Genes and Behaviour

Behaviour is the response of an animal to stimuli in its internal or external environment, ranging from simple reflexive behaviours to those that are more complex and goal directed, such as foraging, finding a mate, or engaging in aggressive interactions. However, even reflexive behaviours can be modified by experience. For example, in the zebrafish, Danio rerio, the decision to escape or swim is influenced by social status, achieved through a shift in the excitability of neural circuits (Miller et al. 2017). Therefore, a behavioural act requires an individual not only to process sensory information and respond with motor output, but also to integrate its current internal motivational state and memory of past experiences (Bendesky and Bargmann 2011; O’Connell and Hofmann 2011). As such, the genes that affect behaviour can act to influence many different layers of the nervous system, ranging from sensory perception to the connectivity and modulation of neural circuits (Marder 2012; McGrath 2013). This feature of behaviour, the ability to be modified at many different levels, may contribute to the high evolvability of behavioural traits (Blomberg et al. 2003). To gain an understanding of how animal behaviour evolves requires an integrative approach that examines how behavioural traits are inherited and also characterizes the genetic variants underlying behaviour and their specific effects on neural processing. In this chapter, we present a current understanding of the relationship between genes (of large effect) and behaviour. We first outline how most phenotypic traits, including behaviour, are controlled by many variants of small effect (see also Chapters 1 and 2). We then describe several well-studied examples of single genes that mediate behaviour, as well as ‘supergenes’ that can control behavioural divergence within species. Next, we discuss how certain classes of genes may be more likely to influence the evolution of behaviour. Finally, we consider whether the genetic architecture of behavioural traits is unique in relation to other phenotypic traits. We conclude the chapter by suggesting that an integrative approach to the study of genes and behaviour will lend the most insight into the forces underlying behavioural and genetic diversity.

[1]  J. Schneider,et al.  Social structure and indirect genetic effects: genetics of social behaviour , 2017, Biological reviews of the Cambridge Philosophical Society.

[2]  J. Saltz,et al.  Trait Correlations in the Genomics Era. , 2017, Trends in ecology & evolution.

[3]  H. Hofmann,et al.  The melanocortin system regulates body pigmentation and social behaviour in a colour polymorphic cichlid fish† , 2017, Proceedings of the Royal Society B: Biological Sciences.

[4]  A. Bendesky,et al.  The genetic basis of parental care evolution in monogamous mice , 2017, Nature.

[5]  Fadi A. Issa,et al.  Social Status–Dependent Shift in Neural Circuit Activation Affects Decision Making , 2017, The Journal of Neuroscience.

[6]  E. C. Stewart,et al.  Estimating heritable genetic contributions to innate immune and endocrine phenotypic correlations: A need to explore repeatability , 2017, Hormones and Behavior.

[7]  Cornelia I Bargmann,et al.  Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans , 2017, Proceedings of the National Academy of Sciences.

[8]  A. M. Allen,et al.  Feeding-Related Traits Are Affected by Dosage of the foraging Gene in Drosophila melanogaster , 2016, Genetics.

[9]  V. Ruta,et al.  Transcriptomics and neuroanatomy of the clonal raider ant implicate an expanded clade of odorant receptors in chemical communication , 2016, Proceedings of the National Academy of Sciences.

[10]  Evan Z. Macosko,et al.  Balancing selection shapes density-dependent foraging behavior , 2016, Nature.

[11]  Peter Carbonetto,et al.  Genome-wide association study of behavioral, physiological and gene expression traits in commercially available outbred CFW mice , 2016, Nature Genetics.

[12]  John Huddleston,et al.  An Incomplete Understanding of Human Genetic Variation , 2016, Genetics.

[13]  E. Tuttle,et al.  Divergence and Functional Degradation of a Sex Chromosome-like Supergene , 2016, Current Biology.

[14]  Alejandro Berrio,et al.  Sexual fidelity trade-offs promote regulatory variation in the prairie vole brain , 2015, Science.

