A naturally occurring variant of Hsp90 that is associated with decanalization

Abstract

The heat shock protein Hsp90 has been the focus of many studies since it was suggested that it acts to mediate the buffering of phenotypic variation. Hsp90-mediated buffering may result in the accumulation of cryptic genetic variation that, when released either as a consequence of environmental or genetic stress, increases the evolvability of a population. Recent studies using laboratory-induced mutations of Hsp90 and/or chemical inhibition to disrupt Hsp90 function confirm that Hsp90 can buffer cryptic genetic variation. We have previously identified a naturally occurring variant in the charged linker region of the Hsp90 gene, and now examine whether this variant is associated with altered levels of trait variability. The variant is associated with the release of cryptic genetic variation for canalized morphological (bristle) traits, but not for uncanalized morphological (wing and bristle) traits, and the effect on canalized traits depends on culture temperature. This suggests that natural genetic variation in Hsp90 may mediate the evolution of canalized morphological traits even if it does not influence the expression of variation for uncanalized traits.

Hsp90 depletion goes wild

“…The inference is that low Hsp90 levels increase sensitivity to mutational perturbations. One other natural polymorphism in the Hsp90 coding sequence had been previously reported [4], and this allele probably also reduces Hsp90 activity, albeit by an unknown amount. This Hsp90 variant was found to release cryptic genetic variation for normally invariant bristle traits, although not for naturally variable ones [4].…”

Cryptic genetic variation: evolution's hidden substrate

“…Several studies have found that naturally occurring polymorphism at Hsp90 can affect fitness and morphology 101,102 , and that natural environmental perturbations, such as the low conductivity in aquatic cave habitats, can reduce Hsp90 function 91 . Other cryptic genetic variants revealed by chemical inhibition of Hsp90 have been confirmed as pre-existing 87 , and evidence also suggests that the reduction in Hsp90 required to affect transposable element activity is greater than that necessary to reveal CGV 103 .…”

Hsp90 is important for fecundity, longevity, and buffering of cryptic deleterious variation in wild fly populations

“…A previous study on naturally occurring Hsp83 variants had identified a nonsynonymous deletion mutation in the Hsp83 coding region, and focused on the effects of this mutation on morphological traits, not on fitness components [27]. In addition, this study perturbed variation buffering only through thermal stress exposure, not through inbreeding, which is especially useful to reveal expression of recessive cryptic genetic variation.…”

“…With some exceptions [8,15,27], most experiments that studied Hsp90's effects on fitness and variation buffering focus on laboratory strains [24,28-30]. In addition, they use strong gain-of-function or loss-of-function mutations with dramatic, often lethal phenotypic effects [31,32].…”