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Fine-scale haplotype structure reveals strong signatures of positive selection in a recombining bacterial pathogen

Brian Arnold, Mashaal Sohail, Crista Wadsworth, Jukka Corander, William P. Hanage, Shamil Sunyaev, Yonatan H. Grad
doi: https://doi.org/10.1101/634147
Brian Arnold
1Division of Informatics, Faculty of Arts and Sciences, Harvard University, Cambridge, MA 02138, USA
2Center for Communicable Disease Dynamics, Harvard T. H. Chan School of Public Health, 677 Huntington Avenue, Boston, MA 02115, USA
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  • For correspondence: brianjohnarnold@gmail.com
Mashaal Sohail
3Division of Genetics, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA
4Department of Biomedical Informatics, Harvard Medical School, Boston, MA 02115, USA
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Crista Wadsworth
5Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, 665 Huntington Ave, Boston, MA 02115, USA
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Jukka Corander
6Department of Biostatistics, University of Oslo, Postboks 1122, Blindern, 0317 Oslo, Norway
7Helsinki Institute for Information Technology HIIT, Department of Computer Science, University of Helsinki, Helsinki, Finland
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William P. Hanage
2Center for Communicable Disease Dynamics, Harvard T. H. Chan School of Public Health, 677 Huntington Avenue, Boston, MA 02115, USA
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Shamil Sunyaev
3Division of Genetics, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA 02115, USA
4Department of Biomedical Informatics, Harvard Medical School, Boston, MA 02115, USA
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Yonatan H. Grad
5Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, 665 Huntington Ave, Boston, MA 02115, USA
8Division of Infectious Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
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ABSTRACT

Identifying the forces that create and shape ecologically meaningful variation in bacteria remains an important challenge. For recombining bacteria, the sign and strength of linkage provide a unique lens into ongoing selection. We show derived alleles less than 300bp apart in Neisseria gonorrhoeae exhibit more coupling linkage than repulsion linkage, a pattern that cannot be explained by limited recombination or neutrality as these couplings are significantly stronger for nonsynonymous alleles compared to synonymous alleles. While linkage is shaped by many evolutionary processes, extensive simulations show only two distinct forms of positive selection can drive an excess of coupling linkage between neighboring nonsynonymous alleles: directional selection on introgressed alleles or selection that maintains distinct haplotypes in the presence of recombination. Our results establish a framework for identifying patterns of selection in fine-scale haplotype structure that indicate specific ecological processes in species that recombine with distantly related lineages or possess coexisting adaptive haplotypes.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted May 10, 2019.
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Fine-scale haplotype structure reveals strong signatures of positive selection in a recombining bacterial pathogen
Brian Arnold, Mashaal Sohail, Crista Wadsworth, Jukka Corander, William P. Hanage, Shamil Sunyaev, Yonatan H. Grad
bioRxiv 634147; doi: https://doi.org/10.1101/634147
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Fine-scale haplotype structure reveals strong signatures of positive selection in a recombining bacterial pathogen
Brian Arnold, Mashaal Sohail, Crista Wadsworth, Jukka Corander, William P. Hanage, Shamil Sunyaev, Yonatan H. Grad
bioRxiv 634147; doi: https://doi.org/10.1101/634147

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