Hsp90 inhibition and the expression of phenotypic
variability in the rainforest species Drosophila birchii
VANESSA M. KELLERMANN
1
*, ARY A. HOFFMANN
1
and CARLA M. SGRÒ
1,2
1
Centre for Environmental Stress and Adaptation Research and Department of Genetics,
The University of Melbourne, Parkville, Melbourne 3010, Australia
2
School of Biological Sciences, Monash University, Melbourne 3800, Australia
Received 6 September 2006; accepted for publication 20 December 2006
Recently a heat shock protein (Hsp90) has been implicated as controlling the expression of cryptic genetic variation
through buffering developmental processes. The release of variability in canalized characters following Hsp90
inhibition has been established in model species including Drosophila melanogaster and Arabidopsis thaliana, but
has not yet been examined in species with limited distributions. To test if Hsp90 has a role in releasing phenotypic
variation in rainforest Drosophila species, developing larvae from a large (> 1000 individuals) outbred population
of Drosophila birchii were treated with the Hsp90 inhibitors geldanamycin and radicicol, and morphological traits,
desiccation resistance, and life-history traits were measured. The means of all traits were influenced by inhibition.
Although only the phenotypic variances of two canalized bristle traits were affected consistently, variability for two
of the continuously varying traits (fecundity and development time) were also affected, albeit inconsistently. There
was also no effect of Hsp90 inhibition on the developmental stability of the morphological traits as measured by
fluctuating asymmetry. Hsp90 inhibition did not increase phenotypic variability in desiccation resistance, a trait
previously shown to represent an evolutionary limit in this species. These results question the extent to which
Hsp90 buffers variation for both quantitative and discrete traits, and highlight the need for further empirical
studies to determine the involvement of Hsp90 in canalization and developmental stability. Nevertheless the
results demonstrated increased variability in canalized traits, consistent with observations in model systems.
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92, 457–465.
ADDITIONAL KEYWORDS: canalization – cryptic genetic variation – developmental instability – discrete –
life history – quantitative.
INTRODUCTION
The expression of phenotypic variability in some
traits is believed to be buffered against the possible
negative effects of environmental and genetic pertur-
bations by some genes that act during development.
This buffering process, termed canalization by Wad-
dington (1942), results in constancy of the phenotype
in spite of any genetic or environmental variation
encountered during development. Canalization may
be partly mediated by Hsp90, one of the heat shock
proteins (Rutherford & Lindquist, 1998). Inhibition
of Hsp90 expression through mutations, chemical
inhibitors, or environmental stress, in both Droso-
phila melanogaster and Arabidopsis thaliana, pro-
duces an array of abnormal phenotypes (Rutherford
& Lindquist, 1998; Queitsch, Sangster & Lindquist,
2002). Through selection these phenotypes became
stably inherited in the absence of Hsp90 suppression.
Thus, Hsp90 has been proposed to be a capacitator for
evolutionary change through release of cryptic varia-
tion. Recent work in fungi has also demonstrated that
Hsp90 may facilitate the evolution of drug resistance
by allowing new mutations to have immediate
phenotypic effects (Cowen & Lindquist, 2005).
These results highlight the potential role of Hsp90
in evolution.
The original results of Rutherford & Lindquist
(1998) in D. melanogaster demonstrate the potential
of Hsp90 to buffer variation in canalized traits. Less
*Corresponding author.
E-mail: v.kellermann@pgrad.unimelb.edu.au
Biological Journal of the Linnean Society, 2007, 92, 457–465. With 3 figures
© 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92, 457–465 457