[15]  J. Oettler,et al.  Expression of the Foraging Gene Is Associated with Age Polyethism, Not Task Preference, in the Ant Cardiocondyla obscurior , 2015, PloS one.

[16]  S. Kerje,et al.  Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax) , 2015, Nature Genetics.

[17]  D. Comas,et al.  Reassessing the Evolutionary History of the 17q21 Inversion Polymorphism , 2015, Genome biology and evolution.

[18]  V. Pravosudov,et al.  Heritability and the evolution of cognitive traits , 2015 .

[19]  J. Wingfield,et al.  A supergene determines highly divergent male reproductive morphs in the ruff , 2015, Nature Genetics.

[20]  Robert M. Waterhouse,et al.  Genomic signatures of evolutionary transitions from solitary to group living , 2015, Science.

[21]  M. Cáceres,et al.  Human inversions and their functional consequences , 2015, Briefings in functional genomics.

[22]  Mario de Bono,et al.  Decoding a neural circuit controlling global animal state in C. elegans , 2015, eLife.

[23]  L. Keller,et al.  Expression of foraging and Gp‐9 are associated with social organization in the fire ant Solenopsis invicta , 2015, Insect molecular biology.

[24]  Joseph M. Troy,et al.  Neuromolecular responses to social challenge: Common mechanisms across mouse, stickleback fish, and honey bee , 2014, Proceedings of the National Academy of Sciences.

[25]  Y. Wurm,et al.  Convergent Genetic Architecture Underlies Social Organization in Ants , 2014, Current Biology.

[26]  Ross M. Fraser,et al.  Defining the role of common variation in the genomic and biological architecture of adult human height , 2014, Nature Genetics.

[27]  Kathryn Roeder,et al.  Most genetic risk for autism resides with common variation , 2014, Nature Genetics.

[28]  H. Schielzeth,et al.  Challenges and prospects in genome‐wide quantitative trait loci mapping of standing genetic variation in natural populations , 2014, Annals of the New York Academy of Sciences.

[29]  Dany Garant,et al.  The effects of others’ genes: maternal and other indirect genetic effects , 2014 .

[30]  Peter M Visscher,et al.  Explaining additional genetic variation in complex traits. , 2014, Trends in genetics : TIG.

[31]  Laurent Keller,et al.  Supergenes and Complex Phenotypes , 2014, Current Biology.

[32]  M. J. Thompson,et al.  Supergenes and their role in evolution , 2014, Heredity.

[33]  Leonid Kruglyak,et al.  A Variant in the Neuropeptide Receptor npr-1 is a Major Determinant of Caenorhabditis elegans Growth and Physiology , 2014, PLoS genetics.

[34]  W. Jeffery,et al.  Loss of Schooling Behavior in Cavefish through Sight-Dependent and Sight-Independent Mechanisms , 2013, Current Biology.

[35]  Anna K. Greenwood,et al.  Genetic and Neural Modularity Underlie the Evolution of Schooling Behavior in Threespine Sticklebacks , 2013, Current Biology.

[36]  E. Marder,et al.  From the connectome to brain function , 2013, Nature Methods.

[37]  Thomas M. Keane,et al.  Combined sequence-based and genetic mapping analysis of complex traits in outbred rats , 2013, Nature Genetics.

[38]  J. Goodson Deconstructing sociality, social evolution and relevant nonapeptide functions , 2013, Psychoneuroendocrinology.

[39]  Patrick T. McGrath Varieties of behavioral natural variation , 2013, Current Opinion in Neurobiology.

[40]  Brant K. Peterson,et al.  Discrete genetic modules are responsible for complex burrow evolution in Peromyscus mice , 2013, Nature.

[41]  L. Keller,et al.  A Y-like social chromosome causes alternative colony organization in fire ants , 2013, Nature.

[42]  E. Marder Neuromodulation of Neuronal Circuits: Back to the Future , 2012, Neuron.

