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.
The preference to hold infants on the left rather than the right side of the body, as reported in human populations
, reflects socio-emotional processes and potentially facilitates mother–infant relationships
Both mother and infant potentially impact on lateralization 12 ; therefore, we aimed to differentiate their roles in asymmetrical positioning and to assess their lateral preferences separately. To record the choice of lateral position in mother–infant pairs, we studied ‘follower-type’ species, in which females and their dependent infants usually move side-by-side on parallel paths (Supplementary Fig. 1). Species with laterally placed eyes and relatively little binocular overlap were chosen because in such animals the expression of brain lateralization through one-sided behavioural biases is especially pronounced 13 . We employed a continuous focal animal sampling method 14 to record spontaneous mother–infant reunions after short-term spatial separations. The choice of lateral position was recorded when one pair member approached the other from behind and positioned itself on either the left or the right side (see Methods for details). This sampling method allowed for a straightforward analysis of individual- and population-level lateralization in a natural setting. Data consisted of 10,905 lateral position choices for 175 individually identified mother–infant pairs.
Hemispheric specialization for perception of conspecifics can be reflected by the physical positioning of individuals within their social environment
A significant population-level bias for keeping mother on the left side was found regardless of the species, behavioural type (with only the exception of resting in reindeer, see Supplementary Tables 1 and 2), or type of analysis (multiple versus single observations). Importantly, a left-side bias existed in infants not only in routine behaviours, but also in stressful situations, such as when fleeing. Our results indicated that a lateral bias reflects the infants’ preference to position the mother in their left hemispace (left visual field) rather than the preference for a particular side of the mother’s body. For example, Pacific walrus calves preferred to keep mother on the left side when resting both in a co-directed position (z = 2.16, P = 0.029) and in a counter-directed position (z = 3.06, P = 0.002) relative to the mother. That is, the leftward bias emerged regardless of which side of the mother’s body was exposed to the infant. The same was true for foals and saiga calves showing a significant preference to keep mother on the left when approaching her for suckling from different sides of her body (see Supplementary Tables 1 and 2). Factors such as an infant’s sex (tested in horses, grey kangaroos and red kangaroos) or age class (tested in walrus, horses and muskox) had no significant effect on lateralization (Supplementary Table 3).
The overall evidence for marine and terrestrial mammal species points to a common pattern of lateralization in an infant’s perception of mother (Fig. 1, Supplementary Tables 4–12). A meta-analytic approach was used for interspecies comparison. First, the meta-analysis based on individual lateral preferences revealed a uniform infant preference to keep mother on the left side, as indicated in the forest plot (Supplementary Fig. 2). Second, the meta-analysis based on single observations per individual showed lateralized spatial positioning to be consistent between infants of 11 non-human mammals approaching mothers (overall meta estimate = 0.74, P < 0.001; Fig. 2) and for human children approaching adults 15 . Similar to mammals in the present study, human children have been investigated unobtrusively in a natural setting that facilitates comparison with our results. It is important to note that the control condition, that is, choosing a position relative to stationary inanimate objects, did not elicit any lateralization either in children 15 or feral horse foals (see Supplementary Table 2). One-sided preferences in spatial positioning relative to a stimulus reflect the differential use of the lateral visual field of the left and right eye, and its underlying hemispheric specialization, as proved by a wide range of studies on vertebrates 13,18,19 . Within this context, the spatial preferences demonstrated here arise from the dominant role of the right hemisphere in an infant’s perception of mother. A left eye/right hemisphere advantage for the socio-emotional processing has been repeatedly reported for both human and non-human primates 5,11 . For example, great apes preferentially keep conspecifics on their left side compared with their right side 16 , much like non-primate infants in the present study. Our findings support the theory that a right lateralized ‘social brain’ in primates, including humans, stems from earlier forms of lateralization common to vertebrates 20 . The preference to keep a parent on the left side when begging for food observed in five out of six juvenile Australian magpies (Gymnorhina tibicen) 21 may imply that the lateralization of parent–offspring interactions is not restricted to the mammalian lineage.
