View Item 

Show simple item record

Hybrid enrichment of adaptive variation revealed by genotype–environment associations in montane sedges

dc.contributor.authorHodel, Richard G. J.
dc.contributor.authorMassatti, Rob
dc.contributor.authorKnowles, L. Lacey
dc.date.accessioned2022-07-05T21:00:49Z
dc.date.available2023-08-05 17:00:46en
dc.date.available2022-07-05T21:00:49Z
dc.date.issued2022-07
dc.identifier.citationHodel, Richard G. J.; Massatti, Rob; Knowles, L. Lacey (2022). "Hybrid enrichment of adaptive variation revealed by genotype–environment associations in montane sedges." Molecular Ecology (13): 3722-3737.
dc.identifier.issn0962-1083
dc.identifier.issn1365-294X
dc.identifier.urihttps://hdl.handle.net/2027.42/172960
dc.description.abstractThe role of hybridization in diversification is complex and may result in many possible outcomes. Not only can hybridization produce new lineages, but those lineages may contain unique combinations of adaptive genetic variation derived from parental taxa that allow hybrid-origin lineages to occupy unique environmental space relative to one (or both) parent(s). We document such a case of hybridization between two sedge species, Carex nova and Carex nelsonii (Cyperaceae), that occupy partially overlapping environmental space in the southern Rocky Mountains, USA. In the region hypothesized to be the origin of the hybrid lineage, one parental taxon (C. nelsonii) is at the edge of its environmental tolerance. Hybrid-origin individuals display mixed ancestry between the parental taxa—of nearly 7000 unlinked loci sampled, almost 30% showed evidence of excess ancestry from one parental lineage—approximately half displayed a genomic background skewed towards one parent, and half skewed towards the other. To test whether excess ancestry loci may have conferred an adaptive advantage to the hybrid-origin lineage, we conducted genotype–environment association analyses on different combinations of loci—with and without excess ancestry—and with multiple contrasts between the hybrids and parental taxa. Loci with skewed ancestry showed significant environmental associations distinguishing the hybrid lineage from one parent (C. nelsonii), whereas loci with relatively equal representation of parental ancestries showed no such environmental associations. Moreover, the overwhelming majority of candidate adaptive loci with respect to environmental gradients also had excess ancestry from a parental lineage, implying these loci have facilitated the persistence of the hybrid lineage in an environment unsuitable to at least one parent.
dc.publisherElsevi er
dc.publisherWiley Periodicals, Inc.
dc.subject.otherRAD-Seq
dc.subject.otherredundancy analysis
dc.subject.otherhybridization
dc.subject.othercandidate adaptive loci
dc.subject.othergenomic cline
dc.subject.othergenotype-environment association
dc.titleHybrid enrichment of adaptive variation revealed by genotype–environment associations in montane sedges
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/172960/1/mec16502_am.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/172960/2/mec16502.pdf
dc.identifier.doi10.1111/mec.16502
dc.identifier.sourceMolecular Ecology
dc.identifier.citedreferencePeterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. ( 2012 ). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS One, 7, e37135.
dc.identifier.citedreferenceMenon, M., Bagley, J. C., Page, G. F. M., Whipple, A. V., Schoettle, A. W., Still, C. J., Wehenkel, C., Waring, K. M., Flores-Renteria, L., Cushman, S. A., & Eckert, A. J. ( 2021 ). Adaptive evolution in a conifer hybrid zone is driven by a mosaic of recently introgressed and background genetic variants. Communications Biology, 4, 1 – 14.
dc.identifier.citedreferenceOksanen, A. J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., & McGlinn, D. ( 2017 ). Vegan: Community ecology package. R package version 2.4-4.
dc.identifier.citedreferenceParchman, T. L., Gompert, Z., Braun, M. J., Brumfield, R. T., McDonald, D. B., Uy, J. A. C., Zhang, G., Jarvis, E. D., Schlinger, B. A., & Buerkle, C. A. ( 2013 ). The genomic consequences of adaptive divergence and reproductive isolation between species of manakins. Molecular Ecology, 22, 3304 – 3317.
dc.identifier.citedreferencePickrell, J. K., & Pritchard, J. K. ( 2012 ). Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genetics, 8, 1002967. https://doi.org/10.1371/journal.pgen.1002967
dc.identifier.citedreferencePritchard, J. K., Stephens, M., & Donnelly, P. ( 2000 ). Inference of population structure using multilocus genotype data. Genetics, 155, 945 – 959.
