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Title: A generalist–specialist trade-off between switchgrass cytotypes impacts climate adaptation and geographic range

Abstract

Polyploidy, which occurs in roughly half of all flowering plants and an even higher percentage of grasses, is thought to be a major driver of adaptation. Higher numbers of copies of each gene in polyploid genomes can increase genetic diversity, which could drive shifts in habitat preference, adaptability, and fitness. To test the effects of increased ploidy, we compared genomic diversity, environmental niche, and fitness responses across climatic gradients between tetraploid and octoploid switchgrass. We found that the octoploids contained novel combinations of the ancestral tetraploid genetic diversity, which was linked to the expansion of switchgrass into unsuitable habitats for tetraploid populations. Our experiments revealed evidence of niche divergence, differential fitness, and a generalist–specialist trade-off between cytotypes.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [2];  [1]; ORCiD logo [2]; ORCiD logo [1];  [3];  [1];  [2];  [2];  [4]; ORCiD logo [5]; ORCiD logo [6]; ORCiD logo [7];  [8]; ORCiD logo [3]; ORCiD logo [7];  [9]; ORCiD logo [10]; ORCiD logo [11] more »;  [2];  [2];  [12]; ORCiD logo [2]; ORCiD logo [13]; ORCiD logo [1] « less
  1. Univ. of Texas, Austin, TX (United States)
  2. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
  3. Michigan State Univ., East Lansing, MI (United States)
  4. South Dakota State Univ., Brookings, SD (United States)
  5. US Department of Agriculture–Agricultural Research Service, Temple, TX (United States)
  6. Univ. of Missouri, Columbia, MO (United States)
  7. Argonne National Lab. (ANL), Lemont, IL (United States)
  8. US Department of Agriculture–Natural Resources Conservation Service, Kingsville, TX (United States)
  9. US Department of Agriculture–Agricultural Research Service, Lincoln, NE (United States)
  10. Texas A&M Univ., Overton, TX (United States)
  11. Oklahoma State Univ., Stillwater, OK (United States)
  12. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  13. HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States); Argonne National Laboratory (ANL), Argonne, IL (United States); Univ. of Texas, Austin, TX (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1863806
Alternate Identifier(s):
OSTI ID: 1865807; OSTI ID: 1902632; OSTI ID: 1958130
Grant/Contract Number:  
SC0018409; SC0014156; SC0021126; SC0017883; AC02-05CH11231; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 119; Journal Issue: 15; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; cytotypes; octoploid; panicum virgatum; cytotypes, octoploid, Panicum virgatum, switchgrass

