Abstract
Author SummaryRobustness is a property of biological systems that ensures the production of reproducible phenotypes in spite of underlying environmental, stochastic, and genetic variability. A consequence of robustness is that potentially functional genetic variation is free to accumulate in natural populations because it is buffered at the phenotypic level. Even if this so-called “cryptic” genetic variation has no obvious effects under standard conditions, it may become phenotypically expressed upon major genetic or environmental perturbations. Here we used the model organism Caenorhabditis elegans to identify genetic variations involved in the cryptic evolution of vulval cell fate induction between wild strains. We found that a mutation in the essential nath-10 gene not only contributes to cryptic genetic variation in the vulval system, but also affects key life history traits that are expected to be under a strong selective pressure (brood size, age at sexual maturity, sperm number and rate of progeny production). Indeed, an allele of nath-10 that emerged during the laboratory domestication of C. elegans about 50 years ago confers a strong competitive advantage over the ancestral allele under laboratory conditions. A genetic variation that is cryptic for a robust trait can therefore affect more sensitive phenotypes and thus evolve under selection.
Highlights
Many developmental systems produce outputs that are insensitive to a wide range of environmental or genetic perturbations
Cryptic variation refers to standing genetic variation that is epistatically masked and conditionally neutral: it is not expressed in most conditions, but it can be revealed based on genotype-by-genotype (GxG) interactions with loci involved in the development of the trait or through genotype-by-environment (GxE) interactions, as in the classical experiments by Waddington [4,5]
We find that a non-synonymous polymorphism in the nath-10 gene explains a major effect quantitative trait locus (QTL). nath-10 is the human N-acetyltransferase 10 homolog and its function is largely unknown in C. elegans
Summary
Many developmental systems produce outputs that are insensitive to a wide range of environmental or genetic perturbations. In these robust systems, buffering may allow for the accumulation of ‘‘cryptic’’ genetic variation affecting the system without changing its end product [1,2,3]. Two different hypotheses could explain the evolutionary origin of cryptic genetic variation. It may accumulate neutrally because it has little or no effect on traits evolving under selection. In only few cases were the underlying polymorphisms precisely mapped [18] and candidate polymorphisms confirmed [19]
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