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.

Figure 1.

Number of flies within each genotype displaying the decanalized scutellar bristle phenotypes at 25°C ((a) females, (b) males) and 29°C ((c) females, (d) males). Deletion homozygous genotype has significantly more flies displaying the decanalized phenotype at 25°C and 29°C in both sexes (black bar, non-deletion homozygous; striped bar, heterozygous; grey bar, deletion homozygous).

Figure 2.

Number of flies within each genotype displaying the decanalized thoracic bristle phenotypes at 25°C ((a) females, (b) males) and 29°C ((c) females, (d) males). Deletion homozygous genotype has significantly more flies displaying the decanalized phenotype at 25°C (females and males) and at 29°C (females only). Black bar, non-deletion homozygous; striped bar, heterozygous; grey bar, deletion homozygous.

Figure 3.

Sternopleural bristle means and phenotypic variances (V_P) at (a,c) 25°C and (b,d) 29°C for non-deletion homozygous (NON-DEL), heterozygous (HET) and deletion homozygous (DEL) genotypes. Means and V_P averaged across all lines within each genotype. Error bars represent one standard error. Closed diamonds, females; open squares, males.

Figure 4.

Centroid size means and phenotypic variances (V_P) at (a,c) 25°C and (b,d) 29°C for non-deletion homozygous (NON-DEL), heterozygous (HET) and deletion homozygous (DEL) genotypes. Means and V_P averaged across all lines within each genotype. Error bars represent one standard error. Closed diamonds, females; open squares, males.

Figure 5.

Response to selection on decanalized scutellar and thoracic bristles at 29°C. Filled diamond, deletion homozygous; filled triangle, deletion homozygous; filled square, deletion homozygous; asterisk, non-deletion homozygous; cross; non-deletion homozygous; open circle, non-deletion homozygous.