Cryptic Genetic Variation Is Enriched for Potential Adaptations

Abstract

Cryptic genetic variation accumulates under weakened selection and has been proposed as a source of evolutionary innovations. Weakened selection may, however, also lead to the accumulation of strongly deleterious or lethal alleles, swamping the effect of any potentially adaptive alleles when they are revealed. Here I model variation that is partially shielded from selection, assuming that unconditionally deleterious variation is more strongly deleterious than variation that is potentially adaptive in a future environment. I find that cryptic genetic variation can be substantially enriched for potential adaptations under a broad range of realistic parameter values, including those applicable to alternative splices and readthrough products generated by the yeast prion [PSI 1 ]. This enrichment is dramatically stronger when multiple simultaneous changes are required to generate a potentially adaptive phenotype. Cryptic genetic variation is likely to be an effective source of useful adaptations at a time of environmental change, relative to an equivalent source of variation that has not spent time in a hidden state.

Prions in Yeast

“…Readthrough of termination codons caused by [PSI + ] was proposed to broaden the adaptation spectrum in changing environments via increasing phenotypic variability (True and Lindquist 2000;True et al 2004). This agrees with the hypothetical consequences of translational ambiguity in general (e.g., see Inge-Vechtomov et al 1994) and is supported by mathematical simulations (Masel and Bergman 2003;Masel 2006;Griswold and Masel 2009). [PSI + ] indeed increases the growth of some laboratory or wild strains in certain conditions (True and Lindquist 2000;True et al 2004;Halfmann et al 2012), although these effects are genotype-specific, and no consistent effect of [PSI + ] on adaptation to novel environments has been detected (Joseph and Kirkpatrick 2008).…”

Culture History and Population Heterogeneity as Determinants of Bacterial Adaptation: the Adaptomics of a Single Environmental Transition

“…In evolution, organisms can theoretically take advantage of beneficial phenotypes generated by error (209,360). Mistranslation errors may cause individuals in a population to be beneficially prepared for a transition to a new environmental challenge, but advantageous phenotypes caused by mistranslation are not obviously heritable.…”

Genomic Consequences of Background Effects onscallopedMutant Expressivity in the Wing ofDrosophila melanogaster

“…In evolutionary genetics, such interactions are usually estimated in QTL (Pavlicev et al 2008) or linkage disequilibrium mapping (Dworkin et al 2003;Caicedo et al 2004;Steiner et al 2007) studies. However, an alternative approach for studying epistasis is to examine the interactions between new alleles in a population (via mutation or gene flow) and the genetic background in which theses alleles occur (Felix 2007) and, in particular, to determine the evolutionary consequencesof these ''genetic background effects'' (Dworkin 2005a;Masel 2006). One example of an interaction between allelic variants and genetic background is the phenomenon described as cryptic genetic variation (CGV).…”