Characterization of Genetic Diversity in the Nematode Pristionchus pacificus from Population-Scale Resequencing Data

Abstract

The hermaphroditic nematode Pristionchus pacificus is an established model system for comparative studies with Caenorhabditis elegans in developmental biology, ecology, and population genetics. In this study, we present whole-genome sequencing data of 104 P. pacificus strains and the draft assembly of the obligate outcrossing sister species P. exspectatus. We characterize genetic diversity within P. pacificus and investigate the population genetic processes shaping this diversity. P. pacificus is 10 times more diverse than C. elegans and exhibits substantial population structure that allows us to probe its evolution on multiple timescales. Consistent with reduced effective recombination in this self-fertilizing species, we find haplotype blocks that span several megabases. Using the P. exspectatus genome as an outgroup, we polarized variation in P. pacificus and found a site frequency spectrum (SFS) that decays more rapidly than expected in neutral models. The SFS at putatively neutral sites is U shaped, which is a characteristic feature of pervasive linked selection. Based on the additional findings (i) that the majority of nonsynonymous variation is eliminated over timescales on the order of the separation between clades, (ii) that diversity is reduced in gene-rich regions, and (iii) that highly differentiated clades show very similar patterns of diversity, we conclude that purifying selection on many mutations with weak effects is a major force shaping genetic diversity in P. pacificus.

Opposing Forces of A/T-Biased Mutations and G/C-Biased Gene Conversions Shape the Genome of the Nematode Pristionchus pacificus

“…This result lends credence to phylogenetic analysis based on molecular clocks, such as our estimation of the TMRCA of the P. pacificus clades, which is at the same order of magnitude as previous mtDNA-based analyses (Molnar et al 2011). The finding of equal mutation rates for nematodes with very different effective population sizes (Rödelsperger et al 2014) and gene numbers (Dieterich et al 2008) is not predicted by the mutation-barrier framework. The genomic content of coding DNA and the effective population size are argued to be the lower limit for an ever-decreasing mutation rate driven by natural selection, as the overwhelming majority of mutations are deleterious (Lynch 2010a;Sung et al 2012).…”

“…DNA was first sheared using the Covaris S2 system. End repair, adenylation, and ligation of one of the 12 index adapters were performed using reagents and the standard protocol of the Illumina TruSeq v2 sample preparation kit as described in Rödelsperger et al (2014) (accompanying article in this issue). Samples were selected for an insert size of 300-400 bp by excision from an agarose gel.…”

“…For the comparison of AT bias between MA lines and natural strains, we used a data set of 104 resequenced strains (Rödelsperger et al 2014). As described in Rödelsperger et al (2014), ancestral alleles were determined based on maximumlikelihood comparison to all 104 sequenced strains and the outgroup species P. exspectatus.…”

“…As described in Rödelsperger et al (2014), ancestral alleles were determined based on maximumlikelihood comparison to all 104 sequenced strains and the outgroup species P. exspectatus. In total, a derived allele in at least one strain was present at 655,705 natural variant sites in the genome.…”

“…A subset of 104 P. pacificus wild isolates had their genome of 169 Mb resequenced, which revealed strong divergence, resulting in .6 million single-nucleotide polymorphisms (SNPs) (Rödelsperger et al 2014). Furthermore, the patterns of divergence and global dispersal between the four P. pacificus clades and the repeated invasion of the geologically young volcanic island of La Reunion (Herrmann et al 2010;McGaughran et al 2013) indicated that the P. pacificus genome is shaped by weakly deleterious mutations and linked selection (Rödelsperger et al 2014). These studies provide a genomic and phylogenetic framework for evolutionary comparisons of mutational patterns.…”