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Phylogenomic Insights Into the Divergent History and Hybridization Within the East Asian Endemic Abelia (Caprifoliaceae)

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Phylogenomic Insights Into the Divergent History and Hybridization Within the East Asian Endemic Abelia (Caprifoliaceae) bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted August 1, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Phylogenomic insights into the divergent history and hybridization within 2 the East Asian endemic Abelia (Caprifoliaceae) 3 4 5 6 Qing-Hui Sun1, Diego F. Morales-Briones2,3, Hong-Xin Wang1,4, Jacob B. Landis5,6 Jun Wen7, 7 Hua-Feng Wang1* 8 9 10 1 Key Laboratory of Tropical Biological Resources of Ministry of Education, College of 11 Tropical Crops, Hainan University, Haikou 570228, China 12 2 Department of Plant and Microbial Biology, College of Biological Sciences, University of 13 Minnesota, 140 Gortner Laboratory, 1479 Gortner Avenue, Saint Paul, MN 55108, USA 14 3 Systematics, Biodiversity and Evolution of Plants, Department of Biology I, 15 Ludwig-Maximilians-Universität München, Menzinger Str. 67, 80638, Munich, Germany 16 4 Zhai Mingguo Academician Work Station, Sanya University, Sanya 572022, China 17 5 School of Integrative Plant Science, Section of Plant Biology and the L.H. Bailey 18 Hortorium, Cornell University, Ithaca, NY 14850, USA 19 6 BTI Computational Biology Center, Boyce Thompson Institute, Ithaca, NY 14853, USA 20 7 Department of Botany, National Museum of Natural History, MRC-166, Smithsonian 21 Institution, PO Box 37012, Washington, DC 20013-7012, USA 22 23 24 25 *Authors for correspondence: 26 Hua-Feng Wang, E-mail: [email protected] 27 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted August 1, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 28 Abstract: 29 • Background and Aims Abelia (Caprifoliaceae) is a small genus with six species (including 30 one artificial hybrid). The genus has a disjunct distribution across mainland China, Taiwan, 31 and the Ryukyu islands, providing a model system to explore mechanisms of species 32 dispersal in the East Asian flora. However, the current phylogenetic relationships within 33 Abelia remain uncertain. 34 • Methods In this study, we reconstructed phylogenetic relationships within Abelia using 35 nuclear loci generated by target enrichment and plastomes from genome skimming. 36 Divergence time estimation, ancestral area reconstruction, and ecological niche modelling 37 (ENM) were used to examine the biogeographic diversification of Abelia. 38 • Key Results We found extensive cytonuclear discordance across the genus. Based on 39 nuclear and plastid phylogenies we proposed to merge A. macrotera var. zabelioides into A. 40 uniflora. Network analyses suggested that A chinensis, A. macrotera and A. uniflora are from 41 complex hybrid origins. These hybridization events may explain the complicated taxonomy 42 of the group. Our results show that Abelia originated in southwest China, with the nuclear 43 haplotype network suggesting an ancestral haplotype from southwest and central China. The 44 diversification of Abelia began in the late Eocene, followed by A. chinensis var. ionandra 45 colonizing the island of Taiwan in the Middle Miocene. The ENM results suggested an 46 expansion of climatically suitable areas during the Last Glacial Maximum and range 47 contraction during the Last Interglacial. Disjunction between the Himalayan-Hengduan 48 Mountain region (HHM) and the island of Taiwan is most likely the consequence of 49 topographic isolation and postglacial contraction. 50 • Conclusions We used genomic data to reconstruct the phylogeny of Abelia and found a 51 clear pattern of reticulate evolution in the group. Overall, our results supported postglacial 52 range contraction together with topographic heterogeneity resulted in the mainland 53 China-Taiwan island disjunction. This study provides important new insights into the 54 speciation process and taxonomy of Abelia. 55 Key words: Abelia; Gene tree discordance; Hybridization; Mainland China-Taiwan island 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted August 1, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 56 disjunction. 