Revisiting the homoiology hypothesis: the impact of phenotypic plasticity on the reconstruction of human population history from craniometric data

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

2011

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158

147

Variation in the masticatory behavior of hunter-gatherer and agricultural populations is hypothesized to be one of the major forces affecting the form of the human mandible. However, this has yet to be analyzed at a global level. Here, the relationship between global mandibular shape variation and subsistence economy is tested, while controlling for the potentially confounding effects of shared population history, geography, and climate. The results demonstrate that the mandible, in contrast to the cranium, significantly reflects subsistence strategy rather than neutral genetic patterns, with hunter-gatherers having consistently longer and narrower mandibles than agriculturalists. These results support notions that a decrease in masticatory stress among agriculturalists causes the mandible to grow and develop differently. This developmental argument also explains why there is often a mismatch between the size of the lower face and the dentition, which, in turn, leads to increased prevalence of dental crowding and malocclusions in modern postindustrial populations. Therefore, these results have important implications for our understanding of human masticatory adaptation.O ne of the major differences categorizing human populations is variation in subsistence strategies and related paramasticatory behavior. A shift from a primarily hunting and gathering strategy to one based on extensive horticulture or animal husbandry is known to have occurred independently on several occasions in human prehistory, yielding a correlated shift in settlement pattern, demography, population expansion, and social reorganization (e.g., 1, 2). Given the wider cultural changes associated with increased food processing and, therefore, consumption of a more homogeneous and softer diet in agriculturalists, it has been hypothesized that the dietary changes associated with agriculture are likely to have had an important effect on the form of the cranium and mandible (e.g., 3-5). Although localized studies comparing hunter-gather and farming populations in Nubia (6), South America (7), the Ohio Valley (8), and the southern Levant (9) have found some support for an associated change between the masticatory apparatus and the initial transition to agriculture, it is currently unclear what effect agriculture has had on global patterns of human mandibular variation when compared against other wider microevolutionary factors, such as gene flow, migration, and natural selection. Hence, this study represents a global comparative analysis of the effects of subsistence strategy on modern human mandibular variation.In recent decades, it has become clear that the majority of modern human cranial shape variation is congruent with a null model of neutral evolution, with relatively few morphological regions being subject to diversifying selection (e.g., 10-19). However, there appear to be two major exceptions to this general pattern. Aspects of facial morphology, and particularly nasal morphology, are likely to have been subject to diversifying natural sele...

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Global human mandibular variation reflects differences in agricultural and hunter-gatherer subsistence strategies

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

2011

Self Cite

158

147

“…In guenons, the morphology of several masticatory regions, the mandible, oral cavity, and zygomatic region, all yielded morphological matrices significantly correlated with genetic distances among taxa, but the non-masticatory chondrocranium did so with a higher correlation coefficient (Cardini and Elton, 2008). Therefore, despite the intuitive link between masticatory strain, plasticity, and homoplasy, the relationship between these factors is complex, and this phenomenon does not necessarily negatively affect the correspondence between cranial morphology and genetic patterns (von Cramon-Taubadel, 2009b;Roseman et al, 2010).…”

Section: Biomechanical Strainmentioning

confidence: 95%

The relative correspondence of cranial and genetic distances in papionin taxa and the impact of allometric adjustments

Smith

Journal of Human Evolution

2015

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The reconstruction of phylogenetic relationships in the primate fossil record is dependent upon a thorough understanding of the phylogenetic utility of craniodental characters. Here, we test three previously proposed hypotheses for the propensity of primate craniomandibular data to exhibit homoplasy using a study design based on the relative congruence between cranial distance matrices and a consensus genetic distance matrix ("genetic congruence") for papionin taxa: 1.Matrices based on cranial regions subjected to less masticatory strain are more genetically congruent than high-strain cranial matrices; 2. Matrices based on cranial regions developing earlier in ontogeny are more genetically congruent than matrices based on regions that develop later; 3.Matrices based on cranial regions with greater anatomical/functional complexity are more genetically congruent than matrices based on anatomically simpler regions.Morphological distance matrices based on the shape of 15 different cranial regions, delineated on the basis of previous catarrhine studies, were statistically compared to matrices of known genetic distances in papionins. Since sexual dimorphism and allometry are known to characterize this clade, several analytical iterations were conducted: 1) mixed-sex, male-only, and female-only analyses; 2) with and without an allometric scaling adjustment. Across all data sets, the chondrocranium matrix was the most consistently correlated with genetic distances, which is also consistent with previous studies of cercopithecoid taxa, however there was no consistent support for the internal predictions of the three hypotheses tested. Allometric scaling corrections had the largest impact on the genetic congruence of facial shape matrices, a result which is consistent with previous studies that have described facial homoplasy in papionin taxa. These findings differ from patterns described for hominoid taxa, suggesting that no single predictive criterion can explain phylogenetic utility of cranial datasets across catarrhine primate taxa. Many of the differences in morphological-genetic matrix correlations could result from different levels of phenotypic integration and evolvability in cercopithecoids and hominoids, suggesting that further study of these phenomena in extant primates is warranted.2

Congruence of Cranial and Genetic Estimates of Old World Primate Phylogeny

Encyclopedia of Life Sciences

2013

Inferring the phylogenetic relationships amongst fossil hominins is necessarily based on morphological data. Attempts to reconstruct fossil hominin phylogeny have yielded inconsistent and inconclusive results. Old world primates – apes and old world monkeys – provide key referents for understanding the phylogenetic signal in cranial data. Application of phylogenetic methods to cranial data from primate taxa has failed to uncover the known molecular genetic relationships of these major primate groups, suggesting that hominin phylogeny based on morphological data cannot be estimated with complete accuracy. Propositions regarding the potential efficacy of individual cranial regions have been empirically tested in both apes and old world monkeys. No clear criteria have been uncovered to predict the potential efficacy of cranial regions. However, recent studies have suggested that the taxonomic scale of the analysis and the allometric scaling relationships amongst taxa may both play key roles in determining the phylogenetic efficacy of cranial data. Key Concepts: Palaeoanthropologists rely on fossilised cranial remains to infer evolutionary history of hominins. Extant primates form necessary inference models for understanding human evolution. Attempts to reconstruct hominin phylogenies have generated inconsistent results. Some cranial traits are likely to be more reliable for reconstructing phylogeny than others. Masticatory traits have higher within‐taxon variance than nonmasticatory traits, but do not have lower phylogenetic efficacy. Basicranial traits may have higher phylogenetic efficacy in some primate groups. No clear rules exist for deciding which cranial traits have the greatest potential to uncover hominin relationships. Allometric scaling relationships among taxa affect the inference of phylogenetic relatedness. Taxonomic scale at which cranial–genetic congruence analyses are conducted may also be important.