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:
-
[1];
- 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}
}
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Works referencing / citing this record:
Variances and covariances of squared linkage disequilibria in finite populations
journal, February 1988
- Hill, W. G.; Weir, B. S.
- Theoretical Population Biology, Vol. 33, Issue 1
1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana
journal, July 2016
- Alonso-Blanco, Carlos; Andrade, Jorge; Becker, Claude
- Cell, Vol. 166, Issue 2
Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution
journal, December 2001
- Mitchell-Olds, Thomas
- Trends in Ecology & Evolution, Vol. 16, Issue 12
The long-term maintenance of a resistance polymorphism through diffuse interactions
journal, July 2014
- Karasov, Talia L.; Kniskern, Joel M.; Gao, Liping
- Nature, Vol. 512, Issue 7515
Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex
journal, October 2016
- Vijay, Nagarjun; Bossu, Christen M.; Poelstra, Jelmer W.
- Nature Communications, Vol. 7, Issue 1
Genomic islands of divergence are not affected by geography of speciation in sunflowers
journal, May 2013
- Renaut, S.; Grassa, C. J.; Yeaman, S.
- Nature Communications, Vol. 4, Issue 1
Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella
journal, August 2015
- Sicard, Adrien; Kappel, Christian; Josephs, Emily B.
- Nature Communications, Vol. 6, Issue 1
Exploring population size changes using SNP frequency spectra
journal, April 2015
- Liu, Xiaoming; Fu, Yun-Xin
- Nature Genetics, Vol. 47, Issue 5
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
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Making sense of genomic islands of differentiation in light of speciation
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Determinants of genetic diversity
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Genomics and the origin of species
journal, February 2014
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- Nature Reviews Genetics, Vol. 15, Issue 3
Young inversion with multiple linked QTLs under selection in a hybrid zone
journal, April 2017
- Lee, Cheng-Ruei; Wang, Baosheng; Mojica, Julius P.
- Nature Ecology & Evolution, Vol. 1, Issue 5
Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis
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Phylogeographic model selection leads to insight into the evolutionary history of four-eyed frogs
journal, July 2016
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Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex
journal, December 2017
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PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses
journal, September 2007
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Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014
- Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern
- Bioinformatics, Vol. 30, Issue 15
Estimating IBD tracts from low coverage NGS data
journal, April 2016
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Genome Wide Analyses Reveal Little Evidence for Adaptive Evolution in Many Plant Species
journal, March 2010
- Gossmann, T. I.; Song, B. -H.; Windsor, A. J.
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Resolution of Brassicaceae Phylogeny Using Nuclear Genes Uncovers Nested Radiations and Supports Convergent Morphological Evolution
journal, October 2015
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- Molecular Biology and Evolution, Vol. 33, Issue 2
Recent Selection Changes in Human Genes under Long-Term Balancing Selection
journal, February 2016
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- Molecular Biology and Evolution, Vol. 33, Issue 6
Variation in Linked Selection and Recombination Drive Genomic Divergence during Allopatric Speciation of European and American Aspens
journal, March 2016
- Wang, Jing; Street, Nathaniel R.; Scofield, Douglas G.
- Molecular Biology and Evolution, Vol. 33, Issue 7
MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets
journal, March 2016
- Kumar, Sudhir; Stecher, Glen; Tamura, Koichiro
- Molecular Biology and Evolution, Vol. 33, Issue 7
SyMAP v3.4: a turnkey synteny system with application to plant genomes
journal, March 2011
- Soderlund, Carol; Bomhoff, Matthew; Nelson, William M.
- Nucleic Acids Research, Vol. 39, Issue 10
agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update
journal, May 2017
- Tian, Tian; Liu, Yue; Yan, Hengyu
- Nucleic Acids Research, Vol. 45, Issue W1
Fast model-based estimation of ancestry in unrelated individuals
journal, July 2009
- Alexander, D. H.; Novembre, J.; Lange, K.
- Genome Research, Vol. 19, Issue 9
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010
- McKenna, A.; Hanna, M.; Banks, E.
- Genome Research, Vol. 20, Issue 9
Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers
journal, September 2015
- Burri, Reto; Nater, Alexander; Kawakami, Takeshi
- Genome Research, Vol. 25, Issue 11
Gene flow, ancient polymorphism, and ecological adaptation shape the genomic landscape of divergence among Darwin's finches
journal, April 2017
- Han, Fan; Lamichhaney, Sangeet; Grant, B. Rosemary
- Genome Research, Vol. 27, Issue 6
Genome-Wide Comparison of Nucleotide-Binding Site-Leucine-Rich Repeat-Encoding Genes in Arabidopsis
journal, August 2011
- Guo, Ya-Long; Fitz, Joffrey; Schneeberger, Korbinian
- Plant Physiology, Vol. 157, Issue 2
A Genome-Wide Survey of R Gene Polymorphisms in Arabidopsis
journal, June 2006
- Bakker, Erica G.; Toomajian, Christopher; Kreitman, Martin
- The Plant Cell, Vol. 18, Issue 8
Strong Selection Genome-Wide Enhances Fitness Trade-Offs Across Environments and Episodes of Selection: Special Section
journal, September 2013
- Anderson, Jill T.; Lee, Cheng-Ruei; Mitchell-Olds, Thomas
- Evolution, Vol. 68, Issue 1
Detecting the number of clusters of individuals using the software structure: a simulation study
journal, July 2005
- Evanno, G.; Regnaut, S.; Goudet, J.
