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Sociogenomics: social life in molecular terms

Key Points

  • Studying the molecular basis of social life (sociogenomics) requires an integration of molecular biology, genomics, neuroscience, behavioural biology, evolutionary biology and new forms of bioinformatics.

  • An eclectic mix of species that show varying levels of sociality is being used to study the molecular basis of social life, especially social behaviour.

  • Sociogenomics is predicated on two of the most significant insights in biology to emerge from the later half of the twentieth century. First, social life has a biological basis and is therefore influenced to some extent by genes and the forces of evolution. Second, the molecular functions of many genes are highly conserved across species, even for complex traits such as behaviour.

  • Genes have been identified that both regulate social behaviour and that are implicated in the evolution of social behaviour.

  • One emerging theme that relates to the relationship between genes and social behaviour is that genes involved in solitary behaviour are also used for social behaviour.

  • A second theme is that the genome is highly sensitive to social influence, through social regulation of gene expression in the brain.

  • A transcriptomics-based approach is the method of gene discovery most easily used for model social species.

Abstract

Spectacular progress in molecular biology, genome-sequencing projects and genomics makes this an appropriate time to attempt a comprehensive understanding of the molecular basis of social life. Promising results have already been obtained in identifying genes that influence animal social behaviour and genes that are implicated in social evolution. These findings — derived from an eclectic mix of species that show varying levels of sociality — provide the foundation for the integration of molecular biology, genomics, neuroscience, behavioural biology and evolutionary biology that is necessary for this endeavour.

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Figure 1: Sociogenomics as an integrative discipline in behavioural biology.
Figure 2: cGMP signalling pathways show strong conservation in the regulation of feeding-related behaviours.
Figure 3: Expression of the immediate early gene zenk in the brain of the zebra finch (Taeniopygia guttata) in response to song.
Figure 4: The vasopressin receptor 1a gene and monogamy in voles.
Figure 5: Brain gene-expression profiles are associated with division of labour in honeybees.

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Acknowledgements

We thank H.A. Hoffman and R.E. Lenski for helpful advice. We also thank A.B. Barron, Y. Ben-Shahar, G. Bloch, S.E. Fahrbach, A.L. Toth, B. Schatz, M.B. Sokolowski and three anonymous reviewers for comments that improved the manuscript. Research by the authors was supported by grants from the US National Institutes of Health, US National Science Foundation, US Department of Agriculture and the Burroughs Wellcome Trust (G.E.R.), a University of Illinois-Beckman Postdoctoral Fellowship (C.M.G.), and a US National Science Foundation Postdoctoral Fellowship in Bioinformatics (C.W.W.).

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DATABASES

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egl-4

EGR1

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FOXP2

Mvl

FURTHER INFORMATION

BeeBase

BeeSpace

Charles Whitfield's web page

Christina Grozinger's web page

Stanford Genome Evolution Center

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Glossary

SOCIETY

A group of organisms from the same species that live in the same area and engage in repeated interactions with each other, both cooperative and competitive. The more extensive the cooperation, the more developed the society.

COMPLEX TRAIT

A measured phenotype, such as disease status or a quantitative character, which is influenced by many environmental and genetic factors, and potentially by interactions in and between them.

MUTUALISM

Social interactions in which both parties benefit.

KIN SELECTION

William D. Hamilton's theory to explain the evolution of the hallmark of social life: altruistic cooperation (carrying out functions that are costly to the individual but that benefit others). By helping a relative, an individual increases its fitness by increasing the number of copies of its genes in the population.

RECIPROCAL ALTRUISM

Robert L. Trivers' theory to explain altruism, according to which altruism occurs when the individual is likely to later be the recipient of similar altruistic acts.

DIVISION OF LABOUR

A key characteristic of the most structured societies those with the highest levels of cooperation in which individuals specialize in specific occupations. In insect societies, queens reproduce while workers engage in all tasks that are related to colony growth and development; young workers tend to work in the nest, whereas older individuals forage outside.

CANDIDATE GENE

A gene that is thought to be more likely to be involved in the control of a trait in one species compared with a random gene from the genome, based on known functions in another species.

TRANSCRIPTOMICS

A global way of looking at gene-expression patterns. This can involve measurements of thousands of genes simultaneously with microarrays or measurements of small numbers of genes that are facilitated by global sequence information from EST or genome-sequencing projects.

PHEROMONE

A chemical released by members of a species that influences the behaviour of other members of that species.

QUANTITATIVE TRAIT LOCI

(QTLs). Loci that control quantitative (that is, continuous) traits. QTLs are identified by showing a statistical association between genetic markers and measurable phenotypes.

GENETIC ARCHITECTURE

Broadly describes the distribution of gene effects that produce a given phenotype. It includes a description of the number of genes that influence the trait, their relative position and magnitude of the effects, and the nature of the interactions between them.

