Evolving allometry

Frankino AW, Zwaan BJ, Stern DL, and Brakefield PM. 2005. Natural selection and developmental constraints in the evolution of allometries. Science 307: 718-720. Science Online

On the subject of allometry between skeletal characters, there is a paper in the Februrary 4, 2005 Science that addresses the issue from the perspective of development. These researchers used an experimental population of butterflies to test the effect of natural selection on scaling relationships between body parts.

The paper begins by noting that body parts usually are scaled relatively tightly around a small range within species, but between species often show very different allometries with a higher range of variation. They considered two hypotheses to be likely explanations for this pattern. The first proposes that developmental constraints within species act to limit variability in scaling among characters. In this hypothesis, there are only certain ranges of sizes that can be taken on by any body part, because the development of that part is to some extent linked to the development of the rest of the body (or of some other part).

The second instead proposes that the variation within species is limited by natural selection underlying the scaling relationship. The hypothesis of selection would predict that some kinds of scaling relationships within a species are disadvantageous (to individuals) because they create a functional mismatch between the size of certain parts and the size of other parts or the whole.

The researchers in this study applied artificial selection to the area of butterfly forewings to study whether developmental constraits are underlying the allometry between this trait and body size. They found that the forewing area shared a strong genetic correlation (0.75) with pupal mass, and hypothesized that selection on forewing area should constrain the phenotypic evolution along the line of the intraspecific allometry.

They found that the forewing area responded rapidly to selection, without being accompanied by corresponding changes in body size. Although the allometry between these traits suggested that body size should change with selection on forewing area, it did not do so.

Our results, together with the few other studies that have used artificial selection to alter scaling relationships between morphological traits in insects, indicate that even strong genetic correlations do not constrain phenotype evolution in the short term. It seems that the developmental basis of these genetic correlations is more important than their strength in determining the response to selection. In particular, under novel selection regimes such as the artificial one we imposed, the developmental program coordinating the growth of the individual traits may influence how these traits and the relationship between them evolves (719).

After this selection, the researchers placed the altered populations in an open greenhouse environment and allowed them to compete with wild-type conspecifics. They assessed their reproductive success by examining marker powder transfer from males to females. They discovered that the wild-type males attained an average of three times as many matings as the males who had undergone selection on forewing area. "These results demonstrate strong stabilizing selection favoring the natural scaling relationship between forewing and body size in B. anynana" (719).

The researchers were not able to determine why males with the wild-type allometry had greater apparent mating success, although they present a number of hypotheses, including decreased locomotor performance, decreased ability to produce mating signals attractive to females, or decreased ability to compete with other males.

The overall conslusion is that the intraspecific allometry in these insects is primarily maintained not by developmental constraints, but instead by stabilizing selection acting on the allometry itself. In the face of strong genetic correlations between traits, the form of stabilizing selection on these allometries may result in