57 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted August 1, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 58 INTRODUCTION 59 The underlying causes of disjunct distributions in various organisms have been a central 60 issue in biogeography (e.g., Xiang et al., 1998; Wen, 2001; Qian and Ricklefs, 2004; Wang et 61 al., 2012; Wen et al., 2013, 2018). Much discussion has focused on two mechanisms, 62 vicariance and long-distance dispersal (Givnish and Renner, 2004; Yoder and Nowak, 2006; 63 Šarhanová et al., 2017; Wang et al., 2020). The emergence of geographic barriers leads to 64 vicariance, resulting in decreased gene flow; while long-distance dispersal in plants usually 65 involves rare events driven by dispersal vectors such as animals, wind or water currents 66 (Nathan et al., 2008). Recent molecular systematic studies have shown that many plant 67 disjunctions are too young to be explained by continental drift or major geographic barriers 68 (Mummenhoff et al., 2004; Yoder and Nowak, 2006; Linder et al., 2013; Jiang et al., 2019). 69 Hence, long-distance dispersal has emerged as a major mechanism to explain many 70 discontinuous distributions in historical biogeography (Wen et al., 2013; Ye et al., 2019; Wen 71 and Wagner, 2020). 72 Biogeographic disjunctions between mainland China-Taiwan island have received 73 considerable attention with the separation of the two regions by 130 km (Wu and Wang, 2001; 74 Xiang and Soltis, 2001; Qiu et al., 2011; Chen et al., 2012; Ye et al., 2014, Jin et al., 2020). 75 The island of Taiwan is the largest subtropical mountainous island in the monsoonal western 76 Pacific region, located on the Tropic of Cancer, and originated in the late Miocene (ca. 9-5 77 million years ago; Sibuet and Hsu, 2004). Molecular phylogenetic analyses have shown that 78 several plant lineages have disjunct distributions between mainland China and Taiwan (e.g., 79 Sassafras J. Presl, Nie et al., 2007; Pseudotsuga Carrière, Wei et al., 2010; Triplostegia Wall. 80 ex DC., Niu et al., 2018; Prinsepia., Jin et al., 2020). Geologically, the island of Taiwan and 81 its adjacent continental margin of mainland China belong to the Eurasian plate; in the Late 82 Cretaceous both were part of the continental block. The continental block has undergone 83 many extensions and rifting events since the Paleocene (Wei, 2010; Suo et al., 2015). Two 84 hypotheses have been proposed to explain the formation of current plant disjunctions in this 85 region: long-distance dispersal and postglacial contraction (Chou et al., 2011; Wang et al., 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted August 1, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 86 2013; Ye et al., 2014; Niu et al., 2018). A phylogeographic study of Cunninghamia R.Br. ex 87 A.Rich. (Taxodiaceae) revealed that populations of Taiwan derived from continental Asia and 88 colonized the island via long-distance seed dispersal (Lu et al., 2001). Factors that have major 89 impacts on population dynamics and genetic variation patterns in plants in this region include 90 past geological and climatic changes, uplift of the Qinghai-Tibet Plateau, global optimum 91 temperature since the Miocene and the Quaternary glacial-interglacial transition (Xu et al., 92 2015; Cao et al., 2016; Chen et al., 2020). Recent studies have suggested that although the ice 93 sheet was not ubiquitous from the Qinling Mountains and Huai River (at ca. 34° N) to the 94 tropical south (≤ 22° N) in China during the Last Glacial period, the temperature in most 95 parts of mainland China was lower than today (Shi et al., 2006). Temperature changes 96 influence species distributions, population sizes, and intraspecific genetic differentiation. The 97 postglacial contraction hypothesis states that many species had a continuous distribution from 98 mainland China to Taiwan prior to the Quaternary glacial period, sometimes with disjunctions 99 between the Himalayan-Hengduan Mountain region and the island of Taiwan occurring when 100 samples migrated to higher altitudes as global temperatures increased (Chen and Ying, 2012). 101 Abelia R.Br. belongs to the subfamily Linnaeoideae Raf. within Caprifoliaceae s.l. 102 (Dipsacales; Yang and Landrein, 2011; Caprifoliaceae; Wang et al., 2021). The genus 103 includes A. chinensis (four varieties), A. forrestii (two varieties), A. × grandiflora, A. 104 macrotera (eight varieties), A. schumannii and A. uniflora (Landrein et al., 2017; 2020; Fig. 105 1). Abelia is a typical East Asian endemic genus with a disjunct distribution in southwestern 106 China, extending to the eastern portion of the island of Taiwan and the Ryukyu islands in 107 Japan. The genus includes an important ornamental species, Abelia × grandiflora, widely 108 cultivated in yards, parks and roadsides of temperate cities (e.g., Beijing, London, 109 Washington D.C., and Wuhan).
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