Speaker Abstracts
The evolution of population-level lateralization: insights from bees
Elisa Frasnelli
Abstract
Evidence of left-right asymmetries in invertebrates has recently emerged, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. As in vertebrates, lateralization can occur both at the individual and at the population-level in invertebrates. Theoretical models on the evolution of lateralization suggest that the alignment of lateralization at the population level may have evolved as an evolutionary stable strategy in which individually-asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. This implies that lateralization at the population-level should be more common for social interactions frequently encountered during the course of evolution. Comparison of lateralization in insects having different levels of sociality has been important to test this hypothesis that population-level, directional asymmetry has evolved as an adjunct to social behaviour. However, recent research shows that population-level asymmetry is present also in so-called solitary insects when individuals engage in aggressive interactions. This result leads to a refinement of the original hypothesis linking directional lateralization to social behaviour: population-level lateralization is present only for social interactions common and frequent in the species’ natural behaviour. This highlights the role of social demands in the evolution of population-level functional asymmetry and suggests that not only does general sociality generate directional laterality but also that it involves engagement in specific social interactions.
Evidence of left-right asymmetries in invertebrates has recently emerged, suggesting that lateralization of the nervous system may be a feature of simpler brains as well as more complex ones. As in vertebrates, lateralization can occur both at the individual and at the population-level in invertebrates. Theoretical models on the evolution of lateralization suggest that the alignment of lateralization at the population level may have evolved as an evolutionary stable strategy in which individually-asymmetrical organisms must coordinate their behaviour with that of other asymmetrical organisms. This implies that lateralization at the population-level should be more common for social interactions frequently encountered during the course of evolution. Comparison of lateralization in insects having different levels of sociality has been important to test this hypothesis that population-level, directional asymmetry has evolved as an adjunct to social behaviour. However, recent research shows that population-level asymmetry is present also in so-called solitary insects when individuals engage in aggressive interactions. This result leads to a refinement of the original hypothesis linking directional lateralization to social behaviour: population-level lateralization is present only for social interactions common and frequent in the species’ natural behaviour. This highlights the role of social demands in the evolution of population-level functional asymmetry and suggests that not only does general sociality generate directional laterality but also that it involves engagement in specific social interactions.
Lateralization of behaviour in social insects - emergent adaptive benefits
Edmund Hunt
Abstract
There is now an increasing amount of evidence for sensory and motor asymmetries in the behaviour of invertebrates. Population-level behavioural lateralization may be more likely to evolve in social rather than solitary species [1]. Alignment of the direction of behavioural asymmetries is favoured as an evolutionarily stable strategy when asymmetrical individuals must coordinate their behaviours [2]. However, evidence for lateral biases in ants and other social insects is relatively limited, though their eusociality makes them inviting subjects in which to investigate this hypothesis.
I have previously studied the nest site exploration behaviour of Temnothorax albipennis ants and found a leftward bias, with about 65% of individuals choosing a left turn as they entered the nest cavity [3]. A population-level bias may be adaptive owing to enhanced group cohesion, reducing predation risk (‘safety in numbers') and speeding up the nest emigration process.
I will present briefly present this work and also the results of recent fieldwork in Sydney, Australia, examining the behaviour of the meat ant Iridomyrmex purpureus as it encounters an unexpected barrier blocking a foraging trail. An initial rightward turning bias is found (60% preferring rightward turns), and in this context adaptive value may similarly be derived from enhanced group cohesion and social resilience.
Population-level lateralization of movement behaviour, rather than being incidental, is argued to have potential adaptive benefits for social insects generally, and is something worth routinely considering in many behavioural experiments going forward.
[1] Anfora G, Frasnelli E, Maccagnani B, Rogers LJ, Vallortigara G. 2010; [2] Ghirlanda S, Vallortigara G. 2004; [3] Hunt ER et al 2014
There is now an increasing amount of evidence for sensory and motor asymmetries in the behaviour of invertebrates. Population-level behavioural lateralization may be more likely to evolve in social rather than solitary species [1]. Alignment of the direction of behavioural asymmetries is favoured as an evolutionarily stable strategy when asymmetrical individuals must coordinate their behaviours [2]. However, evidence for lateral biases in ants and other social insects is relatively limited, though their eusociality makes them inviting subjects in which to investigate this hypothesis.
