. Ruff C (2007) Body size prediction from juvenile skeletal

remains. Am J Phys Anthrop 133:698–716

34. Maresh MM, Washburn AH (1938) Size of the heart in healthy children. Am. J. Dis. Child 56:33–60

35. Maresh MM (1970) Measurements from roentgenograms, heart size, long bone lengths, bone, muscle and fat widths, skeletal maturation. In: McCammon RW (ed) Human growth and development. Charles C. Thomas, Springfield, pp 155-200

36. Mc Cammon RW (1970) Human growth and development.

Charles C. Thomas Publisher, Springfield, 295 p

37. Riolo ML (1974) An Atlas of craniofacial growth: Cephalometric standards from the University School growth study, Center for Human Growth and Development, University of Michigan, Ann Arbor, Monograph n°2, 379 p

38. Watts ES, Gavan JA (1982) Postnatal Growth of Nonhuman Pri- mates: The Problem of the Adolescent Spurt. Hum Biol 54:53–70 39. Nissen HW, Nissen AH (1949) Onset of ossification in the epiph- yses and short bones of the extremities in chimpanzee. Growth 13:45–70

40. Hurme VO, VanWaganen G (1953) Basic data on the emergence of deciduous teeth in the monkey,Macaca mulatta. Proc Am Phil Soc 97:291–315

41. Nissen HW, Riesen AH (1964) The eruption of the permanent dentition of chimpanzee. Am J Phys Anthropol 22:285–94 42. Dean MC, Wood BA (1981) Developing pongid dentition and its

use for ageing crania in comparative cross-sectional growth studies. Folia Primatol 36:111–27

43. Anemone RL, Watts ES, Swindler DR (1991) Dental Develop- ment of Known-Age Chimpanzees, Pan troglodytes (Primates, Pongidae). Am J Phys Anthrop 86:229–41

44. Kuykendall KL, Mahoney J, Conroy C (1992) Probit and sur- vival analysis of tooth emergence ages in a mixed-longitudinal sample of Chimpanzees (Pan troglodytes). Am J Phys Anthrop 89:379–99

45. Smith BH, Crummett TL, Brandt KL (1994) Ages of eruption of primate teeth: a compendium for aging individuals and compar- ing life histories. Yearbook of Phys Anthrop 37:177–231 46. Anemone RL, Mooney MP, Siegel MI (1996) Longitudinal study

of dental development in Chimpanzees of known chronological

age: Implications for understanding the age at death of Plio- Pleistocene hominids. Am J Phys Anthrop 99:119–33

47. McBratney-Owen B, Lieberman DE (2003) Postnatal ontogeny of facial position in Homo sapiens and Pan troglodytes. In:

Thompson JL, Krovitz GE, Nelson AJ (eds) Patterns of Growth and Developement in the genus Homo. Cambridge University Press, Cambridge, pp 45-72

48. Siegel MI, Sadler D (1979) The chimpanzee as a model of anterior facial growth for cleft palate repair. Am J Phys Anthrop 50:481

49. Siegel MI, Mooney MP, Eichberg JW, et al (1992) Tensor analysis of nasal capsule shape changes following septomaxillary ligament resection in chimpanzees. Cleft Palate Craniofac J 29:137–42

50. Swindler DR, Sirianni JE, Tarrant LH (1973) A longitudinal study of cephalofacial growth in Papio cynocephalus and Macaca nemestrinafrom three months to three years. In: Zinge- ser MR (ed) Craniofacial Biology of Primates, Symposium of IVth International Congress of Primatology, vol. 3. Karger, Basen, pp 227-240

51. Sirianni JE, Van Ness AL (1978) Postnatal Growth of the Cranial Base inMacaca nemestrina. Am J Phys Anthrop 49:329–40 52. Lestrel PE, Sirianni JE (1982). The cranial base inMacaca nemes-

trina: Shape changes during adolescence. Hum Biol 54:7–21 53. Sirianni J, Van Ness AL, Swindler DR (1982) Growth of the

Mandible in Adolescent Pigtailed Macaques (Macaca nemestrina). Hum Biol 54:31–44

54. Lestrel PE, Bodt A, Swindler DR (1993) Longitudinal study of cranial base changes inMacaca nemestrina. Am J Phys Anthrop 91:117–29

55. Leigh SR, Cheverud JM (1991) Sexual dimorphism in the baboon facial skeleton. Am J Phys Anthrop 84:193–208 56. Collard M, O’Higgins P (2001) Ontogeny and homoplasy in the

papionin monkey face. Evol Dev 3:322–31

57. Swindler DR, Sirianni JE (1973) Palatal growth rates inMacaca nemestrinaandPapio cynocephalus. Am J Phys Anthrop 38:83–92 58. Van Wagenen G, Catchpole HR (1956) Physical growth of the rhe-

sus monkey (Macaca mulatta). Am J Phys Anthrop 14:245–73 59. Prat S, Berillon G, Herrscher E, et al (2013) Croissance osseuse

chez le babouin olive (Papio anubis): suivi longitudinal en capti- vité et perspectives anthropobiologiques. Bull Mem Soc Anthrop Paris 25:S34

60. Schultz AH, (1926) Fetal Growth of Man and Other Primates.

Q Rev Biol 1:465–521

61. Leigh S, (2001) Evolution of human growth. Evol Anthrop 10:223–36

62. Bogin B, (1999) Evolutionary perspective on human growth.

Annu Rev Anthropol 28:109–53

63. Lieberman DE, (2000) Ontogeny, homology, and phylogeny in the hominid craniofacial skeleton: the problem of the browridge.

In: O’Higgins P, Cohn M (ed) Developement, growth and evolution. Academic Press, London, pp 85-122