[43]  R. Ophoff,et al.  Common inversion polymorphism at 17q21.31 affects expression of multiple genes in tissue-specific manner , 2012, BMC Genomics.

[44]  R. Handsaker,et al.  Structural haplotypes and recent evolution of the human 17q21.31 region , 2012, Nature Genetics.

[45]  Kenneth K. Kidd,et al.  Structural Diversity and African Origin of the 17q21.31 Inversion Polymorphism , 2012, Nature Genetics.

[46]  L. O’Connell,et al.  Evolution of a Vertebrate Social Decision-Making Network , 2012, Science.

[47]  M. Zuk,et al.  Socially flexible female choice differs among populations of the Pacific field cricket: geographical variation in the interaction coefficient psi (Ψ) , 2012, Proceedings of the Royal Society B: Biological Sciences.

[48]  Mario de Bono,et al.  Tonic signaling from O2 sensors sets neural circuit activity and behavioral state , 2012, Nature Neuroscience.

[49]  E. Lander,et al.  The mystery of missing heritability: Genetic interactions create phantom heritability , 2012, Proceedings of the National Academy of Sciences.

[50]  M. Rockman THE QTN PROGRAM AND THE ALLELES THAT MATTER FOR EVOLUTION: ALL THAT'S GOLD DOES NOT GLITTER , 2012, Evolution; international journal of organic evolution.

[51]  Cori Bargmann,et al.  Genetic contributions to behavioural diversity at the gene–environment interface , 2011, Nature Reviews Genetics.

[52]  M. de Bono,et al.  Neuronal and molecular substrates for optimal foraging in Caenorhabditis elegans , 2011, Proceedings of the National Academy of Sciences.

[53]  Camilo Salazar,et al.  Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry , 2011, Nature.

[54]  L. O’Connell,et al.  Genes, hormones, and circuits: An integrative approach to study the evolution of social behavior , 2011, Frontiers in Neuroendocrinology.

[55]  Zuoxin Wang,et al.  The neurobiology of pair bonding: Insights from a socially monogamous rodent , 2011, Frontiers in Neuroendocrinology.

[56]  Jason H. Moore,et al.  Missing heritability and strategies for finding the underlying causes of complex disease , 2010, Nature Reviews Genetics.

[57]  D. Gifford,et al.  Genotype to Phenotype: A Complex Problem , 2010, Science.

[58]  Judy H. Cho,et al.  Finding the missing heritability of complex diseases , 2009, Nature.

[59]  P. Visscher,et al.  Common polygenic variation contributes to risk of schizophrenia and bipolar disorder , 2009, Nature.

[60]  Ralph J. Greenspan,et al.  The Drosophila foraging Gene Mediates Adult Plasticity and Gene–Environment Interactions in Behaviour, Metabolites, and Gene Expression in Response to Food Deprivation , 2009, PLoS genetics.

[61]  E. Brodie,et al.  Indirect Genetic Effects Influence Antipredator Behavior in Guppies: Estimates of the Coefficient of Interaction Psi and the Inheritance of Reciprocity , 2009, Evolution; international journal of organic evolution.

[62]  Jonathan Flint,et al.  Genetic architecture of quantitative traits in mice, flies, and humans. , 2009, Genome research.

[63]  T. Uller,et al.  Evolution of maternal effects: past and present , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  Evan Z. Macosko,et al.  A Hub-and-Spoke Circuit Drives Pheromone Attraction and Social Behavior in C. elegans , 2009, Nature.

[65]  Evan Z. Macosko,et al.  Quantitative Mapping of a Digenic Behavioral Trait Implicates Globin Variation in C. elegans Sensory Behaviors , 2009, Neuron.

[66]  D. Réale,et al.  Indirect genetic effects and the evolution of aggression in a vertebrate system , 2009, Proceedings of the Royal Society B: Biological Sciences.

