Oxytocin variation and brain region‐specific gene expression in a domesticated avian species

The Bengalese finch was domesticated more than 250 years ago from the wild white‐rumped munia (WRM). Similar to other domesticated species, Bengalese finches show a reduced fear response and have lower corticosterone levels, compared to WRMs. Bengalese finches and munias also have different song types. Since oxytocin (OT) has been found to be involved in stress coping and auditory processing, we tested whether the OT sequence and brain expression pattern and content differ in wild munias and domesticated Bengalese finches. We sequenced the OT from 10 wild munias and 11 Bengalese finches and identified intra‐strain variability in both the untranslated and protein‐coding regions of the sequence, with all the latter giving rise to synonymous mutations. Several of these changes fall in specific transcription factor‐binding sites, and show either a conserved or a relaxed evolutionary trend in the avian lineage, and in vertebrates in general. Although in situ hybridization in several hypothalamic nuclei did not reveal significant differences in the number of cells expressing OT between the two strains, real‐time quantitative PCR showed a significantly higher OT mRNA expression in the cerebrum of the Bengalese finches relative to munias, but a significantly lower expression in their diencephalon. Our study thus points to a brain region‐specific pattern of neurochemical expression in domesticated and wild avian strains, which could be linked to domestication and the behavioral changes associated with it.

[1]  K. Okanoya,et al.  Effects of domestication on neophobia: A comparison between the domesticated Bengalese finch (Lonchura striata var. domestica) and its wild ancestor, the white-rumped munia (Lonchura striata) , 2021, Behavioural Processes.

[2]  D. Maney,et al.  Oxytocin receptor antagonism during song tutoring in zebra finches reduces preference for and learning of the tutor’s song , 2021, bioRxiv.

[3]  E. Jarvis,et al.  Universal nomenclature for oxytocin–vasotocin ligand and receptor families , 2021, Nature.

[4]  K. Okanoya,et al.  Domestication effects on aggressiveness: Comparison of biting motivation and bite force between wild and domesticated finches , 2021, Behavioural Processes.

[5]  F. Range,et al.  Endocrine changes related to dog domestication: Comparing urinary cortisol and oxytocin in hand-raised, pack-living dogs and wolves , 2020, Hormones and Behavior.

[6]  M. Clark,et al.  Comparative Genomics , 2020, Springer US.

[7]  K. Conzelmann,et al.  Social touch promotes interfemale communication via activation of parvocellular oxytocin neurons , 2020, Nature Neuroscience.

[8]  Vinod Kumar,et al.  Effects of timed food availability on reproduction and metabolism in zebra finches: Molecular insights into homeostatic adaptation to food-restriction in diurnal vertebrates , 2020, Hormones and Behavior.

[9]  Sergey Koren,et al.  Towards complete and error-free genome assemblies of all vertebrate species , 2020, Nature.

[10]  K. Grogan,et al.  Expression of oxytocin receptors in the zebra finch brain during vocal development , 2019, bioRxiv.

[11]  R. Gulevich,et al.  Neuropeptides as facilitators of domestication , 2018, Cell and Tissue Research.

[12]  R. F. Westbrook,et al.  Oxytocin receptor activation in the basolateral complex of the amygdala enhances discrimination between discrete cues and promotes configural processing of cues , 2018, Psychoneuroendocrinology.

[13]  T. Havránek,et al.  Molecular Mechanisms of Oxytocin Signaling at the Synaptic Connection , 2018, Neural plasticity.

[14]  K. Nishimori,et al.  Oxytocin Signaling in the Lateral Septum Prevents Social Fear during Lactation , 2018, Current Biology.

[15]  G. Erhardt,et al.  Genetic characterization of the oxytocin-neurophysin I gene (OXT) and its regulatory regions analysis in domestic Old and New World camelids , 2018, PloS one.

[16]  Adam G Diehl,et al.  Conserved and species-specific transcription factor co-binding patterns drive divergent gene regulation in human and mouse , 2018, Nucleic acids research.