Citation Formats

Napier, Joseph D., Grabowski, Paul P., Lovell, John T., Bonnette, Jason, Mamidi, Sujan, Gomez-Hughes, Maria Jose, VanWallendael, Acer, Weng, Xiaoyu, Handley, Lori H., Kim, Min K., Boe, Arvid R., Fay, Philip A., Fritschi, Felix B., Jastrow, Julie D., Lloyd-Reilley, John, Lowry, David B., Matamala, Roser, Mitchell, Robert B., Rouquette, Jr., Francis M., Wu, Yanqi, Webber, Jenell, Jones, Teresa, Barry, Kerrie, Grimwood, Jane, Schmutz, Jeremy, and Juenger, Thomas E. A generalist–specialist trade-off between switchgrass cytotypes impacts climate adaptation and geographic range. United States: N. p., 2022. Web. doi:10.1073/pnas.2118879119.
Napier, Joseph D., Grabowski, Paul P., Lovell, John T., Bonnette, Jason, Mamidi, Sujan, Gomez-Hughes, Maria Jose, VanWallendael, Acer, Weng, Xiaoyu, Handley, Lori H., Kim, Min K., Boe, Arvid R., Fay, Philip A., Fritschi, Felix B., Jastrow, Julie D., Lloyd-Reilley, John, Lowry, David B., Matamala, Roser, Mitchell, Robert B., Rouquette, Jr., Francis M., Wu, Yanqi, Webber, Jenell, Jones, Teresa, Barry, Kerrie, Grimwood, Jane, Schmutz, Jeremy, & Juenger, Thomas E. A generalist–specialist trade-off between switchgrass cytotypes impacts climate adaptation and geographic range. United States. https://doi.org/10.1073/pnas.2118879119
Napier, Joseph D., Grabowski, Paul P., Lovell, John T., Bonnette, Jason, Mamidi, Sujan, Gomez-Hughes, Maria Jose, VanWallendael, Acer, Weng, Xiaoyu, Handley, Lori H., Kim, Min K., Boe, Arvid R., Fay, Philip A., Fritschi, Felix B., Jastrow, Julie D., Lloyd-Reilley, John, Lowry, David B., Matamala, Roser, Mitchell, Robert B., Rouquette, Jr., Francis M., Wu, Yanqi, Webber, Jenell, Jones, Teresa, Barry, Kerrie, Grimwood, Jane, Schmutz, Jeremy, and Juenger, Thomas E. Mon . "A generalist–specialist trade-off between switchgrass cytotypes impacts climate adaptation and geographic range". United States. https://doi.org/10.1073/pnas.2118879119. https://www.osti.gov/servlets/purl/1863806.
@article{osti_1863806,
title = {A generalist–specialist trade-off between switchgrass cytotypes impacts climate adaptation and geographic range},
author = {Napier, Joseph D. and Grabowski, Paul P. and Lovell, John T. and Bonnette, Jason and Mamidi, Sujan and Gomez-Hughes, Maria Jose and VanWallendael, Acer and Weng, Xiaoyu and Handley, Lori H. and Kim, Min K. and Boe, Arvid R. and Fay, Philip A. and Fritschi, Felix B. and Jastrow, Julie D. and Lloyd-Reilley, John and Lowry, David B. and Matamala, Roser and Mitchell, Robert B. and Rouquette, Jr., Francis M. and Wu, Yanqi and Webber, Jenell and Jones, Teresa and Barry, Kerrie and Grimwood, Jane and Schmutz, Jeremy and Juenger, Thomas E.},
abstractNote = {Polyploidy, which occurs in roughly half of all flowering plants and an even higher percentage of grasses, is thought to be a major driver of adaptation. Higher numbers of copies of each gene in polyploid genomes can increase genetic diversity, which could drive shifts in habitat preference, adaptability, and fitness. To test the effects of increased ploidy, we compared genomic diversity, environmental niche, and fitness responses across climatic gradients between tetraploid and octoploid switchgrass. We found that the octoploids contained novel combinations of the ancestral tetraploid genetic diversity, which was linked to the expansion of switchgrass into unsuitable habitats for tetraploid populations. Our experiments revealed evidence of niche divergence, differential fitness, and a generalist–specialist trade-off between cytotypes.},
doi = {10.1073/pnas.2118879119},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 15,
volume = 119,
place = {United States},
year = {Mon Apr 04 00:00:00 EDT 2022},
month = {Mon Apr 04 00:00:00 EDT 2022}
}

Works referenced in this record:

Shift in cytotype frequency and niche space in the invasive plant Centaurea maculosa
journal, May 2009

  • Treier, Urs A.; Broennimann, Olivier; Normand, Signe
  • Ecology, Vol. 90, Issue 5
  • DOI: 10.1890/08-0420.1

Alignment‐free methods for polyploid genomes: Quick and reliable genetic distance estimation
journal, September 2021


Chromosome inversions, adaptive cassettes and the evolution of species' ranges
journal, February 2015

  • Kirkpatrick, Mark; Barrett, Brian
  • Molecular Ecology, Vol. 24, Issue 9
  • DOI: 10.1111/mec.13074

The biogeography of plant reproduction: potential determinants of species' range sizes
journal, November 2006


ENMTools 1.0: an R package for comparative ecological biogeography
journal, January 2021

  • Warren, Dan L.; Matzke, Nicholas J.; Cardillo, Marcel
  • Ecography, Vol. 44, Issue 4
  • DOI: 10.1111/ecog.05485

BLAT---The BLAST-Like Alignment Tool
journal, March 2002


Minority Cytotype Exclusion in Local Plant Populations
journal, February 1975


Morphological Variation and Width of Ecological Niche
journal, September 1965

  • Van Valen, Leigh
  • The American Naturalist, Vol. 99, Issue 908
  • DOI: 10.1086/282379

Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae)
journal, December 2011


BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis
journal, April 2019

  • Bouckaert, Remco; Vaughan, Timothy G.; Barido-Sottani, Joëlle
  • PLOS Computational Biology, Vol. 15, Issue 4
  • DOI: 10.1371/journal.pcbi.1006650

Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009


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


Genome-size Variation in Switchgrass (Panicum virgatum): Flow Cytometry and Cytology Reveal Rampant Aneuploidy
journal, January 2010


Establishment of a tetraploid cytotype in a diploid population: Effect of relative fitness of the cytotypes
journal, March 1991


Polyploidy and genome evolution in plants
journal, December 2015

  • Soltis, Pamela S.; Marchant, D. Blaine; Van de Peer, Yves
  • Current Opinion in Genetics & Development, Vol. 35
  • DOI: 10.1016/j.gde.2015.11.003

Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass
journal, January 2021


Genomic Plasticity and the Diversity of Polyploid Plants
journal, April 2008


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

Switchgrass as a sustainable bioenergy crop
journal, April 1996


Latitudinal Adaptation of Switchgrass Populations
journal, January 2004


Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants
journal, July 2017

  • Alix, Karine; Gérard, Pierre R.; Schwarzacher, Trude
  • Annals of Botany, Vol. 120, Issue 2
  • DOI: 10.1093/aob/mcx079