I have previously studied the nest site exploration behaviour of Temnothorax albipennis ants and found a leftward bias, with about 65% of individuals choosing a left turn as they entered the nest cavity [3]. A population-level bias may be adaptive owing to enhanced group cohesion, reducing predation risk (‘safety in numbers') and speeding up the nest emigration process.
I will present briefly present this work and also the results of recent fieldwork in Sydney, Australia, examining the behaviour of the meat ant Iridomyrmex purpureus as it encounters an unexpected barrier blocking a foraging trail. An initial rightward turning bias is found (60% preferring rightward turns), and in this context adaptive value may similarly be derived from enhanced group cohesion and social resilience.
Population-level lateralization of movement behaviour, rather than being incidental, is argued to have potential adaptive benefits for social insects generally, and is something worth routinely considering in many behavioural experiments going forward.
[1] Anfora G, Frasnelli E, Maccagnani B, Rogers LJ, Vallortigara G. 2010; [2] Ghirlanda S, Vallortigara G. 2004; [3] Hunt ER et al 2014
Colony-level, limb preference in the red wood ant
Adrian Bell
Abstract
Lateralisation in limb control has been well-documented across a wide range of vertebrate taxa, including humans who possess population-level lateralisation thought to have evolved in response to social living. In contrast to vertebrates, there has been relatively little research on lateralisation in invertebrates. Individual-level lateralisation, wherein individuals within the population vary in their preference, has been documented in the desert locust (Schistocerca gregaria), which swarms but is not considered social. The red wood ant (Formica rufa) lives in social groups providing an opportunity to study the possible effects of social factors on the evolution of handedness in insects. Whilst crossing a gap in the substrate upon which they are walking, ants use their forelimbs to reach across and contact the opposite side. We investigated whether they displayed a preference for using a particular forelimb. In this context, some individual ants preferred to use their right forelimb, others their left and the remainder showing no preference – the hallmark of individual-level handedness. Remarkably, the preference differed between colonies, the majority of individuals within a colony showing a preference for using the same forelimb to cross the gap. Thus, wood ants exhibit two forms of handedness at the individual and colony-levels the latter being an entirely novel, previously undescribed form of lateralisaton.
Lateralisation in limb control has been well-documented across a wide range of vertebrate taxa, including humans who possess population-level lateralisation thought to have evolved in response to social living. In contrast to vertebrates, there has been relatively little research on lateralisation in invertebrates. Individual-level lateralisation, wherein individuals within the population vary in their preference, has been documented in the desert locust (Schistocerca gregaria), which swarms but is not considered social. The red wood ant (Formica rufa) lives in social groups providing an opportunity to study the possible effects of social factors on the evolution of handedness in insects. Whilst crossing a gap in the substrate upon which they are walking, ants use their forelimbs to reach across and contact the opposite side. We investigated whether they displayed a preference for using a particular forelimb. In this context, some individual ants preferred to use their right forelimb, others their left and the remainder showing no preference – the hallmark of individual-level handedness. Remarkably, the preference differed between colonies, the majority of individuals within a colony showing a preference for using the same forelimb to cross the gap. Thus, wood ants exhibit two forms of handedness at the individual and colony-levels the latter being an entirely novel, previously undescribed form of lateralisaton.
The evolution of colony-level lateralisation in a eusocial insect
Paul Calcraft
Abstract
Individual- and population-level lateralisation is very common in vertebrates, and some invertebrate species have recently been identified to exhibit such biases. However, groups or subpopulations (such as colonies) of any species have not previously been shown to possess directional biases of their own, distinct from other conspecific groups. Remarkably, the red wood ant, Formica rufa, exhibits such ͚colony-level͛ lateralisation in forelimb preference during a gap crossing task. Of the four colonies tested, one colony has more workers with a bias towards the left forelimb, the other three colonies having more workers with a right forelimb bias. Colony-level lateralisation is not predicted by established evolutionary theories of population-level lateralisation. Here, we present a model that offers an evolutionary account of colony-level lateralisation in wood ants by considering interactions among workers within colonies, between colonies, and between ants and their predators/competitors. Our model predicts the degree of lateralisation seen in wood ant colonies by trading off maladaptive predictability to predators/competitors against adaptive predictability to colony-mates. We consider the impact of this model on existing empirical work on population-level lateralisation in eusocial insects, and reveal the conditions under which colony- and population-level lateralisation would be expected to occur more generally.