dc.identifier.citedreferenceRellstab, C., Gugerli, F., Eckert, A. J., Hancock, A. M., & Holderegger, R. ( 2015 ). A practical guide to environmental association analysis in landscape genomics. Molecular Ecology, 24, 4348 – 4370.
dc.identifier.citedreferenceRieseberg, L. H. ( 1997 ). Hybrid origins of plant species. Annual Review of Ecology and Systematics, 28, 359 – 389.
dc.identifier.citedreferenceRieseberg, L. H., Raymond, O., Rosenthal, D. M., Lai, Z., Livingstone, K., Nakazato, T., Durphy, J. L., Schwarzbach, A. E., Donovan, L. A., & Lexer, C. ( 2003 ). Major ecological transitions in wild sunflowers facilitated by hybridization. Science, 301, 1211 – 1216.
dc.identifier.citedreferenceRieseberg, L. H., & Willis, J. H. ( 2007 ). Plant speciation. Science, 317, 910 – 914.
dc.identifier.citedreferenceSeehausen, O. ( 2004 ). Hybridization and adaptive radiation. Trends in Ecology and Evolution, 19, 198 – 207.
dc.identifier.citedreferenceSuarez-Gonzalez, A., Lexer, C., & Cronk, Q. C. B. ( 2018 ). Adaptive introgression: A plant perspective. Biology Letters, 14, 20170688.
dc.identifier.citedreferenceTaylor, S. A., & Larson, E. L. ( 2019 ). Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nature Ecology and Evolution, 3, 170 – 177.
dc.identifier.citedreferenceTaylor, S. A., Larson, E. L., & Harrison, R. G. ( 2015 ). Hybrid zones: Windows on climate change. Trends in Ecology and Evolution, 30, 398 – 406.
dc.identifier.citedreferenceTwyford, A. D., & Ennos, R. A. ( 2012 ). Next-generation hybridization and introgression. Heredity, 108, 179 – 189.
dc.identifier.citedreferenceVanhove, M., Pina-Martins, F., Coelho, A. C., Branquinho, C., Costa, A., Batista, D., Príncipe, A., Sousa, P., Henriques, A., Marques, I., Belkadi, B., Knowles, L. L., & Paulo, O. S. ( 2021 ). Using gradient forest to predict climate response and adaptation in Cork oak. Journal of Evolutionary Biology, 34, 910 – 923.
dc.identifier.citedreferenceWalsh, J., Kovach, A. I., Olsen, B. J., Shriver, W. G., & Lovette, I. J. ( 2018 ). Bidirectional adaptive introgression between two ecologically divergent sparrow species. Evolution, 72, 2076 – 2089.
dc.identifier.citedreferenceWang, X., Ye, X., Zhao, L., Li, D., Guo, Z., & Zhuang, H. ( 2017 ). Genome-wide RAD sequencing data provide unprecedented resolution of the phylogeny of temperate bamboos (Poaceae: Bambusoideae). Scientific Reports, 7, 1 – 11.
dc.identifier.citedreferenceWang, Z., Jiang, Y., Bi, H., Lu, Z., Ma, Y., Yang, X., Chen, N., Tian, B., Liu, B., Mao, X., Ma, T., DiFazio, S. P., Hu, Q., Abbott, R. J., & Liu, J. ( 2021 ). Hybrid speciation via inheritance of alternate alleles of parental isolating genes. Molecular Plant, 14, 208 – 222.
dc.identifier.citedreferenceWaterway, M. J. ( 1994 ). Evidence for the hybrid origin of Carex knieskernii with comments on hybridization in the genus Carex (Cyperaceae). Canadian Journal of Botany, 72, 860 – 871.
dc.identifier.citedreferenceWeber, W. A. ( 2003 ). The middle Asian element in the southern Rocky Mountain flora of the western United States: A critical biogeographical review. Journal of Biogeography, 30, 649 – 685.
dc.identifier.citedreferenceWhitney, K. D., Randell, R. A., & Rieseberg, L. H. ( 2010 ). Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytologist, 187, 230 – 239.
dc.identifier.citedreferenceWięcław, H., Kalinka, A., & Koopman, J. ( 2020 ). Chromosome numbers of Carex (Cyperaceae) and their taxonomic implications. PLoS One, 15, e0228353.