- Molecular Ecology, Vol. 14, Issue 8
Geographic patterns of microsatellite variation in Boechera stricta, a close relative of Arabidopsis: MICROSATELLITE VARIATION IN BOECHERA STRICTA
journal, December 2005
- Song, Bao-Hua; Clauss, Maria J.; Pepper, Alan
- Molecular Ecology, Vol. 15, Issue 2
Divergent selection and heterogeneous genomic divergence
journal, February 2009
- Nosil, Patrik; Funk, Daniel J.; Ortiz-Barrientos, Daniel
- Molecular Ecology, Vol. 18, Issue 3
Quantifying effects of environmental and geographical factors on patterns of genetic differentiation: ENVIRONMENT & GEOGRAPHY OF GENETIC DIVERSITY
journal, October 2011
- Lee, Cheng-Ruei; Mitchell-Olds, Thomas
- Molecular Ecology, Vol. 20, Issue 22
Boechera, a model system for ecological genomics: ECOLOGICAL GENOMICS IN BOECHERA
journal, November 2011
- Rushworth, Catherine A.; Song, Bao-Hua; Lee, Cheng-Ruei
- Molecular Ecology, Vol. 20, Issue 23
Life-History qtls and Natural Selection on Flowering time in Boechera Stricta, a Perennial Relative of Arabidopsis: Flowering time in Boechera Stricta
journal, November 2010
- Anderson, Jill T.; Lee, Cheng-Ruei; Mitchell-Olds, Thomas
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Complex trait divergence contributes to environmental niche differentiation in ecological speciation of Boechera stricta
journal, February 2013
- Lee, Cheng-Ruei; Mitchell-Olds, Thomas
- Molecular Ecology, Vol. 22, Issue 8
Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow
journal, June 2014
- Cruickshank, Tami E.; Hahn, Matthew W.
- Molecular Ecology, Vol. 23, Issue 13
Detecting balancing selection in genomes: limits and prospects
journal, June 2015
- Fijarczyk, Anna; Babik, Wiesław
- Molecular Ecology, Vol. 24, Issue 14
Speciation as a sieve for ancestral polymorphism
journal, September 2017
- Guerrero, Rafael F.; Hahn, Matthew W.
- Molecular Ecology, Vol. 26, Issue 20
Meiotic recombination hotspots - a comparative view
journal, May 2015
- Choi, Kyuha; Henderson, Ian R.
- The Plant Journal, Vol. 83, Issue 1
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
- Ossowski, S.; Schneeberger, K.; Lucas-Lledo, J. I.
- 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
- Patterson, Nick; Price, Alkes L.; Reich, David
- PLoS Genetics, Vol. 2, Issue 12
Genome-Wide Fine-Scale Recombination Rate Variation in Drosophila melanogaster
journal, December 2012
- Chan, Andrew H.; Jenkins, Paul A.; Song, Yun S.
- PLoS Genetics, Vol. 8, Issue 12
Robust Demographic Inference from Genomic and SNP Data
journal, October 2013
- Excoffier, Laurent; Dupanloup, Isabelle; Huerta-Sánchez, Emilia
- PLoS Genetics, Vol. 9, Issue 10
Multilocus Patterns of Nucleotide Diversity, Population Structure and Linkage Disequilibrium in Boechera stricta , a Wild Relative of Arabidopsis
journal, December 2008
- Song, Bao-Hua; Windsor, Aaron J.; Schmid, Karl J.
- Genetics, Vol. 181, Issue 3
Estimating Individual Admixture Proportions from Next Generation Sequencing Data
journal, September 2013
- Skotte, Line; Korneliussen, Thorfinn Sand; Albrechtsen, Anders
- Genetics, Vol. 195, Issue 3
Fast and Efficient Estimation of Individual Ancestry Coefficients
journal, February 2014
- Frichot, Eric; Mathieu, François; Trouillon, Théo
- Genetics, Vol. 196, Issue 4
fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets
journal, April 2014
- Raj, Anil; Stephens, Matthew; Pritchard, Jonathan K.
- Genetics, Vol. 197, Issue 2
Assembly of the Boechera retrofracta Genome and Evolutionary Analysis of Apomixis-Associated Genes
journal, March 2018
- Kliver, Sergei; Rayko, Mike; Komissarov, Alexey
- Genes, Vol. 9, Issue 4
Correction to: Ancient polymorphisms contribute to genome-wide variation by long-term balancing selection and divergent sorting in Boechera stricta
journal, August 2019
- Wang, Baosheng; Mojica, Julius P.; Perera, Nadeesha
- Genome Biology, Vol. 20, Issue 1