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. Genetic diversity is low across much of the globe but high in the Hawaiian Islands and across the Pacific Rim. To 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 comprises moderately moist native forests at high elevations (500-1,500 m) where ambient air temperatures are cool (15-20°C). Compared to other Caenorhabditis species found on the Hawaiian Islands (e.g., Caenorhabditis briggsae and Caenorhabditis tropicalis), we found that C. elegans were enriched in native habitats. We measured levels of genetic diversity and differentiation among Hawaiian C. elegans 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 hyper-divergent regions, which may be maintained by balancing selection and are 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 contribute to our understanding of the forces that shape genetic diversity on the most remote volcanic archipelago in the world.

Natural variation inC. elegansshort tandem repeats

“…The free-living nematode Caenorhabditis elegans is a keystone model organism that has been found across the world ( Brenner 1974 ; Kiontke et al 2011 ; Andersen et al 2012 ; Félix and Duveau 2012 ; Cook et al 2017 ; Crombie et al 2019 , 2022 ; Lee et al 2021 ). The C. elegans Natural Diversity Resource (CeNDR) catalogs and distributes thousands of wild strains, genome sequence data, and genome-wide variation data, including SNVs and short indels ( Andersen et al 2012 ; Cook et al 2017 ; Evans et al 2021a ).…”

Natural variation in C. elegans short tandem repeats

“…The selective sweeps were thought to have purged diversity from the centers of chromosomes I, IV, and V, and the left arm of the X chromosome from the C. elegans global population. However, recent sampling efforts of wild C. elegans revealed higher genetic diversity in strains from the Hawaiian Islands and other regions in the Pacific Rim, which were hypothesized as the geographic origin of the species (Crombie et al 2019; Lee et al 2021; Crombie et al 2022). We have previously classified wild C. elegans into swept and divergent strains based on the proportion of swept haplotypes that were identified using SNVs across the genome (See Materials and Methods) (Crombie et al 2019; Lee et al 2021; Zhang et al 2021).…”

“…However, recent sampling efforts of wild C. elegans revealed higher genetic diversity in strains from the Hawaiian Islands and other regions in the Pacific Rim, which were hypothesized as the geographic origin of the species (Crombie et al 2019;Lee et al 2021;Crombie et al 2022).…”

“…The free-living nematode Caenorhabditis elegans is a keystone model organism that has been found across the world (Brenner 1974;Kiontke et al 2011;Andersen et al 2012;Félix and Duveau 2012;Cook et al 2017;Crombie et al 2019;Lee et al 2021;Crombie et al 2022).…”

“…The free-living nematode Caenorhabditis elegans is a keystone model organism that has been found across the world (Brenner 1974; Kiontke et al 2011; Andersen et al 2012; Félix and Duveau 2012; Cook et al 2017; Crombie et al 2019; Lee et al 2021; Crombie et al 2022). The C. elegans Natural Diversity Resource (CeNDR) catalogs and distributes thousands of wild strains, genome sequence data, and genome-wide variation data, including single-nucleotide variants (SNVs) and short indels (Andersen et al 2012; Cook et al 2017; Evans et al 2021).…”