Local adaptation and spatiotemporal patterns of genetic diversity revealed by repeated sampling of Caenorhabditis elegans across the Hawaiian Islands

Abstract

The nematode Caenorhabditis elegans is among the most widely studied organisms, but relatively little is known about its natural ecology. Wild C. elegans have been isolated from both temperate and tropical climates, where they feed on bacteria associated with decomposing plant material. Genetic diversity is low across much of the globe but high in the Hawaiian Islands and across the Pacific Rim. The high genetic diversity found there suggests that: (1) the origin of the species lies in Hawaii or the surrounding Pacific Rim; and (2) the ancestral niche of the species is likely similar to the Hawaiian niche. A recent study of the Hawaiian niche found that genetically distinct groups appeared to correlate with elevation and temperature, but the study had a limited sample size. To better characterize the niche and genetic diversity of C. elegans on the Hawaiian Islands and to explore how genetic diversity might be influenced by local adaptation, we repeatedly sampled nematodes over a three-year period, measured various environmental parameters at each sampling site, and whole-genome sequenced the C. elegans isolates that we identified. We found that the typical Hawaiian C. elegans niche is moderately moist native forests at high elevations (500 to 1500 meters) where temperatures are cool (15 to 20°C). We measured levels of genetic diversity and differentiation among Hawaiian strains and found evidence of seven genetically distinct groups distributed across the islands. Then, we scanned these genomes for signatures of local adaptation and identified 18 distinct regions that overlap with hyperdivergent regions, which are likely maintained by balancing selection and enriched for genes related to environmental sensing, xenobiotic detoxification, and pathogen resistance. These results provide strong evidence of local adaptation among Hawaiian C. elegans and a possible genetic basis for this adaptation.

Interactions of C. elegans β-tubulins with the microtubule inhibitor albendazole

“…Indeed, tbb-1 and tbb-2 may be specialized for growth at different temperatures, as tbb-1 mutants grew poorly at 11° and tbb-2 mutants had compromised growth at 25° (Figure 1). This range matches the substrate temperatures of C. elegans collected from the Hawaiian Islands (4º to 23º) (CROMBIE et al 2019;CROMBIE et al 2021).…”

“…This range matches the substrate temperatures of C. elegans collected from the Hawaiian Islands (4° to 23°) (C rombie et al . 2019; C rombie et al . 2021).…”

An atlas of gene expression variation across the Caenorhabditis elegans species

“…A likely reason is that most C. elegans research uses the reference strain N2 under laboratory conditions, and the functions of many genes might only be revealed in natural environments or in different genetic backgrounds 56 . In the last decade, wild C. elegans strains have exhibited diverse phenotypic variation in natural ecology studies 16, 25, 29, 57–59 . Here, we provide an unprecedentedly large resource of transcriptome profiles from wild C. elegans strains.…”

Transposon-mediated genic rearrangements underlie variation in small RNA pathways

“…The Crick orientation of the ERI-6 exons in these five strains likely represents the ancestral genetic structure at the eri-6/7 locus, based on the following: 1) eri-6-7 orthologs in C. briggsae and C. brenneri show a simple continuous structure on a single strand (Fig. 2); 2) the XZ1516, ECA36, CB4856, and DL238 strains were found to have patterns of ancestral genetic diversity in the C. elegans species [28][29][30] (Extended Data Fig. 5).…”

“…3, Extended Data Figs. 5, 8), which likely reflects the retention of ancestral diversity [28][29][30] . Strains with an inversion of ERI-6 exons, however, are more widely distributed over the world and predominant in Europe.…”