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Cited by 39Plant Diversity and EvolutionChromosomal and Genetic VariationsPlant Taxonomy and Phylogenetics

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Re-evaluating Homoploid Reticulate Evolution in Helianthus Sunflowers

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Owens, Gregory L, Huang, Kaichi, Todesco, Marco, Rieseberg, Loren H·2023·Molecular Biology and Evolution
DOI 10.1093/molbev/msad013PMC PMC9907532
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Abstract

Sunflowers of the genus Helianthus are models for hybridization research and contain three of the best-studied examples of homoploid hybrid speciation. To understand a broader picture of hybridization within the annual sunflowers, we used whole-genome resequencing to conduct a phylogenomic analysis and test for gene flow between lineages. We find that all annual sunflower species tested have evidence of admixture, suggesting hybridization was common during the radiation of the genus. Support for the major species tree decreases with increasing recombination rate, consistent with hybridization and introgression contributing to discordant topologies. Admixture graphs found hybridization to be associated with the origins of the three putative hybrid species (Helianthus anomalus, Helianthus deserticola, and Helianthus paradoxus). However, the hybridization events are more ancient than suggested by previous work. Furthermore, H. anomalus and H. deserticola appear to have arisen from a single hybridization event involving an unexpected donor, rather than through multiple independent events as previously proposed. This means our results are consistent with, but not definitive proof of, two ancient independent homoploid hybrid speciation events in the genus. Using a broader data set that covers the whole Helianthus genus, including perennial species, we find that signals of introgression span the genus and beyond, suggesting highly divergent introgression and/or the sorting of ancient haplotypes. Thus, Helianthus can be viewed as a syngameon in which largely reproductively isolated species are linked together by occasional or frequent gene flow.

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  • Rates of introgression are positively correlated with recombination rates.

    “As predicted from hybrid zone theory (Barton and Hewitt 1985), rates of introgression are positively correlated with recombination rates (Brandvain et al., 2014; Owens et al., 2021; Owens et al., 2023).”

    From Genomics of plant speciation (2023) · cites this paper as Owens et al., 2023

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References 104 · Cited by 39

