Admixture With Cultivated Sunflower Likely Facilitated Establishment and Spread of Wild Sunflower (Helianthus annuus) in Argentina.
admixture
crop‐wild
haploblocks
invasive
population genomics
sunflower
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
18 Oct 2024
18 Oct 2024
Historique:
revised:
20
08
2024
received:
10
04
2024
accepted:
29
08
2024
medline:
18
10
2024
pubmed:
18
10
2024
entrez:
18
10
2024
Statut:
aheadofprint
Résumé
A better understanding of the genetic and ecological factors underlying successful invasions is critical to mitigate the negative impacts of invasive species. Here, we study the invasion history of Helianthus annuus populations from Argentina, with particular emphasis on the role of post-introduction admixture with cultivated sunflower (also H. annuus) and climate adaptation driven by large haploblocks. We conducted genotyping-by-sequencing of samples of wild populations as well as Argentinian cultivars and compared them with wild (including related annual Helianthus species) and cultivated samples from the native range. We also characterised samples for 11 known haploblocks associated with environmental variation in native populations to test whether haploblocks contributed to invasion success. Population genomics analyses supported two independent geographic sources for Argentinian populations, the central United States and Texas, but no significant contribution of related annual Helianthus species. We found pervasive admixture with cultivated sunflower, likely as result of post-introduction hybridization. Genomic scans between invasive populations and their native sources identified multiple genomic regions of divergence, possibly indicative of selection, in the invaded range. These regions significantly overlapped between the two native-invasive comparisons and showed disproportionally high crop ancestry, suggesting that crop alleles contributed to invasion success. We did not find evidence of climate adaptation mediated by haploblocks, yet outliers of genome scans were enriched in haploblock regions and, for at least two haploblocks, the cultivar haplotype was favoured in Argentina. Our results show that admixture with cultivated sunflower played a major role in the establishment and spread of H. annuus populations in Argentina.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e17560Informations de copyright
© 2024 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.
Références
Alexander, D. H., and K. Lange. 2011. “Enhancements to the ADMIXTURE Algorithm for Individual Ancestry Estimation.” BMC Bioinformatics 12: 246.
Baker, H. G. 1965. “Characteristics and Modes of Origin of Weeds.” In Genetics of Colonizing Species, 147–172. New York: Academic Press.
Barker, B. S., K. Andonian, S. M. Swope, D. G. Luster, and K. M. Dlugosch. 2017. “Population Genomic Analyses Reveal a History of Range Expansion and Trait Evolution Across the Native and Invaded Range of Yellow Starthistle (Centaurea solstitialis).” Molecular Ecology 26: 1131–1147.
Battey, C., P. L. Ralph, and A. D. Kern. 2020. “Predicting Geographic Location From Genetic Variation With Deep Neural Networks.” eLife 9: 1–22.
Battlay, P., J. Wilson, V. C. Bieker, et al. 2023. “Large Haploblocks Underlie Rapid Adaptation in the Invasive Weed Ambrosia artemisiifolia.” Nature Communications 14: 1717.
Badouin, H., J. Gouzy, C. Grassa, et al. 2017. “The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution.” Nature 546: 148–152.
Bertero de Romano, A., and A. N. Vázquez. 2003. “Origin of the Argentine Sunflower Varieties.” Helia 26: 127–136.
Bock, D. G., C. Caseys, R. D. Cousens, et al. 2015. “What We Still Don't Know About Invasion Genetics.” Molecular Ecology 24: 2277–2297.
Bock, D. G., M. B. Kantar, C. Caseys, R. Matthey‐Doret, and L. H. Rieseberg. 2018. “Evolution of Invasiveness by Genetic Accommodation.” Nature Ecology & Evolution 2: 991–999.
Campbell, L. G., A. A. Snow, and C. E. Ridley. 2006. “Weed Evolution After Crop Gene Introgression: Greater Survival and Fecundity of Hybrids in a New Environment.” Ecology Letters 9: 1198–1209.
