Polyploidy promotes species diversification of Allium through ecological shifts.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
01 2020
Historique:
received: 15 04 2019
accepted: 01 08 2019
pubmed: 9 8 2019
medline: 12 11 2020
entrez: 9 8 2019
Statut: ppublish

Résumé

Despite the role of polyploidy in multiple evolutionary processes, its impact on plant diversification remains controversial. An increased polyploid frequency may facilitate speciation through shifts in ecology, morphology or both. Here we used Allium to evaluate: (1) the relationship between intraspecific polyploid frequency and species diversification rate; and (2) whether this process is associated with habitat and/or trait shifts. Using eight plastid and nuclear ribosomal markers, we built a phylogeny of 448 Allium species, representing 46% of the total. We quantified intraspecific ploidy diversity, heterogeneity in diversification rates and their relationship along the phylogeny using trait-dependent diversification models. Finally, we evaluated the association between polyploidisation and habitat or trait shifts. We detected high ploidy diversity in Allium and a polyploidy-related diversification rate shift with a probability of 95% in East Asia. Allium lineages with high polyploid frequencies had higher species diversification rates than those of diploids or lineages with lower polyploid frequencies. Shifts in speciation rates were strongly correlated with habitat shifts linked to particular soil conditions; 81.7% of edaphic variation could be explained by polyploidisation. Our study emphasises the role of intraspecific polyploid frequency combined with ecological drivers on Allium diversification, which may explain plant radiations more generally.

Identifiants

pubmed: 31394010
doi: 10.1111/nph.16098
doi:

Substances chimiques

Soil 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

571-583

Informations de copyright

© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.