Individual- and population-level lateralisation is very common in vertebrates, and some invertebrate species have recently been identified to exhibit such biases. However, groups or subpopulations (such as colonies) of any species have not previously been shown to possess directional biases of their own, distinct from other conspecific groups. Remarkably, the red wood ant, Formica rufa, exhibits such ͚colony-level͛ lateralisation in forelimb preference during a gap crossing task. Of the four colonies tested, one colony has more workers with a bias towards the left forelimb, the other three colonies having more workers with a right forelimb bias. Colony-level lateralisation is not predicted by established evolutionary theories of population-level lateralisation. Here, we present a model that offers an evolutionary account of colony-level lateralisation in wood ants by considering interactions among workers within colonies, between colonies, and between ants and their predators/competitors. Our model predicts the degree of lateralisation seen in wood ant colonies by trading off maladaptive predictability to predators/competitors against adaptive predictability to colony-mates. We consider the impact of this model on existing empirical work on population-level lateralisation in eusocial insects, and reveal the conditions under which colony- and population-level lateralisation would be expected to occur more generally.
Complementary left and right visual hemifield specialization in cuttlefish
Christelle Jozet-Alves
Abstract
While cerebral lateralization appears to be widespread in invertebrates, we do not know whether they possess a common pattern of hemibrain specialization. The common cuttlefish (cephalopod mollusc) displays an eye-use preference strikingly correlated with an asymmetry of brain structures implicated in visual processing. Over several experiments, we have shown that this eye-use preference is stimulus-dependent: the right hemifield being specialized in processing information needed for foraging, whereas the left hemifield is preferentially used when looking for escape routes, being vigilant in an unfamiliar environment and for background matching. Taking all these results together, we could suggest that the left hemifield is specialized in the control of emergency responses, and the right hemifield is specialized for routine behaviours. Even if this pattern seems very similar to the pattern described in vertebrates, further investigation in a wide range of invertebrates is now needed to determine whether lateralization in vertebrates and invertebrates results from homology or convergent evolution.
While cerebral lateralization appears to be widespread in invertebrates, we do not know whether they possess a common pattern of hemibrain specialization. The common cuttlefish (cephalopod mollusc) displays an eye-use preference strikingly correlated with an asymmetry of brain structures implicated in visual processing. Over several experiments, we have shown that this eye-use preference is stimulus-dependent: the right hemifield being specialized in processing information needed for foraging, whereas the left hemifield is preferentially used when looking for escape routes, being vigilant in an unfamiliar environment and for background matching. Taking all these results together, we could suggest that the left hemifield is specialized in the control of emergency responses, and the right hemifield is specialized for routine behaviours. Even if this pattern seems very similar to the pattern described in vertebrates, further investigation in a wide range of invertebrates is now needed to determine whether lateralization in vertebrates and invertebrates results from homology or convergent evolution.
Sources of variability in laterality
Culum Brown
Abstract
Until recently, conventional wisdom suggested that all vertebrates show the same pattern of laterality. That is all animals preferentially analyse specific types of information in a given hemisphere. However, over the last ten years, myself and others have shown that there can be considerable variation within and between species. Some of this variation is induced by phenotypic plasticity as a result of experience with certain stimuli which may change how animals classify and ultimately analyse information pertaining to certain objects and or contexts. We have also shown, that both the pattern and strength of laterality is heritable and seems to be greatly influenced by ecological selective pressures including foraging and predator regimes. In this talk I discuss variation in laterality and the implications for understanding its evolution in vertebrates.
Until recently, conventional wisdom suggested that all vertebrates show the same pattern of laterality. That is all animals preferentially analyse specific types of information in a given hemisphere. However, over the last ten years, myself and others have shown that there can be considerable variation within and between species. Some of this variation is induced by phenotypic plasticity as a result of experience with certain stimuli which may change how animals classify and ultimately analyse information pertaining to certain objects and or contexts. We have also shown, that both the pattern and strength of laterality is heritable and seems to be greatly influenced by ecological selective pressures including foraging and predator regimes. In this talk I discuss variation in laterality and the implications for understanding its evolution in vertebrates.