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  1. Anderson, 1949, Introgressive hybridization, 10.5962/bhl.title.4553 · DOI
  2. Anderson, 1954, Hybridization as an evolutionary stimulus, Evolution, 378, 88
  3. Atlagić, 2006, Cytogenetic study of hexaploid species Helianthus tuberosus and its F1 and BC1F1 hybrids with cultivated sunflower, H. annuus, Genetika, 38, 203, 10.2298/GENSR0603203A · DOI
  4. Baute, 2016, Genome-wide GBS data provide a high-resolution view of wild Helianthus diversity, genetic structure and interspecies gene flow, Am J Bot, 103, 2170, 10.3732/ajb.1600295 · DOI
  5. Beatley, 1963, The sunflowers (genus Helianthus) in Tennessee, J Tennessee Acad Sci, 38, 135
  6. Beckstrom-Sternberg, 1991, Gene lineage analysis of populations of Helianthus niveus and H. petiolaris, Plant Syst Evol, 175, 125, 10.1007/BF00937842 · DOI
  7. Buerkle, 2008, The rate of genome stabilization in homoploid hybrid species, Evolution, 62, 266, 10.1111/j.1558-5646.2007.00267.x · DOI
  8. Calfee, 2021, Selective sorting of ancestral introgression in maize and teosinte along an elevational cline, PLoS genet, 17, e1009810, 10.1371/journal.pgen.1009810 · DOI
  9. Chandler, 1986, Chromosomal differentiation among the annual Helianthus Species, Syst Bot, 11, 354, 10.2307/2419126 · DOI · Paper page
  10. Danecek, 2011, The variant call format and VCFtools, Bioinformatics, 27, 2156, 10.1093/bioinformatics/btr330 · DOI
  11. Danecek, 2021, Twelve years of SAMtools and BCFtools, Gigascience, 10, giab008, 10.1093/gigascience/giab008 · DOI
  12. Darwin, 1859, On the origin of species
  13. Edelman, 2019, Genomic architecture and introgression shape a butterfly radiation, Science, 366, 594, 10.1126/science.aaw2090 · DOI
  14. Ellis, 2006, High genetic diversity in a rare and endangered sunflower as compared to a common congener, Mol Ecol, 15, 2345, 10.1111/j.1365-294X.2006.02937.x · DOI
  15. Farwall, 1916, Contribution to the botany of Michigan. No. 14, Rep Mich Acad Sci, 17, 180
  16. Figueiró, 2017, Genome-wide signatures of complex introgression and adaptive evolution in the big cats, Sci Adv, 3, e1700299, 10.1126/sciadv.1700299 · DOI
  17. Fitak, 2021, Optm: estimating the optimal number of migration edges on population trees using treemix, Biol Methods Protoc, 6, bpab017, 10.1093/biomethods/bpab017 · DOI
  18. Fontaine, 2015, Extensive introgression in a malaria vector species complex revealed by phylogenomics, Science, 347, 1258524, 10.1126/science.1258524 · DOI
  19. Grant, 1958, The regulation of recombination in plants, Cold Spring Harb Symp Quant, 23, 337, 10.1101/SQB.1958.023.01.034 · DOI
  20. Grant, 1981, Plant speciation, 10.7312/gran92318 · DOI
  21. Green, 2010, A draft sequence of the neandertal genome, Science, 328, 710, 10.1126/science.1188021 · DOI · Paper page
  22. Gross, 2004, Reconstructing the origin(s) of Helianthus deserticola: survivorship and selection on the desert floor, Am Nat, 164, 145, 10.1086/422223 · DOI
  23. Gross, 2005, The ecological genetics of homoploid hybrid speciation, J Hered, 96, 241, 10.1093/jhered/esi026 · DOI
  24. Gross, 2003, Origin(s) of the diploid hybrid species Helianthus deserticola (Asteraceae), Am J Bot, 90, 1708, 10.3732/ajb.90.12.1708 · DOI
  25. Haenel, 2018, Meta-analysis of chromosome-scale crossover rate variation in eukaryotes and its significance to evolutionary genomics, Mol Ecol, 27, 2477, 10.1111/mec.14699 · DOI
  26. Heiser, 1947, Hybridization between the sunflower species Helianthus annuus and H. petiolaris, Evolution, 1, 249, 10.2307/2405326 · DOI
  27. Heiser, 1949, Natural hybridization with particular reference to introgression, Bot Rev, 15, 645, 10.1007/BF02861577 · DOI
  28. Heiser, 1949, Study in the evolution of the sunflower species Helianthus annuus and H. bolanderi, UC Pub Bot, 12, 157
  29. Heiser, 1951, Hybridization in the annual sunflowers: helianthus annuus x H. debilis var. cucumerifolius, Evolution, 5, 42, 10.2307/2405429 · DOI