Campbell, L. G., A. A. Snow, P. M. Sweeney, and J. M. Ketner. 2009. “Rapid Evolution in Crop‐Weed Hybrids Under Artificial Selection for Divergent Life Histories.” Evolutionary Applications 2: 172–186.
Cantamutto, M., M. Poverene, and N. Peinemann. 2008. “Multi‐Scale Analysis of Two Annual Helianthus Species Naturalization in Argentina.” Agriculture, Ecosystems and Environment 123: 69–74.
Cantamutto, M., A. Presotto, I. Fernandez‐Moroni, D. Alvarez, M. Poverene, and G. Seiler. 2010a. “High Infraspecific Diversity of Wild Sunflowers (Helianthus annuus L.) Naturally Developed in Central Argentina.” Flora – Morphology, Distribution, Functional Ecology of Plants 205: 306–312.
Cantamutto, M., L. Torres, A. Presotto, A. Gutierrez, S. Ureta, and M. Poverene. 2010b. “Migration Pattern Suggested by Terrestrial Proximity as Possible Origin of Wild Annual Helianthus Populations in Central Argentina.” Biological Invasions 12: 541–551.
Colautti, R. I., J. M. Alexander, K. M. Dlugosch, S. R. Keller, and S. E. Sultan. 2017. “Invasions and Extinctions Through the Looking Glass of Evolutionary Ecology.” Philosophical Transactions of the Royal Society, B: Biological Sciences 372: 1–12.
Colautti, R. I., and S. C. H. Barrett. 2013. “Rapid Adaptation to Climate Facilitates Range Expansion of an Invasive Plant.” Science 342: 364–366.
Cruzan, M. B. 2019. “How to Make a Weed: The Saga of the Slender False Brome Invasion in the North American West and Lessons for the Future.” Bioscience 69: 496–507.
Dlugosch, K. M., S. R. Anderson, J. Braasch, F. A. Cang, and H. D. Gillette. 2015. “The Devil Is in the Details: Genetic Variation in Introduced Populations and Its Contributions to Invasion.” Molecular Ecology 24: 2095–2111.
Dlugosch, K. M., and I. M. Parker. 2008. “Founding Events in Species Invasions: Genetic Variation, Adaptive Evolution, and the Role of Multiple Introductions.” Molecular Ecology 17: 431–449.
Ellstrand, N. C., S. M. Heredia, J. A. Leak‐Garcia, et al. 2010. “Crops Gone Wild: Evolution of Weeds and Invasives From Domesticated Ancestors.” Evolutionary Applications 3: 494–504.
Ellstrand, N. C., and K. A. Schierenbeck. 2000. “Hybridization as a Stimulus for the Evolution of Invasiveness in Plants?” Proceedings of the National Academy of Sciences 97: 7043–7050.
Ellstrand, N. C., and K. A. Schierenbeck. 2006. “Hybridization as a Stimulus for the Evolution of Invasiveness in Plants?” Euphytica 148: 35–46.
Elshire, R. J., J. C. Glaubitz, Q. Sun, et al. 2011. “A Robust, Simple Genotyping‐By‐Sequencing (GBS) Approach for High Diversity Species.” PLoS One 6: 1–10.
Estoup, A., and T. Guillemaud. 2010. “Reconstructing Routes of Invasion Using Genetic Data: Why, How and So What?” Molecular Ecology 19: 4113–4130.
Estoup, A., V. Ravigné, R. Hufbauer, R. Vitalis, M. Gautier, and B. Facon. 2016. “Is There A Genetic Paradox of Biological Invasion?” Annual Review of Ecology, Evolution, and Systematics 47: 51–72.
Excoffier, L., G. Laval, and S. Schneider. 2005. “Arlequin (Version 3.0): An Integrated Software Package for Population Genetics Data Analysis.” Evolutionary Bioinformatics 1: 117693430500100.
Faria, R., K. Johannesson, R. K. Butlin, and A. M. Westram. 2019. “Evolving Inversions.” Trends in Ecology & Evolution 34: 239–248.
