Karina Karenina

Lateralization of mother–infant interactions in a diverse range of mammal species

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.

Lateralization of spatial relationships between wild mother and infant orcas, Orcinus orca

Cooperative interactions have been argued to be a powerful factor mediating the evolution of lateralization in animals. Mother−infant asymmetric spatial relationships represent a case of social coordination among organisms. Although lateralized interactions between mothers and infants have been found in beluga whales, Delphinapterus leucas, whether this is the case in other cetaceans remains unknown. In the current study, we investigated mother–infant spatial laterality, more specifically, the lateral biases in an infants position near its mother in wild orcas, Orcinus orca. Distances between the research boat and whales were categorized into three groups to test the influence of a potential threat on laterality expression. Observations on travelling individually identified mother–infant pairs showed group-level preference for the infant to be on the mothers right side when far from the boat. This bias reversed at close distance. At an intermediate distance, no significant side bias was found; however, when we considered only cases of apparent mother−calf pair avoidance of the boat for analysis, the left-sided bias was again observed. In contrast, when infants were socializing near mothers or when they followed older calves, the infants preferred the right side. We argue that these preferences are associated with right-hemispheric advantage in social responses, while the shift from right-sided to left-sided bias in potentially threatening situations is caused by role reversal between mother and infant in determining their relative position in the dyad. Cetaceans seem to share with primates the pronounced lateralization of parent−offspring relationships.

Limb preferences in a marsupial, Macropus rufogriseus: evidence for postural effect

In many primate species, bipedal stance is a factor increasing manual laterality. To understand this phenomenon better, there is a need to investigate forelimb preferences in nonprimate mammals with bipedal locomotion as the preferred gait, such as bipedal hopping marsupials. We studied laterality in forelimb use in 27 adult red-necked wallabies during their usual daily activity in five zoos. During feeding from the bipedal position adult wallabies displayed group-level left-forelimb preference with the majority of individuals being lateralized. However, no lateralization was found at the group level during feeding from the quadrupedal position, with only a few animals expressing individual preferences. Wallabies showed significant group-level bias while using the right forelimb for supporting the body in the tripedal stance, with nearly half the individuals being lateralized. On a smaller sample of nine wallabies forelimb preferences in unimanual snout autogrooming were studied: seven individuals preferred to use their left forelimb and two displayed no preference. Additionally, we studied asymmetrical limb use during milk suckling in six young-at-foot wallabies. Here, all subjects more often pulled down the mother’s pouch edge with the left forelimb and simultaneously supported the body with the right paw. Our results show that marsupials can display motor laterality at both individual and group levels, comparable with those observed in placentals. Moreover, in red-necked wallabies, much as in primates, the bipedal posture favours the expression of manual laterality, while its direction depends on the functional nature of the motor action. Evolutionary scenarios such as the postural origin theory of behavioural lateralization are discussed.

Eye as a key element of conspecific image eliciting lateralized response in fish

Visual lateralization in different aspects of social behaviour has been found for numerous species of vertebrates ranging from fish to mammals. For inspection of a shoal mate, many fishes show a left eye–right hemisphere preference. Here, we tested the hypothesis that in fish, there is a key cue in the conspecific appearance, which elicits lateralized response to the whole image of the conspecific. In a series of eight experiments, we explored eye preferences in cryptic-coloured Amur sleeper, Perccottus glenii, fry. Fish displayed left-eye preferences at the population level for inspection of a group of conspecifics, their own mirror image, and a motionless flat model of a conspecific. In contrast, no population bias was found for scrutinizing an empty environment or a moving cylinder. When fry were showed a model of a conspecific in a lateral view with the eye displaced from the head to the tail, they again showed a significant preference for left-eye use. On the other hand, ‘eyeless’ conspecific model elicited no lateralized viewing in fry. Finally, the left-eye preference was revealed for scrutiny of the image of a conspecific eye alone. We argue that in Amur sleeper fry, eye is the element of the conspecific image, which can serve as a ‘key’ for the initiation of lateralized social response. This key element may serve as a trigger for the rapid recognition of conspecifics in the left eye–right hemisphere system. Possible causes and advantages of lateralized perception of social stimuli and their key elements are discussed in the context of current theories of brain lateralization.