  30. Heiser, 1958, Three new annual sunflowers from the southwestern United States, Rhodora, 60, 275
  31. Heiser, 1969, The North American sunflowers (Helianthus), 1
  32. Henn, 1998, Regeneration of fertile interspecific hybrids from protoplast fusions between Helianthus annuus L. And wild Helianthus species, Plant Cell Rep, 18, 220, 10.1007/s002990050560 · DOI
  33. Hibbins, 2022, Phylogenomic approaches to detecting and characterizing introgression, Genetics, 220, iyab173, 10.1093/genetics/iyab173 · DOI
  34. Huang, 2020, Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype, Mol Ecol, 29, 2535, 10.1111/mec.15428 · DOI
  35. Hübner, 2019, Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance, Nat Plants, 5, 54, 10.1038/s41477-018-0329-0 · DOI
  36. Jones, 2018, Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares, Science, 360, 1355, 10.1126/science.aar5273 · DOI
  37. Kane, 2009, Comparative genomic and population genetic analyses indicate highly porous genomes and high levels of gene flow between divergent Helianthus species, Evolution, 63, 2061, 10.1111/j.1558-5646.2009.00703.x · DOI
  38. Kearney, 1942, Flowering plants and ferns of Arizona, 10.5962/bhl.title.65599 · DOI
  39. Lai, 2005, Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species, Genetics, 171, 291, 10.1534/genetics.105.042242 · DOI
  40. Lee-Yaw, 2019, An evaluation of alternative explanations for widespread cytonuclear discordance in annual sunflowers (Helianthus), New Phyt, 221, 515, 10.1111/nph.15386 · DOI
  41. Lexer, 2003, The origins of ecological divergence in Helianthus paradoxus (Asteraceae): selection on transgressive characters in a novel hybrid habitat, Evolution, 57, 1989
  42. Li, 2019, Recombination-aware phylogenomics reveals the structured genomic landscape of hybridizing cat species, Mol Biol Evol, 36, 2111, 10.1093/molbev/msz139 · DOI
  43. Ludwig, 2004, Selection on leaf ecophysiological traits in a hybrid Helianthus species and early generation hybrids in a desert dune habitat, Evolution, 58, 2682
  44. Malinsky, 2021, Dsuite-fast D-statistics and related admixture evidence from VCF files, Mol Ecol Resour, 21, 584, 10.1111/1755-0998.13265 · DOI · Paper page
  45. Mallet, 2016, How reticulated are species?, BioEssays, 38, 140, 10.1002/bies.201500149 · DOI
  46. Martin, 2019, Recombination rate variation shapes barriers to introgression across butterfly genomes, PLoS Biol, 17, e2006288, 10.1371/journal.pbio.2006288 · DOI
  47. Martin, 2017, Exploring evolutionary relationships across the genome using topology weighting, Genetics, 206, 429, 10.1534/genetics.116.194720 · DOI
  48. Mason, 2018, How old are sunflowers? A molecular clock analysis of key divergences in the origin and diversification of Helianthus (Asteraceae), Int J Plant Sci, 179, 182, 10.1086/696366 · DOI
  49. Mayr, 1963, Animal species and evolution, 10.4159/harvard.9780674865327 · DOI · Paper page
  50. McKenna, 2010, The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data, Genome Res, 20, 1297, 10.1101/gr.107524.110 · DOI · Paper page
  51. Meier, 2017, Ancient hybridization fuels rapid cichlid fish adaptive radiations, Nat Commun, 8, 14363, 10.1038/ncomms14363 · DOI
  52. Melo, 2009, Assortative mating preferences among hybrids offers a route to hybrid speciation, Evolution, 63, 1660, 10.1111/j.1558-5646.2009.00633.x · DOI
  53. Minh, 2020, New methods to calculate concordance factors for phylogenomic datasets, Mol Biol Evol, 37, 2727, 10.1093/molbev/msaa106 · DOI
  54. Minh, 2020, IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era, Mol Biol Evol, 37, 1530, 10.1093/molbev/msaa015 · DOI · Paper page
  55. Mondon, 2018, Gene flow in argentinian sunflowers as revealed by genotyping by sequencing data, Evol Appl, 11, 193, 10.1111/eva.12527 · DOI
  56. Moody, 2012, Sorting through the chaff, nDNA gene trees for phylogenetic inference and hybrid identification of annual sunflowers (Helianthus sect. Helianthus), Mol Phylogenet Evol, 64, 145, 10.1016/j.ympev.2012.03.012 · DOI