dc.identifier.citedreferenceWięcław, H., & Wilhelm, M. ( 2014 ). Natural hybridization within the Carex flava complex (Cyperaceae) in Poland: Morphometric studies. Annales Botanici Fennici, 51, 129 – 147.
dc.identifier.citedreferenceZheng, X., Levine, D., Shen, J., Gogarten, S. M., Laurie, C., & Weir, B. S. ( 2012 ). A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics, 28, 3326 – 3328. https://doi.org/10.1093/bioinformatics/bts606
dc.identifier.citedreferenceRieseberg, L. H. ( 2006 ). Hybrid speciation in wild sunflowers. Annals of the Missouri Botanical Garden, 93, 34 – 48.
dc.identifier.citedreferenceAbbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Boughman, J., Brelsford, A., Buerkle, C. A., Buggs, R., Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H., Hermansen, J. S., Hewitt, G., Hudson, A. G., Jiggins, C., … Zinner, D. ( 2013 ). Hybridization and speciation. Journal of Evolutionary Biology, 26, 229 – 246.
dc.identifier.citedreferenceAbbott, R. J., Barton, N. H., & Good, J. M. ( 2016 ). Genomics of hybridization and its evolutionary consequences. Molecular Ecology, 25, 2325 – 2332.
dc.identifier.citedreferenceAlbertson, R. C., Markert, J. A., Danley, P. D., & Kocher, T. D. ( 1999 ). Phytogeny of a rapidly evolving clade: The cichlid fishes of Lake Malawi, East Africa. Proceedings of the National Academy of Sciences of the United States of America, 96, 5107 – 5110.
dc.identifier.citedreferenceArnold, M. L., & Kunte, K. ( 2017 ). Adaptive genetic exchange: A tangled history of admixture and evolutionary innovation. Trends in Ecology and Evolution, 32, 601 – 611.
dc.identifier.citedreferenceArnold, M. L., & Martin, N. H. ( 2009 ). Adaptation by introgression. Journal of Biology, 8, 82.
dc.identifier.citedreferenceBlischak, P. D., Chifman, J., Wolfe, A. D., & Kubatko, L. S. ( 2018 ). HyDe: A python package for genome-scale hybridization detection (D posada, Ed). Systematic Biology, 67, 821 – 829.
dc.identifier.citedreferenceBriles, C. E., Whitlock, C., & Meltzer, D. J. ( 2012 ). Last glacial–interglacial environments in the southern Rocky Mountains, USA and implications for younger Dryas-age human occupation. Quaternary Research, 77, 96 – 103.
dc.identifier.citedreferenceCapblancq, T., Luu, K., Blum, M. G. B., & Bazin, E. ( 2018 ). Evaluation of redundancy analysis to identify signatures of local adaptation. Molecular Ecology Resources, 18, 1223 – 1233.
dc.identifier.citedreferenceCatchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. ( 2013 ). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22, 3124 – 3140.
dc.identifier.citedreferenceCayouette, J., & Catling, P. M. ( 1992 ). Hybridization in the genus Carex with special reference to North America. The Botanical Review, 58, 351 – 438.
dc.identifier.citedreferenceChhatre, V. E., Evans, L. M., DiFazio, S. P., & Keller, S. R. ( 2018 ). Adaptive introgression and maintenance of a trispecies hybrid complex in range-edge populations of Populus. Molecular Ecology, 27, 4820 – 4838.
dc.identifier.citedreferenceChifman, J., & Kubatko, L. ( 2014 ). Quartet inference from SNP data under the coalescent model. Bioinformatics, 30, 3317 – 3324.
dc.identifier.citedreferenceDanecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., MA, D. P., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., & McVean, G. ( 2011 ). The variant call format and VCFtools. Bioinformatics, 27, 2156 – 2158.
dc.identifier.citedreferenceDion-Côté, A. M., & Barbash, D. A. ( 2017 ). Beyond speciation genes: An overview of genome stability in evolution and speciation. Current Opinion in Genetics and Development, 47, 17 – 23.
dc.identifier.citedreferenceDray, S., & Dufour, A. B. ( 2007 ). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1 – 20.
dc.identifier.citedreferenceDrury, W. H. ( 1956 ). The ecology of the natural origin of a species of Carex by hybridization. Rhodora, 58, 51 – 72.