Forelimb preferences in quadrupedal marsupials and their implications for laterality evolution in mammals

BackgroundAcquisition of upright posture in evolution has been argued to facilitate manual laterality in primates. Owing to the high variety of postural habits marsupials can serve as a suitable model to test whether the species-typical body posture shapes forelimb preferences in non-primates or this phenomenon emerged only in the course of primate evolution. In the present study we aimed to explore manual laterality in marsupial quadrupeds and compare them with the results in the previously studied bipedal species. Forelimb preferences were assessed in captive grey short-tailed opossum (Monodelphis domestica) and sugar glider (Petaurus breviceps) in four different types of unimanual behaviour per species, which was not artificially evoked. We examined the possible effects of sex, age and task, because these factors have been reported to affect motor laterality in placental mammals.ResultsIn both species the direction of forelimb preferences was strongly sex-related. Male grey short-tailed opossums showed right-forelimb preference in most of the observed unimanual behaviours, while male sugar gliders displayed only a slight, not significant rightward tendency. In contrast, females in both species exhibited consistent group-level preference of the left forelimb. We failed to reveal significant differences in manual preferences between tasks of potentially differing complexity: reaching a stable food item and catching live insects, as well as between the body support and food manipulation. No influence of subjects’ age on limb preferences was found.ConclusionsThe direction of sex-related differences in the manual preferences found in quadrupedal marsupials seems to be not typical for placental mammals. We suggest that the alternative way of interhemispheric connection in absence of corpus callosum may result in a fundamentally distinct mechanism of sex effect on limb preferences in marsupials compared to placentals. Our data confirm the idea that non-primate mammals differ from primates in sensitivity to task complexity. Comparison of marsupial species studied to date indicate that the vertical body orientation and the bipedalism favor the expression of individual– and population–level forelimb preferences in marsupials much like it does in primates. Our findings give the first evidence for the effect of species-typical posture on the manual laterality in non-primate mammals.

An eye for a worm: Lateralisation of feeding behaviour in aquatic anamniotes

Some animals, notably birds, preferentially approach and capture food items in their right visual field. However, this lateralised behaviour has not been studied extensively in anamniotes. Here we test eye preference during feeding for a fish, (Perccottus glenii; Teleostei, Perciformes), a newt, (Pleurodeles walti; Amphibia, Caudata), and a frog, (Xenopus laevis; Amphibia, Anura) using a test chamber that assesses reaction to visual stimuli while blocking olfactory and mechanical input. Both the fish and the newt showed right preferences in reactions to food items, but the frog did not. Our data extend our knowledge of the lateralised behaviours of vertebrates and are the first record of lateralised prey capture in a caudate amphibian. This finding dates back the history of the common pattern for visual lateralisation in vertebrates to Devonian, when the fish and quadruped lineages diverged.

Facing each other: mammal mothers and infants prefer the position favouring right hemisphere processing

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.

Does Bipedality Predict the Group-Level Manual Laterality in Mammals?

Background Factors determining patterns of laterality manifestation in mammals remain unclear. In primates, the upright posture favours the expression of manual laterality across species, but may have little influence within a species. Whether the bipedalism acts the same in non-primate mammals is unknown. Our recent findings in bipedal and quadrupedal marsupials suggested that differences in laterality pattern, as well as emergence of manual specialization in evolution might depend on species-specific body posture. Here, we evaluated the hypothesis that the postural characteristics are the key variable shaping the manual laterality expression across mammalian species. Methodology/Principal Findings We studied forelimb preferences in a most bipedal marsupial, brush-tailed bettong, Bettongia penicillata in four different types of unimanual behavior. The significant left-forelimb preference at the group level was found in all behaviours studied. In unimanual feeding on non-living food, catching live prey and nest-material collecting, all or most subjects were lateralized, and among lateralized bettongs a significant majority displayed left-forelimb bias. Only in unimanual supporting of the body in the tripedal stance the distribution of lateralized and non-lateralized individuals did not differ from chance. Individual preferences were consistent across all types of behaviour. The direction or the strength of forelimb preferences were not affected by the animals’ sex. Conclusions/Significance Our findings support the hypothesis that the expression of manual laterality depends on the species-typical postural habit. The interspecies comparison illustrates that in marsupials the increase of bipedality corresponds with the increase of the degree of group-level forelimb preference in a species. Thus, bipedalism can predict pronounced manual laterality at both intra- and interspecific levels in mammals. We also conclude that quadrupedal position in biped species can slightly hinder the expression of manual laterality, but the evoked biped position in quadrupedal species does not necessarily lead to the enhanced manifestation of manual laterality.