Switchgrass Genomic Diversity, Ploidy, and Evolution: Novel Insights from a Network-Based SNP Discovery Protocol
journal, January 2013


New methods for measuring ENM breadth and overlap in environmental space
journal, September 2018

  • Warren, Dan L.; Beaumont, Linda J.; Dinnage, Russell
  • Ecography, Vol. 42, Issue 3
  • DOI: 10.1111/ecog.03900

Environmental Niche Equivalency Versus Conservatism: Quantitative Approaches to Niche Evolution
journal, November 2008


Cytogeography of Panicum Virgatum in Central North America
journal, October 1959


Complete Switchgrass Genetic Maps Reveal Subgenome Collinearity, Preferential Pairing and Multilocus Interactions
journal, April 2010


Polyploidy, Hybridization, and the Invasion of New Habitats
journal, January 1985

  • Stebbins, G. Ledyard
  • Annals of the Missouri Botanical Garden, Vol. 72, Issue 4
  • DOI: 10.2307/2399224

Chloroplast genomic resources for phylogeny and DNA barcoding: a case study on Fritillaria
journal, January 2018


Polyploidy and its effect on evolutionary success: old questions revisited with new tools
journal, November 2012


QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient
journal, June 2019

  • Lowry, David B.; Lovell, John T.; Zhang, Li
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 26
  • DOI: 10.1073/pnas.1821543116

Bioclimatic evaluation of geographical range in Fragaria (Rosaceae): consequences of variation in breeding system, ploidy and species age: Bioclimatic Evaluation of Range in Fragaria
journal, August 2014

  • Johnson, Anna L.; Govindarajulu, Rajanikanth; Ashman, Tia-Lynn
  • Botanical Journal of the Linnean Society, Vol. 176, Issue 1
  • DOI: 10.1111/boj.12190

WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas: NEW CLIMATE SURFACES FOR GLOBAL LAND AREAS
journal, May 2017

  • Fick, Stephen E.; Hijmans, Robert J.
  • International Journal of Climatology, Vol. 37, Issue 12
  • DOI: 10.1002/joc.5086

Population genomic variation reveals roles of history, adaptation and ploidy in switchgrass
journal, July 2014

  • Grabowski, Paul P.; Morris, Geoffrey P.; Casler, Michael D.
  • Molecular Ecology, Vol. 23, Issue 16
  • DOI: 10.1111/mec.12845

DISCORDANCE BETWEEN NUCLEAR AND CHLOROPLAST PHYLOGENIES IN THE HEUCHERA GROUP (SAXIFRAGACEAE)
journal, August 1995


Transcriptome Analysis of Tetraploid and Octoploid Common Reed (Phragmites australis)
journal, May 2021


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

Switchgrass Germplasm Resources
journal, January 2015


VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing
journal, February 2012


Application of Phylogenetic Networks in Evolutionary Studies
journal, October 2005

  • Huson, Daniel H.; Bryant, David
  • Molecular Biology and Evolution, Vol. 23, Issue 2
  • DOI: 10.1093/molbev/msj030

Mash: fast genome and metagenome distance estimation using MinHash
journal, June 2016


Mistaking geography for biology: inferring processes from species distributions
journal, October 2014

  • Warren, Dan. L.; Cardillo, Marcel; Rosauer, Dan F.
  • Trends in Ecology & Evolution, Vol. 29, Issue 10
  • DOI: 10.1016/j.tree.2014.08.003

Geographical and environmental range expansion through polyploidy in wild potatoes (Solanum section Petota)
journal, July 2007


Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations
journal, April 2018

  • Forester, Brenna R.; Lasky, Jesse R.; Wagner, Helene H.
  • Molecular Ecology, Vol. 27, Issue 9
  • DOI: 10.1111/mec.14584

Second-generation PLINK: rising to the challenge of larger and richer datasets
journal, February 2015


Five Nuclear Loci Resolve the Polyploid History of Switchgrass (Panicum virgatum L.) and Relatives
journal, June 2012


ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R
journal, July 2018


The Evolutionary Consequences of Polyploidy
journal, November 2007


Incompatibility Systems in Switchgrass
journal, January 2002


Adaptations between Ecotypes and along Environmental Gradients in Panicum virgatum
journal, May 2014

  • Lowry, David B.; Behrman, Kathrine D.; Grabowski, Paul
  • The American Naturalist, Vol. 183, Issue 5
  • DOI: 10.1086/675760

Neopolyploidy in Flowering Plants
journal, November 2002


Genetic Diversity, Plant Adaptation Regions, and Gene Pools for Switchgrass
journal, January 2007


