Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation

doi:10.1016/j.pld.2017.05.010

Plant Diversity ›› 2017, Vol. 39 ›› Issue (04): 167-179.DOI: 10.1016/j.pld.2017.05.010

Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation

Frank Hauenschild^a, Adrien Favre^a, Jan Schnitzler^a, Ingo Michalak^a, Martin Freiberg^b, Alexandra N. Muellner-Riehl^a,c

a Leipzig University, Department of Molecular Evolution and Plant Systematics & Herbarium(LZ), Johannisallee 21-23, 04103 Leipzig, Germany;
b Leipzig University, Department of Systematic Botany and Functional Biodiversity Research, Johannisallee 21-23, 04103 Leipzig, Germany;
c German Centre for Integrative Biodiversity Research(iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany

收稿日期:2017-04-05 修回日期:2017-05-31 出版日期:2017-08-25 发布日期:2021-11-05
通讯作者: Alexandra N. Muellner-Riehl
基金资助:
We thank the German Research Foundation for funding of staff (project no. MU 2934/2-1). We also gratefully acknowledge the support of the German Centre for Integrative Biodiversity Research (iDiv) HalleJena-Leipzig funded by the German Research Foundation (FZT 118) for funding of lab expenses.

Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation

Frank Hauenschild^a, Adrien Favre^a, Jan Schnitzler^a, Ingo Michalak^a, Martin Freiberg^b, Alexandra N. Muellner-Riehl^a,c

a Leipzig University, Department of Molecular Evolution and Plant Systematics & Herbarium(LZ), Johannisallee 21-23, 04103 Leipzig, Germany;
b Leipzig University, Department of Systematic Botany and Functional Biodiversity Research, Johannisallee 21-23, 04103 Leipzig, Germany;
c German Centre for Integrative Biodiversity Research(iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany

Received:2017-04-05 Revised:2017-05-31 Online:2017-08-25 Published:2021-11-05
Contact: Alexandra N. Muellner-Riehl
Supported by:
We thank the German Research Foundation for funding of staff (project no. MU 2934/2-1). We also gratefully acknowledge the support of the German Centre for Integrative Biodiversity Research (iDiv) HalleJena-Leipzig funded by the German Research Foundation (FZT 118) for funding of lab expenses.

摘要/Abstract

摘要： A plethora of studies investigating the origin and evolution of diverse mountain taxa has assumed a causal link between geological processes (orogenesis) and a biological response (diversification). Yet, a substantial delay (up to 30 Myr) between the start of orogenesis and diversification is often observed. Evolutionary biologists should therefore identify alternative drivers of diversification and maintenance of biodiversity in mountain systems. Using phylogenetic, biogeographic, and diversification rate analyses, we could identify two independent processes that most likely explain the diversity of the widespread genus Allium in the QinghaieTibet Plateau (QTP) region:(1) While the QTP-related taxa of the subgenus Melanocrommyum diversified in situ, (2) QTP-related taxa of other subgenera migrated into the QTP from multiple source areas. Furthermore, shifts in diversification rates within Allium could not be attributed spatially and temporally to the uplift history of the QTP region. Instead, global cooling and climate oscillations in the Quaternary were major contributors to increased speciation rates in three clades of Allium. Our study therefore adds to the growing evidence supporting the "mountain-geo-biodiversity hypothesis", which highlights the role of climate oscillations for the diversification of mountain organisms.

关键词: Allium, Evolution, Hengduan mountains, Historical biogeography, Molecular dating, QinghaieTibet plateau

Abstract: A plethora of studies investigating the origin and evolution of diverse mountain taxa has assumed a causal link between geological processes (orogenesis) and a biological response (diversification). Yet, a substantial delay (up to 30 Myr) between the start of orogenesis and diversification is often observed. Evolutionary biologists should therefore identify alternative drivers of diversification and maintenance of biodiversity in mountain systems. Using phylogenetic, biogeographic, and diversification rate analyses, we could identify two independent processes that most likely explain the diversity of the widespread genus Allium in the QinghaieTibet Plateau (QTP) region:(1) While the QTP-related taxa of the subgenus Melanocrommyum diversified in situ, (2) QTP-related taxa of other subgenera migrated into the QTP from multiple source areas. Furthermore, shifts in diversification rates within Allium could not be attributed spatially and temporally to the uplift history of the QTP region. Instead, global cooling and climate oscillations in the Quaternary were major contributors to increased speciation rates in three clades of Allium. Our study therefore adds to the growing evidence supporting the "mountain-geo-biodiversity hypothesis", which highlights the role of climate oscillations for the diversification of mountain organisms.

