Genetic variation of morphological scaling in Drosophila

Morphological scaling relationships between the sizes of individual traits
and the body captures the characteristic shape of a species, and the
evolution of scaling is the primary mechanism of morphological
diversification. However, we have almost no knowledge of the genetic
variation of scaling, which is critical if we are to understand how
scaling evolves. Here we explore the genetics of population morphological
scaling relationships – the scaling relationship fit to multiple
genetically-distinct individuals in a population – by describing the
distribution of individual scaling relationships – the genotype-specific
scaling relationships that are unseen or cryptic. These individual scaling
relationships harbor the genetic variation that determines relative trait
growth within individuals, and theoretical studies suggest that their
distribution dictates how the population scaling relationship will respond
to selection. Using variation in nutrition to generate size variation
within 194 isogenic lineages of Drosophila melanogaster,
we reveal extensive variation in the slopes of the wing-body and leg-body
scaling relationships among genotypes. This genetic variation reflects
variation in the nutritionally-induced size plasticity of the wing, leg,
and body. Surprisingly, we find that variation in the slope of individual
scaling relationships primarily results from variation in
nutritionally-induced plasticity of body size, not leg or wing size. These
data allow us to predict how different selection regimes affect scaling
in Drosophila and are the first step in identifying the genetic
targets of such selection. More generally, our approach provides a
framework for understanding the genetic variation of scaling, an important
prerequisite to explaining how selection changes scaling and morphology.