Mutation Is a Sufficient and Robust Predictor of Genetic Variation for Mitotic Spindle Traits in Caenorhabditis elegans

Abstract

Different types of phenotypic traits consistently exhibit different levels of genetic variation in natural populations. There are two potential explanations: Either mutation produces genetic variation at different rates or natural selection removes or promotes genetic variation at different rates. Whether mutation or selection is of greater general importance is a longstanding unresolved question in evolutionary genetics. We report mutational variances (VM) for 19 traits related to the first mitotic cell division in Caenorhabditis elegans and compare them to the standing genetic variances (VG) for the same suite of traits in a worldwide collection C. elegans. Two robust conclusions emerge. First, the mutational process is highly repeatable: The correlation between VM in two independent sets of mutation accumulation lines is 0.9. Second, VM for a trait is a good predictor of VG for that trait: The correlation between VM and VG is 0.9. This result is predicted for a population at mutation-selection balance; it is not predicted if balancing selection plays a primary role in maintaining genetic variation.KEYWORDS mutation accumulation; mutational robustness; mutation-selection balance; mutational variance; persistence time T HE question "What are the factors that govern genetic variation in natural populations?" has been central to the field of evolutionary genetics ever since its inception (Dobzhansky 1937;Lewontin 1974Lewontin , 1997. Within a group of organisms, seemingly similar or related phenotypic traits can vary considerably, and consistently, in the extent of genetic variation in the trait. For example, in many organisms, resistance to acute heat stress is much less heritable and evolvable than resistance to acute cold stress (Hoffmann et al. 2013). If different traits in the same set of organisms have consistently different levels of genetic variation, there are two potential underlying evolutionary causes: mutation and/or selection. Traits may differ in the mutational target they present, i.e., the number and/or types of loci that potentially affect the trait, or in the rate at which those loci mutate. Traits may also differ in the average effect that mutations have on the trait; i.e., they may be differently robust to the effects of mutation. Alternatively, traits may be subject to differing strengths and/or kinds of selection.In quantitative genetics, a few empirical conclusions seem fairly certain. First, traits that are direct components of fitness-life history traits-are typically more genetically variable than other classes of traits (Houle 1992;Lynch et al. 1999). Second, when scaled relative to the trait mean, life history traits experience greater input of genetic variation from mutation than other classes of traits (Houle et al. 1996;Halligan and Keightley 2009). Third, life history traits appear to be under stronger purifying selection than other classes of traits (Houle et al. 1996;Lynch et al. 1999;McGuigan et al. 2015).A longstanding related, but unanswered, question is the relative...

Microtubule Feedback and LET-99-Dependent Control of Pulling Forces Ensure Robust Spindle Position

“…Quantitative genetic studies in C. elegans have found an approximately threefold lower persistence of new mutations on the phenotypic trait positioning the division plane compared to the trait displaying the time between first oscillation peak and mid-elongation (52). We here measured the related parameter, duration of oscillations.…”

“…plane position scale linearly with embryo length within different C. elegans natural isolates and beyond within several nematode species (52). These correlations may be either enforced by natural selection or because of some robustness mechanisms, two nonexclusive possibilities.…”

A broad mutational target explains an evolutionary trend

“…S1) (Braendle et al, 2010). Thus, in this system as for wing shape in drosophilids Fierst, 2013, Houle et al, 2017) or mitotic spindle traits in Caenorhabditids (Farhadifar et al, 2015, Farhadifar et al, 2016, the mutational variance matches the evolutionary pattern, with the added advantage here of comparing homologous cells.…”

Robustness of bristle number to temperature and genetic background varies with bristle type and is regulated by miR-9a

“…Understanding the response of phenotypic variation to mutations and to environmental perturbations is important to explain phenotypic evolution. For example, the pattern of mutational phenotypic variation observed at the microevolutionary level (i.e., within species) can be a good predictor of the pattern of variation observed at the macroevolutionary level (between species) (Farhadifar et al, 2016;Houle et al, 2017),. In this study, we examined whether we could find differences in the robustness of bristle number to genetic and environmental perturbations between 8 bristle types in D. melanogaster which, in principle, share a similar genetic architecture and underlying developmental gene network.…”