Felker‐Quinn, E., J. A. Schweitzer, and J. K. Bailey. 2013. “Meta‐Analysis Reveals Evolution in Invasive Plant Species but Little Support for Evolution of Increased Competitive Ability (EICA).” Ecology and Evolution 3: 739–751.
Fick, S. E., and R. J. Hijmans. 2017. “WorldClim 2: New 1 km Spatial Resolution Climate Surfaces for Global Land Areas.” International Journal of Climatology 37, no. 12: 4302–4315.
Fitak, R. R. 2021. “OptM: Estimating the Optimal Number of Migration Edges on Population Trees Using Treemix.” Biology Methods & Protocols 6: bpab017.
Foll, M., and O. Gaggiotti. 2008. “A Genome‐Scan Method to Identify Selected Loci Appropriate for Both Dominant and Codominant Markers: A Bayesian Perspective.” Genetics 180: 977–993.
Hager, E. R., O. S. Harringmeyer, T. B. Wooldridge, et al. 2022. “A Chromosomal Inversion Contributes to Divergence in Multiple Traits Between Deer Mouse Ecotypes.” Science 377: 399–405.
Hedge, S. G., J. D. Nason, J. M. Clegg, and N. C. Ellstrand. 2006. “The Evolution of California's Wild Radish Has Resulted in the Extinction of Its Progenitors.” Evolution 60: 1187–1197.
Hernández, F., L. Palmieri, and J. Brunet. 2023. “Introgression and Persistence of Cultivar Alleles in Wild Carrot (Daucus carota L.) Populations in the United States.” American Journal of Botany 110: e16242.
Hernández, F., M. Poverene, A. Garayalde, and A. Presotto. 2019. “Re‐Establishment of Latitudinal Clines and Local Adaptation Within the Invaded Area Suggest Rapid Evolution of Seed Traits in Argentinean Sunflower (Helianthus annuus L.).” Biological Invasions 21: 2599–2612.
Hernández, F., M. Poverene, and A. Presotto. 2018. “Heat Stress Effects on Reproductive Traits in Cultivated and Wild Sunflower (Helianthus annuus L.): Evidence for Local Adaptation Within the Wild Germplasm.” Euphytica 214: 146.
Hernández, F., A. Presotto, M. Poverene, and J. R. Mandel. 2019. “Genetic Diversity and Population Structure of Wild Sunflower (Helianthus annuus L.) in Argentina: Reconstructing Its Invasion History.” Journal of Heredity 110: 746–759.
Hernández, F., R. B. Vercellino, C. Pandolfo, J. R. Mandel, and A. Presotto. 2022. “Rapid Evolution of Seed Dormancy During Sunflower De‐Domestication.” Journal of Heredity 113: 288–297.
Hovick, S. M., and K. D. Whitney. 2014. “Hybridisation Is Associated With Increased Fecundity and Size in Invasive Taxa: Meta‐Analytic Support for the Hybridisation‐Invasion Hypothesis.” Ecology Letters 17: 1464–1477.
Huang, K., M. Jahani, J. Gouzy, et al. 2023. “The Genomics of Linkage Drag in Inbred Lines of Sunflower.” Proceedings of the National Academy of Sciences of the United States of America 120, no. 14: e2205783119.
Hübner, S., N. Bercovich, M. Todesco, et al. 2019. “Sunflower Pan‐Genome Analysis Shows That Hybridization Altered Gene Content and Disease Resistance.” Nature Plants 5: 54–62.
Hübner, S., D. Sisou, T. Mandel, M. Todesco, M. Matzrafi, and H. Eizenberg. 2022. “Wild Sunflower Goes Viral: Citizen Science and Comparative Genomics Allow Tracking the Origin and Establishment of Invasive Sunflower in the Levant.” Molecular Ecology 31: 2061–2072.
Hufbauer, R. A., B. Facon, V. Ravigné, et al. 2012. “Anthropogenically Induced Adaptation to Invade (AIAI): Contemporary Adaptation to Human‐Altered Habitats Within the Native Range Can Promote Invasions.” Evolutionary Applications 5: 89–101.
