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Quantitative genetic analyses of complex behaviours in Drosophila

Key Points

  • Behaviours are complex traits determined by the combined effects of many independently segregating genes that are sensitive to the environment. As they are typical quantitative traits they require the use of statistical analyses to describe the genetic basis underlying their phenotypes. They are also highly sensitive to the effects of genetic background, environmental variation and gender-specific effects, thereby requiring that all of these factors are taken into account in studies of behavioural genetics.

  • Drosophila melanogaster is an important model organism for studies of behavioural genetics: the analysis of many genetically identical individuals under controlled environmental conditions is possible, a range of tools are available for genetic manipulation, and a range of databases and genetics resources are available.

  • The first step in any study of behavioural genetics is the design of a quantitative assay, which should be as simple as possible and should take into account the modular nature of behaviours. Many such assays have been developed to study behaviour in D. melanogaster, to study traits such as larval foraging, courtship and olfactory avoidance, to name but a few.

  • Genetic background can be controlled for in D. melanogaster by constructing co-isogenic or recombinant inbred lines, or by comparing the phenotypes of parental and hybrid lines in the case of transgenesis using binary expression systems, such as the widely used Gal4–UAS system.

  • The quantitative and environmentally sensitive nature of behavioural traits necessitates the testing of large numbers of flies to detect statistically significant differences between strains. The number of individuals that need to be tested can be determined using standard statistical methods.

  • Because so many individuals are tested in studies of D. melanogaster behavioural genetics, controlling for environmental variation — for example, spatial or temporal — is of paramount importance. Common strategies are widely used to minimize sources of error that are attributable to these effects.

  • Individuals of different genotypes often vary in their environmental sensitivities — a phenomenon called genotype by environment interaction — which can lead to difficulties in replicating the results of behavioural assays. The effects of genotype by environment interactions can be quantified using the analysis of variance (ANOVA) statistical technique.

  • Genes that contribute to behavioural traits in D. melanogaster can be identified using three main strategies: large-scale mutagenesis screens, mapping of quantitative trait loci and transcriptional profiling studies.

  • As behaviours are generally controlled by complex networks of genes, it is important to determine epistatic relationships between genes identified as contributing to behavioural traits. Many behavioural genes are pleiotropic, and may have effects on a range of other phenotypes.

Abstract

Behaviours are exceptionally complex quantitative traits. Sensitivity to environmental variation and genetic background, the presence of sexual dimorphism, and the widespread functional pleiotropy that is inherent in behavioural phenotypes pose daunting challenges for unravelling their underlying genetics. Drosophila melanogaster provides an attractive system for elucidating the unifying principles of the genetic architectures that drive behaviours, as genetically identical individuals can be reared rapidly in controlled environments and extensive publicly accessible genetic resources are available. Recent advances in quantitative genetic and functional genomic approaches now enable the extensive characterization of complex genetic networks that mediate behaviours in this important model organism.

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Figure 1: Experimental strategies used in quantitative genetic analyses of behavioural traits in Drosophila melanogaster.
Figure 2: Simple behavioural assays that are amenable to high-throughput screening.
Figure 3: Sample sizes required in genetic analyses of complex behaviours.
Figure 4: Genotype by environment interaction.
Figure 5: Microarray analysis of sex-biased transcripts in Drosophila melanogaster.

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Acknowledgements

Work in the authors' laboratories is supported by grants from the National Institutes of Health.

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DATABASES

FlyBase

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FURTHER INFORMATION

Anholt's homepage

DrosDel Drosophila Isogenic Deficiency Kit

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Glossary

PLEIOTROPY

The phenomenon in which a single gene is responsible for several different phenotypic effects.

QUANTITATIVE TRAIT LOCI

(QTLs). One of many genetic loci affecting variation in a complex trait (for example, behaviours, some aspects of morphology, resistance to environmental stress). QTLs have individually small effects, are sensitive to environmental variation, and are initially identified by statistical association of trait phenotypes with polymorphic molecular markers.

PHOTOTAXIS

Movement towards a light source.

GEOTAXIS

Movement upwards or downwards, which requires the perception of and response to gravity.

CIRCADIAN LOCOMOTOR BEHAVIOUR

Variation in endogenous locomotor activity that depends on time of day.

