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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 April 14, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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, Hong-Xin Wang1, Jacob B. Landis3,4, Jun Wen5, 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 School of Integrative Plant Science, Section of Plant Biology and the L.H. Bailey 15 Hortorium, Cornell University, Ithaca, NY 14850, USA 16 4 BTI Computational Biology Center, Boyce Thompson Institute, Ithaca, NY 14853, USA 17 5 Department of Botany, National Museum of Natural History, MRC-166, Smithsonian 18 Institution, PO Box 37012, Washington, DC 20013-7012, USA 19 20 21 22 23 24 *Authors for correspondence: 25 Hua-Feng Wang, E-mail: [email protected] 26 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted April 14, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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. 27 Abstract: 28 • Background and Aims Abelia (Caprifoliaceae) is a small genus with five species 29 (including one artificial hybrid). The genus has a disjunct distribution across mainland China, 30 Taiwan and the Ryukyu Islands, providing a model system to explore species dispersal 31 mechanisms of the East Asian flora. However, the current phylogenetic relationships within 32 Abelia remain controversial. 33 • Methods In this study, we reconstructed the phylogenetic relationships within Abelia using 34 nuclear loci generated by target enrichment and the cpDNA from genome skimming. 35 • Key Results We found large cytonuclear discordance across the genus. Based on the 36 nuclear and chloroplast phylogenies we proposed to merge A. schumannii into A. macrotera, 37 and A. macrotera var. mairei into A. uniflora. Divergence time estimation, ancestral area 38 reconstruction, and ecological niche modelling (ENM) were used to examine the 39 biogeographic history of Abelia. Our results showed that Abelia originated in Southwest 40 China, and diversification began in the Early Eocene, followed by A. chinensis var. ionandra 41 colonizing Taiwan in the Middle Miocene. The ENM results suggested an expansion of 42 climatically suitable areas during the Last Glacial Maximum and range contraction during the 43 Last Interglacial. Disjunction between the Himalaya-Hengduan Mountain region (HHM) and 44 Taiwan is most likely the consequence of topographic isolation and postglacial contraction. 45 • Conclusions Overall, our results supports that postglacial range contraction together with 46 topographic heterogeneity resulted in the Taiwan and China mainland disjunction. 47 Furthermore, when we using genome data to reconstruct the phylogeny of related species, 48 branch evolution and network evolution should be considered, as well as gene flow in 49 historical periods. This research provide new insights for the speciation process and 50 taxonomy of Abelia. 51 52 Key words: Abelia; Phylogeography; Divergence time; Ancestral distribution; Taiwan 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted April 14, 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. 53 54 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted April 14, 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. 55 INTRODUCTION 56 The underlying causes of disjunct distributions in various organisms have been a central 57 issue in biogeography (e.g., Xiang et al., 1998; Wen, 2001; Qian and Ricklefs, 2004; Wang et 58 al., 2012; Wen et al., 2013, 2019). Much discussion has focused on two mechanisms: 59 vicariance and long-distance dispersal (Doyle et al., 2004; Givnish and Renner, 2004; Yoder 60 and Nowak, 2006; Šarhanová et al., 2017; Wang et al., 2020). The emergence of geographic 61 barriers has led to vicariance, resulting in decreased gene flow; while long-distance dispersal 62 in plants usually involves rare events driven by dispersal vectors such as animals, wind or 63 water currents (Nathan et al., 2008). Recent molecular systematic studies have shown that 64 many plant disjunctions are too young to be explained by continental drift or major 65 geographic barriers (Doyle et al., 2004; Mummenhoff et al., 2004; Yoder and Nowak, 2006; 66 Linder et al., 2013; Thomas et al., 2014, 2017; Jiang et al., 2019). Hence, long-distance 67 dispersal has emerged as a major mechanism to explain many discontinuous distributions in 68 historical geography (Wen et al., 2013; Ye et al., 2019; Wen and Wagner, 2020). 