Large Genetic Diversity and Strong Positive Selection in F-Box and GPCR Genes among the Wild Isolates of Caenorhabditis elegans

Abstract

The F-box and chemosensory GPCR (csGPCR) gene families are greatly expanded in nematodes, including the model organism Caenorhabditis elegans, compared to insects and vertebrates. However, the intraspecific evolution of these two gene families in nematodes remain unexamined. In this study, we analyzed the genomic sequences of 330 recently sequenced wild isolates of C. elegans using a range of population genetics approaches. We found that F-box and csGPCR genes, especially the Srw family csGPCRs, showed much more diversity than other gene families. Population structure analysis and phylogenetic analysis divided the wild strains into eight non-Hawaiian and three Hawaiian subpopulations. Some Hawaiian strains appeared to be more ancestral than all other strains. F-box and csGPCR genes maintained a great amount of the ancestral variants in the Hawaiian subpopulation and their divergence among the non-Hawaiian subpopulations contributed significantly to population structure. F-box genes are mostly located at the chromosomal arms and high recombination rate correlates with their large polymorphism. Moreover, using both neutrality tests and Extended Haplotype Homozygosity analysis, we identified signatures of strong positive selection in the F-box and csGPCR genes among the wild isolates, especially in the non-Hawaiian population. Accumulation of high-frequency derived alleles in these genes was found in non-Hawaiian population, leading to divergence from the ancestral genotype. In summary, we found that F-box and csGPCR genes harbour a large pool of natural variants, which may be subjected to positive selection. These variants are mostly mapped to the substrate-recognition domains of F-box proteins and the extracellular and intracellular regions of csGPCRs, possibly resulting in advantages during adaptation by affecting protein degradation and the sensing of environmental cues, respectively.

Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

“…5C). Thus, our studies with the SVs support the findings of previous studies (34, 35) using the SNVs that some Hawaiian strains carry ancestral variants that are highly divergent, while other Hawaiian strains (Hawaii_4-7 groups) are admixed with the European groups.…”

Natural variation inC. elegansshort tandem repeats

“…To understand the evolution of STRs in C. elegans , a more informative comparison might come from choosing a reference from strains that avoided selective sweeps and was isolated from regions nearby the species origins. For example, the Hawaiian strain XZ1516, which likely carries the most ancestral genotypes ( Crombie et al 2019 ; Ma et al 2021 ), has contraction in 66% of the 2400 pSTRs that showed length variation to the reference STRs. Therefore, STR expansion rather than contraction likely occurred from ancestors to descendants in C. elegans if we consider strains that might reflect the ancestral origin of the species.…”

Quasi-prime peptides: identification of the shortest peptide sequences unique to a species

“…In yeast we observe terms associated with cell cycle and plasma membrane among others Supplementary Figure S7a ), whereas in C. elegans , we observe enrichment for terms associated with detection of chemical stimuli, the plasma membrane and sensory perception ( Supplementary Figure S7b ). There is evidence supporting strong positive selection for sensory perception genes in C. elegans ( 19 ), reinforcing the notion that quasi-prime peptides are also associated with rapid, adaptive evolution.…”