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Cryptic Variation in Morphological Evolution: HSP90 as a Capacitor for Loss of Eyes in Cavefish

Science  13 Dec 2013:
Vol. 342, Issue 6164, pp. 1372-1375
DOI: 10.1126/science.1240276

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Eye to Eyeless

To what extent does adaptation rely on de novo mutation, as opposed to preexisting variation? It has been proposed that heat shock protein 90 (HSP90) can act to maintain cryptic variation by correcting misfolded proteins, until the system is taxed under stress conditions. Focusing on the cavefish Astyanax mexicanus, Rohner et al. (p. 1372) provide evidence that this mechanism contributed to morphological evolution in a natural setting where cryptic variation in eye size was masked by HSP90 in the ancestral river but revealed when the fish were reared and selected in caves.

Abstract

In the process of morphological evolution, the extent to which cryptic, preexisting variation provides a substrate for natural selection has been controversial. We provide evidence that heat shock protein 90 (HSP90) phenotypically masks standing eye-size variation in surface populations of the cavefish Astyanax mexicanus. This variation is exposed by HSP90 inhibition and can be selected for, ultimately yielding a reduced-eye phenotype even in the presence of full HSP90 activity. Raising surface fish under conditions found in caves taxes the HSP90 system, unmasking the same phenotypic variation as does direct inhibition of HSP90. These results suggest that cryptic variation played a role in the evolution of eye loss in cavefish and provide the first evidence for HSP90 as a capacitor for morphological evolution in a natural setting.

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