The life history of Ardipithecus ramidus: a heterochronic model of sexual and social maturation

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In this paper we analyse the ontogeny of craniofacial growth in Ardipithecus ramidus in the context of its possible social and environmental determinants. We sought to test the hypothesis that this form of early hominin evolved a specific adult craniofacial morphology via heterochronic dissociation of growth trajectories. We suggest the lack of sexual dimorphism in craniofacial morphology provides evidence for a suite of adult behavioral adaptations, and consequently an ontogeny, unlike any other species of extant ape. The lack of sexually dimorphic craniofacial morphology suggests A. ramidus males adopted reproductive strategies that did not require male on male conflict. Male investment in the maternal metabolic budget and/or paternal investment in offspring may have been reproductive strategies adopted by males. Such strategies would account for the absence of innate morphological armoury in males. Consequently, A. ramidus would have most likely had sub-adult periods of socialisation unlike that of any extant ape. We also argue that A.ramidus and chimpanzee craniofacial morphology are apomorphic, each representing a derived condition relative to that of the common ancestor, with A. ramidus developing its orthognatic condition via paedomoporhosis, and chimpanzees evolving increased prognathism via peramorphosis. In contrast we suggest cranial volume and life history trajectories may be synapomorphic traits that both species inherited and retained form a putative common ancestral condition. Our analysis also provides support for the hypothesis that an intensification of maternal care was central to the process of hominization.

Alba D. 2002. Shape and Stage in Heterechronic Models, In: Minugh-Purvis N, editor. Baltimore: The Johns Hopkins University Press.

Alba D, Moya-Sola S, Kohler M, Rook, L. 2001. Heterochrony and the cranial anatomy of Oreopithecus: some cladistic fallacies ad the significance of developmental constraints in phylogenetic analysis. In: De Bonis L, Koufos G, Andrews P., editors. Hominoid Evolution and Climate Change in Europe: Phylogeny of the Neogene Hominoid Primates of Eurasia. Cambridge: Cambridge University Press. 284–315.

Altmann J. 2001. Baboon Mothers and Infants, 1st edn. Chicago: University of Chicago Press.

Baer KE von 1827. De ovi mammalium et hominis genesi: epistolam ad Academiam Imperialem Scientiarum Petropolitanam. Sumptibus L. Vossii.

Bjorklund DF, Pellegrini AD. 2002. The Origins of Human Nature: Evolutionary Developmental Psychology. Washington, DC: American Psychological Association.

Blount, B. 1990. ‘Issues in Bonobo (Pan Paniscus) Sexual Behavior’. American Anthropologist 92 (3). New Series (September 1): 702–14.

Bolk L. 1929. Origin of racial characteristics in man. Am J Phys Anthropol 13:1–28.

Burkart JM Fehr E, Efferson C, Schaik CP van 2007. Other-regarding preferences in a non-human primate: Common marmosets provision food altruistically. PNAS 104:19762–66.

Carroll SB. 2006. Endless forms most beautiful: the new science of Evo Devo and the making of the animal kingdom. New York: W W Norton & Co.

Cobb SN, O’Higgins P. 2007. The ontogeny of sexual dimorphism in the facial skeleton of the African apes. J Hum Evol 53:176–190.

Coen E. 2000. The art of genes: how organisms make themselves. Oxford: Oxford University Press.

Coolidge, H. 1933. ‘Pan Paniscus. Pigmy Chimpanzee from South of the Congo River’. Am J Phys Anthropol 18 (1): 1–59.

Deanner et. al. 2003. Primate Brains and Life Histories: Renewing the Connection. In: Kappeler P, Pereira M, editors. Primate Life Histories and Socioecology. University of Chicago Press. 233–65.

DeSilva JM. 2011a. A shift toward birthing relatively large infants early in human evolution. PNAS 201003865.

De Waal F. 1987. ‘Tension Regulation and Nonreproductive Functions of Sex in Captive Bonobos (Pan Paniscus)’. Natl Geogr Res 3: 318–35.

