Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta
Abstract
Genomic variation is widespread, and both neutral and selective processes can generate similar patterns in the genome. These processes are not mutually exclusive, so it is difficult to infer the evolutionary mechanisms that govern population and species divergence. Boechera stricta is a perennial relative of Arabidopsis thaliana native to largely undisturbed habitats with two geographic and ecologically divergent subspecies. Here, we delineate the evolutionary processes driving the genetic diversity and population differentiation in this species. Using whole-genome re-sequencing data from 517 B. stricta accessions, we identify four genetic groups that diverged around 30-180 thousand years ago, with long-term small effective population sizes and recent population expansion after the Last Glacial Maximum. We find three genomic regions with elevated nucleotide diversity, totaling about 10% of the genome. These three regions of elevated nucleotide diversity show excess of intermediate-frequency alleles, higher absolute divergence (dXY), and lower relative divergence (FST) than genomic background, and significant enrichment in immune-related genes, reflecting long-term balancing selection. Scattered across the genome, we also find regions with both high FST and dXY among the groups, termed FST-islands. Population genetic signatures indicate that FST-islands with elevated divergence, which have experienced directional selection, are derived from divergent sorting of ancientmore »
- Authors:
-
- Chinese Academy of Sciences, Guangzhou (China); Duke Univ., Durham, NC (United States)
- Duke Univ., Durham, NC (United States)
- National Taiwan Univ., Taipei (Taiwan)
- HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
- USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1580886
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Biology (Online)
- Additional Journal Information:
- Journal Name: Genome Biology (Online); Journal Volume: 20; Journal Issue: 1; Journal ID: ISSN 1474-760X
- Publisher:
- BioMed Central
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Genomic diversity; Ancestral polymorphism; Balancing selection; Speciation
Citation Formats
Wang, Baosheng, Mojica, Julius P., Perera, Nadeesha, Lee, Cheng -Ruei, Lovell, John T., Sharma, Aditi, Adam, Catherine, Lipzen, Anna, Barry, Kerrie, Rokhsar, Daniel S., Schmutz, Jeremy, and Mitchell-Olds, Thomas. Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta. United States: N. p., 2019.
Web. doi:10.1186/s13059-019-1729-9.
Wang, Baosheng, Mojica, Julius P., Perera, Nadeesha, Lee, Cheng -Ruei, Lovell, John T., Sharma, Aditi, Adam, Catherine, Lipzen, Anna, Barry, Kerrie, Rokhsar, Daniel S., Schmutz, Jeremy, & Mitchell-Olds, Thomas. Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta. United States. doi:https://doi.org/10.1186/s13059-019-1729-9
Wang, Baosheng, Mojica, Julius P., Perera, Nadeesha, Lee, Cheng -Ruei, Lovell, John T., Sharma, Aditi, Adam, Catherine, Lipzen, Anna, Barry, Kerrie, Rokhsar, Daniel S., Schmutz, Jeremy, and Mitchell-Olds, Thomas. Fri .
"Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta". United States. doi:https://doi.org/10.1186/s13059-019-1729-9. https://www.osti.gov/servlets/purl/1580886.
@article{osti_1580886,
title = {Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta},
author = {Wang, Baosheng and Mojica, Julius P. and Perera, Nadeesha and Lee, Cheng -Ruei and Lovell, John T. and Sharma, Aditi and Adam, Catherine and Lipzen, Anna and Barry, Kerrie and Rokhsar, Daniel S. and Schmutz, Jeremy and Mitchell-Olds, Thomas},
abstractNote = {Genomic variation is widespread, and both neutral and selective processes can generate similar patterns in the genome. These processes are not mutually exclusive, so it is difficult to infer the evolutionary mechanisms that govern population and species divergence. Boechera stricta is a perennial relative of Arabidopsis thaliana native to largely undisturbed habitats with two geographic and ecologically divergent subspecies. Here, we delineate the evolutionary processes driving the genetic diversity and population differentiation in this species. Using whole-genome re-sequencing data from 517 B. stricta accessions, we identify four genetic groups that diverged around 30-180 thousand years ago, with long-term small effective population sizes and recent population expansion after the Last Glacial Maximum. We find three genomic regions with elevated nucleotide diversity, totaling about 10% of the genome. These three regions of elevated nucleotide diversity show excess of intermediate-frequency alleles, higher absolute divergence (dXY), and lower relative divergence (FST) than genomic background, and significant enrichment in immune-related genes, reflecting long-term balancing selection. Scattered across the genome, we also find regions with both high FST and dXY among the groups, termed FST-islands. Population genetic signatures indicate that FST-islands with elevated divergence, which have experienced directional selection, are derived from divergent sorting of ancient polymorphisms. Our results suggest that long-term balancing selection on disease resistance genes may have maintained ancestral haplotypes across different geographical lineages, and unequal sorting of balanced polymorphisms may have generated genomic regions with elevated divergence. This study highlights the importance of ancestral balanced polymorphisms as crucial components of genome-wide variation.},
doi = {10.1186/s13059-019-1729-9},
journal = {Genome Biology (Online)},
number = 1,
volume = 20,
place = {United States},
year = {2019},
month = {6}
}
Web of Science
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Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin's finches
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Life-History qtls and Natural Selection on Flowering time in Boechera Stricta, a Perennial Relative of Arabidopsis: Flowering time in Boechera Stricta
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journal, September 2017
- Guerrero, Rafael F.; Hahn, Matthew W.
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Meiotic recombination hotspots - a comparative view
journal, May 2015
- Choi, Kyuha; Henderson, Ian R.
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Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana
journal, July 2007
- Clark, R. M.; Schweikert, G.; Toomajian, C.
- Science, Vol. 317, Issue 5836
The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana
journal, December 2009
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- Science, Vol. 327, Issue 5961
A Gain-of-Function Polymorphism Controlling Complex Traits and Fitness in Nature
journal, August 2012
- Prasad, K. V. S. K.; Song, B. -H.; Olson-Manning, C.
- Science, Vol. 337, Issue 6098
Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake
journal, December 2015
- Malinsky, M.; Challis, R. J.; Tyers, A. M.
- Science, Vol. 350, Issue 6267
ANGSD: Analysis of Next Generation Sequencing Data
journal, November 2014
- Korneliussen, Thorfinn Sand; Albrechtsen, Anders; Nielsen, Rasmus
- BMC Bioinformatics, Vol. 15, Issue 1
Clines, Clusters, and the Effect of Study Design on the Inference of Human Population Structure
journal, January 2005
- Rosenberg, Noah A.; Mahajan, Saurabh; Ramachandran, Sohini
- PLoS Genetics, Vol. 1, Issue 6
Balancing Selection and Its Effects on Sequences in Nearby Genome Regions
journal, January 2006
- Charlesworth, Deborah
- PLoS Genetics, Vol. 2, Issue 4
Population Structure and Eigenanalysis
journal, January 2006
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- PLoS Genetics, Vol. 2, Issue 12
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Robust Demographic Inference from Genomic and SNP Data
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Multilocus Patterns of Nucleotide Diversity, Population Structure and Linkage Disequilibrium in Boechera stricta , a Wild Relative of Arabidopsis
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Estimating Individual Admixture Proportions from Next Generation Sequencing Data
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Fast and Efficient Estimation of Individual Ancestry Coefficients
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fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets
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Assembly of the Boechera retrofracta Genome and Evolutionary Analysis of Apomixis-Associated Genes
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Correction to: Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta
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