Jay, P., A. Whibley, L. Frézal, et al. 2018. “Supergene Evolution Triggered by the Introgression of a Chromosomal Inversion.” Current Biology 28: 1839–1845.e3.
Jombart, T. 2008. “adegenet: A R Package for the Multivariate Analysis of Genetic Markers.” Bioinformatics 24: 1403–1405.
Jones, F. C., M. G. Grabherr, Y. F. Chan, et al. 2012. “The Genomic Basis of Adaptive Evolution in Threespine Sticklebacks.” Nature 484: 55–61.
Keller, S. R., P. D. Fields, A. E. Berardi, and D. R. Taylor. 2014. “Recent Admixture Generates Heterozygosity‐Fitness Correlations During the Range Expansion of an Invading Species.” Journal of Evolutionary Biology 27: 616–627.
Keller, S. R., and D. R. Taylor. 2008. “History, Chance and Adaptation During Biological Invasion: Separating Stochastic Phenotypic Evolution From Response to Selection.” Ecology Letters 11: 852–866.
Kim, A., J. Kreiner, F. Hernandez, D. Bock, K. Hodgins, and L. Rieseberg. 2023. “Temporal Collections to Study Invasion Biology.” Molecular Ecology 32: 6729–6742.
Kirkpatrick, M., and N. Barton. 2006. “Chromosome Inversions, Local Adaptation and Speciation.” Genetics 173: 419–434.
Kuester, A., J. K. Conner, T. Culley, and R. S. Baucom. 2014. “How Weeds Emerge: A Taxonomic and Trait‐Based Examination Using United States Data.” New Phytologist 202: 1055–1068.
Le Corre, V., M. Siol, Y. Vigouroux, M. I. Tenaillon, and C. Délye. 2020. “Adaptive Introgression From Maize Has Facilitated the Establishment of Teosinte as a Noxious Weed in Europe.” Proceedings of the National Academy of Sciences 117: 25618–25627.
Leigh, D. M., H. E. L. Lischer, F. Guillaume, C. Grossen, and T. Günther. 2021. “Disentangling Adaptation From Drift in Bottlenecked and Reintroduced Populations of Alpine Ibex.” Molecular Ecology Resources 21: 2350–2363.
Li, H., and R. Durbin. 2009. “Fast and Accurate Short Read Alignment With Burrows‐Wheeler Transform.” Bioinformatics 25: 1754–1760.
Li, H., B. Handsaker, A. Wysoker, et al. 2009. “The Sequence Alignment/Map Format and SAMtools.” Bioinformatics 25: 2078–2079.
Liao, H., C. M. D'Antonio, B. Chen, Q. Huang, and S. Peng. 2016. “How Much Do Phenotypic Plasticity and Local Genetic Variation Contribute to Phenotypic Divergences Along Environmental Gradients in Widespread Invasive Plants? A Meta‐Analysis.” Oikos 125: 905–917.
Liaw, A., and M. Wiener. 2002. “Classification and Regression by random Forest.” R News 2: 18–22.
Liu, C., C. Wolter, W. Xian, and J. M. Jeschke. 2004. “Most Invasive Species Largely Conserve Their Climatic Niche.” PNAS 117: 23643–23651.
Lowry, D. B., S. Hoban, J. L. Kelley, et al. 2017. “Breaking RAD: An Evaluation of the Utility of Restriction Site‐Associated DNA Sequencing for Genome Scans of Adaptation.” Molecular Ecolology Resources 17: 142–152.
Lowry, D. B., and J. H. Willis. 2010. “A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life‐History Transition, Local Adaptation, and Reproductive Isolation.” PLoS Biology 8: e1000500.
Malinsky, M., M. Matschiner, and H. Svardal. 2021. “Dsuite – Fast D‐Statistics and Related Admixture Evidence From VCF Files.” Molecular Ecology Resources 21: 584–595.