De Waal F. 1996. ‘The chimpanzees’ adaptive potential: a comparison of social life in the captive and wild conditions.’ In: Wrangham R., editor. Chimpanzee Cultures. Harvard University Press.

De Waal F. and Lanting F. 1998. Bonobo: The Forgotten Ape. Berkeley: University of California Press.

Dunsworth HM, Warrener AG, Deacon T, Ellison PT, Pontzer H, 2012. Metabolic hypothesis for human altriciality. PNAS 109:15212–16.

Goodall J. 1968. The behaviour of free-living chimpanzees in the Gombe Stream Reserve / Jane van Lawick-Goodall. London: Baillière, Tindall & Cassell.

Gould SJ. 1977. Ontogeny and phylogeny. Cambridge, Mass.: Belknap Press of Harvard University Press.

Gould SJ. 2002. The structure of evolutionary theory. Cambridge, Mass.: Belknap Press of Harvard University Press.

Gould S,J, Vrba E,S 1982. Exaptation-A Missing Term in the Science of Form. Paleobiology 8:4–15.

Groves CP. 1991. A Theory of Human and Primate Evolution, Revised edition. Oxford; New York: Oxford University Press.

Haile-Selassie Y. 2004. Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science 303:1503–5.

Haile-Selassie Y. Woldegabriel G. 2009. Ardipithecus Kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia. Berkeley: University of California Press.

Hall BK. 1999. Evolutionary developmental biology. Dordrecht; Boston; London: Kluwer Academic Publishers.

Hare B, Wobber V and Wrangham R. 2012. ‘The Self-domestication Hypothesis: Evolution of Bonobo Psychology Is Due to Selection Against Aggression’. Anim Behav 83 (3) (March): 573–85.

Harrison T. 1986. A reassessment of the phylogenetic relationships of Oreopithecus bambolii gervais. J Hum Evol 15:541–83.

Harrison T. 2010. Apes among the tangled branches of human origins. Science 327, 532–534.

Harvey PH, Kavanagh M, Clutton-Brock TH. 1978. Sexual dimorphism in primate teeth. J Zool 186:475–85.

Hawkes K. 2006. Life history theory and human evolution. A chronicle of ideas and findings. In: Hawkes K, Paine RR, editors. The Evolution of Human Life History. Santa Fe: School of American Research Press: Santa Fe, pp. 45–93.

Holloway RL. 1967. Tools and Teeth: Some Speculations Regarding Canine Reduction1. Am Anthropol 69:63–7.

Hylander WL. 2013. Functional links between canine height and jaw gape in catarrhines with special reference to early hominins. Am J Phys Anthropol 150:247–59.

Isler K, Christopher Kirk E, Miller JMA, Albrecht G, A Gelvin BR, Martin RD. 2008. Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. J Hum Evol 55:967–78.

Isler K, Van Schaik CP. 2012. Allomaternal care, life history and brain size evolution in mammals. J Hum Evol 63:52–63.

Kappeler PM, Pereira ME, editors. 2003. Primate life histories and socioecology. Chicago; London: University of Chicago Press.

Kelley J. 1997. Paleoecological and Phylogenetic Significance of Life History in Miocene Hominoids. In: Begun D, editor, New York: Plenum Press.

Kimbel WH, Suwa G, Asfaw B, Rak Y, White TD. 2014. Ardipithecus ramidus and the evolution of the human cranial base. PNAS 111:948–53.

Kirschner M, Gerhart J. 2005. The plausibility of life: resolving Darwin’s dilemma. New Haven: Yale University Press.

Konner M. 2010. Evolution of Childhood: Relationships, Emotion, Mind. Boston: Harvard University Press.

Laitman T. Heimbuch R. 1984. ‘A Measure of Basicranial Flexion in Pan Paniscus, the Pygmy Chimpanzee’. In: Susman R, editor. 1984. The Pygmy Chimpanzee: Evolutionary Biology and Behavior. 1st edn. Springer: pp. 49–63.