Behavioural asymmetries in cetaceans
Yegor B. Malashichev
Department of Vertebrate Zoology, Faculty of Biology, Saint-Petersburg State University, Russia
and
Laboratory of Molecular Neurobiology, Department of Physiological Ecology, Institute of Experimental Medicine, Saint-Petersburg, Russia.
Abstract
Motor lateralizations and lateralization of behavioural responses to various stimuli are wide spread among vertebrates of different classes, but are studied not equivalently. Within the mammalian class, the most investigated group remains the order of primates, while other mammals are missed of focused attention. One of such groups was cetaceans up to recently. Although the interest to their behavioural lateralizations certainly existed, the majority of studies had been conducted in captivity and the number of studied individuals in trials was not great. This caused in that this taxon appeared to be understudied and seemed to be different from other mammals in some parameters of lateralization, thus representing both a “blank spot” and a somewhat unusual group. Most recently, a number of studies on lateralization in wild cetaceans have been undertaken allowing us to summarize and reevaluate the data from this interesting group. In this talk I show that the lateralized behaviours in cetaceans correspond to the common pattern of lateralization of other mammals and, more generally, of other vertebrates. Particularly, I consider in detail asymmetric eye-mediated responses to socially significant stimuli (e.g. mother-calf interactions), novelty, and food. Other motor behaviours like rotational swimming, flipper use, and breeching will be also discussed.
Motor lateralizations and lateralization of behavioural responses to various stimuli are wide spread among vertebrates of different classes, but are studied not equivalently. Within the mammalian class, the most investigated group remains the order of primates, while other mammals are missed of focused attention. One of such groups was cetaceans up to recently. Although the interest to their behavioural lateralizations certainly existed, the majority of studies had been conducted in captivity and the number of studied individuals in trials was not great. This caused in that this taxon appeared to be understudied and seemed to be different from other mammals in some parameters of lateralization, thus representing both a “blank spot” and a somewhat unusual group. Most recently, a number of studies on lateralization in wild cetaceans have been undertaken allowing us to summarize and reevaluate the data from this interesting group. In this talk I show that the lateralized behaviours in cetaceans correspond to the common pattern of lateralization of other mammals and, more generally, of other vertebrates. Particularly, I consider in detail asymmetric eye-mediated responses to socially significant stimuli (e.g. mother-calf interactions), novelty, and food. Other motor behaviours like rotational swimming, flipper use, and breeching will be also discussed.
Smelling emotions through the dog nose: sniffing canine and human
emotionally arousing odours produces asymmetric nostril use
and enhances dog's emotional response
Serenella d'Ingeo
Abstract
Previous studies on dogs have reported asymmetric nostril use in processing odours that differ in terms of emotional valence. In our research we collected human sweat samples in different emotional conditions ("joy", "fear", "physical stress" and "neutral) and dog emotional odours from perianal, interdigital and salivary secretions, in an "isolation", "disturbance", "play" situation and in a "neutral" one. The cotton swabs impregnated with the eight different odours were presented to 31 dogs, while their cardiac activity and their behaviour were recorded. Results showed that dogs consistently used the left nostril to sniff "fear" and "physical stress" human odours, suggesting the prevalent activation of the left hemisphere. On the other hand, dogs consistently used their right nostril (right hemisphere) when they sniffed a conspecific "isolation" odour. The opposite bias shown in nostril use during sniffing canine versus human odours suggests that chemosignals communicate conspecific and heterospecific emotional cues using different sensory pathways.
Previous studies on dogs have reported asymmetric nostril use in processing odours that differ in terms of emotional valence. In our research we collected human sweat samples in different emotional conditions ("joy", "fear", "physical stress" and "neutral) and dog emotional odours from perianal, interdigital and salivary secretions, in an "isolation", "disturbance", "play" situation and in a "neutral" one. The cotton swabs impregnated with the eight different odours were presented to 31 dogs, while their cardiac activity and their behaviour were recorded. Results showed that dogs consistently used the left nostril to sniff "fear" and "physical stress" human odours, suggesting the prevalent activation of the left hemisphere. On the other hand, dogs consistently used their right nostril (right hemisphere) when they sniffed a conspecific "isolation" odour. The opposite bias shown in nostril use during sniffing canine versus human odours suggests that chemosignals communicate conspecific and heterospecific emotional cues using different sensory pathways.
