Molecular hyperdiversity defines populations of the nematode Caenorhabditis brenneri

Abstract

The biology of Sydney Brenner's eponymous species of nematode, Caenorhabditis brenneri, is little known to science, despite its famous sibling Caenorhabditis elegans. Here we demonstrate that C. brenneri harbors the most molecular diversity of any eukaryote, with its 14.1% of polymorphic synonymous sites between individuals being 150-fold greater than humans and most comparable to hyperdiverse bacteria. This diversity is not an artifact of cryptic species divergence but reflects an enormous pan-tropical population, confirmed by fully viable genetic crosses between continents, extensive intralocus recombination, selection on codon use, and only weak geographic genetic structure. These findings in an animal galvanize tests of theory about the evolution of complexity in genomes and phenotypes and enable molecular population genetics methods to finely resolve uncharacterized functional noncoding elements.

Keywords: biodiversity; genetic variation; genome evolution; molecular evolution; nucleotide polymorphism.

Fig. 1.

C. brenneri is hyperdiverse. (A) C. brenneri shows hyperdiverse nucleotide variability (π_syn-JC, the mean number of pairwise differences at synonymous sites with Jukes-Cantor correction for multiple hits; dark purple) for haplotypes pooled across the species range, for analysis restricted to a single haplotype per collection locality (scattered) or a single local population or when quantified for alleles seen in residual heterozygosity of the draft genome assembly. Pale bar behind C. brenneri values indicates estimated π_neu = 0.164. Comparable measures of diversity are shown for other biological model organisms (orange). Error bars for C. brenneri indicate SEM (23 nuclear gene loci for pooled, scattered, and local samples; 3,265 gene loci for genome analysis). (B) The reticulated neighbor-network for globally sampled C. brenneri, based on concatenated sequence of 23 nuclear loci, indicates extensive recombination and little genetic structure among the strain collection locations (color coded). Nucleotide distances for third positions of codons (Jukes-Cantor corrected) exclude gaps. (C) Linkage disequilibrium (r²) decays rapidly with distance in the scattered sample of C. brenneri. Data for 23 nuclear loci are superimposed; solid red line indicates a loose spline fit for all loci; blue lines show loose spline fits for each locus separately.

Fig. 2.

No hybrid breakdown between strains from different continents. (A) F₁ and (B) F₂ progeny production does not differ significantly among crosses made within populations or between populations of C. brenneri (EI, East India; FG, French Guiana; F₁ one-way ANOVA, F_2,34 = 0.77, P = 0.47; F₂ one-way ANOVA, F_2,37 = 0.066, P = 0.94). Error bars indicate SEM.