[67]  D. Reiss,et al.  Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans , 2008, Proceedings of the National Academy of Sciences.

[68]  L. Keller,et al.  Pleiotropy in the melanocortin system, coloration and behavioural syndromes. , 2008, Trends in ecology & evolution.

[69]  Zhaoshi Jiang,et al.  Evolutionary toggling of the MAPT 17q21.31 inversion region , 2008, Nature Genetics.

[70]  K. Ross,et al.  Experimental Conversion of Colony Social Organization in Fire Ants (Solenopsis invicta): Worker Genotype Manipulation in the Absence of Queen Effects , 2008, Journal of Insect Behavior.

[71]  R. Mott,et al.  Prospects for complex trait analysis in the mouse , 2008, Mammalian Genome.

[72]  W. G. Hill,et al.  Heritability in the genomics era — concepts and misconceptions , 2008, Nature Reviews Genetics.

[73]  S. Phelps,et al.  Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings , 2008, Proceedings of the National Academy of Sciences.

[74]  Gene E Robinson,et al.  Evo-devo and the evolution of social behavior. , 2007, Trends in genetics : TIG.

[75]  L. Simmons,et al.  Paternal Indirect Genetic Effects on Offspring Viability and the Benefits of Polyandry , 2007, Current Biology.

[76]  Masakatsu Watanabe,et al.  Divergent Selection on Opsins Drives Incipient Speciation in Lake Victoria Cichlids , 2006, PLoS biology.

[77]  T. Linksvayer DIRECT, MATERNAL, AND SIBSOCIAL GENETIC EFFECTS ON INDIVIDUAL AND COLONY TRAITS IN AN ANT , 2006, Evolution; international journal of organic evolution.

[78]  Martin S. Taylor,et al.  Genome-wide genetic association of complex traits in heterogeneous stock mice , 2006, Nature Genetics.

[79]  T. Piersma,et al.  Permanent female mimics in a lekking shorebird , 2006, Biology Letters.

[80]  B. Aragona,et al.  Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles , 2006, Neuroscience Letters.

[81]  Michael J. Wade,et al.  The Evolutionary Origin And Elaboration Of Sociality In The Aculeate Hymenoptera: Maternal Effects, Sib‐social Effects, And Heterochrony , 2005, The Quarterly Review of Biology.

[82]  H. Rundle,et al.  Genetic variance in female condition predicts indirect genetic variance in male sexual display traits , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[83]  William Valdar,et al.  Strategies for mapping and cloning quantitative trait genes in rodents , 2005, Nature Reviews Genetics.

[84]  Deborah M Gordon,et al.  Task‐specific expression of the foraging gene in harvester ants , 2005, Molecular ecology.

[85]  Mark J. Fitzpatrick,et al.  Candidate genes for behavioural ecology. , 2005, Trends in ecology & evolution.

[86]  H. Stefánsson,et al.  A common inversion under selection in Europeans , 2005, Nature Genetics.

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

[88]  Cornelia I. Bargmann,et al.  Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue , 2004, Nature.

[89]  Trudy F C Mackay,et al.  The genetic architecture of quantitative traits: lessons from Drosophila. , 2004, Current opinion in genetics & development.

[90]  T. Kocher Adaptive evolution and explosive speciation: the cichlid fish model , 2004, Nature Reviews Genetics.

[91]  D. Murphy,et al.  Abnormal anxiety‐related behavior in serotonin transporter null mutant mice: the influence of genetic background , 2003, Genes, brain, and behavior.

[92]  O. Marín,et al.  Cell migration in the forebrain. , 2003, Annual review of neuroscience.

[93]  Jennifer R. Harris,et al.  Heritability of Adult Body Height: A Comparative Study of Twin Cohorts in Eight Countries , 2003, Twin Research.

[94]  T. Wen,et al.  Developmental Control of Foraging and Social Behavior by the Drosophila Neuropeptide Y-like System , 2003, Neuron.

