Multiple capacitors for natural genetic variation in Drosophila melanogaster

Abstract

Cryptic genetic variation (CGV) or a standing genetic variation that is not ordinarily expressed as a phenotype is released when the robustness of organisms is impaired under environmental or genetic perturbations. Evolutionary capacitors modulate the amount of genetic variation exposed to natural selection and hidden cryptically; they have a fundamental effect on the evolvability of traits on evolutionary timescales. In this study, I have demonstrated the effects of multiple genomic regions of Drosophila melanogaster on CGV in wing shape. I examined the effects of 61 genomic deficiencies on quantitative and qualitative natural genetic variation in the wing shape of D. melanogaster. I have identified 10 genomic deficiencies that do not encompass a known candidate evolutionary capacitor, Hsp90, exposing natural CGV differently depending on the location of the deficiencies in the genome. Furthermore, five genomic deficiencies uncovered qualitative CGV in wing morphology. These findings suggest that CGV in wing shape of wild-type D. melanogaster is regulated by multiple capacitors with divergent functions. Future analysis of genes encompassed by these genomic regions would help elucidate novel capacitor genes and better understand the general features of capacitors regarding natural genetic variation.

Cryptic genetic variation: evolution's hidden substrate

“…These results demonstrate that Hsp90 is a legitimate proof of principle for CGV. For now Hsp90 remains the standout example of a mechanism for revealing CGV, but recent experiments in Drosophila suggest that many genes may function to hide CGV at other loci 96,104 . Future work in this promising area will surely show whether Hsp90 is unique or simply an early herald of an important evolutionary mechanism.…”

Pervasive robustness in biological systems

“…Both natural variation [40][41][42][43] and induced mutations [44][45][46][47] have the potential to affect robustness to noise among isogenic individuals.…”

“…4a) are difficult and have rarely been performed, even for intensely studied systems such as C. elegans vulval patterning. Nevertheless, experiments using Drosophila melanogaster deficiency lines have identified multiple genomic regions encompassing loci that are involved in buffering wing shape to genetic variation or sensory bristle traits to environmental variation 46,121 .…”

Genomics and the Evolution of Phenotypic Traits

“…A dramatic illustration of this phenomenon is the phenotypic variation unmasked when the function of the chaperone hsp90 is compromised: Numerous morphological phenotypes that map to loci throughout the genome appear, indicating that they are genetic based on variants that do not affect trait variation when hsp90 functions normally (Rutherford & Lindquist 1998, Queitsch et al 2002. Hsp90 is a particularly potent evolutionary "capacitor" by virtue of its role in stabilizing protein structure and its interactions with many other proteins, but it is certainly not unique (Takahashi 2012). Although cryptic genetic variation is probably a normal part of most complex genetic systems, its extent and role in trait evolution is not well understood.…”