Key words: Allium, Evolution, Hengduan mountains, Historical biogeography, Molecular dating, QinghaieTibet plateau

Frank Hauenschild, Adrien Favre, Jan Schnitzler, Ingo Michalak, Martin Freiberg, Alexandra N. Muellner-Riehl. Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation[J]. Plant Diversity, 2017, 39(04): 167-179.

参考文献

Antonelli, A., Sanmartín, I., 2011. Why are there so many plant species in the neotropics? Taxon 60, 403-414.
Banfi, E., Galasso, G., Soldano, A., 2011. Notes on systematics and taxonomy for the Italian vascular flora. 2. Nat. Hist. Sci. 152, 85-106.
Barthlott, W., Lauer, W., Placke, A., 1996. Global distribution of species diversity in vascular plants:towards a world map of phytodiversity (Globale Verteilung der Artenvielfalt Höherer P flanzen:Vorarbeiten zu einer Weltkarte der Phytodiversität). Erdkunde 317-327.
Barthlott, W., Mutke, J., Rafiqpoor, D., Kier, G., Kreft, H., 2005. Global centers of vascular plant diversity. Nova Acta Leopoldina NF 92 (342), 61-83.
Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., Sayers, E.W., 2013. GenBank. Nucleic Acids Res. 41, D36-D42.
Bouckaert, R., Heled, J., Kuhnert, D., Vaughan, T., Wu, C.H., Xie, D., Suchard, M.A., Rambaut, A., Drummond, A.J., 2014. BEAST 2:a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10.
Chase, M.W., Reveal, J.L., Fay, M.F., 2009. A subfamilial classification for the expanded asparagalean families Amaryllidaceae, Asparagaceae and Xanthorrhoeaceae. Bot. J. Linn. Soc. 161, 132-136.
Chen, S., Kim, D.-K., Chase, M.W., 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.
Choi, H.J., Oh, B.U., 2011. A partial revision of Allium (Amaryllidaceae) in Korea and north-eastern China. Bot. J. Linn. Soc. 167, 153-211.
Condamine, F.L., Sperling, F.A., Wahlberg, N., Rasplus, J.Y., Kergoat, G.J., 2012. What causes latitudinal gradients in species diversity? Evolutionary processes and ecological constraints on swallowtail biodiversity. Ecol. Lett. 15, 267-277.
Conrad, F., 2008. Molecular Systematics, Biogeography and Dating of the Tribe Haemantheae (Amaryllidaceae) and the Phylogeography of Clivia. University of Cape Town.
Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973.
Dufour, A., Gadallah, F., Wagner, H.H., Guisan, A., Buttler, A., 2006. Plant species richness and environmental heterogeneity in a mountain landscape:effects of variability and spatial configuration. Ecography 29, 573-584.
Ebersbach, J., Muellner-Riehl, A.N., Michalak, I., Tkach, N., Hoffmann, M.H., Röser, M., Sun, H., Favre, A., 2016. In and out of the Qinghai eTibet Plateau:divergence time estimation and historical biogeography of the large arcticalpine genus Saxifraga L. J. Biogeogr. 44, 900-910.
Ehlers, J., Gibbard, P.L., 2004. Quaternary glaciations-extent and chronology:part I:Europe, vol. 2. Elsevier.
Favre, A., Michalak, I., Chen, C.-H., Wang, J.-C., Pringle, J.S., Matuszak, S., Sun, H., Yuan, Y.-M., Struwe, L., Muellner-Riehl, A.N., 2016. Out-of-Tibet:the spatiotemporal evolution of Gentiana (Gentianaceae). J. Biogeogr. 43, 1967-1978.
Favre, A., Päckert, M., Pauls, S.U., J ahnig, S.C., Uhl, D., Michalak, I., MuellnerRiehl, A.N., 2015. The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biol. Rev. 90, 236-253.
Fjeldså, J., Bowie, R.C.K., Rahbek, C., 2012. The role of mountains in the diversification of birds. Annu. Rev. Ecol. Evol. Syst. 43, 249-265.
Friesen, N., Fritsch, R.M., Blattner, F.R., 2006. Phylogeny and new intrageneric classification of Allium (Alliaceae) based on nuclear ribosomal DNA ITS sequences. Aliso 22, 372-395.
Gao, Q.B., Li, Y.H., Gornall, R.J., Zhang, Z.X., Zhang, F.Q., Xing, R., Fu, P.C., Wang, J.L., Liu, H.R., Tian, Z.Z., Chen, S.L., 2015. Phylogeny and speciation in Saxifraga sect.Ciliatae (Saxifragaceae):evidence from psbA-trnH, trnL-F and ITS sequences.Taxon 64, 703-713.
