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Title: 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 sortingmore » 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.« less

Authors:
ORCiD logo [1];  [2];  [2];  [3];  [4];  [5];  [5];  [5];  [5];  [5];  [6];  [2]
  1. Chinese Academy of Sciences, Guangzhou (China); Duke Univ., Durham, NC (United States)
  2. Duke Univ., Durham, NC (United States)
  3. National Taiwan Univ., Taipei (Taiwan)
  4. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  5. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. 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: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: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 referenced in this record:

Boechera, a model system for ecological genomics: ECOLOGICAL GENOMICS IN BOECHERA
journal, November 2011


Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana
journal, July 2007


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
  • DOI: 10.1105/tpc.106.042614

Estimating Individual Admixture Proportions from Next Generation Sequencing Data
journal, September 2013


Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex
journal, December 2017

  • Ma, Tao; Wang, Kun; Hu, Quanjun
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 2
  • DOI: 10.1073/pnas.1713288114

Genome-Wide Fine-Scale Recombination Rate Variation in Drosophila melanogaster
journal, December 2012


Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake
journal, December 2015


Fast model-based estimation of ancestry in unrelated individuals
journal, July 2009


Balancing Selection and Its Effects on Sequences in Nearby Genome Regions
journal, January 2006


Resolution of Brassicaceae Phylogeny Using Nuclear Genes Uncovers Nested Radiations and Supports Convergent Morphological Evolution
journal, October 2015

  • Huang, Chien-Hsun; Sun, Renran; Hu, Yi
  • Molecular Biology and Evolution, Vol. 33, Issue 2
  • DOI: 10.1093/molbev/msv226

PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses
journal, September 2007

  • Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe
  • The American Journal of Human Genetics, Vol. 81, Issue 3
  • DOI: 10.1086/519795

Fast and Efficient Estimation of Individual Ancestry Coefficients
journal, February 2014


Detecting balancing selection in genomes: limits and prospects
journal, June 2015

  • Fijarczyk, Anna; Babik, Wiesław
  • Molecular Ecology, Vol. 24, Issue 14
  • DOI: 10.1111/mec.13226

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
  • DOI: 10.1038/s41559-017-0119

Trimmomatic: a flexible trimmer for Illumina sequence data
journal, April 2014


Making sense of genomic islands of differentiation in light of speciation
journal, November 2016

  • Wolf, Jochen B. W.; Ellegren, Hans
  • Nature Reviews Genetics, Vol. 18, Issue 2
  • DOI: 10.1038/nrg.2016.133

Arabidopsis thaliana and its wild relatives: a model system for ecology and evolution
journal, December 2001


Variances and covariances of squared linkage disequilibria in finite populations
journal, February 1988


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
  • DOI: 10.1111/evo.12259

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
  • DOI: 10.1111/mec.12250

A Gain-of-Function Polymorphism Controlling Complex Traits and Fitness in Nature
journal, August 2012


Detecting the number of clusters of individuals using the software structure: a simulation study
journal, July 2005


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
  • DOI: 10.1038/ncomms13195

Genomics and the origin of species
journal, February 2014

  • Seehausen, Ole; Butlin, Roger K.; Keller, Irene
  • Nature Reviews Genetics, Vol. 15, Issue 3
  • DOI: 10.1038/nrg3644

Assembly of the Boechera retrofracta Genome and Evolutionary Analysis of Apomixis-Associated Genes
journal, March 2018


Determinants of genetic diversity
journal, June 2016

  • Ellegren, Hans; Galtier, Nicolas
  • Nature Reviews Genetics, Vol. 17, Issue 7
  • DOI: 10.1038/nrg.2016.58

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
  • DOI: 10.1093/molbev/msw051

A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011

  • DePristo, Mark A.; Banks, Eric; Poplin, Ryan
  • Nature Genetics, Vol. 43, Issue 5
  • DOI: 10.1038/ng.806

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
  • DOI: 10.1093/nar/gkx382

Estimating IBD tracts from low coverage NGS data
journal, April 2016


The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana
journal, December 2009


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
  • DOI: 10.1104/pp.111.181990

Phylogeographic model selection leads to insight into the evolutionary history of four-eyed frogs
journal, July 2016

  • Thomé, Maria Tereza C.; Carstens, Bryan C.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 29
  • DOI: 10.1073/pnas.1601064113

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.
  • Molecular Biology and Evolution, Vol. 27, Issue 8
  • DOI: 10.1093/molbev/msq079

