Canalization and evolvability: Tempering the effects of mutation in a changing environment

Abstract

The biological consequences of mutation depend on the translation of genotype into phenotype. The genotype-phenotype map is controlled by developmental and physiological processes, including genetic buffering by the Hsp90 protein chaperone. Hsp90 supports over 150 signal transduction proteins, maintaining the strength of signaling through developmental pathways. During stress, Hsp90 buffering is reduced, and the expressed mutation rate is suddenly increased causing dramatic morphological changes in previously invariable quantitative and qualitative traits. Our recent work suggests that traits controlled by Hsp90 be protected by thresholds, a natural consequence of non-linear biological responses to genetic and environmental factors. A threshold model makes several predictions for the effect of Hsp90 on individual development and the behavior of populations. These include: the existence of upper and lower thresholds, the independence and cumulative effects of buffered genetic variants, the dependence on proximity to the threshold of genetic, environmental or stochastic effects, and the saturation of biological responses and insensitivity (canalization) over a wide range of genetic or environmental effects. We show here how Hsp90-buffered variation meets the predictions of threshold trait models, and suggest that the distinction by Hsp90 between continuous and discrete traits may be more fundamental than the classical division of quantitative and qualitative traits. © 2006 Springer.