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  • Review Article
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Drosophila: Genetics meets behaviour

Key Points

  • The challenges of behavioural genetics research include: the difficulty in defining and quantifying behaviour, environmental influences on behaviour, within- and between-individual variation in behaviour, the involvement of many genes, and the fact that different genes function in different tissues at different times during the ontogeny of an organism, all of which combine to influence a single pattern of behaviour.

  • Drosophila is an exceptionally useful genetic model used for the study of simple and complex behaviours, and its use has given an important insight into the molecular, cellular and evolutionary underpinnings of behaviour.

  • Behavioural researchers study both natural variants and single-gene Drosophila mutants. The study of single-gene mutants has advanced our understanding of the mechanisms that underlie many neurobiological and behavioural phenotypes, including circadian rhythms, courtship, and learning and memory. Natural variants inform us about the nature of the genes and allelic variants that affect normal individual differences in behaviour; how they evolved and how they might differ from laboratory-generated mutants.

  • The existence of genetic-background effects indicates that behavioural phenotypes are highly sensitive to interacting networks of genes and environments throughout the development and adulthood of a fly.

  • To understand how genes contribute to behaviour, we must identify and characterize the units of behavioural function: the neuronal networks that produce movements and organize them into the appropriate temporal and spatial patterns that characterize a given behaviour.

Abstract

Genes are understandably crucial to physiology, morphology and biochemistry, but the idea of genes contributing to individual differences in behaviour once seemed outrageous. Nevertheless, some scientists have aspired to understand the relationship between genes and behaviour, and their research has become increasingly informative and productive over the past several decades. At the forefront of behavioural genetics research is the fruitfly Drosophila melanogaster, which has provided us with important insights into the molecular, cellular and evolutionary bases of behaviour.

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Figure 1: Sequence of courtship behaviours shown by Drosophila melanogaster males towards females.
Figure 2: Sitter and rover foraging behaviour.
Figure 3: Eclosion and circadian rhythms in flies.
Figure 4: Genomic and transcript map of the fru locus.
Figure 5: A model for olfactory-based shock-avoidance learning in Drosophila mushroom body neurons.

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Acknowledgements

Thanks to G. Robinson, M. Suster, M. Fitzpatrick, R. Greenspan, D. Sebastian and C. Riedl for comments on a preliminary version of the manuscript. Thanks to M. Busto who compiled table 1, and J. Hall who commented on it. M. Fitzpatrick and C. Riedl helped prepare drafts of the figures. This research was supported by NSERC and MRC grants to M.B.S. M.B.S. is a Canada Research Chair Holder in Genetics.

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DATABASES

LocusLink 

amn

Clk

Cyc

dbt

dnc

for

fru

lat

per

PER2

rut

sbb

tim 

WormBase 

npr-1 

OMIM 

FASPS

Huntington disease

Parkinson disease 

FlyBase 

CaMKII

FURTHER INFORMATION

Flybrain

Marla Sokolowski's homepage

Seymour Benzer

The Interactive Fly

Glossary

ACTIVITY–REST CYCLE

This refers to the rhythm of the locomotor activity of a fly during its 24-h activity cycle. It is also called the circadian locomotor activity rhythm.

PLEIOTROPY

The phenomenon in which a single gene is responsible for several distinct and seemingly unrelated phenotypic effects.

HYPOMORPHIC MUTATION

A mutation that does not completely eliminate the wild-type function of a gene and therefore causes a less severe phenotype than a loss-of-function (or null) mutation.

QUANTITATIVE TRAIT LOCUS

A genetic locus that is identified through the statistical analysis of a complex trait. These traits are typically affected by more than one gene and by the environment.

HERITABILITY

The fraction of the phenotypic variance that is due to additive genetic variance.

PHENOTYPIC PLASTICITY

The modifiability of the phenotype by the environment.

ECLOSION RHYTHM

The timing of the emergence of the adult fly from its pupal case, which usually occurs at dawn.

MOSAIC ANALYSIS

The process of following the progenitors of a single cell (a clone). Clonal analysis can be used to infer several things, such as when gene action takes place and if lineage has a role in cell-fate determination.

ASSOCIATIVE LEARNING

A form of learning whereby the subject learns about the relationship between two stimuli, or between a stimulus and a behaviour.

OLFACTORY-BASED SHOCK-AVOIDANCE LEARNING

A learning model whereby a shock is paired with one of two olfactory stimuli offered to the animal, so that the animal learns to avoid the stimulus paired with the shock in a subsequent choice test that does not include a shock.

MUSHROOM BODIES

Two prominent bilaterally symmetrical structures in the fly brain that are crucial for olfactory learning and memory.

FORWARD GENETICS

A genetic analysis that proceeds from phenotype to genotype by positional cloning or candidate-gene analysis.

EPISTASIS

An interaction between non-allelic genes, such that one gene masks or interferes with the expression of the other gene.

GAL4/UAS SYSTEM

Used in Drosophila to target the expression of specific genes to specific tissues. UAS stands for the upstream-activating system of the yeast GAL4 gene.

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Sokolowski, M. Drosophila: Genetics meets behaviour. Nat Rev Genet 2, 879–890 (2001). https://doi.org/10.1038/35098592

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