Lathouwers M,D, Elsacker LV. 2005. Reproductive parameters of femalePan paniscus and P. troglodytes: Quality versus quantity. Int J Primatol 26:55–71.

Laubichler MD, Maienschein J. 2007. From embryology to evo-devo: a history of developmental evolution. Cambridge, MA: MIT Press.

Lieberman DE. 2011. The Evolution of the Human Head, 1st edn. Cambridge, MA: Harvard University Press.

Lieberman DE, Ross CF, Ravosa MJ. 2000. The primate cranial base: ontogeny, function, and integration. Am J Phys Anthropol. Suppl 31:117–69.

Lovejoy CO. 2009. Reexamining Human origins in light of Ardipithecus ramidus. Science 326, 74–74e8.

Lovejoy O. 2014. Ardipithecus and earliest human evolution in light of 21st century developmental biology. Anthropol Res 70:337–363.

Martin RD. 1983. Human brain evolution in an ecological context (James Arthur lecture on the evolution of the human brain, no. 52, 1982). New York, NY: American Museum of Natural History.

Martin RD. 1996. Scaling of the mammalian brain: the maternal energy hypothesis. News Physiol Sci 11:146–56.

Martin RD. 1998. Comparative aspects of human brain evolution: Scaling energy costs and confounding variables. In: Jablonski NG, Aiello LC, editors. The Origin and Diversification of Language, pp. 35–68.

Martin RD. 2007. The evolution of human reproduction: A primatological perspective. Yrbk Phys Anthropol 50:59–84.

Martin RD. 2008. Evolution of placentation in primates: Implications of mammalian Phylogeny. Evol Biol 35:125–45.

Martin RD. 2013. How We Do It: The Evolution and Future of Human Reproduction, 5.12.2013 edition. New York: Basic Books.

Martin RD, Genoud M, Hemelrijk CK. 2005. Problems of allometric scaling analysis: examples from mammalian reproductive biology. J Exp Biol 208:1731–1747.

McIntyre, M., Herrmann E, Wobber V, Halbwax M, Mohamba C, de Sousa N, Atencia R, Cox D, and Hare B. 2009. ‘Bonobos Have a More Human-like Second-to-fourth Finger Length Ratio (2D:4D) Than Chimpanzees: a Hypothesized Indication of Lower Prenatal Androgens’. J Hum Evol 56(4): 361–5.

Minugh-Purvis N. McNamara KJ. 2002. Human Evolution through Developmental Change. Baltimore: Johns Hopkins University Press.

Moyà-Solà S, Alba DM, Almécija S, Casanovas-Vilar I, Köhler M, Esteban-Trivigno S, de Robles JM, Galindo J, Fortuny J, Pilbeam D. 2009. A unique Middle Miocene European hominoid and the origins of the great ape and human clade. PNAS 106:9601–6.

O’Higgins P, Jones N. 1998. Facial growth in Cercocebus torquatus: an application of three-dimensional geometric morphometric techniques to the study of morphological variation. J Anat 193:251–72.

O’Higgins P, Collard M. 2002. Sexual dimorphism and facial growth in papionin monkeys. J Zool 257:255–72.

Plavcan JM, Van Schaik CP. 1992. Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87:461–77.

Plavcan JM, Van Schaik CP, Kappeler PM. 1995. Competition, coalitions and canine size in primates. J Hum Evol 28:245–76.

Portmann A. 1945. Die Ontogenese des Menschen als Problem der Evolutionsforschung. Verh Schweiz Naturf Ges 125:44–53.

Portmann A. 1990. A zoologist looks at humankind. New York: Columbia University Press.

Raff RA. 1996. The shape of life: genes, development, and the evolution of animal form. Chicago: University of Chicago Press.

Robson SL, Wood B. 2008. Hominin life history: reconstruction and evolution. J Anat 212:394–425.

Ross C. 1988. The intrinsic rate of natural increase and reproductive effort in primates. J Zool 214:199–219.

Ross C. 2003. Life History, Infant Care Strategies, and Brain Size in Primates, In: Kappeler PM, editor. Primate Life Histories and Socioecology. Chicago: The of Chicago Press, pp. 266–98.