It is reasonable to suggest that a prevalent left-sided bias may confer advantages for an infant. To test this hypothesis, we analysed the behaviour of infants within the equal time intervals that they spent in different lateral positions (see Methods). First, we found that feral horse foals initiated more bonding behaviour (positive social contacts) with mother when they kept her on the left side, rather than the right side (paired t-test: t 18 = 4.97, P < 0.001, n = 19). Second, we showed that the frequency of spatial separations between the pair members (when the infant was left behind the mother) was lower when the infant kept its mother on the left side before the separation, both in feral horses (paired t-test: t 19 = 3.65, P = 0.002, n = 20) and Pacific walrus (paired t-test: t 10 = 6.25, P < 0.001, n = 11). Thus, when perceiving a mother predominantly via the left eye–right hemisphere system, infants initiated more bonding behaviour and maintained the spatial proximity to mother more successfully than when perceiving her predominantly via the right eye–left hemisphere system (Supplementary Fig. 4). This may derive from a more general specialization of the right hemisphere for visuospatial processing, resulting in the attentional bias for the left visual hemifield 22 . Facilitation of bonding with mother and the maintenance of spatial proximity are obviously beneficial for an infant’s survival 23 . From the point of view of selective pressures, our findings indicate that it is advantageous for an infant to be left-lateralized.
We further demonstrate that the left-side bias in infants is not a specific response to mother, but derives from a more general lateralization in social behaviour. For example, all muskox calves studied showed individual preferences for a particular lateral position when approaching other familiar calves of the same age class (z = 3.18, P < 0.001, n = 12). A population-level preference to keep age mates to the left rather that the right side was found (W = 76, P < 0.001). Analyses based on single observations per individual pair indicated similar left-side biases in infant–infant interactions of saiga antelope (z = 2.59, P = 0.008, n = 18), feral horses (z = 2.18, P = 0.027, n = 29), beluga 24 and orca 25 . These results are consistent with the lateralization in human children when approaching a peer 15 . Lateral preferences in positioning towards conspecifics previously shown in interactions between adult mammals 16,17 were found to occur also in interactions between immature individuals.
In contrast to the infants’ lateral preferences, lateralization in a mother’s choice of position was behaviour-type-specific (Supplementary Tables 13 and 14). In feral horses, the numbers of lateralized and non-lateralized mares were compared, with significantly more mares showing no side preference for slow travelling (z = −2.62, P = 0.007, n = 21) and resting (z = −2.58, P = 0.007, n = 15). No population-level biases were found in these behaviours (slow travelling: W = −48, P = 0.383; resting: W = −59, P = 0.097). Conversely, when fleeing, the majority of mares were lateralized (z = 3.18, P < 0.001, n = 12) with a population-level preference for keeping foals on the left side (W = 76, P < 0.001). A similar pattern was observed in wild eastern grey kangaroos. In slowly travelling pairs, the significant majority of females had no preference for a particular lateral position relative to an infant (z = −2.02, P = 0.039, n = 12), and there was no population-level bias (one-sample t-test: t 11 = 1.67, P = 0.123, n = 12). However, analysis based on single observations per individual showed that, when fleeing, grey kangaroo mothers kept their infants predominantly on the left side (z = 3.21, P < 0.001, n = 28). Our results indicate that maternal lateralization was not pronounced in routine non-threatening circumstances, but emerged in stressful, potentially threatening situations. A left-sided bias has also been suggested for orca mothers when stressed by a vessel approach 25 . We can assume that a left-side bias in mothers is related to the increased need to monitor the infant in an unsafe environment. The left eye–right hemisphere system provides higher accuracy and speed for many types of social responses compared with the right eye–left hemisphere system 5,10,18 . Therefore, when keeping an infant in the left visual field, the mother may derive optimal control of the infant state. This is generally consistent with human studies that have demonstrated that a left-cradling bias is most pronounced during the first weeks of an infant’s life, when maternal visual monitoring of the infant’s state is most critical 6 .
Our results demonstrate that humans are one of many species showing strongly lateralized mother–infant spatial relations. The remarkably consistent occurrence of lateralization in interactions between an infant and its mother indicate that this is likely to be a pervasive mammalian feature of ancient evolutionary origin. Previous studies have shown maternal lateralization for holding an infant 1,6,26 in human and non-human primates. In this study we provide the first direct demonstration of lateralization in an infant’s active choice of spatial position near the mother in a diverse range of mammal species. Our findings suggest that sensory lateralization facilitates mother–infant bonding. We empirically demonstrate the advantages of lateralized infant behaviour in both marine and terrestrial mammals in support of the hypothesis that lateralization contributes to biological fitness 19,20,27 .
