Scaling is central to the expression of morphology, and variation in the slopes and intercepts of morphological scaling relationships account for most morphological diversity within biological Classes (more details on scaling here). Despite very well documented patterns of variation in the intercepts and slopes within and among biological groups, very little is known about how selection might act to alter these parameters to generate morphological diversity. Moreover, essentially nothing is known about the degree to which elements of the scaling relationship (mean trait size, the intercept and the slope of the relationship) are evolutionarily independent. Over the last few years, Alex Shingleton, Ian Dworkin and I have taken an integrative approach to study the evolution and expression of morphological scaling relationships in flies. We devised a novel artificial selection approach and applied it for several generations to large populations of fruit flies in an attempt to alter the slope of the wing:body size scaling relationship without altering mean trait size. Our results revealed that the slope can evolve independently of mean trait size but that this is unlikely in nature because of the particular pattern of selection needed to rotate the slope about the bivariate trait mean.
While our work demonstrated that the slope can evolve independently of mean trait size, the response to selection was less than we had expected. Explaining why this was so presented a great challenge. Eventually Alex Shingleton and I realized that we, along with all others that work on the expression and evolution of scaling relationships, have focused attention exclusively on the population-level scaling relationship parameters. This makes sense, as scaling relationships are a property of a group; individual animals do not express morphological scaling relationships. However, individual genotypes regulate the expression of morphology in response to environmental variation (e.g., varying access to nutrition during growth), and therefore an individual may differ in size and shape depending on where it developed. This means that individuals must possess an unseen scaling relationship that describes the phenotypes that would be produced across developmental environments; the observed phenotype is a single point that is realized along this unseen, or ‘cryptic’ individual scaling relationship. Moreover, variation at loci regulating the growth of traits will produce genotype-specific responses to environmental variation, meaning that these cryptic individual scaling relationships may differ in slope and intercept.
Armed with this insight, Alex and his group generated a model of scaling relationship expression that focused on how variation in loci controlling the growth of traits produced variation within populations in the cryptic individual scaling relationships. They then simulated the response to selection in populations that differed only in their distributions of the cryptic individual scaling relationships. The simulations revealed that, even when populations are phenotypically indistinguishable, evolution of the population-level scaling relationship is determined nearly entirely by the distribution of the unseen, individual cryptic scaling relationships. This revelation has the potential to explain conflicting findings among empirical and mathematical tests of scaling relationship evolution and directs researcher attention away from population-level scaling relationship parameters and toward the actual targets of selection - the among individual variation in the developmental mechanisms that regulate growth.
Dreyer, A.P., O. Saleh Ziabari, E.M. Swanson, A. Chawla, W.A. Frankino, A.W. Shingleton. 2016 Cryptic individual scaling relationships and the evolution of morphological scaling. Evolution 70:1703-1716.
Mirth, C.K., W. A. Frankino and A.W. Shingleton. 2016. Allometry and Size Control. invited submission. Current Opinion in Insect Science 13:93-98.
Stillwell, R.C., A.W. Shingleton, I. Dworkin and W.A. 2016. Frankino. Tipping the scales: Evolution of the allometric slope independent of average trait size. Evolution 70:433-444.
Shingleton, A.W. and W. A. Frankino. 2013. New perspectives on the evolution of exaggerated traits. BioEssays 35:100-107. DOI 10.1002/bies.201200139
Stillwell, R. C., I. M. Dworkin, A. W. Shingleton, W. Anthony Frankino. 2011. Experimental manipulation of body size to estimate morphological scaling relationships in Drosophila. Journal of Visualized Experiments (56) e3162. DOI 10.3791/3162
Shingleton, A., W. A. Frankino, T. Flatt, F. Nijhout, and D. Emlen. 2007. Size and Shape: The regulation of static allometry in insects. BioEssays 29:536-548.
Frankino, W. A. Experimental approaches to studying the evolution of morphological allometries: The shape of things to come. Invited submission in: Experimental Evolution: Concepts, Methods, and Applications, T. Garland and M. Rose, eds. University of California Press.