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. These genes are mostly located at the chromosomal arms and high recombination rate correlates with their large polymorphism. Gene flow might also contribute to their diversity. Moreover, we identified signatures of strong positive selection in the F-box and csGPCR genes in the non-Hawaiian population using both neutrality tests and Extended Haplotype Homozygosity analysis. Accumulation of high frequency derived alleles in these genes were found in non-Hawaiian population, leading to divergence from the ancestral genotype found in Hawaiian strains. In summary, we found that F-box and csGPCR genes harbour a large pool of natural variants, which may be subjected to positive selection during the recent selective sweep in non-Hawaiian population. These variants are mostly mapped to the substrate-recognition domains of F-box proteins and the extracellular regions of csGPCRs, possibly resulting in advantages during adaptation by affecting protein degradation and the sensing of environmental cues, respectively.
Significance statement The small nematode Caenorhabditis elegans has emerged as an important organism in studying the genetic mechanisms of evolution. F-box and chemosensory GPCR are two of the largest gene families in C. elegans, but their intraspecific evolution within C. elegans was not studied before. In this work, using the nonsynonymous SNV data of 330 C. elegans wild isolates, we found that F-box and chemosensory GPCR genes showed larger polymorphisms and stronger positive selection than other genes. The large diversity is likely the result of rapid gene family expansion, high recombination rate, and gene flow. Analysis of subpopulation suggests that positive selection of these genes occurred most strongly in the non-Hawaiian population, which underwent a selective sweep possibly linked to human activities.
Competing Interest Statement
The authors have declared no competing interest.