ANGSD: Analysis of Next Generation Sequencing Data
journal, November 2014

  • Korneliussen, Thorfinn Sand; Albrechtsen, Anders; Nielsen, Rasmus
  • BMC Bioinformatics, Vol. 15, Issue 1
  • DOI: 10.1186/s12859-014-0356-4

Meiotic recombination hotspots - a comparative view
journal, May 2015

  • Choi, Kyuha; Henderson, Ian R.
  • The Plant Journal, Vol. 83, Issue 1
  • DOI: 10.1111/tpj.12870

Divergent selection and heterogeneous genomic divergence
journal, February 2009


fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets
journal, April 2014


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
  • DOI: 10.1111/mec.12796

1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana
journal, July 2016


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
  • DOI: 10.1093/molbev/msw054

Clines, Clusters, and the Effect of Study Design on the Inference of Human Population Structure
journal, January 2005


The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
journal, July 2010


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
  • DOI: 10.1038/ncomms8960

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
  • DOI: 10.1101/gr.212522.116

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
  • DOI: 10.1038/nature13439

Exploring population size changes using SNP frequency spectra
journal, April 2015

  • Liu, Xiaoming; Fu, Yun-Xin
  • Nature Genetics, Vol. 47, Issue 5
  • DOI: 10.1038/ng.3254

Speciation as a sieve for ancestral polymorphism
journal, September 2017

  • Guerrero, Rafael F.; Hahn, Matthew W.
  • Molecular Ecology, Vol. 26, Issue 20
  • DOI: 10.1111/mec.14290

Population Structure and Eigenanalysis
journal, January 2006


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
  • DOI: 10.1093/nar/gkr123

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
  • DOI: 10.1038/ncomms2833

Robust Demographic Inference from Genomic and SNP Data
journal, October 2013


Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis
journal, May 2005

  • Feder, J. L.; Xie, X.; Rull, J.
  • Proceedings of the National Academy of Sciences, Vol. 102, Issue Supplement 1
  • DOI: 10.1073/pnas.0502099102

Recent Selection Changes in Human Genes under Long-Term Balancing Selection
journal, February 2016

  • de Filippo, Cesare; Key, Felix M.; Ghirotto, Silvia
  • Molecular Biology and Evolution, Vol. 33, Issue 6
  • DOI: 10.1093/molbev/msw023

    Works referencing / citing this record:

    Variances and covariances of squared linkage disequilibria in finite populations
    journal, February 1988


    1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana
    journal, July 2016


    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
    • DOI: 10.1038/nature13439

    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
    • DOI: 10.1038/ncomms13195

    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
    • DOI: 10.1038/ncomms2833

    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
    • DOI: 10.1038/ncomms8960

    Exploring population size changes using SNP frequency spectra
    journal, April 2015

    • Liu, Xiaoming; Fu, Yun-Xin
    • Nature Genetics, Vol. 47, Issue 5
    • DOI: 10.1038/ng.3254

    A framework for variation discovery and genotyping using next-generation DNA sequencing data
    journal, April 2011

    • DePristo, Mark A.; Banks, Eric; Poplin, Ryan
    • Nature Genetics, Vol. 43, Issue 5
    • DOI: 10.1038/ng.806

    Making sense of genomic islands of differentiation in light of speciation
    journal, November 2016

    • Wolf, Jochen B. W.; Ellegren, Hans
    • Nature Reviews Genetics, Vol. 18, Issue 2
    • DOI: 10.1038/nrg.2016.133

    Determinants of genetic diversity
    journal, June 2016

    • Ellegren, Hans; Galtier, Nicolas
    • Nature Reviews Genetics, Vol. 17, Issue 7
    • DOI: 10.1038/nrg.2016.58

    Genomics and the origin of species
    journal, February 2014

    • Seehausen, Ole; Butlin, Roger K.; Keller, Irene
    • Nature Reviews Genetics, Vol. 15, Issue 3
    • DOI: 10.1038/nrg3644

    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
    • DOI: 10.1038/s41559-017-0119

    Mayr, Dobzhansky, and Bush and the complexities of sympatric speciation in Rhagoletis
    journal, May 2005

    • Feder, J. L.; Xie, X.; Rull, J.
    • Proceedings of the National Academy of Sciences, Vol. 102, Issue Supplement 1
    • DOI: 10.1073/pnas.0502099102

    Phylogeographic model selection leads to insight into the evolutionary history of four-eyed frogs
    journal, July 2016

