The heritability of chimpanzee and human brain asymmetry

Abstract

Human brains are markedly asymmetric in structure and lateralized in function, which suggests a relationship between these two properties. The brains of other closely related primates, such as chimpanzees, show similar patterns of asymmetry, but to a lesser degree, indicating an increase in anatomical and functional asymmetry during hominin evolution. We analysed the heritability of cerebral asymmetry in chimpanzees and humans using classic morphometrics, geometric morphometrics, and quantitative genetic techniques. In our analyses, we separated directional asymmetry and fluctuating asymmetry (FA), which is indicative of environmental influences during development. We show that directional patterns of asymmetry, those that are consistently present in most individuals in a population, do not have significant heritability when measured through simple linear metrics, but they have marginally significant heritability in humans when assessed through three-dimensional configurations of landmarks that reflect variation in the size, position, and orientation of different cortical regions with respect to each other. Furthermore, genetic correlations between left and right hemispheres are substantially lower in humans than in chimpanzees, which points to a relatively stronger environmental influence on left-right differences in humans. We also show that the level of FA has significant heritability in both species in some regions of the cerebral cortex. This suggests that brain responsiveness to environmental influences, which may reflect neural plasticity, has genetic bases in both species. These results have implications for the evolvability of brain asymmetry and plasticity among humans and our close relatives.

Reproducibility of leftward planum temporale asymmetries in two genetically isolated populations of chimpanzees ( Pan troglodytes )

“…If brain asymmetries reflect specific left or right hemisphere genetic regulation, then more lateralized brain regions would presumably have weaker interhemispheric correlations. This interpretation is supported by the results reported here, but whether this pattern could be expanded to additional brain regions remains unclear [58].…”

“…However, very few individual genes have so far been implicated in any aspect of lateralization of the human brain [46][47][48][49], and the genetic determinants of cerebral asymmetries are unknown and remain elusive [19,50,51]. Studies in humans suggest that there is heritability of brain asymmetries, notably within the PT [52][53][54], but this issue has not been explored in a wide range of nonhuman primates [55][56][57][58] or, to any extent, in our closest living relatives, the chimpanzees.…”

Mapping Cortical Brain Asymmetry in 17,141 Healthy Individuals Worldwide via the ENIGMA Consortium

“…Interestingly, cortical asymmetry of the human brain may also be associated with interhemispheric differences in gene expression (78,79). Moreover, besides the directional asymmetry (DA) studied in this study, fluctuating asymmetry (FA), defined as the distance from the populationlevel mean directional asymmetry, reflects environmental influences during development but shows significant heritability (80). In future ENIGMA genome-wide association studies of brain asymmetries, both indexes may be included as the phenotypes.…”

Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium

“…Finally, future research may also consider the degree of laterality (e.g., the unsigned magnitude of the asymmetry index) as being potentially both heritable and linked to other biological factors. Comparative analysis of human and chimpanzee data has indicated that the degree of laterality in either direction (left or right) may be a distinct and partly heritable aspect of human brain asymmetry (83).…”