A geometric morphometric analysis of heterochrony in the cranium of chimpanzees and bonobos

Lieberman, Daniel E.; Carlo, Julian; León, Marcia Ponce de; Zollikofer, Christoph P.E.

doi:10.1016/j.jhevol.2006.12.005

Cited by 94 publications

(110 citation statements)

References 57 publications

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“…Indirect support for this view comes from the skulls of primates that are frequently cited as examples of parallel evolution of human-like cranial base morphology. For example, whereas the foramen magnum of the neurocranially "pedomorphic" bonobo (P. pansicus) skull tends to be located slightly more anterior than in the chimpanzee (19)(20)(21), its external base is relatively just as long and narrow as in the other African apes, and none of the derived tympanic and petrous anatomy is present (Fig. S2).…”

Section: Resultsmentioning

confidence: 99%

Ardipithecus ramidus and the evolution of the human cranial base

Kimbel

Suwa

Asfaw

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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The early Pliocene African hominoid Ardipithecus ramidus was diagnosed as a having a unique phylogenetic relationship with the Australopithecus + Homo clade based on nonhoning canine teeth, a foreshortened cranial base, and postcranial characters related to facultative bipedality. However, pedal and pelvic traits indicating substantial arboreality have raised arguments that this taxon may instead be an example of parallel evolution of human-like traits among apes around the time of the chimpanzee-human split. Here we investigated the basicranial morphology of Ar. ramidus for additional clues to its phylogenetic position with reference to African apes, humans, and Australopithecus. Besides a relatively anterior foramen magnum, humans differ from apes in the lateral shift of the carotid foramina, mediolateral abbreviation of the lateral tympanic, and a shortened, trapezoidal basioccipital element. These traits reflect a relative broadening of the central basicranium, a derived condition associated with changes in tympanic shape and the extent of its contact with the petrous. Ar. ramidus shares with Australopithecus each of these human-like modifications. We used the preserved morphology of ARA-VP 1/500 to estimate the missing basicranial length, drawing on consistent proportional relationships in apes and humans. Ar. ramidus is confirmed to have a relatively short basicranium, as in Australopithecus and Homo. Reorganization of the central cranial base is among the earliest morphological markers of the Ardipithecus + Australopithecus + Homo clade.A s the confluence of the neural, locomotor, and masticatory systems, the cranial base has been the site of profound structural change in human evolution. The modern human basicranium differs from that of our closest living relatives, the great apes, in numerous aspects of shape and morphological detail (1-4). In humans, the foramen magnum and occipital condyles are more anteriorly located, the midline basicranial axis is relatively short anteroposteriorly and strongly "flexed" internally, and the bilateral structures marking vascular and neural pathways through the central part of the base are more widely separated. This organization alters the relationships between the petrous and tympanic parts of the temporal bone. These phylogenetically derived features are already seen in the earliest known skulls of Australopithecus, ca. 3.0-3.4 Ma (5, 6).The cranium of Ardipithecus ramidus, an early Pliocene (4.4 Ma) hominoid from Ethiopia, was shown to have a relatively anterior foramen magnum on a short basicranium, corroborating evidence of nonhoning canine teeth and terrestrial bipedality for phylogenetic attribution of this taxon. These sets of derived characters are shared uniquely with the Australopithecus + Homo clade (7-10). At the same time, pelvic and pedal characters indicate that Ar. ramidus also retained considerable arboreal capabilities (11)(12)(13)(14). Despite the evidence for a unique phylogenetic relationship with the Australopithecus + Homo clade, it has been a...

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Section: Resultsmentioning

confidence: 99%

Ardipithecus ramidus and the evolution of the human cranial base

Kimbel

Suwa

Asfaw

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Modularity of the primate face is a likely advantage of these more structured facial colour patterns because it can enable higher levels of interspecific diversity 10,36,37 that would in turn be beneficial for species recognition. A modular framework characterizes the cranial morphology of many mammals, including primates [38][39][40] ; however, facial colour patterns have not been investigated in the context of modularity even though research suggests that various aspects of this system might be modular. First, work on mammal and insect colour patterns indicates that there is modular genetic control to the presence of colour patches and types of colouration 41,42 .…”

Section: Discussionmentioning

confidence: 99%

Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines

et al. 2013

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The faces of Old World monkeys and apes (Catarrhini) exhibit every possible hue in the spectrum of mammal colours. Animal colouration experiences selection for communication, physiology and ecology; however, the relative importance of these factors in producing facial diversity in catarrhines is not known. Here we adopt a comparative approach to test whether facial traits have evolved in tandem with social, geographic and ecological pressures across four catarrhine radiations. Our analyses reveal the underlying correlates of two major axes in the evolution of facial diversity. Facial colour patterns are linked to social factors, such that gregarious and highly sympatric species have evolved more colours in their faces. Facial pigmentation tends to be dominated by ecological factors, and species living in tropical, densely forested and humid habitats in Africa have evolved darker faces. Thus, both sociality and ecology have played a role in producing the highest diversity of faces within mammals.

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“…However, based on the patterns of cranial anatomy, it has been suggested that bonobos are pedomorphic relative to chimpanzees (e.g. Shea 1983, Lieberman et al 2007, and recent behavioral studies have reported species differences that are also indicative of pedomorphism (Hare et al 2012, reviewed in Wobber et al (2010). Two general possibilities that would be in line with the presumed heterochrony are that adrenarche in bonobos is either delayed or occurs earlier than in chimpanzees.…”

Section: Introductionmentioning

confidence: 99%

Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels

Behringer¹,

Hohmann²,

Stevens³

et al. 2012

Journal of Endocrinology

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Adrenarche is characterized by the onset of adrenal secretions of increasing amounts of dehydroepiandrosterone-sulfate (DHEA-S). While the function of adrenarche remains a matter of speculation, evidence suggests that the morphological and physiological changes related to it are restricted to humans and closely related primates. Within the primate order, adrenarche has been described only in humans and chimpanzees, but bonobos, the sister species of chimpanzees, have not yet been studied regarding the early ontogenetic changes such as adrenarche. While bonobos and chimpanzees share many morphological and behavioral characteristics, they differ in a number of behavioral traits, and there is a growing interest in terms of the physiological differences that can be linked to species-specific patterns of social behavior. In this study, we measured urinary DHEA-S levels to determine whether bonobos experience physiological changes that are indicative of adrenarche. We measured DHEA-S in urine using ELISA and analyzed its levels in the samples from 53 bonobos aged 1-18 years. Our results show that bonobos experience an increase in DHEA-S levels after 5 years of age, which is comparable with the patterns observed in humans and chimpanzees. This indicates that bonobos do undergo adrenarche and that the timing of onset is similar to that of the two Pan species. The extraction procedures described in this report demonstrate the use of urine for monitoring ontogenetic changes in DHEA-S excretion. If applicable to other species, the technique would facilitate more research on the evolutionary origin of adrenarche and other developmental processes.

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A geometric morphometric analysis of heterochrony in the cranium of chimpanzees and bonobos

Cited by 94 publications

References 57 publications

Ardipithecus ramidus and the evolution of the human cranial base

Ardipithecus ramidus and the evolution of the human cranial base

Adaptive response to sociality and ecology drives the diversification of facial colour patterns in catarrhines

Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels

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