Evolution of foraging behaviour in response to chronic malnutrition in Drosophila melanogaster

Abstract

Chronic exposure to food of low quality may exert conflicting selection pressures on foraging behaviour. On the one hand, more active search behaviour may allow the animal to find patches with slightly better, or more, food; on the other hand, such active foraging is energetically costly, and thus may be opposed by selection for energetic efficiency. Here, we test these alternative hypotheses in Drosophila larvae. We show that populations which experimentally evolved improved tolerance to larval chronic malnutrition have shorter foraging path length than unselected control populations. A behavioural polymorphism in foraging path length (the rover-sitter polymorphism) exists in nature and is attributed to the foraging locus (for). We show that a sitter strain (for(s2)) survives better on the poor food than the rover strain (for(R)), confirming that the sitter foraging strategy is advantageous under malnutrition. Larvae of the selected and control populations did not differ in global for expression. However, a quantitative complementation test suggests that the for locus may have contributed to the adaptation to poor food in one of the selected populations, either through a change in for allele frequencies, or by interacting epistatically with alleles at other loci. Irrespective of its genetic basis, our results provide two independent lines of evidence that sitter-like foraging behaviour is favoured under chronic larval malnutrition.

Figure 1.

Larval traits of the selected (dark grey bars) and control (light grey bars) populations; for each trait, data indicate (i) selection regime means ± s.e. and (ii) means ± s.e. of individual replicate populations within each selection regime. (a) Path length traversed by larvae during foraging on yeast in 5 min. (b) Path length traversed by larvae on agar in 2 min. (c) Relative expression level of for transcripts.

Figure 2.

Developmental traits (mean ± s.e.) of foraging strains for^R (light grey bars) and for^s2 (dark grey bars) on poor and standard larval food. (a) Egg-to-adult viability. (b) Egg-to-adult developmental rate. Both strains were maintained for three generations on standard food before the assay.

Figure 3.

Quantitative complementation assays measuring egg-to-adult viability on poor larval food of (a) four crosses between one control population (C1), one selected population (S1) and foraging strains (for^R and for^s2), and (b) the four parental strains used for the crosses.