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

Homoiologies are homoplasies that are caused by nongenetic environmental factors. The homoiology hypothesis predicts that osseous regions subject to repeated biomechanical stress during growth should be more variable and, therefore, less reliable for the reconstruction of phylogeny compared with osseous regions relatively unaffected by stress. Previous studies based on the analysis of multiple primate species found that regions of the cranium subject to masticatory-induced stress were significantly more variable than non-masticatory regions, as predicted by the homoiology hypothesis. However, these studies also found that the masticatory regions were no less reliable for reconstructing primate phylogenetic relationships when subjected to parsimony analysis. It was suggested, therefore, that homoiology may be a more potent problem for the reconstruction of phylogeny at the intraspecific level rather than interspecific phylogenetics. This suggestion was tested here using matched molecular and craniometric data for 12 modern human populations. The results show that, as predicted by the homoiology hypothesis, regions of the human cranium related to mastication were more variable than non-masticatory regions. However, masticatory regions were no less reliable for inferring human population history. Therefore, the results match those found from the interspecific analysis of primate species and do not support the suggestion that homoiology is a greater problem for the analysis of intraspecific taxa. The results also suggest that within-taxon variability cannot be relied upon to predict the phylogenetic efficacy of morphometric characters.

von Cramon-Taubadel N 《-》

Do homoiologies impede phylogenetic analyses of the fossil hominids? An assessment based on extant papionin craniodental morphology.

Homoiologies are phylogenetically misleading resemblances among taxa that can be attributed to phenotypic plasticity. Recently, it has been claimed that homoiologies are widespread in the hominid skull, especially in those regions affected by mastication-related strain, and that their prevalence is a major reason why researchers have so far been unable to obtain a reliable estimate of hominid phylogeny. To evaluate this "homoiology hypothesis", we carried out analyses of a group of extant primates for which a robust molecular phylogeny is available-the papionins. We compiled a craniometric dataset from measurements that differ in their susceptibility to mastication-related strain according to developmental considerations and experimental evidence. We used the coefficient of variation and analysis of variance with post hoc least significant difference comparisons in order to evaluate the variability of the measurements. The prediction from the homoiology hypothesis was that dental measurements, which do not remodel in response to strain, should be less variable than low-to-moderate-strain measurements, and that the latter should be less variable than high-strain measurements. We then performed phylogenetic analyses using characters derived from the measurements and compared the resulting phylogenetic hypotheses to the group's consensus molecular phylogeny. The prediction was that, if the homoiology hypothesis is correct, the agreement between the craniometric and molecular phylogenies would be best in the analyses of dental characters, intermediate in the analyses of low-to-moderate-strain characters, and least in the analyses of high-strain characters. The results of this study support the suggestion that mastication-related mechanical loading can result in variation in hominid cranial characters. However, they do not support the hypothesis that homoiology is a major reason why phylogenetic analyses of hominid crania have so far yielded conflicting and weakly supported hypotheses of relationship. These findings are consistent with a recent test of the homoiology hypothesis using craniodental data from extant hominoids, and cast doubt on the validity of the homoiology hypothesis, as originally formulated.

Lycett SJ ，Collard M 《journal of human evolution》

Hominin homoiology: an assessment of the impact of phenotypic plasticity on phylogenetic analyses of humans and their fossil relatives.

Homoiologies are phylogenetically misleading morphological similarities that are due to nongenetic factors. It has been claimed that homoiologies are common in the hominin skull, especially in regions affected by masticatory strain, and that their prevalence is one reason why reconstructing hominin phylogenetic relationships is difficult. To evaluate this "homoiology hypothesis," we performed analyses on a group of extant primates for which a robust molecular phylogeny is available--the hominoids. We compiled a data set from measurements that developmental considerations and experimental evidence suggest differ in their likelihood of exhibiting masticatory-strain-induced phenotypic plasticity. We then used the coefficient of variation and t-tests to evaluate the phenotypic plasticity of the measurements. We predicted that, if the hypothesis is correct, the measurements of skeletal features that do not remodel and therefore are unaffected by phenotypic plasticity should be less variable than the measurements of skeletal features that remodel and are subject to low-to-moderate strains, and that the latter should be less variable than the measurements of skeletal features that remodel and are subject to moderate-to-high strains. Subsequently, we performed phylogenetic analyses on character state data derived from the measurements and compared the resulting phylogenetic hypotheses to the consensus molecular phylogeny for the hominoids. We predicted that, if the hypothesis is correct, agreement between the phylogenies should be best for the non-phenotypically-plastic characters, intermediate for the low-to-moderate-strain characters, and worst for the moderate-to-high-strain characters. The results of the coefficient of variation/t-test analyses were consistent with the predictions of the hypothesis to the extent that the moderate-to-high-strain measurements exhibited significantly more variability than the non-phenotypically-plastic and low-to-moderate-strain measurements. In contrast, the results of the phylogenetic analyses were not those predicted. The phylogeny derived from the moderate-to-high-strain characters matched the molecular phylogeny better than those obtained using the non-phenotypically-plastic and low-to-moderate-strain characters. Thus, our study supports the suggestion that mechanical loading results in phenotypic plasticity in the hominin skull, but it does not support the notion that homoiologies have a significant negative impact on hominin phylogenetics.