[17]  K. Tsutsui,et al.  Strain differences in intermale aggression and possible factors regulating increased aggression in Japanese quail. , 2018, General and comparative endocrinology.

[18]  Pedro Tiago Martins,et al.  Self-domestication in Homo sapiens: Insights from comparative genomics , 2017, PloS one.

[19]  K. Iremonger,et al.  Regulation of hypothalamic corticotropin‐releasing hormone neurone excitability by oxytocin , 2017, Journal of neuroendocrinology.

[20]  E. Jarvis,et al.  A hypothesis on a role of oxytocin in the social mechanisms of speech and vocal learning , 2017, Proceedings of the Royal Society B: Biological Sciences.

[21]  M. Goldstein,et al.  Early life manipulations of vasopressin-family peptides alter vocal learning , 2017, Proceedings of the Royal Society B: Biological Sciences.

[22]  E. Kubinyi,et al.  Lessons from the canine Oxtr gene: populations, variants and functional aspects , 2017, Genes, brain, and behavior.

[23]  Zachary V Johnson,et al.  Oxytocin receptors modulate a social salience neural network in male prairie voles , 2017, Hormones and Behavior.

[24]  K. Okanoya Sexual communication and domestication may give rise to the signal complexity necessary for the emergence of language: An indication from songbird studies , 2017, Psychonomic bulletin & review.

[25]  Zhibin Zhang,et al.  Laboratory domestication changed the expression patterns of oxytocin and vasopressin in brains of rats and mice , 2016, Anatomical Science International.

[26]  C. Scharff,et al.  Genoarchitecture of the extended amygdala in zebra finch, and expression of FoxP2 in cell corridors of different genetic profile , 2016, Brain Structure and Function.

[27]  M. Nagasawa,et al.  Oxytocin-gaze positive loop and the coevolution of human-dog bonds , 2015, Science.

[28]  J. Goodson,et al.  Oxytocin mechanisms of stress response and aggression in a territorial finch , 2015, Physiology & Behavior.

[29]  A. Wilkins,et al.  The “Domestication Syndrome” in Mammals: A Unified Explanation Based on Neural Crest Cell Behavior and Genetics , 2014, Genetics.

[30]  D. Maney,et al.  Evaluation of reference genes for quantitative real-time PCR in the brain, pituitary, and gonads of songbirds , 2014, Hormones and Behavior.

[31]  D. Slattery,et al.  Brain Oxytocin in Social Fear Conditioning and Its Extinction: Involvement of the Lateral Septum , 2014, Neuropsychopharmacology.

[32]  J. Goodson,et al.  Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches , 2014, Proceedings of the National Academy of Sciences.

[33]  K. Okanoya,et al.  The impact of domestication on fearfulness: A comparison of tonic immobility reactions in wild and domesticated finches , 2013, Behavioural Processes.

[34]  J. Goodson,et al.  What's in a name? Considerations of homologies and nomenclature for vertebrate social behavior networks , 2013, Hormones and Behavior.

[35]  J. Goodson,et al.  Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird , 2013, Proceedings of the Royal Society B: Biological Sciences.

[36]  K. Okanoya,et al.  Decreased fecal corticosterone levels due to domestication: a comparison between the white-backed Munia (Lonchura striata) and its domesticated strain, the Bengalese finch (Lonchura striata var. domestica) with a suggestion for complex song evolution. , 2012, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[37]  T. Serikawa,et al.  Origins of Albino and Hooded Rats: Implications from Molecular Genetic Analysis across Modern Laboratory Rat Strains , 2012, PloS one.

[38]  M. Tomaszycki,et al.  Oxytocin antagonist treatments alter the formation of pair relationships in zebra finches of both sexes , 2012, Hormones and Behavior.

[39]  Sarah E. Earp,et al.  Neural distribution of vasotocin receptor mRNA in two species of songbird. , 2011, Endocrinology.

[40]  D. Slattery,et al.  The Neuropeptide Oxytocin Facilitates Pro-Social Behavior and Prevents Social Avoidance in Rats and Mice , 2011, Neuropsychopharmacology.