69 Biogeographic disjunctions between mainland China and Taiwan have received 70 considerable attention with the separation of the two regions by 130 km (Wu and Wang, 2001; 71 Xiang and Soltis, 2001; Qiu et al., 2011; Chen et al., 2012; Ye et al., 2014). Taiwan is the 72 largest subtropical mountainous island in the monsoonal western Pacific region, located on 73 the Tropic of Cancer and originating in the late Miocene (ca. 9-5 million years ago; Sibuet 74 and Hsu, 2004). Molecular phylogenetic analyses have shown that several plant lineages have 75 disjunct distributions between mainland China and Taiwan (e.g., Sassafras J. Presl, Nie et al., 76 2007; Pseudotsuga Carrière, Wei et al., 2010; Triplostegia Wall. ex DC., Niu et al., 2018). 77 Geologically, Taiwan and its adjacent continental margin of China belong to the Eurasian 78 plate; in the Late Cretaceous both of these were part of the continental block. The continental 79 block has undergone many extensions and rifting events since the Paleocene (Zhang, 1995; 80 Suo et al., 2015). Two hypotheses have been proposed to explain the formation of current 81 plant disjunctions in this region: long-distance dispersal and postglacial contraction (Chou et 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted April 14, 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. 82 al., 2011; Wang et al., 2013; Ye et al., 2014; Niu et al., 2018). A phylogeographic study of 83 Cunninghamia R.Br. ex A.Rich. (Taxodiaceae) revealed that populations in Taiwan were 84 derived from continental Asia via long-distance seed dispersal (Lu et al., 2001). Factors that 85 have had major impacts on population dynamics and genetic variation patterns in plants 86 include past geological and climatic changes, uplift of the Qinghai-Tibet Plateau, global 87 optimum temperature since the Miocene and the Quaternary glacial-interglacial transition 88 (Xu et al., 2015; Cao et al., 2016; Chen et al., 2020). Recent studies have suggested that 89 although the ice sheet was not ubiquitous from the Qinling Mountains and Huai River (at ca. 90 34° N) to the tropical south (≤ 22° N) in China during the Last Glacial period, the 91 temperature in most parts of mainland China was lower than today (Shi et al., 2006). 92 Temperature changes influence species distribution, population sizes, and intraspecific 93 genetic differentiation. The postglacial contraction hypothesis states that many species had a 94 continuous distribution from mainland China to Taiwan during the Quaternary glacial period, 95 sometimes with disjunctions between the Himalaya-Hengduan Mountain region and Taiwan 96 occurring when taxa migrated to higher altitudes as global temperatures increased (Chen and 97 Ying, 2012). 98 Abelia R.Br. belongs to the subfamily Linnaeoideae Raf. within Caprifoliaceae s.l. 99 (Dipsacales; Yang and Landrein, 2011; Caprifoliaceae; Wang et al., 2021). The genus 100 includes A. chinensis (four varieties), A. forrestii (two varieties), A. schumannii, A. macrotera 101 (eight varieties) and A. uniflora (Landrein et al., 2017; 2020; Fig. 1). Abelia is a typical East 102 Asian endemic genus with a disjunct distribution between mainland China and Taiwan, 103 mainly distributed in southwestern China, extending to eastern Taiwan and the Ryukyu 104 Islands of Japan. The genus includes an important ornamental species, Abelia × grandiflora, 105 widely cultivated in the yards, parks and roadsides of temperate cities (e.g., Beijing, London, 106 Wuhan and Washington D.C; Fig. 1). However, the phylogenetic relationships within Abelia 107 remain controversial due to limited markers and sampling, and hence the biogeographic 108 history and process of speciation are still unclear. Kim (1998) used one nuclear (ITS) and one 109 plastid (matK) marker to infer the phylogenetic relationships within Abelia. However, species 5 bioRxiv preprint doi: https://doi.org/10.1101/2021.04.13.439739; this version posted April 14, 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.
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