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Hsp90 as a capacitor for morphological evolution

Abstract

The heat-shock protein Hsp90 supports diverse but specific signal transducers and lies at the interface of several developmental pathways. We report here that when Drosophila Hsp90 is mutant or pharmacologically impaired, phenotypic variation affecting nearly any adult structure is produced, with specific variants depending on the genetic background and occurring both in laboratory strains and in wild populations. Multiple, previously silent, genetic determinants produced these variants and, when enriched by selection, they rapidly became independent of the Hsp90 mutation. Therefore, widespread variation affecting morphogenic pathways exists in nature, but is usually silent; Hsp90 buffers this variation, allowing it to accumulate under neutral conditions. When Hsp90 buffering is compromised, for example by temperature, cryptic variants are expressed and selection can lead to the continued expression of these traits, even when Hsp90 function is restored. This provides a plausible mechanism for promoting evolutionary change in otherwise entrenched developmental processes.

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Figure 1: Developmental abnormalities associated with Hsp90 deficits.
Figure 2: Selection experiments.
Figure 3: Variation within and between high-expression lines with the deformed-eye trait.
Figure 4: Partitioning of the wing-vein trait between lines.
Figure 5: Temperature–response curves (norm of reaction) for the deformed-eye trait.
Figure 6: Genetic interactions in the HE lines.
Figure 7: Genotyping of the 19F2 (R48C) Hsp83 mutation.
Figure 8: Wild-type Hsp90 buffered the deformed-eye trait.

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Acknowledgements

We thank M. Wade for discussions, J. Segre for assistance in devising the PCR genotyping strategy, laboratories that supplied fly strains (see Table 2), and T. Mackay for insight into the quantitative analysis of threshold traits.

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Rutherford, S., Lindquist, S. Hsp90 as a capacitor for morphological evolution. Nature 396, 336–342 (1998). https://doi.org/10.1038/24550

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