Références

Abbott RJ, Lowe AJ. 2004. Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles. Biological Journal of the Linnean Society 82: 467-474.
Aryakia E, Karimi HR, Naghavi MR, Fazeli SAS. 2016. Morphological characterization of intra- and interspecific diversity in some Iranian wild Allium species. Euphytica 211: 185-200.
Baduel P, Bray S, Vallejo-Marin M, Kolář F, Yant L. 2018. The “Polyploid Hop”: shifting challenges and opportunities over the evolutionary lifespan of genome duplications. Frontiers in Ecology and Evolution 6: 1-19.
Beaulieu JM, O'Meara BC. 2016. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Systematic Biology 65: 583-601.
Bruggeman J, Heringa J, Brandt BW. 2009. PhyloPars: estimation of missing parameter values using phylogeny. Nucleic Acids Research 37(suppl_2): W179-W184.
Cai L, Xi Z, Amorim AM, Sugumaran M, Rest JS, Liu L, Davis CC. 2019. Widespread ancient whole-genome duplications in Malpighiales coincide with Eocene global climatic upheaval. New Phytologist 221: 565-576.
Čertner M, Sudová R, Weiser M, Suda J, Kolář F. 2019. Ploidy-altered phenotype interacts with local environment and may enhance polyploid establishment in Knautia serpentinicola (Caprifoliaceae). New Phytologist 221: 1117-1127.
Chao D-Y, Dilkes B, Luo H, Douglas A, Yakubova E, Lahner B, Salt DE. 2013. Polyploids exhibit higher potassium uptake and salinity tolerance in Arabidopsis. Science 341: 658-659.
Chapman MA, Abbott RJ. 2010. Introgression of fitness genes across a ploidy barrier. New Phytologist 186: 63-71.
Chen S, Kim D-K, Chase MW, Kim J-H. 2013. Networks in a large-scale phylogenetic analysis: reconstructing evolutionary history of Asparagales (Lilianae) based on four plastid genes. PLoS ONE 8: e59472.
Chester M, Gallagher JP, Symonds VV, da Silva AVC, Mavrodiev EV, Leitch AR, Soltis PS, Soltis DE. 2012. Extensive chromosomal variation in a recently formed natural allopolyploid species, Tragopogon miscellus (Asteraceae). Proceedings of the National Academy of Sciences, USA 109: 1176-1181.
Cui X-K, Ao C-Q, Zhang Q, Chen L-T, Liu J-Q. 2008. Diploid and tetraploid distribution of Allium przewalskianum Regel. (Liliaceae) in the Qinghai-Tibetan Plateau and adjacent regions. Caryologia 61: 192-200.
Drummond AJ, Suchard MA, Xie D, Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969-1973.
Ebersbach J, Muellner-Riehl A, Favre A, Paule J, Winterfeld G, Schnitzler J. 2018. Driving forces behind evolutionary radiations: Saxifraga section Ciliatae (Saxifragaceae) in the region of the Qinghai-Tibet Plateau. Botanical Journal of the Linnean Society 186: 304-320.
Ebersbach J, Schnitzler J, Favre A, Muellner-Riehl A. 2017. Evolutionary radiations in the species-rich mountain genus Saxifraga L. BMC Evolutionary Biology 17: 119.
Estep MC, McKain MR, Diaz DV, Zhong J, Hodge JG, Hodkinson TR, Layton DJ, Malcomber ST, Pasquet R, Kellogg EA. 2014. Allopolyploidy, diversification, and the Miocene grassland expansion. Proceedings of the National Academy of Sciences, USA 111: 15149-15154.
FitzJohn RG. 2010. Quantitative traits and diversification. Systematic Biology 59: 619-633.
FitzJohn RG. 2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods in Ecology and Evolution 3: 1084-1092.
Fowler NL, Levin DA. 2016. Critical factors in the establishment of allopolyploids. American Journal of Botany 103: 1236-1251.
Freeling M. 2017. Picking up the ball at the K/Pg boundary: the distribution of ancient polyploidies in the plant phylogenetic tree as a spandrel of asexuality with occasional sex. Plant Cell 29: 202-206.
Friesen N, Fritsch RM, Blattner FR. 2006. Phylogeny and new intrageneric classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS sequences. Aliso 22: 372-395.
Fritsch RM, Fritsch N. 2002. Evolution, domestication and taxonomy. In: Rabinowitch HD, Currah L, eds. Allium crop science: recent advances. London, UK: CABI Publishing, 5-30.
Godfree RC, Marshall DJ, Young AG, Miller CH, Mathews S. 2017. Empirical evidence of fixed and homeostatic patterns of polyploid advantage in a keystone grass exposed to drought and heat stress. Royal Society Open Science 4: 170934.