  57. Murray, 1980, Rapid isolation of high molecular weight plant DNA, Nucleic Acids Res, 8, 4321, 10.1093/nar/8.19.4321 · DOI
  58. Nachman, 2012, Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice, Philos Trans R Soc Lond, B, Biol Sci, 367, 409, 10.1098/rstb.2011.0249 · DOI
  59. Ortíz-Barrientos, 2002, Genetics of Mate choice: from sexual selection to sexual isolation, 167, 10.1007/978-94-010-0265-3_2 · DOI
  60. Ostevik, 2016, Multiple reproductive barriers separate recently diverged sunflower ecotypes, Evolution, 70, 2322, 10.1111/evo.13027 · DOI · Paper page
  61. Ostevik, 2020, Ancestral reconstruction of karyotypes reveals an exceptional rate of nonrandom chromosomal evolution in sunflower, Genetics, 214, 1031, 10.1534/genetics.120.303026 · DOI · Paper page
  62. Owens, 2016, Revisiting a classic case of introgression: hybridization and gene flow in californian sunflowers, Mol Ecol, 25, 2630, 10.1111/mec.13569 · DOI
  63. Owens, 2014, Hybrid incompatibility is acquired faster in annual than in perennial species of sunflower and tarweed, Evolution, 68, 893, 10.1111/evo.12297 · DOI
  64. Oziolor, 2019, Adaptive introgression enables evolutionary rescue from extreme environmental pollution, Science, 364, 455, 10.1126/science.aav4155 · DOI
  65. Pease, 2013, More accurate phylogenies inferred from low-recombination regions in the presence of incomplete lineage sorting, Evolution, 67, 2376, 10.1111/evo.12118 · DOI
  66. Pockrandt, 2020, Genmap: ultra-fast computation of genome mappability, Bioinform, 36, 3687, 10.1093/bioinformatics/btaa222 · DOI
  67. R Core Team, 2021, R: A language and environment for statistical computing
  68. Rieseberg, 1991, Homoploid reticulate evolution in Helianthus: evidence from ribosomal genes, Am J Bot, 78, 1218, 10.1002/j.1537-2197.1991.tb11415.x · DOI
  69. Rieseberg, 1997, Hybrid origins of plant species, Ann Rev Ecol Syst, 28, 359, 10.1146/annurev.ecolsys.28.1.359 · DOI · Paper page
  70. Rieseberg, 2000, Crossing relationships among ancient and experimental sunflower hybrid lineages, Evolution, 54, 859
  71. Rieseberg, 2006, Hybrid speciation in wild sunflowers, Ann Mo Bot Gard, 93, 34, 10.3417/0026-6493(2006)93[34:HSIWS]2.0.CO;2 · DOI
  72. Rieseberg, 1998, Patterns of mating in wild sunflower hybrid zones, Evolution, 52, 713, 10.2307/2411266 · DOI
  73. Rieseberg, 1990, Helianthus annuus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius, PNAS, 87, 593, 10.1073/pnas.87.2.593 · DOI
  74. Rieseberg, 1991, Phylogenetic and systematic inferences from chloroplast DNA and isozyme variation in Helianthus sect. Helianthus, Syst Bot, 16, 50, 10.2307/2418973 · DOI
  75. Rieseberg, 1990, Molecular tests of the hypothesized hybrid origin of two diploid Helianthus species (Asteraceae), Evolution, 44, 1498, 10.2307/2409332 · DOI
  76. Rieseberg, 2003, Major ecological transitions in annual sunflowers facilitated by hybridization, Science, 301, 1211, 10.1126/science.1086949 · DOI
  77. Rieseberg, 1996, Role of gene interactions in hybrid speciation: evidence from ancient and experimental hybrids, Science, 272, 741, 10.1126/science.272.5262.741 · DOI
  78. Rieseberg, 1988, A molecular reexamination of introgression between Helianthus annuus and H. bolanderi, Evolution, 42, 227
  79. Rieseberg, 1995, Hybrid speciation accompanied by genomic reorganization in wild sunflowers, Nature, 375, 313, 10.1038/375313a0 · DOI
  80. Schemske, 2000, Understanding the origin of species, Evolution, 54, 1069
  81. Schilling, 2020, Flora of North America editorial committee, eds. 1993, 141
  82. Schumer, 2014, How common is hybrid speciation?, Evolution, 68, 1553, 10.1111/evo.12399 · DOI · Paper page
  83. Schumer, 2018, Natural selection interacts with recombination to shape the evolution of hybrid genomes, Science, 360, 656, 10.1126/science.aar3684 · DOI · Paper page
