Changes Across Development Influence Visible and Cryptic Natural Variation of Drosophila melanogaster Olfactory Response

Abstract

Relative to an equivalent source of variation that do not present a hidden state, cryptic genetic variation is likely to be an effective source for possible adaptations at times of atypical environmental conditions. In addition to environmental perturbations, it has also been proposed that genetic disturbances can generate release of cryptic genetic variation. The genetic basis and physiology of olfactory response in Drosophila melanogaster is being studied profusely, but almost no analysis has addressed the question if populations harbor cryptic genetic variation for this trait that only manifests when populations experiences a typical or novel conditions. We quantified olfactory responses to benzaldehyde in both larval and adult lifecycle stages among samples of chromosome two substitution lines extracted from different natural populations of Argentina and substituted into a common inbred background. We also evaluated whether an effect of genetic background change, occurred during chromosome substitution, affect larval and adult olfactory response in terms of release of cryptic genetic variation. Results indicate the presence of genetic variation among chromosome substitution lines in both lifecycle stages analyzed. The comparative analyses between chromosome 2 substitution lines and isofemale lines used to generate the chromosome 2 substitution lines shown that only adults exhibited decanalizing process for olfactory response to benzaldehyde in natural populations of D. melanogaster, i.e., release of hidden genetic variation. We propose that this release of hidden genetic variation in adult flies is a consequence of the shift in genetic background context that happens in chromosome 2 substitution lines, that implies the disruption of natural epistatic interactions and generation of novel ones. All in all, we have found that changes across D. melanogaster development influence visible and cryptic natural variation of olfactory behavior. In this sense, changes in the genetic background can affect gene-by-gene interactions (epistasis) generating different or even novel phenotypes as consequence of phenotypic outcome of cryptic genetic variation.