Heritability of hand preference in chimpanzees (Pan troglodytes): Evidence from a partial interspecies cross-fostering study.

Abstract

Heritability of hand preference was tested in a sample of 188 chimpanzees (Pan troglodytes). Hand preference was measured by coordinated bimanual actions, and concordance percentages were compared between parents and offspring and siblings. Among siblings, concordance percentages were compared for dyads in which both individuals were raised by chimpanzees, both were raised by humans, or 1 was raised in each environment. The results indicated population-level right hand preferences for coordinated bimanual actions. There were no significant associations in hand preference between parents and offspring. In full and maternal half siblings, concordance in hand preference was significantly greater than chance in mother-and human-reared individuals but not in cross-fostered dyads. The cumulative results suggest that the direction of hand preference is heritable in chimpanzees but the mechanism of transmission is not genetic. Several environmental explanations are proposed to explain the findings, including the potential role of maternal cradling bias and in utero fetal position.Approximately 75% to 90% of modern humans report themselves as being right-handed (Annett, 1985;Porac & Coren, 1981). The general view is that human right-handedness evolved within the past 2 to 5 million years, as evidenced by the archeological data suggesting righthand use in tool use and other activities in early hominids (Bradshaw & Rogers, 1993;Corballis, 1991). The pervasiveness of human right-handedness has led to numerous debates about the mechanisms involved in the expression of hand preference (B. Hopkins & Ronnqvist, 1998). Both genetic models (Annett, 1985;Corballis, 1997;Laland, Kumm, Van Horn, & Feldman, 1995;McManus, 1985;Yeo & Gangestad, 1993) and environmental models (Collins, 1985;Provins, 1997) have been proposed to explain the origin of human hand preference. The principal data in support of a genetic basis for hand preference are that it runs in families (Curt, De Agostini, Maccario, & Dellatolas, 1995;Laland et al., 1995;McGee & Cozad, 1980;McManus & Bryden, 1992) and that offspring typically exhibit patterns of hand preference more similar to their biological parents compared with offspring who have been adopted or raised by stepparents (Carter-Saltzman, 1980;Hicks & Kinsbourne, 1976).In contrast with humans, the historical view has been that nonhuman animals, particularly nonhuman primates, do not exhibit population-level handedness (see Ettlinger, 1988;Warren, 1980). In recent years, behavioral research in a variety of nonhuman primate species has revealed that population-level handedness can be found in some species for certain measures (Bradshaw & Rogers, 1993;Fagot & Vauclair, 1991;W. D. Hopkins, 1996b Studdert-Kennedy, & Lindblom, 1987;Ward & Hopkins, 1993). Notwithstanding, considerable disagreement remains about the interpretation of the findings in nonhuman primates as they pertain to human handedness. For instance, McGrew and Marchant (1997) argued that the evidence for population-level handedness in no...

Laterality in Maternal Cradling and Infant Positional Biases: Implications for the Development and Evolution of Hand Preferences in Nonhuman Primates

“…In captive chimpanzees, full-and maternal half-siblings raised in the same environment exhibit concordant hand preferences that are significantly greater than chance for ≥2 measures of hand preference (Hopkins, 1999; Fig. 3).…”

“…Predicting significant associations in hand preference between offspring and parents, particularly maternal effects, are contingent upon whether the females cradle or carry their offspring due to inherent biases in their hand preference. In chimpanzees, there is no association between female maternal cradling biases and their hand preference, nor is there a strong association between maternal and offspring hand preference (Hopkins, 1999). Salk (1973) argued that hand preferences are unrelated to maternal cradling biases in humans (Salk, 1973).…”

“…In nonhuman primates, there is some evidence that hand preferences run in families (Hopkins et al, 1994;Matoba et al, 1991) but not all researchers have reported significant associations (Boesch, 1991;Brooker et al, 1981;Byrne and Byrne, 1991;Westergaard and Suomi, 1997), and in most studies the independent effect of genetic from nongenetic factors cannot be easily dissociated (Hopkins, 1999;Hopkins et al, 2001). In other words, the evidence of heritability has mostly come from family studies in which no differential rearing or cross-fostering comparisons are made in the phenotypic expression of handedness.…”

Comparative and familial analysis of handedness in great apes.

“…Warren (1980) was a strong proponent of the view that population-level handedness was uniquely human and that genetic factors determined human handedness, whereas nongenetic factors determined nonhuman limb preferences. Approximately 20 years ago very few studies existed on heritability of hand preference in nonhuman primates, and the results were equivocal (see Hopkins, 1999a, for review). Furthermore, paw preference studies failed to reveal any evidence that directional biases in paw use could be selectively bred for in certain strains of mice, although it should pointed out that strength in paw preference could be selectively bred for (Collins, 1985).…”

Posture and laterality in human and non-human primates: Asymmetries in maternal handling and the infant's early motor asymmetries

“…Their results were in favour of the existence of a hereditary component for the expression of handedness. Using the coordinated bimanual tube task to test parent and offspring chimpanzees, Hopkins (1999) suggests that the direction of hand preference is heritable, although it is unlikely that the mechanism of transmission is genetic. It could be instead that it is behavioural, with infant handedness being determined by the behaviour of the mother.…”