Laterality in the Damaraland Mole-Rat: Insights from a Eusocial Mammal

Simple Summary Side biases observed in behavior are thought to reflect underlying asymmetric brain function or hemispheric specialization. These asymmetries occur at the individual and population level, although population-level laterality normally is only evident in social species. In a previous study, we found both individual- and population-level laterality in a solitary mole rat species. Here, we assessed laterality in a eusocial mole rat species, the Damaraland mole rat, Fukomys damarensis, using turning biases. All individuals combined demonstrated left-turning biases, which was also significant at the population level. Wild-caught animals were more strongly lateralized, but lacked the population-level left-turning bias that was observed in captive mole rats. This emphasizes the importance of context and animal handling when measuring and interpreting behavioral asymmetries. Abstract Lateralization is the functional control of certain behaviors in the brain being processed by either the left or right hemisphere. Behavioral asymmetries can occur at an individual and population level, although population-level lateralization is less common amongst solitary species, whereas social species can benefit more from aligning and coordinating their activities. We assessed laterality (individual and population) through turning biases in the eusocial Damaraland mole rat, Fukomys damarensis. We considered factors such as breeding status (queen or subordinate), environment (wild-caught or captive), sex (male or female), colony and body mass. All individuals together demonstrated significant left-turning biases, which was also significant at the population level. Wild-caught animals were more strongly lateralized, had a wider spread over a laterality index and lacked the population-level left-turning bias as compared to captive mole rats. Subordinate animals were more lateralized than queens, demonstrating social status differences in turning biases for social mole rats. This emphasizes the importance of animal handling and context when measuring and interpreting behavioral asymmetries.

[1]  T. Clutton‐Brock,et al.  Odour-based social recognition in Damaraland mole-rats, Fukomys damarensis , 2021, Animal Behaviour.

[2]  L. Rogers Brain Lateralization and Cognitive Capacity , 2021, Animals : an open access journal from MDPI.

[3]  Culum Brown,et al.  Laterality and fish welfare - A review , 2021, Applied Animal Behaviour Science.

[4]  P. Jacobs,et al.  Laterality in the Cape mole-rat, Georychus capensis , 2021, Behavioural Processes.

[5]  C. G. Faulkes,et al.  Social Evolution in African Mole-Rats - A Comparative Overview. , 2021, Advances in experimental medicine and biology.

[6]  T. Clutton‐Brock,et al.  Breeders are less active foragers than non-breeders in wild Damaraland mole-rats , 2020, Biology Letters.

[7]  Amanda M. Lauer,et al.  Functional, Morphological, and Evolutionary Characterization of Hearing in Subterranean, Eusocial African Mole-Rats , 2020, Current Biology.

[8]  Sayan Mukherjee,et al.  Morphological and genomic shifts in mole-rat ‘queens’ increase fecundity but reduce skeletal integrity , 2020, bioRxiv.

[9]  M. K. Oosthuizen,et al.  Exploratory behaviour, memory and neurogenesis in the social Damaraland mole-rat (Fukomys damarensis) , 2020, Journal of Experimental Biology.

[10]  L. Morrell,et al.  Consistency in the strength of laterality in male, but not female, guppies across different behavioural contexts , 2020, Biology Letters.

[11]  G. Vallortigara,et al.  Brain and Behavioral Asymmetry: A Lesson From Fish , 2020, Frontiers in Neuroanatomy.

[12]  Benjamin L. de Bivort,et al.  Individual, but not population asymmetries, are modulated by social environment and genotype in Drosophila melanogaster , 2019, Scientific Reports.

[13]  Elia Gatto,et al.  Individual differences in numerical skills are influenced by brain lateralization in guppies (Poecilia reticulata) , 2019, Intelligence.

[14]  Thomas A. O'Shea-Wheller Honeybees show a context-dependent rightward bias , 2019, Biology Letters.

[15]  Giorgio Vallortigara,et al.  Individual-Level and Population-Level Lateralization: Two Sides of the Same Coin , 2018, Symmetry.

[16]  N. Bennett,et al.  Non-invasive assessment of glucocorticoid and androgen metabolite levels in cooperatively breeding Damaraland mole-rats (Fukomys damarensis). , 2018, General and comparative endocrinology.

