Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans

Abstract

An understanding of the relative contributions of different evolutionary forces on an organism's genome requires an accurate description of the patterns of genetic variation within and between natural populations. To this end, I report a survey of nucleotide polymorphism in six loci from 118 strains of the nematode Caenorhabditis elegans. These strains derive from wild populations of several regions within France, Germany, and new localities in Scotland, in addition to stock center isolates. Overall levels of silent-site diversity are low within and between populations of this self-fertile species, averaging 0.2% in European samples and 0.3% worldwide. Population structure is present despite a lack of association of sequences with geography, and migration appears to occur at all geographic scales. Linkage disequilibrium is extensive in the C. elegans genome, extending even between chromosomes. Nevertheless, recombination is clearly present in the pattern of polymorphisms, indicating that outcrossing is an infrequent, but important, feature in this species ancestry. The range of outcrossing rates consistent with the data is inferred from linkage disequilibrium, using "scattered" samples representing the collecting phase of the coalescent process in a subdivided population. I propose that genetic variation in this species is shaped largely by population subdivision due to self-fertilization coupled with long- and short-range migration between subpopulations.

Figure 1.

Summary of sequenced regions, polymorphic sites, and haplotypes.

Figure 2.

Linkage disequilibrium in C. elegans European strains (A) and CGC strains (B). Different loci are demarcated by lines and chromosomes are indicated on the left. Shadings indicate Fisher's exact test significance levels: light shading, P < 0.05; medium shading, P < 0.01; dark shading, significant after Bonferroni correction. (C) Multilocus linkage disequilibrium levels for the standardized index of association (I_A) for different collections of strains (all P < 0.001).

Figure 3.

Linkage disequilibrium between SNPs of C. elegans. Sites from different chromosomes are demarcated by lines. Shadings indicate Fisher's exact test significance levels: light shading, P < 0.05; dark shading, P < 0.01. Rectangles with light shading along the perimeter indicate short stretches of sequence on chromosomes I and III with many SNPs (Koch et al. 2000).

Figure 4.

Unrooted neighbor-joining tree for haplotypes derived from a concatenated sequence of 105 European and 12 CGC strains of C. elegans. Subscripts indicate the number of strains per haplotype and strain origin (Fra, France; Ger, Germany; Sco, Scotland). Bootstrap values >70% are indicated below the branches. Haplotype designations are as in Figure 1.

Figure 5.

(A) Relationship between the rate of outcrossing (1 − s) and linkage disequilibrium (r²) for freely recombining sites (c = 0.5) over a range of effective population sizes (N_e). The shaded region corresponds to plausible values in C. elegans based on estimates of N_e and pairwise linkage disequilibrium as estimated by r². (B) Outcrossing rates inferred from linkage disequilibrium for all pairs of sites between chromosomes (II–X) and between loci i and j within a chromosome (II_ij, X_ij; 1, Y25C1A.5; 2, ZK430.1; 3, E01G4.6; 4, D1005.1; 5, R160.7; 6, T24D11.1). Error bars indicate the outcrossing rates derived from the 2.5% linkage disequilibrium percentiles of 1000 random “scattered” samples, with values above the bars showing the corresponding mean estimates of linkage disequilibrium (r²).