Sarmiento EE. 2010. Comment on the Paleobiology and Classification of Ardipithecus ramidus. Science 328:1105.

Sayers K, Raghanti MA, Lovejoy CO. 2012. Human evolution and the chimpanzee referential doctrine. Annu Rev Anthropol 41:119–38.

Schaefer K, Mitteroecker P, Gunz P, Bernhard M, Bookstein FL. 2004 Craniofacial sexual dimorphism patterns and allometry among extant hominids Ann Anat 186:471–78.

Schultz AH. 1924. Growth studies on primates bearing upon man’s evolution. Am J Phys Anthropol 7:149–64.

Schultz AH. 1936. Characters common to higher primates and characters specific for man. Q Rev Biol 11:259–83.

Shea B. 1983. Paedomorphosis and neoteny in the pygmy chimpanzee. Science 222:521–22.

Shea B. 1984. ‘An Allometric Perspective on the Morphological and Evolutionary Relationships Between Pygmy (Pan Paniscus) and Common (Pan Troglodytes) Chimpanzees’. In: Susman R., editor. The Pygmy Chimpanzee, Springer 89–130.

Smith BH, Tompkins RL. 1995. Toward a life history of the Hominidae. Annu Rev Anthropol 24:257–279.

Smuts BB. 2007. Sex and Friendship in Baboons. New Brunswick, NJ: Aldine Transaction.

Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW. 1987. Primate Societies, 1st edition. Chicago: University of Chicago Press.

Stanford CB. 2001. The Hunting Apes: Meat Eating and the Origins of Human Behavior, new edition. Princeton, NJ: Princeton University Press.

Stanford CB. 2012. Chimpanzees and the behavior of Ardipithecus ramidus. Annu Rev Anthropol 41:139–49.

Strauss WL, Schon MA. 1960. Cranial Capacity of Oreopithecus bambolii. Science. 9;132: 670–2.

Suwa G, Asfaw B, Kono RT, Kubo D, Lovejoy OC, White TD. 2009a. The Ardipithecus ramidus Skull and Its Implications for Hominid Origins. Science 326:68–68e7.

Suwa G, Kono RT, Simpson SW, Asfaw B, Lovejoy OC, White TD. 2009b. Paleobiological Implications of the Ardipithecus ramidus Dentition. Science 326:94–9.

Tanner N, Zihlman A. 1976. Women in Evolution. Part I: Innovation and Selection in Human Origins. Signs 1:585–608.

Thompson JL, Krovitz GE, Nelson AJ. 2003. Patterns of Growth and Development in the Genus Homo. 1st edn. Cambridge: Cambridge University Press.

Trivers R. 1972. Parental Investment and Sexual Selection, In: Campbell B, editior. Sexual Selection and the Descent of Man: 1871–1971. Chicago: Aldine Transaction.

West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford, New York: Oxford University Press.

Williams F, Godfrey L, Sutherland M. 2002. Heterochrony and the Evolution of Neandertal and Modern Human Craniofacial Form, In: Minugh-Purvis N, McNamara K, editors, Human Evolution Through Developmental Change. Baltimore: Johns Hopkins University Press.

Wrangham RW, Peterson D. 1997. Demonic Males: Apes and the Origins of Human Violence. London: Bloomsbury Publishing.

Zihlman A. 1981. Women as Shapers of the Human Adaptation, in: Dahlberg (Ed.), Women the Gatherer. New Haven: Yale University Press.

Zihlman A. 1978. Women and Evolution, Part II: Subsistence and Social Organization among Early Hominids. Signs 4.

Zihlman A, Cronin J, Cramer D and Sarich V. 1978. ‘Pygmy Chimpanzee as a Possible Prototype for the Common Ancestor of Humans, Chimpanzees and Gorillas’. Nature 275 (5682) (October 26): 744–6.

Zollikofer CPE, Ponce de León MS. 2010. The evolution of hominin ontogenies. Semin Cell Dev Biol 21:441–52.

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