Martin, M. 2011. “Cutadapt Removes Adapter Sequences From High‐Throughput Sequencing Reads.” EMBnet.Journal 17: 10.
Mercer, K. L., D. A. Andow, D. L. Wyse, and R. G. Shaw. 2007. “Stress and Domestication Traits Increase the Relative Fitness of Crop‐Wild Hybrids in Sunflower.” Ecology Letters 10: 383–393.
Mollot, G., J. H. Pantel, and T. N. Romanuk. 2017. “The Effects of Invasive Species on the Decline in Species Richness: A Global Meta‐Analysis.” In Advances in Ecological Research, 61–83. Cambridge, Massachusetts: Academic Press Inc.
Mondon, A., G. L. Owens, M. Poverene, M. Cantamutto, and L. H. Rieseberg. 2018. “Gene Flow in Argentinian Sunflowers as Revealed by Genotyping‐By‐Sequencing Data.” Evolutionary Applications 11: 193–204.
Muller, M. H., M. Latreille, and C. Tollon. 2011. “The Origin and Evolution of a Recent Agricultural Weed: Population Genetic Diversity of Weedy Populations of Sunflower (Helianthus annuus L.) in Spain and France.” Evolutionary Applications 4: 499–514.
Oduor, A. M. O., R. Leimu, and M. van Kleunen. 2016. “Invasive Plant Species Are Locally Adapted Just as Frequently and at Least as Strongly as Native Plant Species.” Journal of Ecology 104: 957–968.
O'Neill, E. M., E. J. Hearn, J. M. Cogbill, and Y. Kajita. 2017. “Rapid Evolution of a Divergent Ecogeographic Cline in Introduced Lady Beetles.” Evolutionary Ecology 31: 695–705.
Ortiz‐Barrientos, D., J. Engelstädter, and L. H. Rieseberg. 2016. “Recombination Rate Evolution and the Origin of Species.” Trends in Ecology & Evolution 31: 226–236.
Owens, G. L., M. Todesco, N. Bercovich, et al. 2021. “Standing Variation Rather Than Recent Adaptive Introgression Probably Underlies Differentiation of the Texanus Subspecies of Helianthus annuus.” Molecular Ecology 30: 6229–6245.
Pandolfo, C. E., A. Presotto, F. T. Carbonell, S. Ureta, M. Poverene, and M. Cantamutto. 2016. “Transgenic Glyphosate‐Resistant Oilseed Rape (Brassica napus) as an Invasive Weed in Argentina: Detection, Characterization, and Control Alternatives.” Environmental Science and Pollution Research 23: 24081–24091.
Poplin, R., V. Ruano‐Rubio, M. A. DePristo, et al. 2017. “Scaling Accurate Genetic Variant Discovery to Tens of Thousands of Samples.” bioRxiv, e201178.
Poverene, M., M. Cantamutto, and G. J. Seiler. 2008. “Ecological Characterization of Wild Helianthus annuus and Helianthus petiolaris Germplasm in Argentina.” Plant Genetic Resources: Characterisation and Utilisation 7: 42–49.
Prentis, P. J., J. R. U. Wilson, E. E. Dormontt, D. M. Richardson, and A. J. Lowe. 2008. “Adaptive Evolution in Invasive Species.” Trends in Plant Science 13: 288–294.
Presotto, A., F. Hernández, R. Boris Vercellino, et al. 2023. “Introgression From Local Cultivars Is a Driver of Agricultural Adaptation in Argentinian Weedy Rice.” Molecular Ecology 33: e17368.
Presotto, A., F. Hernández, and K. L. Mercer. 2019. “Phenotypic Selection Under Two Contrasting Environments in Wild Sunflower and Its Crop–Wild Hybrid.” Evolutionary Applications 12: 1–15.
Presotto, A., M. S. Ureta, M. Cantamutto, and M. Poverene. 2012. “Effects of Gene Flow From IMI Resistant Sunflower Crop to Wild Helianthus annuus Populations.” Agriculture, Ecosystems and Environment 146: 153–161.