COMPLEMENTARY SEX DETERMINATION

Unfertilized eggs produce males and fertilized eggs produce females. This results in certain asymmetries in relatedness, including sisters being more closely related to each other than mothers and daughters. Recognition of this in the Hymenoptera (ants, bees, wasps) led Hamilton to propose kin selection as a principal force in the evolution of eusociality.

GREEN BEARD GENE

A type of gene predicted by Richard Dawkins that shows the following three effects: production of a recognizable trait (for example, a green beard), recognition of that trait in others and preferential treatment of those with the trait.

MONOGYNY

In this context, an insect society that is headed by a single female (the queen).

POLYGYNY

In this context, an insect society that is headed by many females (queens).

GENOMIC IMPRINTING

Expression of only one of two alleles of a gene owing to differential methylation of either the maternal or paternal copy.

SEXUAL SELECTION THEORY

Derived from sex-specific differences in gamete size that led to predictions of sex-specific differences in mating strategies, parental investment and genomic imprinting.

SUBTRACTIVE HYBRIDIZATION

A technique used to identify differentially expressed genes. The DNA species present in one sample are specifically enriched by hybridizing with nucleic acids from another sample and removing the associated double-stranded molecules.

IMMEDIATE EARLY GENES

The first genes expressed in response to cell stimulation that then lead to cascades of expression of other genes.

GENOMIC ACTION POTENTIAL

David F. Clayton invoked the classical neuronal action potential to describe by analogy how gene expression, beginning with activation of immediate early genes, increases the responsiveness of neurons to key environmental stimuli.

EPIGENETIC

Modifications of chromatin or DNA (for example, histone deacetylation and cytosine methylation) that can be stably transmitted through many cell divisions, but can also be reset (unlike changes in DNA sequence).

LORDOSIS BEHAVIOUR

The posture of a female rodent when receptive to mating; includes raised tail and hind quarters, and an arched back.

CLOCK GENES

Genes that are involved in the production and regulation of circadian (intrinsic daily) rhythms.

ACTIVATIONAL EFFECT

In behavioural endocrinology, relatively rapid behavioural effects that are caused by actions of a hormone increase or decrease on established neural systems. This concept can also be usefully applied to describe similar effects that are caused by gene products.

ORGANIZATIONAL EFFECT

In behavioural endocrinology, hormone effects that occur early in development and result in permanent changes in adult neural systems, and so behaviour. This concept can also be usefully applied to describe similar effects that are caused by gene products.

SEROTONIN

A biogenic amine that can function as a neurotransmitter, neuromodulator or neurohormone, and controls many physiological and behavioural processes.

GENOTYPE X ENVIRONMENT INTERACTION

The influence of specific combinations of genetic and environmental factors on a trait that goes beyond the additive action of these factors. This can refer to genes that control sensitivity to the environment or environmental factors that influence gene expression.

AMYGDALA

Region of the vertebrate brain that is involved with emotions, including anger and fear.

TELEOST

A group of bony fish that includes nearly all the important food and game fish, and many aquarium fish.

HYPOTHALAMIC PITUITARY AXIS

Endocrine and neuroendocrine tissues that together control physiological and behavioural aspects of reproductive maturation in vertebrates. Gonadotropin-releasing hormone (GnRH), made in the hypothalamus, causes the pituitary to release gonadotropins, which leads to the release of gonadal steroid hormones.

EUSOCIAL

Social species that show three features: an extreme dominance hierarchy with some individuals reproducing a great deal and others little or not at all overlapping generations of adults in the nest and cooperative care of offspring.

CASTE

In insect societies, a group of individuals that specialize in carrying out particular tasks. This behavioural specialization is often associated with differences in age, anatomy and morphology.

COLONY-LEVEL SELECTION

A special form of group selection, first described by Charles Darwin, to explain the evolution of altruistic (sterile) workers in insect societies.

RNA DIFFERENTIAL DISPLAY

A technique for detecting those genes that are expressed only under specific conditions. It involves isolation and comparison of mRNA from two or more populations, PCR amplification of mRNA and resolution on a DNA-sequencing gel.

ENDOPHENOTYPE

A component of a complex behavioural phenotype that can facilitate the identification of relevant genes and elucidate their function. An endophenotype can involve a simpler behaviour or an underlying endocrine or neural mechanism.

MUSHROOM BODIES

A region of the insect brain that is involved in multimodal sensory integration, learning and memory.

CHRONOBIOLOGY

The study of how organisms keep time, from circadian rhythms to seasonal changes, at all levels of biological organization.

NANOVECTOR

A nanoparticle that can be used to deliver nucleic acids and drugs.

HOMEOBOX GENES

Genes that contain a 180-base-pair sequence involved in the regulation of animal and plant development. This sequence encodes a DNA-binding helix–turn–helix motif, indicating that homeobox-containing gene products function as transcription factors.

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Robinson, G., Grozinger, C. & Whitfield, C. Sociogenomics: social life in molecular terms. Nat Rev Genet 6, 257–270 (2005). https://doi.org/10.1038/nrg1575

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