    • Thomé, Maria Tereza C.; Carstens, Bryan C.
    • Proceedings of the National Academy of Sciences, Vol. 113, Issue 29
    • DOI: 10.1073/pnas.1601064113

    Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex
    journal, December 2017

    • Ma, Tao; Wang, Kun; Hu, Quanjun
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 2
    • DOI: 10.1073/pnas.1713288114

    PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses
    journal, September 2007

    • Purcell, Shaun; Neale, Benjamin; Todd-Brown, Kathe
    • The American Journal of Human Genetics, Vol. 81, Issue 3
    • DOI: 10.1086/519795

    Trimmomatic: a flexible trimmer for Illumina sequence data
    journal, April 2014


    Estimating IBD tracts from low coverage NGS data
    journal, April 2016


    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.
    • Molecular Biology and Evolution, Vol. 27, Issue 8
    • DOI: 10.1093/molbev/msq079

    Resolution of Brassicaceae Phylogeny Using Nuclear Genes Uncovers Nested Radiations and Supports Convergent Morphological Evolution
    journal, October 2015

    • Huang, Chien-Hsun; Sun, Renran; Hu, Yi
    • Molecular Biology and Evolution, Vol. 33, Issue 2
    • DOI: 10.1093/molbev/msv226

    Recent Selection Changes in Human Genes under Long-Term Balancing Selection
    journal, February 2016

    • de Filippo, Cesare; Key, Felix M.; Ghirotto, Silvia
    • Molecular Biology and Evolution, Vol. 33, Issue 6
    • DOI: 10.1093/molbev/msw023

    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
    • DOI: 10.1093/molbev/msw051

    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
    • DOI: 10.1093/molbev/msw054

    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
    • DOI: 10.1093/nar/gkr123

    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
    • DOI: 10.1093/nar/gkx382

    Fast model-based estimation of ancestry in unrelated individuals
    journal, July 2009


    The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data
    journal, July 2010


    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
    • DOI: 10.1101/gr.212522.116

    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
    • DOI: 10.1104/pp.111.181990

    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
    • DOI: 10.1105/tpc.106.042614

    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
    • DOI: 10.1111/evo.12259

    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
    • DOI: 10.1111/mec.12250

    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
    • DOI: 10.1111/mec.12796

    Detecting balancing selection in genomes: limits and prospects
    journal, June 2015

    • Fijarczyk, Anna; Babik, Wiesław
    • Molecular Ecology, Vol. 24, Issue 14
    • DOI: 10.1111/mec.13226

    Speciation as a sieve for ancestral polymorphism
    journal, September 2017

    • Guerrero, Rafael F.; Hahn, Matthew W.
    • Molecular Ecology, Vol. 26, Issue 20
    • DOI: 10.1111/mec.14290

    Meiotic recombination hotspots - a comparative view
    journal, May 2015

    • Choi, Kyuha; Henderson, Ian R.
    • The Plant Journal, Vol. 83, Issue 1
    • DOI: 10.1111/tpj.12870

    Common Sequence Polymorphisms Shaping Genetic Diversity in Arabidopsis thaliana
    journal, July 2007


    The Rate and Molecular Spectrum of Spontaneous Mutations in Arabidopsis thaliana
    journal, December 2009


    A Gain-of-Function Polymorphism Controlling Complex Traits and Fitness in Nature
    journal, August 2012


    Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake
    journal, December 2015


    ANGSD: Analysis of Next Generation Sequencing Data
    journal, November 2014

    • Korneliussen, Thorfinn Sand; Albrechtsen, Anders; Nielsen, Rasmus
    • BMC Bioinformatics, Vol. 15, Issue 1
    • DOI: 10.1186/s12859-014-0356-4

    Clines, Clusters, and the Effect of Study Design on the Inference of Human Population Structure
    journal, January 2005


    Balancing Selection and Its Effects on Sequences in Nearby Genome Regions
    journal, January 2006


    Population Structure and Eigenanalysis
    journal, January 2006


    Genome-Wide Fine-Scale Recombination Rate Variation in Drosophila melanogaster
    journal, December 2012


    Robust Demographic Inference from Genomic and SNP Data
    journal, October 2013


    Estimating Individual Admixture Proportions from Next Generation Sequencing Data
    journal, September 2013


    Fast and Efficient Estimation of Individual Ancestry Coefficients
    journal, February 2014


    fastSTRUCTURE: Variational Inference of Population Structure in Large SNP Data Sets
    journal, April 2014


    Assembly of the Boechera retrofracta Genome and Evolutionary Analysis of Apomixis-Associated Genes
    journal, March 2018