The more the better? The role of polyploidy in facilitating plant invasions
journal, October 2011

  • te Beest, M.; Le Roux, J. J.; Richardson, D. M.
  • Annals of Botany, Vol. 109, Issue 1
  • DOI: 10.1093/aob/mcr277

Homoeologous Exchanges, Segmental Allopolyploidy, and Polyploid Genome Evolution
journal, August 2020


References
book, January 2012


phangorn: phylogenetic analysis in R
journal, December 2010


Genetic and Epigenetic Aspects of Polyploid Evolution in Plants
journal, January 2013

  • Madlung, A.; Wendel, J. F.
  • Cytogenetic and Genome Research, Vol. 140, Issue 2-4
  • DOI: 10.1159/000351430

Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Née
journal, June 2013

  • Gugger, Paul F.; Ikegami, Makihiko; Sork, Victoria L.
  • Molecular Ecology, Vol. 22, Issue 13
  • DOI: 10.1111/mec.12317

An introduction to ROC analysis
journal, June 2006


Pathways, Mechanisms, and Rates of Polyploid Formation in Flowering Plants
journal, November 1998


nQuire: a statistical framework for ploidy estimation using next generation sequencing
journal, April 2018


The Analysis of Polyploid Genetic Data
journal, January 2018

  • Meirmans, Patrick G.; Liu, Shenglin; van Tienderen, Peter H.
  • Journal of Heredity, Vol. 109, Issue 3
  • DOI: 10.1093/jhered/esy006

A practical guide to environmental association analysis in landscape genomics
journal, August 2015

  • Rellstab, Christian; Gugerli, Felix; Eckert, Andrew J.
  • Molecular Ecology, Vol. 24, Issue 17
  • DOI: 10.1111/mec.13322

Widespread generalist clones are associated with range and niche expansion in allopolyploids of Pacific Northwest Hawthorns ( Crataegus L.)
journal, September 2017

  • Coughlan, J. M.; Han, S.; Stefanović, S.
  • Molecular Ecology, Vol. 26, Issue 20
  • DOI: 10.1111/mec.14331

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


Multiple genomes give switchgrass an advantage
journal, February 2021


The variant call format and VCFtools
journal, June 2011


Polyploidy and ecological adaptation in wild yarrow
journal, March 2011


Natural Hybrids and Gene Flow between Upland and Lowland Switchgrass
journal, January 2011


Higher ploidy is associated with reduced range breadth in the Potentilleae tribe
journal, April 2018

  • Brittingham, Hayley A.; Koski, Matthew H.; Ashman, Tia‐Lynn
  • American Journal of Botany, Vol. 105, Issue 4
  • DOI: 10.1002/ajb2.1046

ggtree : an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data
journal, September 2016

  • Yu, Guangchuang; Smith, David K.; Zhu, Huachen
  • Methods in Ecology and Evolution, Vol. 8, Issue 1
  • DOI: 10.1111/2041-210X.12628

adegenet: a R package for the multivariate analysis of genetic markers
journal, April 2008


LDheatmap : An R Function for Graphical Display of Pairwise Linkage Disequilibria Between Single Nucleotide Polymorphisms
journal, January 2006

  • Shin, Ji-Hyung; Blay, Sigal; Graham, Jinko
  • Journal of Statistical Software, Vol. 16, Issue Code Snippet 3
  • DOI: 10.18637/jss.v016.c03

Mixed-Ploidy Species: Progress and Opportunities in Polyploid Research
journal, December 2017


APE: Analyses of Phylogenetics and Evolution in R language
journal, January 2004


Evolutionary consequences of autopolyploidy: Research review
journal, January 2010


The Sequence Alignment/Map format and SAMtools
journal, June 2009


Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives
journal, October 2019

  • Baniaga, Anthony E.; Marx, Hannah E.; Arrigo, Nils
  • Ecology Letters, Vol. 23, Issue 1
  • DOI: 10.1111/ele.13402

Selection of preadapted populations allowed Senecio inaequidens to invade Central Europe: Genetic differentiation in Senecio inaequidens
journal, March 2008


Genomic expression dominance in the natural allopolyploid Coffea arabica is massively affected by growth temperature
journal, July 2011


The role of genetic and genomic attributes in the success of polyploids
journal, June 2000

  • Soltis, P. S.; Soltis, D. E.
  • Proceedings of the National Academy of Sciences, Vol. 97, Issue 13
  • DOI: 10.1073/pnas.97.13.7051

Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes
journal, December 2015

  • Forester, Brenna R.; Jones, Matthew R.; Joost, Stéphane
  • Molecular Ecology, Vol. 25, Issue 1
  • DOI: 10.1111/mec.13476