Social lateralization in wild Asian elephants: visual preferences of mothers and offspring

Theoretical and empirical evidence suggest that socio-biological factors determine the expression of behavioural lateralization across species. One would expect the same association at the intraspecific level, that is, that the differences in social strategies of the two sexes entail the sex differences in the lateralized social processing. This study aimed to test whether this hypothesis applies to the lateralized behaviour of offspring towards a mother. The preferences in the use of the lateral visual field of the left and right eye were assessed in wild Asian elephant, Elephas maximus mothers and their young sons and daughters. The spatial positioning relative to a social partner during approach was used as a behavioural indicator of visual lateralization. At the population level, elephant mothers preferred to keep the young in their left visual field during slow travelling. In contrast, young did not display a one-sided bias for the whole sample. The lateralization, however, was pronounced in a sex-specific manner—sons preferentially kept their mothers in the right visual field, while daughters preferred to keep mothers in the left visual field. Intriguingly, both sons and daughters preferentially kept the familiar older young in the left visual field. Sons, thus, showed oppositely directed lateral preferences towards mother and non-mother companion. Presumably, sons aim to approach the mother from her left side (rather than to keep her in the right visual field) and benefit from optimized maternal perception, while daughters facilitate their own perception of the mother by keeping her in the left visual field. These sex-related differences in lateralized behaviour may result from strikingly different social strategies of two sexes.Significance statementYoung mammals show robust lateralization in the form of one-sided behavioural preferences in the interactions with their mother. Previous studies suggest that the social lifestyle may serve as a driving force in the evolution of behavioural lateralization. To test this proposition, we investigated behavioural lateralization in young subjects of Asian elephants, a species in which females are more gregarious than males. The lateralized behaviour of offspring towards the mother was found to be strongly sex-specific. In contrast, interactions with older young were lateralized in a similar manner in sons and daughters. Our results suggest that the benefits of a left-sided or right-sided position relative to mother have different significance for sons and daughters because of the distinctive social strategies of two sexes.

Early Expression of Manual Lateralization in Bipedal Marsupials.

Robust lateralization in forelimb use has recently been found in bipedal, but not quadrupedal, marsupial mammals. The link between bipedality and handedness, occurring in both marsupials and primates, remains to be investigated. To shed light on the developmental origins of marsupial manual lateralization, infants of macropod marsupials were examined before and shortly after the acquisition of habitual bipedal posture and locomotion. Forelimb preferences were assessed in natural, not artificially evoked, behaviors of infant red-necked wallaby in the wild and infant eastern gray kangaroo in free-ranging captivity. Pouch young of both species showed population-level left-forelimb preference when manipulating food objects, such as leaves and grass blades. This result provides the first report of lateralization in pouch young marsupials and rare evidence of lateralized manual activity in early mammalian ontogenesis. Young-at-foot juveniles of eastern gray kangaroo preferred to use the left forelimb to manipulate the mother’s pouch edge as previously shown for red-necked wallaby. In both species, the direction of biases in manipulative behavior for young-at-foot and pouch young was the same as in adults. Forelimb preferences in offspring were positively correlated with the forelimb preferences of their mothers. Our results strongly suggest that the emergence of individual and population-level forelimb preferences in macropod infants precedes the onset of independent standing and locomotion. In all probability, manual lateralization in bipedal marsupials, such as kangaroos and wallabies, is not determined by the acquisition of habitual bipedality in the course of ontogenesis.