Collard M ，Wood B 《journal of human evolution》

Homoplasy and the early hominid masticatory system: inferences from analyses of extant hominoids and papionins.

Early hominid masticatory characters are widely considered to be more prone to homoplasy than characters from other regions of the early hominid skull and therefore less reliable for phylogenetic reconstruction. This hypothesis has important implications for current reconstructions of early hominid phylogeny, but it has never been tested. In this paper we evaluate the likely veracity of the hypothesis using craniometric data from extant primate groups for which reliable consensus molecular phylogenies are available. Datasets representing the extant large-bodied hominoid genera and the extant papionin genera were compiled from standard measurements. The data were adjusted to minimise the confounding effects of body size, and then converted into discrete character states using divergence coding. Each dataset was divided into four regional character groups: (1) palate and upper dentition, (2) mandible and lower dentition, (3) face and (4) cranial vault and base. Thereafter, the regional character groups were analysed using cladistic methods and the resulting phylogenetic hypotheses judged against the consensus molecular phylogenies for the hominoids and papionins. The analyses indicated that the regions dominated by masticatory characters-the palate and upper dentition, and the mandible and lower dentition-are no less reliable for phylogenetic reconstruction than the other regions of the skull. The four regions were equally affected by homoplasy and were, therefore, equally unreliable for phylogenetic reconstruction. This finding challenges the recent suggestion that Paranthropus is polyphyletic, which is based on the assumption that masticatory characters are especially prone to homoplasy. Our finding also suggests that, contrary to current practice, there is no a priori reason to de-emphasise the phylogenetic significance of the masticatory similarities between Homo rudolfensis and the australopiths. The corollary of this is that H. rudolfensis is unlikely to be a member of the Homo clade and should therefore be allocated to another genus.

Collard M ，Wood B 《journal of human evolution》

The relative efficacy of functional and developmental cranial modules for reconstructing global human population history.

This study tests the relative efficacy of human cranial modules, defined on the basis of developmental and functional criteria, for reconstructing neutral genetic population history. Specifically, two hypotheses were tested: 1) The "basicranial hypothesis" predicts that the endochondrally ossifying basicranium will be more reliable for reconstructing population history than intramembranously ossifying regions of the human cranium. This is based on the assumption that early ossification of the basicranium and its distinct functional constraints produce a cranial structure that is relatively immune to non-neutral evolutionary forces. 2) The "single function hypothesis" predicts that cranial regions associated with a single (sensory) function are less reliable indicators of neutral genetic history. Here the prediction is based on the logic that complex, multi-functional, integrated cranial regions are less likely toexhibit homoplasy and, therefore, provide a more accurate morphological proxy for genetic relationships. The congruence between craniometric affinity matrices and neutral genetic population matrices based on autosomal microsatellite and classical markers was assessed using a series of Mantel and Dow-Cheverud tests. The results did not support the predictions of the "basicranial hypothesis," as the endochondrally ossifying basicranium was not significantly more congruent with the genetic data than intramembraneously ossifying modules. Moreover, although the results provided some support for the "single function hypothesis," defining cranial modules on the basis of anatomical or functional complexity did not provide a consistent means of predicting their phylogenetic efficacy. These results have important implications for building an accurate inference model of cranial evolution in the human fossil record.

von Cramon-Taubadel N 《-》