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Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity

Abstract

The nematode Caenorhabditis elegans is central to research in molecular, cell and developmental biology, but nearly all of this research has been conducted on a single strain of C. elegans. Little is known about the population genomic and evolutionary history of this species. We characterized C. elegans genetic variation using high-throughput selective sequencing of a worldwide collection of 200 wild strains and identified 41,188 SNPs. Notably, C. elegans genome variation is dominated by a set of commonly shared haplotypes on four of its six chromosomes, each spanning many megabases. Population genetic modeling showed that this pattern was generated by chromosome-scale selective sweeps that have reduced variation worldwide; at least one of these sweeps probably occurred in the last few hundred years. These sweeps, which we hypothesize to be a result of human activity, have drastically reshaped the global C. elegans population in the recent past.

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Figure 1: Global sampling locations of C. elegans strains.
Figure 2: Neighbor-joining tree of 97 C. elegans isotypes.
Figure 3: Chromosomal patterns of sequence polymorphism.
Figure 4: Extensive sharing of large blocks of near-identical haplotypes.
Figure 5: High-frequency extended haplotypes on chromosomes I, IV, V and X.
Figure 6: Modeled effects of selection.

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Acknowledgements

We thank all the contributors who provided strains to make this study possible, including M. Ailion (University of Washington), A. Cutter (University of Toronto), D. Denver (Oregon State University), S. Estes (Portland State University), J. Hodgkin (University of Oxford), J. Kammenga (Wageningen University), P. McGrath (Rockefeller University), M. Rockman (New York University) and the Caenorhabditis Genetics Center. We also thank the Waksman Genomics Core Facility and the Lewis-Sigler Institute Microarray Facility for the Illumina sequencing. We also thank P. Andolfatto, M. Rockman, H. Seidel, R. Tanny and the members of the Kruglyak laboratory for helpful discussions and comments on the manuscript. This work was supported by a US National Institutes of Health (NIH) Ruth L. Kirschstein National Research Service Award (E.C.A.), the Merck Fellowship of the Life Science Research Foundation (J.P.G.), a National Science Foundation graduate research fellowship (J.S.B.), a James S. McDonnell Foundation Centennial Fellowship, the Howard Hughes Medical Institute and NIH grants R01-HG004321, R37-MH59520 (L.K.) and P50-GM071508 to the Center for Quantitative Biology at the Lewis-Sigler Institute of Princeton University.

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E.C.A. and J.P.G. conceived of and carried out the experiments and data analyses. J.A.S. conceived of and carried out the data processing, simulations and analysis. J.R.C. assisted with DNA preparations. R.G. performed the abamectin sensitivity assays. J.S.B. analyzed and plotted the LD data. M.-A.F. provided the unpublished wild strains. L.K. supervised all aspects of the study. The manuscript was written by E.C.A., J.P.G., J.A.S. and L.K.

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Correspondence to Leonid Kruglyak.

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The authors declare no competing financial interests.

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Supplementary Figures 1–9 and Supplementary Table 2 (PDF 5274 kb)

Supplementary Table 1

C. elegans strains used in our study (XLSX 62 kb)

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Andersen, E., Gerke, J., Shapiro, J. et al. Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet 44, 285–290 (2012). https://doi.org/10.1038/ng.1050

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