Data collection procedure
Data were collected in the course of 11 expeditions from 2012 to 2016. In addition, we analysed the photographs of southern right whales obtained during aerial surveys in 2005, 2008, 2010 and 2011. The data on beluga whales and orcas used here for interspecies comparisons were obtained during three expeditions from 2009 to 2011 25,28 . The total number of subjects for each species varied according to the type of behaviour studied (see Supplementary Tables 1, 2 and 4–14). The study sites, observational conditions, total sample sizes and infant ages are given in the Supplementary Methods.
Observations with binoculars and video recording of animal behaviour were conducted for 5–9 hours per day during 37–62 days per species (with the exception of southern right whales, for which pre-existing aerial photographs were examined). Every effort was made to minimize any possible disturbance of animals during observations. After the animals were approached, we waited at least 10 minutes before beginning data collection. If the animal displayed a flight response, it was not chased. Observational conditions allowed for a reliable visual estimation of infants’ sex only in feral horses, wild grey kangaroos and red kangaroos. Types of behaviour investigated in each species, and the photo-identification method used for recognition of individual pairs, are described in the Supplementary Methods.
We observed mother–infant pairs continuously and registered the choice of lateral position by pair members. The single choice of lateral position by an infant was defined as follows: after a pair member’s spatial separation, the infant approached the mother from behind at a distance of less than one adult animal length, and then positioned itself on one side of the mother, that is, the infant chose a side-by-side parallel position relative to the mother. This was the most typical variant of mother–infant reunions, and all other variants were discarded from the analysis. The only exception was resting in a counter-directed position studied in Pacific walrus. In this case the infant approached the resting mother from the front, and then took a lateral position near her. Discrete responses were obtained as follows: after a single choice of lateral position was registered, a subsequent choice was taken into account only after the pair had separated by a distance of more than one adult animal length, when the infant again approached the mother from behind (or from the front in Pacific walrus when resting in a counter-directed position).
To ensure that the infant’s choice of position was independent, we included only the events when the infant actively approached the mother, who moved forward or was motionless (depending on the type of behaviour investigated), and remained in an unbiased position (that is, the longitudinal axis of her body and head remained straight). If the mother turned her head or directed any other social response to the infant just before or during the infant’s position choice (that is, before it took a lateral position), the event was excluded from the study. Mother–infant reunions from a focal pair were included in the analysis only when there were no other conspecifics within approximately five adult animal lengths. If any feature of the landscape could potentially prevent the infant from choosing one of the lateral positions (for example, there was a cliff, dense vegetation or the water’s edge) on one side of the mother, such an event was discarded from the analysis.
The mother’s choice of lateral position after approaching the infant from behind was investigated in feral horses and eastern grey kangaroos. A mother’s lateral position choice was registered using the same inclusion criteria applied for an infant’s choice. In muskox, saiga antelope and feral horses, the choice of lateral position in infant–infant interactions was scored using a similar method.
In further analyses for infants and mothers, we used a lateral position preference as a behavioural marker of lateralization. This non-invasive and unobtrusive approach has proved to be informative in assessing lateralized social behaviour in natural settings 16,17,25,28,29 . The preference to keep conspecifics on one side of the body is widely accepted as a reflection of brain lateralization in social processing 10,15,16 . Such interpretation of animal behaviour in a natural social environment is based on early experimental studies that have demonstrated that one-sided behavioural preferences are underpinned by hemispheric specialization 19,20 .
In southern right whales, in contrast to other species studied, we analysed still images of mother–infant pairs. Images were selected that met the criteria as described previously 28 (see also Supplementary Methods for details).
Analysis of individual preferences
Preferences in lateral position choice were investigated in individual infants and mothers separately for each type of behaviour. Only the individuals with at least 15 position choice events were assessed for individual preferences.
The number of times an individual chose to keep the other pair member on the left side or on the right side was compared using a binomial test (z). As a result, each individual was classified as having no preference, or a preference for keeping the other pair member on the left/right side (Supplementary Tables 1 and 4–14). A binomial test was also used to examine the difference between the number of lateralized and non-lateralized individuals.