[41]  K. Okanoya,et al.  Identification, Localisation and Functional Implication of 26RFa Orthologue Peptide in the Brain of Zebra Finch (Taeniopygia guttata) , 2011, Journal of neuroendocrinology.

[42]  E. Reuveni The Genetic Background Effect on Domesticated Species: A Mouse Evolutionary Perspective , 2011, TheScientificWorldJournal.

[43]  Michael D. Wilson,et al.  Five-Vertebrate ChIP-seq Reveals the Evolutionary Dynamics of Transcription Factor Binding , 2010, Science.

[44]  Federico Abascal,et al.  TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations , 2010, Nucleic Acids Res..

[45]  Albert J. Vilella,et al.  The genome of a songbird , 2010, Nature.

[46]  J. Goodson,et al.  Mesotocin and Nonapeptide Receptors Promote Estrildid Flocking Behavior , 2009, Science.

[47]  Zoe R. Donaldson,et al.  Oxytocin, Vasopressin, and the Neurogenetics of Sociality , 2008, Science.

[48]  C. Cannings Statistical Methods in Molecular Evolution , 2006 .

[49]  A. Lucion,et al.  Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats , 2005, Physiology & Behavior.

[50]  K. Morgan,et al.  Evolution of GnRH ligand precursors and GnRH receptors in protochordate and vertebrate species. , 2004, General and comparative endocrinology.

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

[52]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[53]  Landgraf,et al.  Brain Oxytocin Inhibits Basal and Stress‐Induced Activity of the Hypothalamo‐Pituitary‐Adrenal Axis in Male and Female Rats: Partial Action Within the Paraventricular Nucleus , 2000, Journal of neuroendocrinology.

[54]  Kazuo Okanoya,et al.  Acoustical and Syntactical Comparisons between Songs of the White-backed Munia (Lonchura striata) and Its Domesticated Strain, the Bengalese Finch (Lonchura striata var. domestica) , 1999 .

[55]  R. Grossmann,et al.  Mesotocin Gene Expression in the Diencephalon of Domestic Fowl: Cloning and Sequencing of the MT cDNA and Distribution of MT Gene Expressing Neurons in the Chicken Hypothalamus , 1997, Journal of neuroendocrinology.

[56]  Robin L. Restall Munias and Mannikins , 1997 .

[57]  H. Akil,et al.  Regulation of hypothalamic magnocellular neuropeptides and their mRNAs in the Brattleboro rat: coordinate responses to further osmotic challenge , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  C. Pedersen,et al.  Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[59]  F. Vandesande,et al.  Immunocytochemical investigation of the hypothalamo-neurohypophysial system in birds , 1977, Cell and Tissue Research.

[60]  Anthony F. Depalma Book Review: Clinical Physiology , 1963 .

[61]  Jennifer K. Link Domestication Syndrome , 2021, Encyclopedia of Animal Cognition and Behavior.

[62]  D. Pfaff,et al.  Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior: Oxytocin and vasopressin systems , 2013 .

[63]  L. Young,et al.  Oxytocin, Vasopressin and Related Peptides in the Regulation of Behavior: Oxytocin, vasopressin, and the evolution of mating systems in mammals , 2013 .

[64]  T. Hasegawa,et al.  Ecological correlates of song complexity in white-rumped munias: The implication of relaxation of selection as a cause for signal variation in birdsong , 2012 .

[65]  David Haussler,et al.  Phylogenetic Hidden Markov Models , 2005 .

[66]  N. Bons The topography of mesotocin and vasotocin systems in the brain of the domestic mallard and japanese quail: Immunocytochemical identification , 2004, Cell and Tissue Research.

[67]  K. Okanoya,et al.  Sexing White-rumped Munias in Taiwan, using morphology, DNA and distance calls , 2003 .

[68]  I. Neumann Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo-pituitary-adrenal axis. , 2002, Progress in brain research.

[69]  I. Robinson Oxytocin and the Milk-Ejection Reflex , 1986 .

[70]  W. Klemm,et al.  Neurophysiologic studies of the immobility reflex ("animal hypnosis"). , 1971, Neurosciences research.