Richards, C. L., O. Bossdorf, N. Z. Muth, J. Gurevitch, and M. Pigliucci. 2006. “Jack of all Trades, Master of Some? On the Role of Phenotypic Plasticity in Plant Invasions.” Ecology Letters 9: 981–993.
Rieseberg, L. H., O. Raymond, D. M. Rosenthal, et al. 2003. “Major Ecological Transtitions in Wild Sunflower Facilitated by Hybridization.” Science 301: 1211–1216.
Schrieber, K., and S. Lachmuth. 2017. “The Genetic Paradox of Invasions Revisited: The Potential Role of Inbreeding × Environment Interactions in Invasion Success.” Biological Reviews 92: 939–952.
Seiler, G. J., T. O. M. J. Gulya, G. Kong, S. U. E. Thompson, and J. Mitchell. 2007. “Collection of Wild Naturalized Sunflowers From the Land Down Under.” http://www.sunflowernsa.com/uploads/research/317/Seiler_etal_DownUnder_08.pdf.
Sherpa, S., and L. Després. 2021. “The Evolutionary Dynamics of Biological Invasions: A Multi‐Approach Perspective.” Evolutionary Applications 14: 1463–1484.
Szűcs, M., B. A. Melbourne, T. Tuff, C. Weiss‐Lehman, and R. A. Hufbauer. 2017. “Genetic and Demographic Founder Effects Have Long‐Term Fitness Consequences for Colonising Populations.” Ecology Letters 20: 436–444.
Todesco, M., G. L. Owens, N. Bercovich, et al. 2020. “Massive Haplotypes Underlie Ecotypic Differentiation in Sunflowers.” Nature 584: 602–607.
Turner, K. G., R. A. Hufbauer, and L. H. Rieseberg. 2013. “Rapid Evolution of an Invasive Weed.” New Phytologist 202: 309–321.
Ureta, M. S., M. Cantamutto, A. Carrera, C. Delucchi, and M. Poverene. 2008. “Natural Hybrids Between Cultivated and Wild Sunflowers (Helianthus Spp.) in Argentina.” Genetic Resources and Crop Evolution 55: 1267–1277.
van Boheemen, L. A., E. Lombaert, K. A. Nurkowski, B. Gauffre, L. H. Rieseberg, and K. A. Hodgins. 2017. “Multiple Introductions, Admixture and Bridgehead Invasion Characterize the Introduction History of Ambrosia artemisiifolia in Europe and Australia.” Molecular Ecology 26: 5421–5434.
van Kleunen, M., M. Röckle, and M. Stift. 2015. “Admixture Between Native and Invasive Populations May Increase Invasiveness of Mimulus guttatus.” Proceedings of the Royal Society B: Biological Sciences 282: 20151487.
Vercellino, R. B., F. Hernández, C. Pandolfo, S. Ureta, and A. Presotto. 2023. “Agricultural Weeds: The Contribution of Domesticated Species to the Origin and Evolution of Feral Weeds.” Pest Management Science 79: 922–934.
Vercellino, R. B., F. Hernández, and A. Presotto. 2023. “The Role of Intraspecific Crop–Weed Hybridization in the Evolution of Weediness and Invasiveness: Cultivated and Weedy Radish (Raphanus sativus) as a Case Study.” American Journal of Botany 110: e16217.
Vilatersana, R., M. Sanz, A. Galian, and E. Castells. 2016. “The Invasion of Senecio pterophorus Across Continents: Multiple, Independent Introductions, Admixture and Hybridization.” Biological Invasions 18: 2045–2065.
Wellenreuther, M., and L. Bernatchez. 2018. “Eco‐Evolutionary Genomics of Chromosomal Inversions.” Trends in Ecology & Evolution 33: 427–440.
Zheng, X., D. Levine, J. Shen, S. M. Gogarten, C. Laurie, and B. S. Weir. 2012. “A High‐Performance Computing Toolset for Relatedness and Principal Component Analysis of SNP Data.” Bioinformatics 28: 3326–3328.