[95]  E. Tuttle Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence , 2003 .

[96]  T. Garland,et al.  TESTING FOR PHYLOGENETIC SIGNAL IN COMPARATIVE DATA: BEHAVIORAL TRAITS ARE MORE LABILE , 2003, Evolution; international journal of organic evolution.

[97]  Jennifer L. Regan,et al.  Nonadditive Genetic Effects in Animal Behavior , 2002, The American Naturalist.

[98]  Tanya Pankiw,et al.  Genotype and rearing environment affect honeybee perception and foraging behaviour , 2002, Animal Behaviour.

[99]  M. Murray,et al.  All that's gold does not glitter: effects of an increase in respiratory rate on pulmonary mechanics and CO2 kinetics in acute respiratory failure. , 2002, Critical care medicine.

[100]  Julia Krüger,et al.  Influence of Gene Action Across Different Time Scales on Behavior , 2002, Science.

[101]  L. Keller,et al.  Experimental conversion of colony social organization by manipulation of worker genotype composition in fire ants (Solenopsis invicta) , 2002, Behavioral Ecology and Sociobiology.

[102]  Ralph J. Greenspan,et al.  The flexible genome , 2001, Nature Reviews Genetics.

[103]  J. Weber,et al.  Olfactory receptor-gene clusters, genomic-inversion polymorphisms, and common chromosome rearrangements. , 2001, American journal of human genetics.

[104]  L. Keller,et al.  Genetic control of social organization in an ant. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[105]  Cori Bargmann,et al.  Natural Variation in a Neuropeptide Y Receptor Homolog Modifies Social Behavior and Food Response in C. elegans , 1998, Cell.

[106]  H. Orr THE POPULATION GENETICS OF ADAPTATION: THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION , 1998, Evolution; international journal of organic evolution.

[107]  A. J. Moore,et al.  Evolutionary consequences of indirect genetic effects. , 1998, Trends in ecology & evolution.

[108]  A. J. Moore,et al.  INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS: I. DIRECT AND INDIRECT GENETIC EFFECTS OF SOCIAL INTERACTIONS , 1997, Evolution; international journal of organic evolution.

[109]  R. Greenspan,et al.  Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. , 1997, Science.

[110]  B. Charlesworth,et al.  The evolution of chromosomal sex determination and dosage compensation , 1996, Current Biology.

[111]  Constance M. Smith,et al.  Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax , 1995, Nature.

[112]  L. Keller,et al.  ECOLOGY AND EVOLUTION OF SOCIAL ORGANIZATION: Insights from Fire Ants and Other Highly Eusocial Insects , 1995 .

[113]  C. Ferris,et al.  Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[114]  Thomas R. Insel,et al.  A role for central vasopressin in pair bonding in monogamous prairie voles , 1993, Nature.

[115]  M. Sokolowski,et al.  Genetic localization of foraging (for): a major gene for larval behavior in Drosophila melanogaster. , 1989, Genetics.

[116]  D. Roff,et al.  Quantitative genetics and fitness: lessons from Drosophila , 1987, Heredity.

[117]  G. Robinson,et al.  Behavioral Genetic Toolkits: Toward the Evolutionary Origins of Complex Phenotypes. , 2016, Current topics in developmental biology.

[118]  P. Visscher,et al.  Meta-analysis of the heritability of human traits based on fifty years of twin studies. , 2015, Nature genetics.

[119]  R. Greenspan Selection, gene interaction, and flexible gene networks. , 2009, Cold Spring Harbor symposia on quantitative biology.

[120]  Evan Z. Macosko,et al.  A huband-spoke circuit drives pheromone attraction and social behaviour in C . elegans , 2009 .

[121]  Jonathan Flint,et al.  Analysis of quantitative trait loci that influence animal behavior. , 2003, Journal of neurobiology.

[122]  L. Meffert,et al.  Bottleneck effects on genetic variance for courtship repertoire. , 1995, Genetics.