OLFACTORY CONDITIONING PARADIGM

An experimental procedure in which subjects learn to avoid a particular odour through the pairing of exposure to that odour with an aversive stimulus, such as an electric shock.

CANTON-S FLIES

A standard wild-type D. melanogaster strain, genetically different from Samarkand (another standard wild-type D. melanogaster strain)

P-ELEMENTS

A family of transposable elements that are widely used as the basis of tools for mutating and manipulating the D. melanogaster genome.

CO-ISOGENIC LINES

Homozygous lines that differ only by the presence of a single mutation.

RECOMBINANT INBRED LINES

A population of fully homozygous lines derived by 20 or more generations of full-sibling mating from the F2 derived from a cross between two different inbred lines. Each line comprises 50% of each parental strain in different combinations.

PHENOTYPIC REVERSION

Demonstration of restoration of the wild-type phenotype by construction of an allele in which a P-element associated with a mutation has been precisely excised.

TRANSGENIC RESCUE

Restoration of the wild-type phenotype in a mutant background by a construct containing the wild-type copy of the gene that has been introduced into the genome by germ-line transformation.

COMPLEMENTATION TESTS

In classical genetics, two mutations with the same phenotype are said to complement if their F1 hybrid is wild type, and fail to complement if the F1 hybrid exhibits the mutant phenotype. Failure to complement can arise if the mutations are alleles of the same locus, or are alleles of different loci that interact epistatically in the same genetic pathway.

LINKAGE DISEQUILIBRIUM

Non-random association of gene frequencies at two or more polymorphic loci in a population; that is, alleles of two different genes are not present together in gametes in the frequencies predicted by the product of their frequencies.

LINKAGE MAPPING

Markers that are physically close to a locus of interest segregate 'tightly' with the locus and will statistically be more closely associated with the observed variance of a trait. This property can be used to detect association in a population between a genetic marker and a locus that contributes to a particular phenotype.

F2

A segregating generation of an intercross between F1 individuals derived from two parental lines.

PERMUTATION TESTING

A method for obtaining appropriate significance thresholds for data sets in which multiple statistical tests are performed. The original analysis is repeated many times on data sets generated by appropriate random scrambling of the original data, generating an empirical distribution of the test under the null hypothesis.

INBREEDING DEPRESSION

The reduction in viability and fertility of inbred offspring compared with outbred offspring.

GENETIC DRIFT

Also known as random drift. A phenomenon whereby the frequency of a gene in a population changes over time owing to random sampling in finite populations.

RECOMBINATION MAPPING

Determining the order and location of genes on a chromosome in terms of the rate of recombination between them. When applied to QTL mapping, the position and effect of the QTL is inferred by linkage disequilibrium of the trait phenotype with the genotype of flanking molecular markers.

BACKCROSS

A segregating generation in which F1 hybrids derived from two inbred parents are crossed to one of those parents.

ADVANCED INTERCROSS POPULATION

A population derived from several generations of crosses among F2 individuals to maximize recombination for high resolution QTL mapping.

DEFICIENCY CHROMOSOME

A chromosome in which a defined region has been deleted.

BALANCER CHROMOSOME

A chromosome with one or more inverted segments that suppress recombination, ideally over the length of the chromosome. It is usually identified in crosses by a dominant marker, and carries at least one recessive lethal mutation. They allow lethal mutations to be maintained without selection, as the only offspring that will be viable from an intercross will be those that carry the mutation and are heterozygous for the balancer chromosome.

QUANTITATIVE TRAIT NUCLEOTIDE

Molecular polymorphisms(s) associated with naturally occurring variation in a quantitative trait.

CHROMOSOME SUBSTITUTION LINE

A stock in which a single homozygous chromosome from one strain is introduced into the homozygous genetic background of a second, unrelated strain. It is possible to construct chromosome substitution lines in a few generations using D. melanogaster balancer chromosomes.

ADMIXTURE

The mixture of two or more genetically distinct populations.

HALF-DIALLEL CROSS

Construction of all possible n(n−1)/2 heterozygous genotypes between n homozygous lines, excluding reciprocal crosses.

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Anholt, R., Mackay, T. Quantitative genetic analyses of complex behaviours in Drosophila. Nat Rev Genet 5, 838–849 (2004). https://doi.org/10.1038/nrg1472

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