dc.identifier.citedreferenceEaton, D. A. R. ( 2014 ). PyRAD: Assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics, 30, 1844 – 1849.
dc.identifier.citedreferenceEaton, D. A. R., & Overcast, I. ( 2020 ). Ipyrad: Interactive assembly and analysis of RADseq datasets. Bioinformatics, 36, 2592 – 2594.
dc.identifier.citedreferenceFitak, R. R. ( 2021 ). OptM: Estimating the optimal number of migration edges on population trees using Treemix. Biology Methods and Protocols, 6, 1 – 6. https://doi.org/10.1093/biomethods/bpab017
dc.identifier.citedreferenceForester, B. R., Lasky, J. R., Wagner, H. H., & Urban, D. L. ( 2018 ). Comparing methods for detecting multilocus adaptation with multivariate genotype-environment associations. Molecular Ecology, 27, 2215 – 2233.
dc.identifier.citedreferenceFowler, J. F., Nelson, B. E., & Hartman, R. L. ( 2014 ). Vascular plant flora of the alpine zone in the southern Rocky Mountains, USA. Journal of the Botanical Research Institute of Texas, 8, 611 – 636.
dc.identifier.citedreferenceGalaverni, M., Caniglia, R., Pagani, L., Fabbri, E., Boattini, A., & Randi, E. ( 2017 ). Disentangling timing of admixture, patterns of introgression, and phenotypic indicators in a hybridizing wolf population. Molecular Biology and Evolution, 34, 2324 – 2339.
dc.identifier.citedreferenceGizaw, A., Wondimu, T., Mugizi, T. F., Masao, C. A., Abdi, A. A., Popp, M., Ehrich, D., Nemomissa, S., & Brochmann, C. ( 2016 ). Vicariance, dispersal, and hybridization in a naturally fragmented system: The afro-alpine endemics Carex monostachya and C. runssoroensis (Cyperaceae). Alpine Botany, 126, 59 – 71.
dc.identifier.citedreferenceGompert, Z., & Buerkle, C. A. ( 2011 ). Bayesian estimation of genomic clines. Molecular Ecology, 20, 2111 – 2127.
dc.identifier.citedreferenceGompert, Z., & Buerkle, C. A. ( 2012 ). Bgc: Software for Bayesian estimation of genomic clines. Molecular Ecology Resources, 12, 1168 – 1176.
dc.identifier.citedreferenceGompert, Z., Lucas, L. K., Fordyce, J. A., Forister, M. L., & Nice, C. C. ( 2010 ). Secondary contact between Lycaeides idas and L. melissa in the Rocky Mountains: Extensive admixture and a patchy hybrid zone. Molecular Ecology, 19, 3171 – 3192.
dc.identifier.citedreferenceGompert, Z., Mandeville, E. G., & Buerkle, C. A. ( 2017 ). Analysis of population genomic data from hybrid zones. Annual Review of Ecology, Evolution, and Systematics, 48, 207 – 229.
dc.identifier.citedreferenceGoulet, B. E., Roda, F., & Hopkins, R. ( 2017 ). Hybridization in plants: Old ideas, new techniques. Plant Physiology, 173, 65 – 78.
dc.identifier.citedreferenceGrant, P. R., & Grant, B. R. ( 1994 ). Phenotypic and genetic effects of hybridization in Darwin’s finches. Evolution, 48, 297 – 316.
dc.identifier.citedreferenceHedrick, P. W. ( 2013 ). Adaptive introgression in animals: Examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology, 22, 4606 – 4618.
dc.identifier.citedreferenceHijmans, R. J. ( 2017 ). dismo: Species distribution modeling. R package version 1.1-4. https://CRAN.R-project.org/package=dismo
dc.identifier.citedreferenceHijmans, R. J. ( 2019 ). Raster: Geographic data analysis and modeling. R package version 3.0-2. https://CRAN.R-project.org/package=raster
dc.identifier.citedreferenceHijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. ( 2005 ). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965 – 1978.
dc.identifier.citedreferenceHipp, A. L. ( 2007 ). Nonuniform processes of chromosome evolution in sedges ( Carex: Cyperaceae). Evolution, 61, 2175 – 2194.