  84. Schwarzbach, 2002, Likely multiple origins of a diploid hybrid sunflower species, Mol Ecol, 11, 1703, 10.1046/j.1365-294X.2002.01557.x · DOI
  85. Sedlazeck, 2013, Nextgenmap: fast and accurate read mapping in highly polymorphic genomes, Bioinform, 29, 2790, 10.1093/bioinformatics/btt468 · DOI
  86. Stebbins, 1957, The hybrid origin of microspecies in the Elymus glaucus complex, Cytologia (Tokyo)., 36, 336
  87. Stephens, 2015, Species tree estimation of diploid Helianthus (Asteraceae) using target enrichment, Am J Bot, 102, 910, 10.3732/ajb.1500031 · DOI
  88. Strasburg, 2008, Molecular demographic history of the annual sunflowers Helianthus annuus and H. petiolaris—large effective population sizes and rates of long-term gene flow, Evolution, 62, 1936, 10.1111/j.1558-5646.2008.00415.x · DOI
  89. Suarez-Gonzalez, 2018, Adaptive introgression: a plant perspective, Biol Lett, 14, 20170688, 10.1098/rsbl.2017.0688 · DOI · Paper page
  90. Sun, 2020, Genomic basis of homoploid hybrid speciation within chestnut trees, Nat Commun, 11, 1
  91. Suvorov, 2022, Widespread introgression across a phylogeny of 155 Drosophila genomes, Curr Biol, 32, 111, 10.1016/j.cub.2021.10.052 · DOI
  92. Todesco, 2020, Massive haplotypes underlie ecotypic differentiation in sunflowers, Nature, 584, 602, 10.1038/s41586-020-2467-6 · DOI · Paper page
  93. Ungerer, 1998, Rapid hybrid speciation in wild sunflowers, PNAS, 95, 11757, 10.1073/pnas.95.20.11757 · DOI
  94. Ungerer, 2006, Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation, Curr Biol, 16, R872, 10.1016/j.cub.2006.09.020 · DOI
  95. Wang, 2021, Hybrid speciation via inheritance of alternate alleles of parental isolating genes, Mol Plant, 14, 208, 10.1016/j.molp.2020.11.008 · DOI
  96. Wang, 2022, Genomic evidence for homoploid hybrid speciation between ancestors of two different genera, Nat commun, 13, 1
  97. Welch, 2002, Habitat divergence between a homoploid hybrid sunflower species, Helianthus paradoxus (Asteraceae), and its progenitors, Am J Bot, 89, 472, 10.3732/ajb.89.3.472 · DOI
  98. Wickham, 2011, Ggplot2, Wiley Interdiscip Rev Comput Stat, 3, 180, 10.1002/wics.147 · DOI
  99. Xiong, 2022, Admixture of evolutionary rates across a butterfly hybrid zone, eLife, 11, e78135, 10.7554/eLife.78135 · DOI
  100. Yatabe, 2007, Rampant gene exchange across a strong reproductive barrier between the annual sunflowers, Helianthus annuus and H. petiolaris, Genetics, 175, 1883, 10.1534/genetics.106.064469 · DOI
  101. Zeng, 2002, Preparation of total DNA from recalcitrant plant taxa, Acta Bot Sin, 44, 694
  102. Zhang, 2019, Intraspecific genetic divergence within Helianthus niveus and the status of two new morphotypes from Mexico, Am J Bot, 106, 1229, 10.1002/ajb2.1349 · DOI
  103. Zhang, 2018, ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees, BMC Bioinform, 19, 153, 10.1186/s12859-018-2129-y · DOI · Paper page

Metadata

Authors
Owens, G. L., Huang, K., Todesco, M., & Rieseberg, L. H.
Affiliations
  • University of Victoria (CA)
  • University of British Columbia (CA)
Corresponding author
Owens, Gregory L
ORCID
Venue
Molecular Biology and Evolution
Publisher
Oxford University Press (OUP)
Published
2023-01-17
Volume
40
Issue
2
ISSN
  • 0737-4038 (ISSN-L)
  • 1537-1719
DOI
10.1093/molbev/msad013
PMC
PMC9907532
OpenAlex
W4316814335
Cited by
39
References
104
Citations by year
2026: 12 · 2025: 12 · 2024: 9 · 2023: 6
FWCI
10.13
Type
journal article
Language
en
Open access
Licence
Locations
  • Molecular Biology and Evolution (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Diversity and Evolution
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant Taxonomy and Phylogenetics
Keywords
homoploid hybrid speciation, Helianthus, sunflower, hybridization, introgression, admixture, recombination rate, syngameon, gene flow
MeSH terms
Haplotypes, Helianthus, Hybridization, Genetic, Phylogeny, Gene Flow

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