Abstract
Genetic and developmental architecture may bias the mutationally available phenotypic spectrum. Although such asymmetries in the introduction of variation may influence possible evolutionary trajectories, we lack quantitative characterization of biases in mutationally inducible phenotypic variation, their genotype-dependence, and their underlying molecular and developmental causes. Here we quantify the mutationally accessible phenotypic spectrum of the vulval developmental system using mutation accumulation (MA) lines derived from four wild isolates of the nematodes Caenorhabditis elegans and C. briggsae. The results confirm that on average, spontaneous mutations degrade developmental precision, with MA lines showing a low, yet consistently increased, proportion of developmental defects and variants. This result indicates strong purifying selection acting to maintain an invariant vulval phenotype. Both developmental system and genotype significantly bias the spectrum of mutationally inducible phenotypic variants. First, irrespective of genotype, there is a developmental bias, such that certain phenotypic variants are commonly induced by MA, while others are very rarely or never induced. Second, we found that both the degree and spectrum of mutationally accessible phenotypic variation are genotype-dependent. Overall, C. briggsae MA lines exhibited a two-fold higher decline in precision than the C. elegans MA lines. Moreover, the propensity to generate specific developmental variants depended on the genetic background. We show that such genotype-specific developmental biases are likely due to cryptic quantitative variation in activities of underlying molecular cascades. This analysis allowed us to identify the mutationally most sensitive elements of the vulval developmental system, which may indicate axes of potential evolutionary variation. Consistent with this scenario, we found that evolutionary trends in the vulval system concern the phenotypic characters that are most easily affected by mutation. This study provides an empirical assessment of developmental bias and the evolution of mutationally accessible phenotypes and supports the notion that such bias may influence the directions of evolutionary change.
Highlights
A principal quest in biology is to disentangle the relative contribution and interplay of mutational versus selective forces in the evolutionary process [1]
Mutational decay of developmental precision The developmental system underlying Caenorhabditis vulva precursor cell fate patterning was consistently degraded in mutation accumulation (MA) lines derived from all four isolates
Many MA lines showed multiple, distinct variants and we never found a line in which a specific variant pattern was fixed
Summary
A principal quest in biology is to disentangle the relative contribution and interplay of mutational versus selective forces in the evolutionary process [1]. While biological research is predominated by the search for adaptive explanation underlying phenotypic evolution, it is of critical importance to study how the mutational process alone produces phenotypic variation. Such studies indicate which phenotypic space can be explored by mutation to generate variation for selection to act upon. The mutationally inducible phenotypic spectrum is the fundamentally limiting force constraining and biasing potential evolutionary trajectories of the phenotype. The mutational variance VM of the phenotype represents the amount of variation introduced into the population by mutation each generation and can be extended to a multidimensional phenotypic space, theoretically the M matrix of mutational variance-covariance between phenotypic traits [2,3,4]. No study has attempted to characterize the multivariate mutational structure of a developmental system
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