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Genetic contributions to behavioural diversity at the gene–environment interface

Nature Reviews Genetics volume 12, pages 809–820 (2011)Cite this article

Subjects

Key Points

  • Animal behaviour and human behaviour have a hereditary component.

  • Natural variation in behaviour has a complex genetic makeup: many genetic variants contribute to the differences in behaviour between individuals.

  • Behavioural genes can have functions that are conserved across different species.

  • Common genetic variants interact with the environment to affect behaviour. Many common genetic variants affect an individual's detection of, response to, or interaction with the environment.

  • Some classes of genes, such as those affecting sensory systems and neuromodulatory pathways, are frequently associated with variation in behaviour.

  • Behavioural variability within a species can be maintained by balancing selection.

Abstract

Recent work on behavioural variation within and between species has furthered our understanding of the genetic architecture of behavioural traits, the identities of relevant genes and the ways in which genetic variants affect neuronal circuits to modify behaviour. Here we review our understanding of the genetics of natural behavioural variation in non-human animals and highlight the implications of these findings for human genetics. We suggest that gene–environment interactions are central to natural genetic variation in behaviour and that genes affecting neuromodulatory pathways and sensory processing are preferred sites of naturally occurring mutations.

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Figure 1: Strategies for linkage-based mapping.
Figure 2: Differential gene expression analysis to identify genetic pathways mediating variation in behaviour.
Figure 3: Olfactory receptor gene evolution in primates.

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Acknowledgements

We thank P. McGrath, S. Flavell and E. Glater for discussions.

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Authors and Affiliations

  1. Howard Hughes Medical Institute and Laboratory for Neural Circuits and Behavior, The Rockefeller University, New York, 10065, New York, USA

    Andres Bendesky & Cornelia I. Bargmann

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Correspondence to Cornelia I. Bargmann.

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FURTHER INFORMATION

The Drosophila Genetic Reference Panel (DGRP)

Mouse Genome Informatics

Glossary

Plasticity

The ability of nervous systems to change molecularly, physiologically or anatomically based on experience.

Evolvability

The ability of organisms to respond to selective pressures with adaptive genetic changes. By analogy, a gene's propensity to acquire adaptive mutations under selective pressures. Among other properties, evolvability is affected by the mutation rate, directed mutation, the degree of pleiotropy and epistasis and system robustness.

Balancing selection

Selection that maintains trait variation. Two alleles can be balanced if a heterozygote is more successful than either homozygote, if each of the two alleles is better-adapted to one of two alternative environments or if each allele promotes a different, but equally successful, survival strategy in the same environment.

Ethological approach

The study of animal behaviours motivated by their observation in nature.

Genetic architecture

The number, frequency, effect size, dominance relationship and interactions of genetic variants that affect a trait in populations of a species.

Linkage-based mapping

A genetic mapping technique that uses pedigree information and genetic markers to link a trait to a genomic location.

QTL mapping

QTL mapping of progeny from an intercross measures the correlation between trait values and DNA markers across the genome and infers the number of loci that affect the trait, their location and the contribution of each locus to the total trait variance.

Genetic association

A population-based mapping technique that measures the correlation between a DNA polymorphism and a trait.

Recombinant inbred lines

(RILs). Strains that are derived from crosses between two or more parental strains, followed by recombination of chromosomes and inbreeding to homozygosity. Typically, RILs are carefully genotyped at many loci. A panel of RILs can be a stable resource for QTL mapping.

Emotionality

A set of fear- and anxiety-related behaviours, such as avoidance of exposed areas and inhibition of movement after foot shock.

Introgression strains

Strains into which defined DNA segments have been introduced from a different strain background through backcrossing. The introduced segments can be full chromosomes, as in chromosome substitution strains (CSSs) or smaller chromosomal intervals, as in congenics.

lod

Logarithm of the odds ratio. A term that indicates the likelihood that a genomic region is linked to the trait being measured. A genome-wide lod threshold is set to correct for multiple comparisons.

Quantitative complementation test

A variant of the classical genetic complementation test that measures the interaction between genetic mutations and two naturally occurring alleles to determine whether the natural alleles are allelic to the mutants.

RMG neurons

Caenorhabditis elegans neurons that are essential for aggregation and are linked by electrical synapses to multiple classes of sensory neurons that detect oxygen, pheromones, noxious cues and nutrients.

Stomatogastric ganglion

A part of the crustacean nervous system that coordinates digestive tract movements. It consists of 30 defined neurons and has been extensively used to study neural circuit dynamics, connections and modulation.

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Bendesky, A., Bargmann, C. Genetic contributions to behavioural diversity at the gene–environment interface. Nat Rev Genet 12, 809–820 (2011). https://doi.org/10.1038/nrg3065

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