Full-genome evolutionary histories of selfing, splitting, and selection in Caenorhabditis

Abstract

The nematode Caenorhabditis briggsae is a model for comparative developmental evolution with C. elegans. Worldwide collections of C. briggsae have implicated an intriguing history of divergence among genetic groups separated by latitude, or by restricted geography, that is being exploited to dissect the genetic basis to adaptive evolution and reproductive incompatibility; yet, the genomic scope and timing of population divergence is unclear. We performed high-coverage whole-genome sequencing of 37 wild isolates of the nematode C. briggsae and applied a pairwise sequentially Markovian coalescent (PSMC) model to 703 combinations of genomic haplotypes to draw inferences about population history, the genomic scope of natural selection, and to compare with 40 wild isolates of C. elegans. We estimate that a diaspora of at least six distinct C. briggsae lineages separated from one another approximately 200,000 generations ago, including the “Temperate” and “Tropical” phylogeographic groups that dominate most samples worldwide. Moreover, an ancient population split in its history approximately 2 million generations ago, coupled with only rare gene flow among lineage groups, validates this system as a model for incipient speciation. Low versus high recombination regions of the genome give distinct signatures of population size change through time, indicative of widespread effects of selection on highly linked portions of the genome owing to extreme inbreeding by self-fertilization. Analysis of functional mutations indicates that genomic context, owing to selection that acts on long linkage blocks, is a more important driver of population variation than are the functional attributes of the individually encoded genes.

Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins

“…Mutations that ablate Cbr-mss-3-ps function in the AF16 reference strain also occur in 11 wild isolates that span the known diversity of C. briggsae (fig. S7 (20, 27)). Orthologs of all three C. nigoni mss genes were therefore present in the common ancestor of C. nigoni and C. briggsae, but were lost in C. briggsae before its global diversification.…”

“…Spontaneous short (1–5 nt) mutations in C. elegans are biased towards insertions rather than deletions (34), though biases in formation of larger indels remain uncharacterized. Regardless, the relative rates of insertion and deletion mutations likely evolve too slowly to explain C. briggsae ’s reduced genome size, given its recent divergence from C. nigoni (27). Gene loss can sometimes be adaptive (35, 36), and has been proposed as a factor promoting genome shrinkage in selfing Caenorhabditis (10).…”

X exceptionalism in Caenorhabditis speciation

“…The three species C. elegans, C. briggsae and C. tropicalis are the only species in the genus known to have evolved selfing hermaphroditism, which arose independently in the ancestry of each of them (Kiontke et al, 2011). The genetic differentiation among lineages within these species gets magnified by very strong linkage disequilibrium across the genome (Barri ere & F elix, 2005;Cutter, 2006;Cutter, F elix, Barriere, & Charlesworth, 2006;Gimond et al, 2013;Haber et al, 2005;Thomas et al, 2015) and may foster the evolution of genetic incompatibilities among conspecific lineages.…”

“…This might even occur despite the small absolute divergence among interfertile populations relative to the huge molecular divergence observed between "good" species of Caenorhabditis (Cutter, 2008;Dey et al, 2012;Thomas et al, 2015). Such withinspecies incompatibility is indeed observed, often termed outbreeding depression (Dolgin, Charlesworth, Baird, & Cutter, 2007;Gimond et al, 2013).…”

“…Caenorhabditis briggsae is the species most investigated as a model for incipient speciation, given the divergence among phylogeographic groups and hybrid dysfunction in some intergroup crosses Dolgin, F elix, & Cutter, 2008;Ross et al, 2011;Thomas et al, 2015). Crosses between some strain combinations yield outbreeding depression or a developmental-delay phenotype indicative of reduced hybrid fitness (Baird & Stonesifer, 2012;Dolgin et al, 2008;Ross et al, 2011).…”