Quantitative trait symmetry independent of Hsp90 buffering: distinct modes of genetic canalization and developmental stability.
The Hsp90 chaperone buffers development against a wide range of morphological changes in many organisms and in Drosophila masks the effects of hidden genetic variation. Theory predicts that genetic and nongenetic buffering will share common mechanisms. For example, it is argued that Hsp90 genetic buffering evolved solely as a by-product of environmental buffering, and that Hsp90 should mask morphological deviations from any source. To test this idea, we examined the effect of Hsp90 on purely nongenetic variation in phenotype, measured as differences between the left and right sides of several bilaterally symmetrical bristle and wing traits in individual flies. Consistent with previous reports, Hsp90 buffered the expression of rare morphogenic variants specific to particular genetic backgrounds. However, neither trait-by-trait nor global asymmetry was affected in outbred flies treated with an Hsp90 inhibitor or across a series of inbred genetic backgrounds from a wild population tested in isogenic F1 heterozygotes carrying either (i) a dominant negative Hsp90 allele on a mutant 3rd chromosome or (ii) a null P-insertion mutation, which was introgressed into the control genetic background on all chromosomes. By contrast, Hsp90-regulated trait means and significant effects of sex, temperature, and genetic background on trait symmetry were clearly detected. We conclude that, by maintaining the function of signaling proteins, Hsp90 masks variation affecting target pathways and traits in populations independent of purely nongenetic sources of variation, refuting the idea that a single Hsp90-dependent process generally controls genetic canalization and developmental stability.
Centre for Environmental Stress and Adaptation Research, Department of Genetics, University of Melbourne, Victoria 3010, Australia.
Claire C
CC
Milton
Brandon
B
Huynh
Philip
P
Batterham
Suzanne L
SL
Rutherford
Ary A
AA
Hoffmann
D000483:Alleles; D000818:Animals; D002875:Chromosomes; D003433:Crosses, Genetic; D004330:Drosophila; D005260:Female; D005838:Genotype; D018841:HSP90 Heat-Shock Proteins / Q000235:genetics* / Q000502:physiology; D006579:Heterozygote; D008297:Male; D009154:Mutation; D010641:Phenotype; D019655:Quantitative Trait, Heritable; D012737:Sex Factors; D013696:Temperature; D014921:Wings, Animal / Q000502:physiology
D018841:HSP90 Heat-Shock Proteins