Analysis of population-level lateralization
The individual infants and mothers, for whom individual preferences were assessed, were included in population-level analyses. A widely applied laterality index (LI) 15,25 was calculated for each individual using the formula LI = (L−R)/(L + R), where L and R are the number of times the individual chose to keep the other pair member on the left or right side, respectively. LI scores range on a continuum from −1.0 to 1.0, with negative values indicating the right-side bias and positive values indicating the left-side bias. According to a Shapiro–Wilks test, the data were not normally distributed, therefore nonparametric tests were used. A one-sample Wilcoxon signed-rank test (W) was applied to evaluate the significance of population-level bias. All tests in the study were two-tailed and the level of significance was set at 0.05.
Besides the population-level analyses based on multiple observations (≥15) of focal individuals, we conducted analyses based on single observations per individual (see Supplementary Methods for details). The first observation of lateral position choice from each individual was included in the analysis. This method was used to enhance comparability of data across studies (for example, to compare our data with data on human children 15 ), and to increase the variety of studied species and behaviours. In argali and southern right whales, the analysis of single observations per individual pair was the only method of population-level analysis.
The consistency of lateralization across species was estimated using a meta-analytic approach. Random-effect subgroup meta-analysis (with each species as a subgroup) for multiple observations on focal individuals and random-effect meta-analysis for single observations per individual were computed using Open Meta-Analyst software, Tufts University, USA.
Estimating the advantages of lateralization
Here we aimed to exclude the influence of the infant’s preference for a particular lateral position. Therefore, in the analysis, the time intervals that infants spent keeping mother on the left and right side were equal. For each infant, in each day of observations, such intervals were equal to the least amount of time the infant spent keeping the mother on either side. First, we investigated the frequency of bonding behaviour initiation by feral horse foals in different lateral positions. Bonding behaviour was defined as positive social contacts easily recognizable by the observer, such as grooming (soft nibbling with teeth) and rubbing with the head or lips only 23 . Second, the frequency of spatial separations between the pair members was investigated. In feral horses and Pacific walrus, we analysed situations when the pair members travelled slowly side-by-side until the mother kept moving forward, while the infant was left behind her at an approximate distance of 10 m or more. We included in the analysis only the situation when the infant was alarmed after the spatial separation 23 and tried to rejoin the mother, that is, the infant most likely did not leave the mother intentionally. Finally, we tested whether the frequency of both types of event (spatial separations and initiation of bonding behaviour) differed significantly between two lateral positions (when the foals kept their mother on the left or the right side). Parametric paired t-tests were conducted as the data were normally distributed (Shapiro–Wilks test).
The data supporting the findings of the study are available within the article and its Supplementary Information.
How to cite this article: Karenina, K., Giljov, A., Ingram, J., Rowntree, V. J. & Malashichev, Y. Lateralization of mother–infant interactions in a diverse range of mammal species. Nat. Ecol. Evol. 1, 0030 (2017).
We thank the administration of the protected areas where data were collected for their cooperation and support. We thank A. Smorkatcheva, A. Vashurkina, V. Kalmikov, A. Kochnev, K. Leggett and S. Nicol for help in the organization of the field studies. The collection of data on lateralization in Pacific walrus, Siberian tundra reindeer, argali and southern right whales (inspection of aerial photographs), and all analytical work, was funded by the Russian Science Foundation (grant no. 14-14-00284). Field studies on grey and red kangaroos were supported by the National Geographic Society Committee for Research and Exploration (grant no. 9261-13). Field studies on saiga antelope, muskox and feral horses were supported by the Russian Foundation for Basic Research (grant no. 14-04-31390), and Saint Petersburg University (grant no.1.42.508.2013). The data on southern right whales were provided by Ocean Alliance and the Instituto de Conservacion de Ballenas, and were collected under research permits from the Dirección de Fauna y Flora Silvestre and the Subsecretaría de Turismo y Áreas Protegidas of Chubut Province, Argentina. Work was conducted with the approval of each protected area’s authorities and St Petersburg State University ethical committee (permit no. 131-03-5).
Supplementary Tables 4–14