[17]  N. Bennett,et al.  Reproductive status‐dependent kisspeptin and RFamide‐related peptide (Rfrp) gene expression in female Damaraland mole‐rats , 2018, Journal of neuroendocrinology.

[18]  Matthew J. . Anderson,et al.  Lateral asymmetry in the freely occurring behaviour of budgerigars (Melopsittacus undulatus) and its relation to cognitive performance , 2017, Laterality.

[19]  Mallory L Wiper Evolutionary and mechanistic drivers of laterality: A review and new synthesis , 2017, Laterality.

[20]  T. Groothuis,et al.  Investigating Effects of Steroid Hormones on Lateralization of Brain and Behavior , 2017 .

[21]  M. C. Ferrari,et al.  At odds with the group: changes in lateralization and escape performance reveal conformity and conflict in fish schools , 2016, Proceedings of the Royal Society B: Biological Sciences.

[22]  O. Güntürkün,et al.  Stress and laterality – The comparative perspective , 2016, Physiology & Behavior.

[23]  L. Rogers,et al.  Lateralized antennal control of aggression and sex differences in red mason bees, Osmia bicornis , 2016, Scientific Reports.

[24]  Catarina Vila Pouca,et al.  Laterality strength is linked to stress reactivity in Port Jackson sharks (Heterodontus portusjacksoni) , 2016, Behavioural Brain Research.

[25]  J. Herman,et al.  Regulation of the Hypothalamic-Pituitary-Adrenocortical Stress Response. , 2016, Comprehensive Physiology.

[26]  G. Bauer,et al.  Behavioral lateralization in the Florida manatee (Trichechus manatus latirostris) , 2016 .

[27]  Marco Dadda,et al.  Laterality enhances numerical skills in the guppy, Poecilia reticulata , 2015, Front. Behav. Neurosci..

[28]  N. Ferri,et al.  Laterality as an indicator of emotional stress in ewes and lambs during a separation test , 2015, Animal Cognition.

[29]  J. Steffensen,et al.  Severe hypoxia impairs lateralization in a marine teleost fish , 2014, Journal of Experimental Biology.

[30]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[31]  M. Gahr,et al.  Breeding status and social environment differentially affect the expression of sex steroid receptor and aromatase mRNA in the brain of female Damaraland mole-rats , 2014, Frontiers in Zoology.

[32]  M. Siniscalchi Divided brains. The biology and behaviour of brain asymmetries , 2014 .

[33]  E. Frasnelli Brain and behavioral lateralization in invertebrates , 2013, Front. Psychol..

[34]  Culum Brown,et al.  Laterality Influences Schooling Position in Rainbowfish, Melanotaenia spp , 2013, PloS one.

[35]  T. Ariyomo,et al.  Aggression and sex differences in lateralization in the zebrafish , 2013, Animal Behaviour.

[36]  J. Wingfield,et al.  Importance of the glucocorticoid stress response in a changing world: theory, hypotheses and perspectives. , 2013, General and comparative endocrinology.

[37]  G. Vallortigara,et al.  A right antenna for social behaviour in honeybees , 2013, Scientific Reports.

[38]  B. Bonati,et al.  Looking at a predator with the left or right eye: Asymmetry of response in lizards , 2013, Laterality.

[39]  J. Jarvis,et al.  The Long-Lived Queen: Reproduction and Longevity in Female Eusocial Damaraland Mole-Rats (Fukomys damarensis) , 2013 .

[40]  J. Cockrem Individual variation in glucocorticoid stress responses in animals. , 2013, General and comparative endocrinology.

[41]  Stephen W. Wilson,et al.  Encoding asymmetry within neural circuits , 2012, Nature Reviews Neuroscience.

[42]  G. Vallortigara,et al.  Left–right asymmetries of behaviour and nervous system in invertebrates , 2012, Neuroscience & Biobehavioral Reviews.

[43]  L. Rogers,et al.  Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus , 2012, Animal Behaviour.

[44]  L. Rogers,et al.  Strength of hand preference and dual task performance by common marmosets , 2012, Animal Cognition.

[45]  Culum Brown,et al.  The Evolution of lateralized foot use in parrots : a phylogenetic approach , 2011 .

