Genes, brains and mammalian social bonds.

Recent studies of monogamous species have revealed the role of the neuropeptides oxytocin and vasopressin in activating reward mechanisms of the brain that are involved in establishing partner recognition and selective 'bonding'. The evolutionary history of these findings resides, at a mechanistic level, in the reciprocal bonding between mother and infant that is common to all mammals. However, in Old World primates, where mother and infant alone would not survive, living in large social groups brings extended family relationships and provides for alloparenting. This has required the emancipation of parenting behaviour from the constraints of hormonal state and the evolution of large brains for decision making that was previously restricted and determined by hormonal state. How this has been achieved, what conserved mechanisms underpin social bonding, and what genetic and mechanistic changes have occurred in the evolution of social bonds are the issues addressed here.

[1]  Daniel Osorio,et al.  Evolution and selection of trichromatic vision in primates , 2003 .

[2]  S. Kikuyama,et al.  Involvement of arginine vasotocin in reproductive events in the male newt Cynops pyrrhogaster , 2003, Hormones and Behavior.

[3]  H. Innan,et al.  Relaxed selective pressure on an essential component of pheromone transduction in primate evolution , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  K. Kendrick,et al.  Facial and vocal discrimination in sheep , 1995, Animal Behaviour.

[5]  Thomas R Insel,et al.  Neuropeptides and the evolution of social behavior , 2000, Current Opinion in Neurobiology.

[6]  E. Keverne,et al.  Oxytocin and vasopressin release in the olfactory bulb of parturient ewes: changes with maternal experience and effects on acetylcholine, γ-aminobutyric acid, glutamate and noradrenaline release , 1995, Brain Research.

[7]  L. Young,et al.  The neurobiology of pair bonding , 2004, Nature Neuroscience.

[8]  R. Vollmer,et al.  Anxiety and Stress Responses in Female Oxytocin Deficient Mice , 2004, Journal of neuroendocrinology.

[9]  S. O’Brien,et al.  Placental mammal diversification and the Cretaceous–Tertiary boundary , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  C. Marler,et al.  Vasopressin and Aggression in Cross-Fostered California Mice (Peromyscus californicus) and White-Footed Mice (Peromyscus leucopus) , 2001, Hormones and Behavior.

[11]  S. Firestein,et al.  The olfactory receptor gene superfamily of the mouse , 2002, Nature Neuroscience.

[12]  Larry J Young,et al.  Profound Impairment in Social Recognition and Reduction in Anxiety-Like Behavior in Vasopressin V1a Receptor Knockout Mice , 2004, Neuropsychopharmacology.

[13]  K. D. Punta,et al.  Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes , 2002, Nature.

[14]  E B Keverne,et al.  Primate brain evolution : genetic and functional considerations , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[15]  N. Mundy,et al.  Isolation of novel olfactory receptor genes in marmosets (Callithrix): insights into pseudogene formation and evidence for functional degeneracy in non-human primates. , 2003, Gene.

[16]  Ajit Varki,et al.  How to make an ape brain , 2004, Nature Genetics.

[17]  T. Insel,et al.  Oxytocin Administered Centrally Facilitates Formation of a Partner Preference in Female Prairie Voles (Microtus ochrogaster) , 1994, Journal of neuroendocrinology.

[18]  Thomas R. Insel,et al.  Social amnesia in mice lacking the oxytocin gene , 2000, Nature Genetics.

[19]  T. Clutton‐Brock,et al.  The Evolution of Parental Care , 2019 .

[20]  B. Trainor,et al.  Arginine Vasotocin Interacts with the Social Environment to Regulate Advertisement Calling in the Gray Treefrog (Hyla versicolor) , 2003, Brain, Behavior and Evolution.

[21]  Jianzhi Zhang,et al.  Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkeys. , 2004, Molecular biology and evolution.

[22]  E. Keverne,et al.  Genomic imprinting and the differential roles of parental genomes in brain development. , 1996, Brain research. Developmental brain research.

[23]  D. Wildman,et al.  Accelerated evolution of the electron transport chain in anthropoid primates. , 2004, Trends in genetics : TIG.

[24]  E. Keverne,et al.  Early Learning and the Social Bond , 1997, Annals of the New York Academy of Sciences.

[25]  C. Carter,et al.  The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). , 1999, Behavioral neuroscience.

[26]  K. P. Bhatnagar,et al.  Comparison of brain structure volumes in Insectivora and Primates. III. Main olfactory bulb (MOB). , 1983, Journal fur Hirnforschung.

[27]  L. Young,et al.  Viral vector‐mediated gene transfer of the vole V1a vasopressin receptor in the rat septum: improved social discrimination and active social behaviour , 2003, The European journal of neuroscience.

[28]  K. Laland,et al.  Social intelligence, innovation, and enhanced brain size in primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  T. Insel,et al.  Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole , 1999, Nature.

[30]  F. Zufall,et al.  Altered sexual and social behaviors in trp2 mutant mice , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Jianzhi Zhang,et al.  Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Robin I. M. Dunbar,et al.  Neocortex size and social network size in primates , 2001, Animal Behaviour.

