Left-cradling bias is a distinctive feature of maternal behaviour in humans and great apes, but its evolutionary origin remains unknown. In 11 species of marine and terrestrial mammal, we demonstrate consistent patterns of lateralization in mother-infant interactions, indicating right hemisphere dominance for social processing. In providing clear evidence that lateralized positioning is beneficial in mother-infant interactions, our results illustrate a significant impact of lateralization on individual fitness.

BackgroundBehavioral laterality is known for a variety of vertebrate and invertebrate animals. Laterality in social interactions has been described for a wide range of species including humans. Although evidence and theoretical predictions indicate that in social species the degree of population level laterality is greater than in solitary ones, the origin of these unilateral biases is not fully understood. It is especially poorly studied in the wild animals. Little is known about the role, which laterality in social interactions plays in natural populations. A number of brain characteristics make cetaceans most suitable for investigation of lateralization in social contacts.Methodology/Principal FindingsObservations were made on wild beluga whales (Delphinapterus leucas) in the greatest breeding aggregation in the White Sea. Here we show that young calves (in 29 individually identified and in over a hundred of individually not recognized mother-calf pairs) swim and rest significantly longer on a mother's right side. Further observations along with the data from other cetaceans indicate that found laterality is a result of the calves' preference to observe their mothers with the left eye, i.e., to analyze the information on a socially significant object in the right brain hemisphere.Conclusions/SignificanceData from our and previous work on cetacean laterality suggest that basic brain lateralizations are expressed in the same way in cetaceans and other vertebrates. While the information on social partners and novel objects is analyzed in the right brain hemisphere, the control of feeding behavior is performed by the left brain hemisphere. Continuous unilateral visual contacts of calves to mothers with the left eye may influence social development of the young by activation of the contralateral (right) brain hemisphere, indicating a possible mechanism on how behavioral lateralization may influence species life and welfare. This hypothesis is supported by evidence from other vertebrates.

The right hemisphere plays a crucial role in social processing. Human mothers show a robust left cradling/holding bias providing greater right-hemispheric involvement in the exchange of social information between mother and infant. Here, we demonstrate that a similar bias is evident in face-to-face spatial interactions in marine and terrestrial non-primate mammals. Walruses and Indian flying foxes showed a significant population-level preference for the position which facilitates the use of the left visual field in both mother and infant. This behavioural lateralization may have emerged owing to benefits conferred by the enhanced right-hemispheric social processing providing the mother and infant an optimal perception of each other.

Recent studies have demonstrated a close resemblance between some handedness patterns in great apes and humans. Despite this, comparative systematic investigations of manual lateralization in non-primate mammals are very limited. Among mammals, robust population-level handedness is still considered to be a distinctive human trait. Nevertheless, the comprehensive understanding of handedness evolution in mammals cannot be achieved without considering the other large mammalian lineage, marsupials. This study was designed to investigate manual lateralization in non-primate mammals using the methodological approach applied in primate studies. Here we show that bipedal macropod marsupials display left-forelimb preference at the population level in a variety of behaviors in the wild. In eastern gray and red kangaroos, we found consistent manual lateralization across multiple behaviors. This result challenges the notion that in mammals the emergence of strong "true" handedness is a unique feature of primate evolution. The robust lateralization in bipedal marsupials stands in contrast to the relatively weak forelimb preferences in marsupial quadrupeds, emphasizing the role of postural characteristics in the evolution of manual lateralization as previously suggested for primates. Comparison of forelimb preferences in seven marsupial species leads to the conclusion that the interspecies differences in manual lateralization cannot be explained by phylogenetic relations, but rather are shaped by ecological adaptations. Species' postural characteristics, especially bipedality, are argued to be instrumental in the origin of handedness in mammals.