Govaerts, R., Friesen, N., Fritsch, R., Snijman, D.A., Marcucci, R., SilverstoneSopkin, P.A., Brullo, S., 2016. World Checklist of Allium. Royal Botanic Gardens.http://apps.kew.org/wcsp/.
Graham, C.H., Carnaval, A.C., Cadena, C.D., Zamudio, K.R., Roberts, T.E., Parra, J.L., McCain, C.M., Bowie, R.C., Moritz, C., Baines, S.B., 2014. The origin and maintenance of montane diversity:integrating evolutionary and ecological processes. Ecography 37, 711-719.
Gregory, M., Fritsch, R.M., Friesen, N.W., Khassanov, F.O., McNeal, D.W., 1998.Nomenclator alliorum:Allium names and synonyms:a world guide. Royal Botanic Gardens, Kew, ISBN 1900347644, p. 83.
Haffer, J., 1969. Speciation in Amazonian forest birds. Science 165, 131-137.
Heled, J., Bouckaert, R.R., 2013. Looking for trees in the forest:summary tree from posterior samples. BMC Evol. Biol. 13, 1.
Herden, T., Hanelt, P., Friesen, N., 2016. Phylogeny of Allium L. subgenus Anguinum (G.Don. ex W.D.J. Koch) N. Friesen (Amaryllidaceae). Mol. Phylogenet. Evol. 95, 79-93.
Hoorn, C., Mosbrugger, V., Mulch, A., Antonelli, A., 2013. Biodiversity from mountain building. Nat. Geosci. 6, 154.
Huang, D.-Q., Yang, J.-T., Zhou, C.-J., Zhou, S.-D., He, X.-J., 2014. Phylogenetic reappraisal of Allium subgenus Cyathophora (Amaryllidaceae) and related taxa, with a proposal of two new sections. J. Plant Res. 127, 275-286.
Hughes, C.E., Atchison, G.W., 2015. The ubiquity of alpine plant radiations:from the Andes to the Hengduan Mountains. New Phytol. 207, 275-282.
Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7:improvements in performance and usability. Mol. Biol. Evol. 30, 772-780.
Kaufman, D.S., Manley, W.F., 2004. Pleistocene maximum and Late Wisconsinan glacier extents across Alaska, USA. Dev. Quat. Sci. 2, 9-27.
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.
Lagomarsino, L.P., Condamine, F.L., Antonelli, A., Mulch, A., Davis, C.C., 2016. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol. 210, 1430-1442.
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.Mol. Phylogenet. Evol. 94, 802-813.
Li, Q.-Q., Zhou, S.-D., He, X.-J., Yu, Y., Zhang, Y.-C., Wei, X.-Q., 2010. Phylogeny and biogeography of Allium (Amaryllidaceae:Allieae) based on nuclear ribosomal internal transcribed spacer and chloroplast rps16 sequences, focusing on the inclusion of species endemic to China. Ann. Bot. 106, 709-733.
Linder, H.P., 2008. Plant species radiations:where, when, why? Philos. Trans. R. Soc.B Biol. Sci. 363, 3097-3105.
Mabberley, D.J., 2008. Mabberley's Plant-Book:a Portable Dictionary of Plants, Their Classifications and Uses. Camb. Univ. Press.
Maddison, W.P., Midford, P.E., Otto, S.P., 2007. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56, 701-710.
Magallón, S., Gomez-Acevedo, S., Sanchez-Reyes, L.L., Hernandez-Hernandez, T., 2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207, 437-453.
Manafzadeh, S., Staedler, Y.M., Conti, E., 2016. Visions of the past and dreams of the future in the Orient:the Irano-Turanian region from classical botany to evolutionary studies. Biol. Rev. http://dx.doi.org/10.1111/brv.12287.
Matzke, N.J., 2014. Model selection in historical biogeography reveals that founderevent speciation is a crucial process in Island clades. Syst. Biol. 63, 951-970.
Moore, B.R., Höhna, S., May, M.R., Rannala, B., Huelsenbeck, J.P., 2016. Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. Proc. Natl. Acad. Sci. U. S. A. 113, 9569-9574.
Mosbrugger, V., Favre, A., Muellner-Riehl, A.N., Päckert, M., Mulch, A., 2018. Ceno- zoic evolution of geo-biodiversity in the Tibeto-Himalayan region. In:Hoorn, C., Antonelli, A. (Eds.), Mountains, Climate, and Biodiversity. Wiley-Blackwell, ISBN 978-1-119-15987-2 (in press).
Nee, S., May, R.M., Harvey, P.H., 1994. The reconstructed evolutionary process. Phil.Trans. R. Soc. London B 344, 305-311.
