Many ways to be small: different environmental regulators of size generate distinct scaling relationships in Drosophila melanogaster

Abstract

Static allometries, the scaling relationship between body and trait size, describe the shape of animals in a population or species, and are generated in response to variation in genetic or environmental regulators of size. In principle, allometries may vary with the different size regulators that generate them, which can be problematic since allometric differences are also used to infer patterns of selection on morphology. We test this hypothesis by examining the patterns of scaling in Drosophila melanogaster subjected to variation in three environmental regulators of size: nutrition, temperature and rearing density. Our data indicate that different environmental regulators of size do indeed generate different patterns of scaling. Consequently, flies that are ostensibly the same size may have very different body proportions. These data indicate that trait size is not simply a read-out of body size, but that different environmental factors may regulate body and trait size, and the relationship between the two, through different developmental mechanisms. It may therefore be difficult to infer selective pressures that shape scaling relationships in a wild population without first elucidating the environmental and genetic factors that generate size variation among members of the population.

Figure 1

Illustration of D. melanogaster showing the range of body part sizes for OreR flies reared on different diets. For each body part, the organ on the left is from a fly reared on a 100% diet, while the organ on the right is from a fly reared on a 2% diet. Images are shown at the same scale within body parts but at different scales across body parts. Morphological measurements are outlined in black.

Figure 2

Loadings of the first eigenvector of multivariate allometries for different environmental variables and genotypes. Horizontal grey lines indicate expected loadings if trait is isometric to body size. Loadings above this line indicate hyperallometry, loadings below this line indicate hypoallometry. Error bars are 95% confidence intervals. (a) Density, (b) nutrition (25°C), (c) temperature and (d) nutrition (17°C). Dark grey bars, 157; light grey bars, 187; and white bars, OreR.

Figure 3

Trait plasticity in response to different environmental variables. Error bars are 95% confidence intervals. (a) Density, (b) nutrition (25°C), (c) temperature and (d) nutrition (17°C).

Figure 4

Distance tree summarizing similarity among multivariate allometries in different genotypes under different environmental conditions. Grey internal branches have less than 50% bootstrap support. Black internal branches have greater than 50% bootstrap support, with bootstrap values shown adjacent to branch. Branch lengths indicate angular difference (in degrees) between multivariate allometric vectors.

Figure 5

Genetically identical flies of the same ‘size’ had different body proportions. 157 flies reared on 100% food at 25°C (grey bars) had slightly larger thoraces but considerably smaller wings than 157 flies reared on 20% food at 17°C (white bars). Error bars are standard errors. Thoraces and wings are significantly different in size at p<0.05.