Correlations of Genotype with Climate Parameters Suggest Caenorhabditis elegans Niche Adaptations

Abstract

Species inhabit a variety of environmental niches, and the adaptation to a particular niche is often controlled by genetic factors, including gene-by-environment interactions. The genes that vary in order to regulate the ability to colonize a niche are often difficult to identify, especially in the context of complex ecological systems and in experimentally uncontrolled natural environments. Quantitative genetic approaches provide an opportunity to investigate correlations between genetic factors and environmental parameters that might define a niche. Previously, we have shown how a collection of 208 whole-genome sequenced wild Caenorhabditis elegans can facilitate association mapping approaches. To correlate climate parameters with the variation found in this collection of wild strains, we used geographic data to exhaustively curate daily weather measurements in short-term (3 month), middle-term (one year), and long-term (three year) durations surrounding the date of strain isolation. These climate parameters were used as quantitative traits in association mapping approaches, where we identified 11 quantitative trait loci (QTL) for three climatic variables: elevation, relative humidity, and average temperature. We then narrowed the genomic interval of interest to identify gene candidates with variants potentially underlying phenotypic differences. Additionally, we performed two-strain competition assays at high and low temperatures to validate a QTL that could underlie adaptation to temperature and found suggestive evidence supporting that hypothesis.

Keywords: C. elegans; climate; natural variation; niche; weather.

Figure 1

Global distribution of wild isolates and NOAA weather stations. (A) Map of 27,447 ISD NOAA weather stations (blue), and 149 C. elegans wild isolate locations (red). Three isotypes are not depicted as they have no known location of isolation. (B) Histogram of station distance from wild isolate, measured in km. Data from the three-year weather dataset are shown.

Figure 2

GWA of elevation. (A) GWA of elevation of strain isolation shown as Manhattan plots. Genomic position is plotted on the x-axis against the negative log-transformed p-value on the y-axis. SNVs that are above the Bonferroni-corrected significance threshold, indicated by the dotted gray line, are shown in red, and SNVs below the Bonferroni threshold are shown in black. Confidence intervals are represented by the pink bars. (B) Box plots show strain isolation elevations (m), separated by the genotype at the peak marker location. Each point represents one strain. The reference genotype (REF) refers to strains that share the genotype of the reference strain, N2. The alternative genotype (ALT) refers to all other strains that do not have the reference genotype at the peak marker position.

Figure 3

GWA of humidity traits. GWA of relative humidity for three different time periods are visualized as Manhattan plots: 3-month (A), one year (B), three year (C) durations. Genomic position is plotted on the x-axis against the negative log-transformed p-value on the y-axis. SNVs that are above the Bonferroni-corrected significance threshold, indicated by the dotted gray line, are shown in red, and SNVs below the Bonferroni threshold are shown in black. Confidence intervals are represented by the pink bars.

Figure 4

GWA of temperature. (A) GWA of three-year average temperature is visualized as a Manhattan plot. Genomic position is plotted on the x-axis against the negative log-transformed p-value on the y-axis. SNVs that are above the Bonferroni-corrected significance threshold, indicated by the dotted gray line, are shown in red, and SNVs below the Bonferroni threshold are shown in black. Confidence intervals are represented by the pink bars. (B) Box plots show the strain three-year average temperatures, measured in degrees Celsius, separated by genotype at the peak marker locus. Each point represents one strain. The reference genotype (REF) refers to strains that share the genotype of the reference strain, N2. The alternative genotype (ALT) refers to all other strains that do not have the reference genotype at the peak marker position.

Figure 5

Two-strain temperature competition assay. JU847 (isolated at low temperature) was competed against CX11314 (isolated at high temperature) at both 15° (indicated in blue) and 25° (indicated in red). The mean frequency of the JU847 allele in the population is plotted on the y-axis. Error bars represent 1 SD from the mean. Data were collected from nine experimental and five technical replicates.