Han T-S, Wu Q, Hou X-H, Li Z-W, Zou Y-P, Ge S, Guo Y-L. 2015. Frequent introgressions from diploid species contribute to the adaptation of the tetraploid Shepherd's purse (Capsella bursa-pastoris). Molecular Plant 8: 427-438.
Harvey MG, Rabosky DL. 2018. Continuous traits and speciation rates: alternatives to state-dependent diversification models. Methods in Ecology and Evolution 9: 984-993.
Hauenschild F, Favre A, Schnitzler J, Michalak I, Freiberg M, Muellner-Riehl AN. 2017. Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region: immigration and in situ radiation. Plant Diversity 39: 167-179.
Herden T, Hanelt P, Friesen N. 2016. Phylogeny of Allium L. subgenus Anguinum (G. Don. ex WDJ Koch) N. Friesen (Amaryllidaceae). Molecular Phylogenetics and Evolution 95: 79-93.
Huang D-Q, Li Q-Q, Zhou C-J, Zhou SD, He X-J. 2014. Intraspecific differentiation of Allium wallichii (Amaryllidaceae) inferred from chloroplast DNA and internal transcribed spacer fragments. Journal of Systematics and Evolution 52: 341-354.
Husband BC. 2000. Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proceedings of the Royal Society of London. Series B: Biological Sciences 267: 217-223.
Husband BC. 2004. The role of triploid hybrids in the evolutionary dynamics of mixed-ploidy populations. Biological Journal of the Linnean Society 82: 537-546.
Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772-780.
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649.
Kellogg EA. 2016. Has the connection between polyploidy and diversification actually been tested? Current Opinion in Plant Biology 30: 25-32.
Köhler C, Scheid OM, Erilova A. 2010. The impact of the triploid block on the origin and evolution of polyploid plants. Trends in Genetics 26: 142-148.
Kolář F, Čertner M, Suda J, Schönswetter P, Husband BC. 2017. Mixed-ploidy species: progress and opportunities in polyploid research. Trends in Plant Science 22: 1041-1055.
Kreiner JM, Kron P, Husband BC. 2017. Frequency and maintenance of unreduced gametes in natural plant populations: associations with reproductive mode, life history and genome size. New Phytologist 214: 879-889.
Leigh JW, Susko E, Baumgartner M, Roger AJ. 2008. Testing congruence in phylogenomic analysis. Systematic Biology 57: 104-115.
Leitch A, Leitch I. 2008. Genomic plasticity and the diversity of polyploid plants. Science 320: 481-483.
Levan A. 1931. Cytological studies in Allium: a preliminary note. Hereditas 15: 347-356.
Levin DA. 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35-43.
Levin DA. 2019. Why polyploid exceptionalism is not accompanied by reduced extinction rates. Plant Systematics and Evolution 305: 1-11.
Levin DA, Soltis DE. 2018. Factors promoting polyploid persistence and diversification and limiting diploid speciation during the K-Pg interlude. Current Opinion in Plant Biology 42: 1-7.
Li M-J, Tan J-B, Xie D-F, Huang D-Q, Gao Y-D, He X-J. 2016. Revisiting the evolutionary events in Allium subgenus Cyathophora (Amaryllidaceae): insights into the effect of the Hengduan Mountains Region (HMR) uplift and Quaternary climatic fluctuations to the environmental changes in the Qinghai-Tibet Plateau. Molecular Phylogenetics and Evolution 94: 802-813.
Li Q-Q, Zhou S-D, Huang D-Q, He X-J, Wei X-Q. 2016. Molecular phylogeny, divergence time estimates and historical biogeography within one of the world's largest monocot genera. Annals of Botany 8: 1-17.
Luebert F, Weigend M. 2014. Phylogenetic insights into Andean plant diversification. Frontiers in Ecology and Evolution 2: 1-17.
Magallón S, Gómez-Acevedo S, Sánchez-Reyes LL, Hernández-Hernández T. 2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207: 437-453.
Mandakova T, Lysak MA. 2018. Post-polyploid diploidization and diversification through dysploid changes. Current Opinion in Plant Biology 42: 55-65.
Marchant DB, Soltis DE, Soltis PS. 2016. Patterns of abiotic niche shifts in allopolyploids relative to their progenitors. New Phytologist 212: 708-718.
Marques I, Loureiro J, Draper D, Castro M, Castro S. 2018. How much do we know about the frequency of hybridisation and polyploidy in the Mediterranean region? Plant Biology 20: 21-37.
Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, Rieseberg LH, Otto SP. 2011. Recently formed polyploid plants diversify at lower rates. Science 333: 1257.
Onstein RE, Jordan GJ, Sauquet H, Weston PH, Bouchenak-Khelladi Y, Carpenter RJ, Linder HP. 2016. Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats. Global Ecology and Biogeography 25: 1239-1251.
Orme D, Freckleton R, Thomas G, Petzoldt T. 2013. The caper package: comparative analysis of phylogenetics and evolution in R. R Package v. 5 [WWW document] URL https://CRAN.R-project.org/package=caper.
Parisod C, Broennimann O. 2016. Towards unified hypotheses of the impact of polyploidy on ecological niches. New Phytologist 212: 540-542.
Peruzzi L, Carta A, Altinordu F. 2017. Chromosome diversity and evolution in Allium (Allioideae, Amaryllidaceae). Plant Biosystems 151: 212-220.
Petit C, Bretagnolle F, Felber F. 1999. Evolutionary consequences of diploid-polyploid hybrid zones in wild species. Trends in Ecology & Evolution 14: 306-311.
Pigg KB, Bryan FA, DeVore ML. 2018. Paleoallium billgenseli gen. et sp. nov.: Fossil Monocot remains from the Latest Early Eocene Republic Flora, Northeastern Washington State, USA. International Journal of Plant Sciences 179: 477-486.
R Core Team. 2018. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rabosky DL. 2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9: 1-15.
Rabosky DL, Grundler M, Anderson C, Title P, Shi JJ, Brown JW, Huang H, Larson JG. 2014. BAMM tools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods in Ecology and Evolution 5: 701-707.
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA, Susko E. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901-904.
Ramsey J. 2011. Polyploidy and ecological adaptation in wild yarrow. Proceedings of the National Academy of Sciences, USA 108: 7096-7101.
Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Philosophical Transactions of the Royal Society B: Biological Sciences 369: 1-20.
Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annual Review of Ecology and Systematics 29: 467-501.
Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annual Review of Ecology and Systematics 33: 589-639.
Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J. 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Molecular Plant 11: 414-428.
Rice A, Glick L, Abadi S, Einhorn M, Kopelman NM, Salman-Minkov A, Mayzel J, Chay O, Mayrose I. 2015. The Chromosome Counts Database (CCDB)-a community resource of plant chromosome numbers. New Phytologist 206: 19-26.
Rice A, Šmarda P, Novosolov M, Drori M, Glick L, Sabath N, Meiri S, Belmaker J, Mayrose I. 2019. The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265-273.
Rodriguez DJ. 1996. A model for the establishment of polyploidy in plants. The American Naturalist 147: 33-46.
Rothfels CJ, Otto SP. 2016. Polyploid speciation. In: Kliman RM, ed. Encyclopedia of evolutionary biology. Oxford, UK: Academic Press, 317-326.
Salman-Minkov A, Sabath N, Mayrose I. 2016. Whole-genome duplication as a key factor in crop domestication. Nature Plants 2: 1-4.
Savidan Y, Pernès J. 1982. Diploid-tetraploid-dihaploid cycles and the evolution of Panicum maximum Jacq. Evolution 36: 596-600.
Schranz ME, Mohammadin S, Edger PP. 2012. Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Current Opinion in Plant Biology 15: 147-153.
Segraves KA. 2017. The effects of genome duplications in a community context. New Phytologist 215: 57-69.
Segraves KA, Anneberg TJ. 2016. Species interactions and plant polyploidy. American Journal of Botany 103: 1326-1335.
Smith SA, Brown JW, Yang Y, Bruenn R, Drummond CP, Brockington SF, Walker JF, Last N, Douglas NA, Moore MJ. 2018. Disparity, diversity, and duplications in the Caryophyllales. New Phytologist 217: 836-854.
Soltis DE, Segovia-Salcedo MC, Jordon-Thaden I, Majure L, Miles NM, Mavrodiev EV, Mei W, Cortez MB, Soltis PS, Gitzendanner MA. 2014. Are polyploids really evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytologist 202: 1105-1117.
Soltis DE, Soltis PS. 1999. Polyploidy: recurrent formation and genome evolution. Trends in Ecology & Evolution 14: 348-352.
Soltis PS, Soltis DE. 2016. Ancient WGD events as drivers of key innovations in angiosperms. Current Opinion in Plant Biology 30: 159-165.
