Why does allometry evolve so slowly?

Abstract

Morphological allometry is striking due to its evolutionary conservatism, making it an example of a certain sort of evolutionary stasis. Organisms that vary in size, whether for developmental, environmental, or evolutionary reasons, adopt shapes that are predictable from that size alone. There are two major hypotheses to explain this. It may be that natural selection strongly favors each allometric pattern, or that organisms lack the development and genetic capacity to produce variant shapes for selection to act on. Using a high-throughput system for measuring the size and shape of Drosophila wings, we documented an allometric pattern that has been virtually unchanged for 40 million years. We performed an artificial selection experiment on the static allometric slope within one species. In just 26 generations, we were able to increase the slope from 1.1 to 1.4, and decrease it to 0.8. Once artificial selection was suspended, the slope rapidly evolved back to a value near the initial static slope. This result decisively rules out the hypothesis that allometry is preserved due to a lack of genetic variation, and provides evidence that natural selection acts to maintain allometric relationships. On the other hand, it seems implausible that selection on allometry in the wing alone could be sufficiently strong to maintain static allometries over millions of years. This suggests that a potential explanation for stasis is selection on a potentially large number of pleiotropic effects. This seems likely in the case of allometry, as the sizes of all parts of the body may be altered when the allometric slope of one body part is changed. Unfortunately, hypotheses about pleiotropy have been very difficult to test. We lay out an approach to begin the systematic study of pleiotropic effects using genetic manipulations and high-throughput phenotyping.