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The Life History of Ardipithecus Ramidus: a Heterochronic Model of Sexual and Social Maturation

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The Life History of Ardipithecus Ramidus: a Heterochronic Model of Sexual and Social Maturation Early origins of human sexual and social maturation Gary Clark, Maciej Henneberg ANTHROPOLOGICAL REVIEW • Vol. 78 (2), 109–132 (2015) The life history of Ardipithecus ramidus: a heterochronic model of sexual and social maturation Gary Clark, Maciej Henneberg Biological Anthropology and Comparative Anatomy Unit University of Adelaide Medical School, Australia ABSTRACT: 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. rami- dus 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 inher- ited 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. KEY WORDS: facial growth, alloparenting, paedomorphosis, peramorphosis, cooperation, sexual dimorphism Introduction Ardipithecus genus. A. ramidus is thought to have inhabited a forest or woodland Debate over the early stages of human niche in Ethiopia approximately 4.5 Ma evolution has deepened in recent years (Lovejoy 2009). A. kadabba inhabited with the discovery of two putative fossil the same region from 5.8 to 5.2 Ma and hominins, classified as members of the is believed to be ancestral to A. ramidus Original Article: Received: March 2, 2015; Accepted for publication: May 16, 2015 DOI: 10.1515/anre-2015-0009 © 2015 Polish Anthropological Society 110 Gary Clark, Maciej Henneberg (Haile-Selassie and Woldegabriel 2009). 2012). However, the lack of sexual di- Objections have been raised as to wheth- morphism and male canine armoury ev- er A. ramidus is in actual fact a hominin ident in A. ramidus, as well as numerous (Sarmiento 2010; Harrison 2010). In re- anatomical affinities with Miocene apes, sponse to these objections it was argued has led researchers to question models of that significant behavioral and anatomi- early hominin social behaviour based on cal affinities betweenA. ramidus and other extrapolations from chimpanzees (Say- hominins (Sayers, Raghanti and Lovejoy ers, Raghanti and Lovejoy 2012), which 2012), as well as very detailed affinities are most likely derived in relation to the in the anatomy of the cranial base (Kim- common ancestral condition. Since hom- bel et al. 2014), confirm its hominin sta- inins and chimpanzees both seem to be tus. In this paper we will proceed under derived, it has been argued we need to the assumption A. ramidus is a hominin, look more carefully at the Miocene ape an assumption that may be validated or radiation in order to gain insight into the disproven by future research. common ancestral condition from which The published analysis of A. ramidus both lineages evolved (Lovejoy 2014). indicates an absence of male canine ar- A. ramidus consequently enables a more moury (Suwa et al. 2009b). This conclu- nuanced consideration of different de- sion was reached based on a sample of grees of differentiation from a Miocene canines from at least fourteen individu- great ape bauplan or body plan evident als, a sample larger enough for research- in the chimpanzee and hominin lineages ers to conclude the presence of males and (Lovejoy 2014). In this sense phyloge- females. Consequently a lack of canine netic diversity may be explained in terms sexual dimorphism was inferred from of differing degrees of differentiation or the absence of a bimodal distribution. departure from embryonic form (Baer Although reconstruction of the skull 1827), a situation in which differing on- morphology was based on one individu- togenies assume significant importance al, it is safe to infer from the monomor- in accounting for phylogenetic diversity. phic canine morphology the lack of a C/ The implication is that in order to P3 complex and consequently an atten- develop adult traits such as reduced dant reduction in facial prognathism as canines and minimal craniofacial sex- species specific traits in both males and ual dimorphism, A. ramidus must have females. had an ontogeny that distinguishes it Consequently the absence of cra- quite clearly from that of chimpanzees. nio-facial and postcranial sexual dimor- Given that selection does not act on phism has led to the conclusion that the adult characters, but on developmental species evolved male reproductive strate- processes themselves (West-Eberhard gies unlike those evident in any other spe- 2003), the A. ramidus fossils provide evi- cies of extant great ape (Lovejoy 2009). dence for a unique ontogeny at the base It has been common in the literature on of the hominin clade unlike that of any human evolution to use chimpanzee so- extant primate (Lovejoy 2014). In this cial and mating behaviour as a model for sense the fossils contribute a great deal reconstructing the social and mating sys- to our understanding of the evolution of tems of early hominins (Wrangham and early hominin social behaviour and life Peterson 1997; Stanford 2001; Stanford history. Early origins of human sexual and social maturation 111 The ontogeny of primates and homi- suggests the dissociation of craniofacial nins was studied quite extensively in the growth from other ontogenetic trajecto- first half of the twentieth century (Bolk ries that Gould analysed in the Australo- 1929; Schultz 1924; Schultz 1936; Port- pithecines may have much more ancient mann 1945). In his Ontogeny and Phyloge- origins than he originally assumed. ny (1977) Gould built on this early work Over the last fifty years comparative in his heterochronic model of human studies of primate morphology have en- evolution, suggesting that the retention hanced our understanding of the ontoge- of juvenile characters into sexual matu- ny of extinct hominins (Smith and Tomp- rity was fundamental to the process of kins 1995; Mann 1975; Bromage 1985). hominization (Gould 1977). According Notably Smith and Tompkins (1995) to Gould, heterochronic dissociation of argued that in hominoids major life his- developmental trajectories is an impor- tory trajectories evolved in tandem with tant evolutionary mechanism whereby increases in brain size. A significant body the rates of growth in different ontoge- of literature has consequently built on netic fields can be altered in relation to these studies, resulting in an increas- one another. In arguing that taxonomic ingly refined understanding of the life diversity results from altering an ances- history and ontogeny of fossil hominins tral bauplaun or body plan, Gould sought (Minugh-Purvis and McNamara 2002; to resurrect older models of evolutionary Thompson, Krovitz and Nelson 2003; change based on alterations of develop- Hawkes et al. 2006; Robson and Wood ment timing, an approach that underpins 2008; Zollikofer and Ponce de León current research in evolutionary devel- 2010). In terms of craniofacial variation opmental biology (Hall 1999; Raff 1996; amongst primates, it has been suggest- Coen 2000; West-Eberhard 2003; Kirsch- ed that males and females share juvenile ner and Gerhart 2005; Laubichler and and sub-adult growth trajectories, but Maienschein 2007; Carroll 2006; Gould diverge significantly during the period 2002). Gould’s model has also been ap- of sexual maturation. Consequently, sex- plied in a number of studies of fossil based differences in ontogeny associated species and of human and primate evo- with reproductive biology are thought to lution (Groves 1991; Shea 1983; Alba et account for sexual dimorphism in adult al. 2001; Bjorklund and Pellegrini 2002; craniofacial form (O’Higgins and Jones Konner 2010). 1998). It is likely that the lack of cran- In Ontogeny and Phylogeny Gould dis- iofacial sexual dimorphism evident in cussed heterocrhony in relation to the A. ramidus may be a result of changes in craniofacial form of Australopithecines and ontogeny associated with sexual matura- Homo sapiens. What is interesting to note tion, social behaviour and reproductive is that the orthognathic skull morpholo- strategies – strategies unlike those evi- gy of A. ramidus suggests this species may dent in any other extant nonhuman spe- have evolved via heterochronic dissocia- cies of the hominoid clade. tion of craniofacial growth trajectories In order to test the hypothesis that from those of sexual maturation. A. rami- craniofacial growth was decoupled from dus therefore provides
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