Palazzesi, L., Barreda, V.D., Cuitiño, J.I., Guler, M.V., Tellería, M.C., Ventura Santos, R., 2014. Fossil pollen records indicate that Patagonian desertification was not solely a consequence of Andean uplift. Nat. Commun. 5, 3558.
Pattengale, N.D., Alipour, M., Bininda-Emonds, O.R., Moret, B.M., Stamatakis, A., 2010. How many bootstrap replicates are necessary? J. Comput. Biol. 17, 337-354.
R. Core Team, 2015. R:a language and environment for statistical computing.Vienna, Austria.
Rabosky, D.L., 2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543.
Rabosky, D.L., Grundler, M., Anderson, C., Shi, J.J., Brown, J.W., Huang, H., Larson, J.G., 2014. BAMMtools:an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5, 701-707.
Rabosky, D.L., Mitchell, J.S., Chang, J., 2017. Is BAMM flawed? Theoretical and practical concerns in the analysis of multi-rate diversification models. Syst. Biol.http://dx.doi.org/10.1093/sysbio/syx037.
Ree, R.H., 2005. Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59, 257-265.
Ree, R.H., Smith, S.A., 2008. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst. Biol. 57, 4-14.
Renner, S.S., 2016. Available data point to a 4-km-high Tibetan Plateau by 40 Ma, but 100 molecular-clock papers have linked supposed recent uplift to young node ages. J. Biogeogr. 43, 1479-1487.
Ronquist, F., Cannatella, D., 1997. Dispersal-vicariance analysis:a new approach to the quantification of historical biogeography. Syst. Biol. 46, 195-203.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P., 2012. MrBayes 3.2:efficient Bayesian phylogenetic inference and model choice across a large model space.Syst. Biol. 61, 539-542.
Schwery, O., Onstein, R.E., Bouchenak-Khelladi, Y., Xing, Y., Carter, R.J., Linder, H.P., 2015. As old as the mountains:the radiations of the Ericaceae. New Phytol. 207, 355-367.
Sennikov, A.N., Seregin, A.P., 2015. What happens to Allium saxatile M. Bieb.(Amaryllidaceae)? An unknown story of the well-known name. Taxon 64, 1294-1300.
Smith, S.Y., 2013. The fossil record of non-commelinid monocots. In:Wilkin, P., Mayo, S. (Eds.), Early Events in Monocot Evolution, Systematics Association Special Volume Series. Cambridge University Press, Cambridge. http://dx.doi.org/10.1017/CBO9781139002950.003.
Silvestro, D., Schnitzler, J., Zizka, G., 2011. A Bayesian framework to estimate diversification rates and their variation through time and space. BMC Evol.Biol. 11.
Silvestro, D., Schnitzler, J., 2018. Inferring macroevolutionary dynamics in mountain systems from fossils. In:Hoorn, C., Antonelli, A. (Eds.), Mountains, Climate, and Biodiversity. Wiley-Blackwell, ISBN 978-1-119-15987-2.
Stamatakis, A., 2014. RAxML version 8:a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30, 1312-1313.
Tang, Z., Wang, Z., Zheng, C., Fang, J., 2006. Biodiversity in China's mountains. Front.Ecol. Environ. 4, 347-352.
Wang, C., Dai, J., Zhao, X., Li, Y., Graham, S.A., He, D., Ran, B., Meng, J., 2014. Outwardgrowth of the Tibetan Plateau during the Cenozoic:a review. Tectonophysics 621, 1-43.
Xing, Y., Ree, R.H., 2017. Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc. Natl. Acad. Sci. U. S. A. 114, E3444-E3451.
Xu, J., Kamelin, R., 2000. In:Wu, Z., Raven, P.H., Deyuan, H. (Eds.), Allium L. Flora of China, vol. 24. Missouri Botanical Garden Press & Science Press, St. Louis, Beijing, pp. 165-202.
Xu, B., Li, Z., Sun, H., 2014. Plant diversity and floristic characters of the alpine subnival belt flora in the Hengduan Mountains, SW China. J. Syst. Evol. 52, 271-279.
Zhang, D.C., Ye, J.X., Sun, H., 2016. Quantitative approaches to identify floristic units and centres of species endemism in the Qinghai-Tibetan Plateau, south-western China. J. Biogeogr. 43, 2465-2476.

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Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation

Spatio-temporal evolution of Allium L. in the Qinghai-Tibet-Plateau region:Immigration and in situ radiation

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