[33]  Robin I. M. Dunbar,et al.  Evolution of the Social Brain , 2003, Science.

[34]  J. Goodson,et al.  Effects of central vasotocin and mesotocin manipulations on social behavior in male and female zebra finches , 2004, Hormones and Behavior.

[35]  Eric B. Keverne,et al.  Something in the Air? New Insights into Mammalian Pheromones , 2004, Current Biology.

[36]  E. Keverne,et al.  Physiological, Sensory, and Experiential Factors of Parental Care in Sheep , 1996 .

[37]  H. Frahm,et al.  Comparison of brain structure volumes in Insectivora and Primates. II. Accessory olfactory bulb (AOB). , 1982, Journal fur Hirnforschung.

[38]  Robin I. M. Dunbar.  Neocortex size as a constraint on group size in primates , 1992 .

[39]  R. Axel,et al.  A novel family of genes encoding putative pheromone receptors in mammals , 1995, Cell.

[40]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[41]  Robin I. M. Dunbar.  Psychology. Evolution of the social brain. , 2003 .

[42]  Markus Meister,et al.  Loss of Sex Discrimination and Male-Male Aggression in Mice Deficient for TRP2 , 2002, Science.

[43]  L. Young.  Oxytocin and Vasopressin Receptors and Species-Typical Social Behaviors , 1999, Hormones and Behavior.

[44]  C. Dulac,et al.  A Novel Family of Putative Pheromone Receptors in Mammals with a Topographically Organized and Sexually Dimorphic Distribution , 1997, Cell.

[45]  Jianzhi Zhang,et al.  Evolution of the human ASPM gene, a major determinant of brain size. , 2003, Genetics.

[46]  L. Young,et al.  Species Differences in Paternal Behavior and Aggression in Peromyscus and Their Associations with Vasopressin Immunoreactivity and Receptors , 1999, Hormones and Behavior.

[47]  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.

[48]  Larry J. Young,et al.  Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene , 2004, Nature.

[49]  Zuoxin Wang,et al.  Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles , 2003, Neuroscience.

[50]  Doron Lancet,et al.  Human specific loss of olfactory receptor genes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[51]  S. Pääbo,et al.  Loss of Olfactory Receptor Genes Coincides with the Acquisition of Full Trichromatic Vision in Primates , 2004, PLoS biology.

[52]  E. Ginns,et al.  Vasopressin V1b receptor knockout reduces aggressive behavior in male mice , 2002, Molecular Psychiatry.

[53]  T. Insel,et al.  Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse , 2001, The Journal of Neuroscience.

[54]  Jeanne Altmann,et al.  Social Bonds of Female Baboons Enhance Infant Survival , 2003, Science.

[55]  D. Kleiman,et al.  Monogamy in Mammals , 1977, The Quarterly Review of Biology.

[56]  L. Young,et al.  Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole , 2004, Neuroscience.

[57]  L. Young,et al.  Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): Patterns of variation and covariation , 2003, The Journal of comparative neurology.

[58]  R. Manchester,et al.  A radio pulsar with an 8.5-second period that challenges emission models , 1999, Nature.

[59]  Bruce T Lahn,et al.  Reconstructing the evolutionary history of microcephalin, a gene controlling human brain size. , 2004, Human molecular genetics.

[60]  W. Smeets,et al.  Vasotocin and mesotocin in the brains of amphibians: State of the art , 2001, Microscopy research and technique.

[61]  Larry J Young,et al.  Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster) , 2004, The Journal of comparative neurology.

[62]  E. Keverne.  Pheromones, Vomeronasal Function, and Gender-Specific Behavior , 2002, Cell.

[63]  E. Keverne,et al.  Vasopressin, oxytocin and social behaviour , 2004, Current Opinion in Neurobiology.

[64]  Peter T. Fox,et al.  Mosaic evolution of brain structure in mammals , 2022 .

[65]  C. H. Hoyle.  Neuropeptide families and their receptors: evolutionary perspectives , 1999, Brain Research.

[66]  N. Mundy,et al.  Trans‐specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates , 2002, Molecular ecology.

[67]  Eric B. Keverne,et al.  Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships , 1989, Psychoneuroendocrinology.

[68]  D C Van Essen,et al.  Information processing in the primate visual system: an integrated systems perspective. , 1992, Science.

[69]  R. Sapolsky,et al.  A Pacific Culture among Wild Baboons: Its Emergence and Transmission , 2004, PLoS biology.

[70]  S. Holman,et al.  Experiential and Hormonal Correlates of Care-Giving in Rhesus Macaques , 1995 .

[71]  Bruce T Lahn,et al.  Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. , 2004, Human molecular genetics.

[72]  Larry J Young,et al.  Functional microsatellite polymorphism associated with divergent social structure in vole species. , 2004, Molecular biology and evolution.

[73]  R. Barton.  Visual specialization and brain evolution in primates , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[74]  Robin I. M. Dunbar.  Social Brain Hypothesis , 1998, Encyclopedia of Evolutionary Psychological Science.