Stebbins GL. 1950. Variation and evolution in plants. New York, NY, USA: Columbia University Press.
Suda J, Herben T. 2013. Ploidy frequencies in plants with ploidy heterogeneity: fitting a general gametic model to empirical population data. Proceedings of the Royal Society B: Biological Sciences 280: 1-10.
Suda J, Meyerson LA, Leitch IJ, Pyšek P. 2015. The hidden side of plant invasions: the role of genome size. New Phytologist 205: 994-1007.
Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nature Reviews Genetics 18: 411-424.
Van Drunen WE, Husband BC. 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytologist 224: 1266-1277.
Veselý P, Bureš P, Šmarda P, Pavlíček T. 2011. Genome size and DNA base composition of geophytes: the mirror of phenology and ecology? Annals of Botany 109: 65-75.
Walczyk AM, Hersch-Green EI. 2019. Impacts of soil nitrogen and phosphorus levels on cytotype performance of the circumboreal herb Chamerion angustifolium: implications for polyploid establishment. American Journal of Botany 106: 1-16.
Wang X, Li Y, Liang Q, Zhang L, Wang Q, Hu H, Sun Y. 2015. Contrasting responses to Pleistocene climate changes: a case study of two sister species Allium cyathophorum and A. spicata (Amaryllidaceae) distributed in the eastern and western Qinghai-Tibet Plateau. Ecology and Evolution 5: 1513-1524.
Wei N, Cronn R, Liston A, Ashman TL. 2019. Functional trait divergence and trait plasticity confer polyploid advantage in heterogeneous environments. New Phytologist 221: 2286-2297.
Wen J, Zhang J, Nie Z-L, Zhong Y, Sun H. 2014. Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Frontiers in Genetics 5: 1-16.
Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. Proceedings of the National Academy of Sciences, USA 106: 13875-13879.
Wu L-L, Cui X-K, Milne RI, Sun Y-S, Liu J-Q. 2010. Multiple autopolyploidizations and range expansion of Allium przewalskianum Regel. (Alliaceae) in the Qinghai-Tibetan Plateau. Molecular Ecology 19: 1691-1704.
Xie C, Xie D-f, Zhong Y, Guo X-L, Liu Q, Zhou S-D, He X-J. 2019. The effect of Hengduan Mountains Region (HMR) uplift to environmental changes in the HMR and its eastern adjacent area: tracing the evolutionary history of Allium section Sikkimensia (Amaryllidaceae). Molecular Phylogenetics and Evolution 130: 380-396.
Xing Y, Ree RH. 2017. Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proceedings of the National Academy of Sciences, USA 114: E3444-E3451.
Zhang H, Bian Y, Gou X, Zhu B, Xu C, Qi B, Li N, Rustgi S, Zhou H, Han F. 2013. Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat. Proceedings of the National Academy of Sciences, USA 110: 3447-3452.
Zhang Y, Yu Q, Zhang Q, Hu X, Hu J, Fan B. 2017. Regional-scale differentiation and phylogeography of a desert plant Allium mongolicum (Liliaceae) inferred from chloroplast DNA sequence variation. Plant Systematics and Evolution 303: 451-466.

Auteurs

Ting-Shen Han (TS)

CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China.
Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China.
Department of Biology, Duke University, Box 90338, Durham, NC, 27708, USA.

Quan-Jing Zheng (QJ)

CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.

Renske E Onstein (RE)

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, Leipzig, D-04103, Germany.

Blanca M Rojas-Andrés (BM)

Department of Molecular Evolution and Plant Systematics & Herbarium (LZ), Leipzig University, Johannisallee 21-23, Leipzig, D-04103, Germany.

Frank Hauenschild (F)

Department of Molecular Evolution and Plant Systematics & Herbarium (LZ), Leipzig University, Johannisallee 21-23, Leipzig, D-04103, Germany.

Alexandra N Muellner-Riehl (AN)

German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, Leipzig, D-04103, Germany.
Department of Molecular Evolution and Plant Systematics & Herbarium (LZ), Leipzig University, Johannisallee 21-23, Leipzig, D-04103, Germany.

Yao-Wu Xing (YW)

CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China.
Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Mengla, Yunnan, 666303, China.

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