dc.identifier.citedreferenceHodel, R. G. J., Massatti, R., Bishop, S. G. D., & Knowles, L. L. ( 2021 ). Testing which axes of species differentiation underlie covariance of phylogeographic similarity among montane sedge species. Evolution, 75, 349 – 364.
dc.identifier.citedreferenceJombart, T., & Ahmed, I. ( 2011 ). Adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 27, 3070 – 3071.
dc.identifier.citedreferenceKadereit, J. W. ( 2015 ). The geography of hybrid speciation in plants. Taxon, 64, 673 – 687.
dc.identifier.citedreferenceKim, S.-C., & Rieseberg, L. H. ( 1999 ). Genetic architecture of species differences in annual sunflowers: Implications for adaptive trait introgression. Genetics, 153, 965 – 977.
dc.identifier.citedreferenceKnowles, L. L., & Richards, C. L. ( 2005 ). Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation. Molecular Ecology, 14, 4023 – 4032.
dc.identifier.citedreferenceKou, Y., Zhang, L., Fan, D., Cheng, S., Li, D., Hodel, R. G. J., & Zhang, Z. ( 2020 ). Evolutionary history of a relict conifer, Pseudotaxus chienii (Taxaceae), in Southeast China during the late Neogene: Old lineage, young populations. Annals of Botany, 125, 105 – 117.
dc.identifier.citedreferenceKozak, K. M., Wahlberg, N., Neild, A. F. E., Dasmahapatra, K. K., Mallet, J., & Jiggins, C. D. ( 2015 ). Multilocus species trees show the recent adaptive radiation of the mimetic Heliconius butterflies. Systematic Biology, 64, 505 – 524.
dc.identifier.citedreferenceKunte, K., Shea, C., Aardema, M. L., Scriber, J. M., Juenger, T. E., Gilbert, L. E., & Kronforst, M. R. ( 2011 ). Sex chromosome mosaicism and hybrid speciation among tiger swallowtail butterflies (NA Moran, Ed). PLoS Genetics, 7, e1002274.
dc.identifier.citedreferenceLamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., Promerová, M., Rubin, C. J., Wang, C., Zamani, N., Grant, B. R., Grant, P. R., Webster, M. T., & Andersson, L. ( 2015 ). Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature, 518, 371 – 375.
dc.identifier.citedreferenceLeducq, J.-B., Nielly-Thibault, L., Charron, G., Eberlein, C., Verta, J.-P., Samani, P., Sylvester, K., Hittinger, C. T., Bell, G., & Landry, C. R. ( 2016 ). Speciation driven by hybridization and chromosomal plasticity in a wild yeast. Nature Microbiology, 1 ( 1 ). https://doi.org/10.1038/nmicrobiol.2015.3
dc.identifier.citedreferenceLegendre, P., & Legendre, L. ( 2012 ). Numerical ecology. Elsevi er.
dc.identifier.citedreferenceLuu, K., Bazin, E., & Blum, M. G. B. ( 2017 ). Pcadapt: An R package to perform genome scans for selection based on principal component analysis. Molecular Ecology Resources, 17, 67 – 77.
dc.identifier.citedreferenceMallet, J. ( 2005 ). Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20, 229 – 237.
dc.identifier.citedreferenceMassatti, R., & Knowles, L. L. ( 2014 ). Microhabitat differences impact phylogeographic concordance of codistributed species: Genomic evidence in montane sedges ( Carex L.) from the Rocky Mountains. Evolution, 68, 2833 – 2846.
dc.identifier.citedreferenceMassatti, R., & Knowles, L. L. ( 2016 ). Contrasting support for alternative models of genomic variation based on microhabitat preference: Species-specific effects of climate change in alpine sedges. Molecular Ecology, 25, 3974 – 3986.
dc.identifier.citedreferenceMassatti, R., & Knowles, L. L. ( 2020 ). The historical context of contemporary climatic adaptation: A case study in the climatically dynamic and environmentally complex southwestern United States. Ecography, 43, 735 – 746.
dc.identifier.citedreferenceMeier, J. I., Marques, D. A., Mwaiko, S., Wagner, C. E., Excoffier, L., & Seehausen, O. ( 2017 ). Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nature Communications, 8, 14363.
dc.working.doiNOen
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
mec16502_am.pdf
Size:
11.01MB
Format:
PDF
View/Open
Name:
mec16502.pdf
Size:
7.691MB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.