Lateral biases in navigational paths of great apes and children
Gillian Forrester
Department of Psychology, University of Westminster, London, UK
Department of Psychological Sciences, Birkbeck, University of London, London, UK
Abstract
Cerebral lateralization of function and their associated contralateral motor biases may reflect an evolutionary adaptive characteristic of the vertebrate brain, facilitating reflexive and automatic responses to increase the survival of individuals. Right hemisphere dominant patterns have been reported in a range of animal species for social processing. For example, vertebrate species, ranging from fishes to great apes, demonstrate a bias to keep conspecifics situated on the left side, suggesting that the social environment may have been a critical pressure in aligning population behaviour for both predator defense and cooperation. Recently, we demonstrated how motor biases in social environment impacts upon modern human behaviour, by revealing that children expressed a significant bias for choosing a rightward navigational path around a human target, but no side preference for navigation around an inanimate object (Forrester et al. 2014). A right-biased path around another individual provides an advantage for the left visual field and the right hemisphere, thus facilitating the processing of social-emotion stimuli. These studies indicate that the social environment elicits predictive behavior and that lateralized motor actions can acts as an indirect marker of the cerebral lateralization. Extensions of these investigations may shed light on both the evolution of modern human sociality, and additionally lead to a new generation of developmental interventions and diagnostic measures for individuals at risk for neurodevelopmental disorders characterized by decreased cerebral lateralization (e.g. autism).
Cerebral lateralization of function and their associated contralateral motor biases may reflect an evolutionary adaptive characteristic of the vertebrate brain, facilitating reflexive and automatic responses to increase the survival of individuals. Right hemisphere dominant patterns have been reported in a range of animal species for social processing. For example, vertebrate species, ranging from fishes to great apes, demonstrate a bias to keep conspecifics situated on the left side, suggesting that the social environment may have been a critical pressure in aligning population behaviour for both predator defense and cooperation. Recently, we demonstrated how motor biases in social environment impacts upon modern human behaviour, by revealing that children expressed a significant bias for choosing a rightward navigational path around a human target, but no side preference for navigation around an inanimate object (Forrester et al. 2014). A right-biased path around another individual provides an advantage for the left visual field and the right hemisphere, thus facilitating the processing of social-emotion stimuli. These studies indicate that the social environment elicits predictive behavior and that lateralized motor actions can acts as an indirect marker of the cerebral lateralization. Extensions of these investigations may shed light on both the evolution of modern human sociality, and additionally lead to a new generation of developmental interventions and diagnostic measures for individuals at risk for neurodevelopmental disorders characterized by decreased cerebral lateralization (e.g. autism).
An examination of the origins, functions and development of the left-side bias in infant-holding by human mothers
Brenda K. Todd(1) and Robin Banerjee(2)
1Department of Psychology, City University London, London, UK;
2School of Psychology, University of Sussex, Brighton, UK
Abstract
The bias human mothers show in holding infants on the left, rather than right, side of the body was examined longitudinally, with attention to 4 explanations: maternal monitoring of infant state, maternal handedness, infant proximity to the mother’s heartbeat and preferred infant head position. Both the side and the site of holding were measured over the first 12 weeks of the lives of 24 infants. A strong bias to hold on the left dropped below significance when the infants were aged 12 weeks and was limited to specific holding positions. Some variation between individual mothers’ preferred holding side was found. Information about group and individual consistency in holding side allowed evaluation of the theories and has implications for future research. In general, results were consistent with the hypothesis that mothers’ hold infants on the left to facilitate infant monitoring via the right hemisphere, and little support was found for alternative explanations.
The bias human mothers show in holding infants on the left, rather than right, side of the body was examined longitudinally, with attention to 4 explanations: maternal monitoring of infant state, maternal handedness, infant proximity to the mother’s heartbeat and preferred infant head position. Both the side and the site of holding were measured over the first 12 weeks of the lives of 24 infants. A strong bias to hold on the left dropped below significance when the infants were aged 12 weeks and was limited to specific holding positions. Some variation between individual mothers’ preferred holding side was found. Information about group and individual consistency in holding side allowed evaluation of the theories and has implications for future research. In general, results were consistent with the hypothesis that mothers’ hold infants on the left to facilitate infant monitoring via the right hemisphere, and little support was found for alternative explanations.