[46]  R. Sainburg,et al.  Motor asymmetry reduction in older adults , 2011, Neuroscience Letters.

[47]  A. J. Young,et al.  MORPHOLOGICAL DIVERGENCE OF BREEDERS AND HELPERS IN WILD DAMARALAND MOLE‐RAT SOCIETIES , 2010, Evolution; international journal of organic evolution.

[48]  Lesley J. Rogers,et al.  Relevance of brain and behavioural lateralization to animal welfare , 2010 .

[49]  M. Nowak,et al.  The evolution of eusociality , 2010, Nature.

[50]  D. Lavinsky,et al.  Lateralized and sex-dependent behavioral and morphological effects of unilateral neonatal cerebral hypoxia-ischemia in the rat , 2010, Behavioural Brain Research.

[51]  I. George Hemispheric Asymmetry of Songbirds , 2010 .

[52]  A. J. Young,et al.  Physiological suppression eases in Damaraland mole-rat societies when ecological constraints on dispersal are relaxed , 2010, Hormones and Behavior.

[53]  G. Vallortigara,et al.  Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee , 2010, Behavioural Brain Research.

[54]  A. Gardner,et al.  Capturing the superorganism: a formal theory of group adaptation , 2009, Journal of evolutionary biology.

[55]  B. Czéh,et al.  Hemispheric differences in basilar dendrites and spines of pyramidal neurons in the rat prelimbic cortex: activity- and stress-induced changes , 2009, The European journal of neuroscience.

[56]  Jamie L. Russell,et al.  Handedness for tool use in captive chimpanzees (Pan troglodytes): Sex differences, performance, heritability and comparison to the wild. , 2009, Behaviour.

[57]  S. Lhota,et al.  Patterns and laterality of hand use in free-ranging aye-ayes (Daubentonia madagascariensis) and a comparison with captive studies , 2009, Journal of Ethology.

[58]  S. Ghirlanda,et al.  Intraspecific competition and coordination in the evolution of lateralization , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[59]  T. Groothuis,et al.  Does testosterone affect lateralization of brain and behaviour? A meta-analysis in humans and other animal species , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[60]  Marna S. Costanzo Aspects of memory in the Damaraland mole-rat, Cryptomys damarensis : spatial learning and kin recognition , 2007 .

[61]  N. Bennett,et al.  Burrow architecture and burrowing dynamics of the endangered Namaqua dune mole rat (Bathyergus janetta) (Rodentia: Bathyergidae) , 2006 .

[62]  G. Vallortigara The evolutionary psychology of left and right: costs and benefits of lateralization. , 2006, Developmental psychobiology.

[63]  J. M. Ramírez,et al.  Aggression and Brain Asymmetries: A Theoretical Review , 2006 .

[64]  K. Foster,et al.  Conflict resolution in insect societies. , 2006, Annual review of entomology.

[65]  E. Wilson,et al.  Eusociality: origin and consequences. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[66]  G. Vallortigara,et al.  survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization , 2005, Behavioral and Brain Sciences.

[67]  L. Rogers,et al.  Motor and sensory laterality in thoroughbred horses , 2005 .

[68]  J. R. Miller,et al.  Interpreting animal wall-following behavior , 1990, Experientia.

[69]  Pud W. Sherman The eusociality continuum , 2005 .

[70]  R. Cabeza,et al.  Age-related changes in hemispheric organization , 2005 .

[71]  John R. Hetling,et al.  Features of visual function in the naked mole-rat Heterocephalus glaber , 2005, Journal of Comparative Physiology A.

[72]  Erina Hara,et al.  Aggression in females is also lateralized: left-eye bias during aggressive courtship rejection in lizards , 2004, Animal Behaviour.

[73]  M. Kuba,et al.  Lateralized eye use in Octopus vulgaris shows antisymmetrical distribution , 2004, Animal Behaviour.

[74]  K. Kendrick,et al.  Face pictures reduce behavioural, autonomic, endocrine and neural indices of stress and fear in sheep , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[75]  J. Jarvis,et al.  A field assessment of reproductive seasonality in the threatened wild Namaqua dune mole-rat (Bathyergus janetta) , 2004 .

[76]  R. Sullivan,et al.  Hemispheric Asymmetry in Stress Processing in Rat Prefrontal Cortex and the Role of Mesocortical Dopamine , 2004, Stress.

[77]  S. Ghirlanda,et al.  The evolution of brain lateralization: a game-theoretical analysis of population structure , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[78]  B. G. Lovegrove,et al.  The evolution of eusociality in molerats (Bathyergidae): a question of risks, numbers, and costs , 2004, Behavioral Ecology and Sociobiology.

[79]  A. Bisazza,et al.  Lateralization of aggression in fish , 2003, Behavioural Brain Research.

[80]  Timothy J. Crow,et al.  Comparative vertebrate lateralization , 2003 .

[81]  R. Cabeza,et al.  Hemispheric asymmetry and aging: right hemisphere decline or asymmetry reduction , 2002, Neuroscience & Biobehavioral Reviews.

[82]  L. Rogers Lateralised brain function in anurans: Comparison to lateralisation in other vertebrates , 2002, Laterality.

[83]  J. Jarvis,et al.  Eusociality in African mole-rats: new insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis) , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[84]  R. Cabeza Hemispheric asymmetry reduction in older adults: the HAROLD model. , 2002, Psychology and aging.

[85]  G. Heth,et al.  African Mole-rats. Ecology and Eusociality , 2000, Animal Behaviour.

[86]  G. Vallortigara,et al.  Population lateralisation and social behaviour: A study with 16 species of fish , 2000, Laterality.

[87]  N. Bennett,et al.  Anovulation in non-reproductive female Damaraland mole-rats (Cryptomys damarensis). , 2000, Journal of reproduction and fertility.

[88]  L. Rogers,et al.  Hand preference of the common marmoset (Callithrix jacchus): Problem solving and responses in a novel setting. , 1999 .

[89]  G. Vallortigara,et al.  The Origins of Cerebral Asymmetry: A Review of Evidence of Behavioural and Brain Lateralization in Fishes, Reptiles and Amphibians , 1998, Neuroscience & Biobehavioral Reviews.

[90]  P. Neveu,et al.  In the mouse, the corticoid stress response depends on lateralization , 1997, Brain Research.

[91]  N. Bennett,et al.  Recrudescence of sexual activity in a reproductively quiescent colony of the Damaraland mole-rat (Cryptomys damarensis), by the introduction of an unfamiliar and genetically unrelated male—a case of incest avoidance in‘queenless’colonies , 1997 .

[92]  C. G. Faulkes,et al.  Reproductive suppression in subordinate, non-breeding female Damaraland mole-rats: two components to a lifetime of socially induced infertility , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[93]  L. Santín,et al.  Behaviour laterality in male rats: Influence of practice and stress , 1996, Physiology & Behavior.

[94]  Bernard J. Crespi,et al.  The definition of eusociality , 1995 .

[95]  M. O'Riain,et al.  Mammalian eusociality: a family affair. , 1994, Trends in ecology & evolution.

[96]  J. Jarvis,et al.  LH responses to single doses of exogenous GnRH by freshly captured Damaraland mole-rats, Cryptomys damarensis. , 1993, Journal of reproduction and fertility.

[97]  G. Körtner,et al.  The magnetic compass orientation of the burrows of the Damara mole‐rat Cryptomys damarensis (Bathyergidae) , 1992 .

[98]  V. Denenberg Hemispheric laterality in animals and the effects of early experience , 1981, Behavioral and Brain Sciences.

[99]  R. Lehman Lateralized asymmetry of behavior in animals at the population and individual level , 1981, Behavioral and Brain Sciences.

[100]  S. D. Glick,et al.  Right-sided population bias and lateralization of activity in normal rats , 1981, Brain Research.

[101]  G. C. Hickman,et al.  A Live-Trap and Trapping Technique for Fossorial Mammals , 1979 .

[102]  M. Coltheart Hemispheric asymmetry , 1978, Nature.

[103]  Charles D. Michener,et al.  Comparative Social Behavior of Bees , 1969 .

[104]  W. Hamilton The Evolution of Altruistic Behavior , 1963, The American Naturalist.