Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing

doi:10.1016/j.pld.2024.02.004

Plant Diversity ›› 2024, Vol. 46 ›› Issue (02): 169-180.DOI: 10.1016/j.pld.2024.02.004

Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing

Yumeng Ren^a, Lushui Zhang^a, Xuchen Yang^a,c, Hao Lin^a, Yupeng Sang^a, Landi Feng^a, Jianquan Liu^a,b, Minghui Kang^a,b

a. Key Laboratory of Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China;
b. State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, China;
c. Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design, Guangzhou Key Laboratory of Crop Gene Editing, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510006, China

收稿日期:2023-11-02 修回日期:2024-02-05 出版日期:2024-03-25 发布日期:2024-04-07
通讯作者: Jianquan Liu,E-mail:liujq@nwipb.ac.cn;Minghui Kang,E-mail:kangminghui0106@gmail.com
基金资助:
This study was supported by the Second Tibetan Plateau Scientific Expedition and Research program (No. 2019QZKK0502), Strategic Priority Research Program of Chinese Academy of Sciences (No. XDB31010300), Fundamental Research Funds for the Central Universities, and International Collaboration 111 Program (BP0719040).

Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing

Yumeng Ren^a, Lushui Zhang^a, Xuchen Yang^a,c, Hao Lin^a, Yupeng Sang^a, Landi Feng^a, Jianquan Liu^a,b, Minghui Kang^a,b

a. Key Laboratory of Bio-resource and Eco-environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, China;
b. State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystem, College of Ecology, Lanzhou University, Lanzhou 730000, China;
c. Guangdong Provincial Key Laboratory of Plant Adaptation and Molecular Design, Guangzhou Key Laboratory of Crop Gene Editing, Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510006, China

Received:2023-11-02 Revised:2024-02-05 Online:2024-03-25 Published:2024-04-07
Contact: Jianquan Liu,E-mail:liujq@nwipb.ac.cn;Minghui Kang,E-mail:kangminghui0106@gmail.com
Supported by:
This study was supported by the Second Tibetan Plateau Scientific Expedition and Research program (No. 2019QZKK0502), Strategic Priority Research Program of Chinese Academy of Sciences (No. XDB31010300), Fundamental Research Funds for the Central Universities, and International Collaboration 111 Program (BP0719040).

摘要/Abstract

摘要： The identification and understanding of cryptic intraspecific evolutionary units (lineages) are crucial for planning effective conservation strategies aimed at preserving genetic diversity in endangered species. However, the factors driving the evolution and maintenance of these intraspecific lineages in most endangered species remain poorly understood. In this study, we conducted resequencing of 77 individuals from 22 natural populations of Davidia involucrata, a “living fossil” dove tree endemic to central and southwest China. Our analysis revealed the presence of three distinct local lineages within this endangered species, which emerged approximately 3.09 and 0.32 million years ago. These divergence events align well with the geographic and climatic oscillations that occurred across the distributional range. Additionally, we observed frequent hybridization events between the three lineages, resulting in the formation of hybrid populations in their adjacent as well as disjunct regions. These hybridizations likely arose from climate-driven population expansion and/or long-distance gene flow. Furthermore, we identified numerous environment-correlated gene variants across the total and many other genes that exhibited signals of positive evolution during the maintenance of two major local lineages. Our findings shed light on the highly dynamic evolution underlying the remarkably similar phenotype of this endangered species. Importantly, these results not only provide guidance for the development of conservation plans but also enhance our understanding of evolutionary past for this and other endangered species with similar histories.

关键词: Davidia involucrata, Cryptic lineage, Hybridization, Population genomics, Positive evolution

Abstract: The identification and understanding of cryptic intraspecific evolutionary units (lineages) are crucial for planning effective conservation strategies aimed at preserving genetic diversity in endangered species. However, the factors driving the evolution and maintenance of these intraspecific lineages in most endangered species remain poorly understood. In this study, we conducted resequencing of 77 individuals from 22 natural populations of Davidia involucrata, a “living fossil” dove tree endemic to central and southwest China. Our analysis revealed the presence of three distinct local lineages within this endangered species, which emerged approximately 3.09 and 0.32 million years ago. These divergence events align well with the geographic and climatic oscillations that occurred across the distributional range. Additionally, we observed frequent hybridization events between the three lineages, resulting in the formation of hybrid populations in their adjacent as well as disjunct regions. These hybridizations likely arose from climate-driven population expansion and/or long-distance gene flow. Furthermore, we identified numerous environment-correlated gene variants across the total and many other genes that exhibited signals of positive evolution during the maintenance of two major local lineages. Our findings shed light on the highly dynamic evolution underlying the remarkably similar phenotype of this endangered species. Importantly, these results not only provide guidance for the development of conservation plans but also enhance our understanding of evolutionary past for this and other endangered species with similar histories.

Key words: Davidia involucrata, Cryptic lineage, Hybridization, Population genomics, Positive evolution

Yumeng Ren, Lushui Zhang, Xuchen Yang, Hao Lin, Yupeng Sang, Landi Feng, Jianquan Liu, Minghui Kang. Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing[J]. Plant Diversity, 2024, 46(02): 169-180.

参考文献

[1] Adams, M., Raadik, T.A., Burridge, C.P., et al., 2014. Global biodiversity assessment and hyper-cryptic species complexes:more than one species of elephant in the room? Syst. Biol. 63, 518-533.
[2] Al-Younis, I., Moosa, B., Kwiatkowski, M., et al., 2021. Functional crypto-adenylate cyclases operate in complex plant proteins. Front. Plant Sci. 12, 711749.
[3] Alexa, A., Rahnenfuhrer, J., 2022. topGO:Enrichment Analysis for Gene Ontology. R Package Version 2.48.0.
[4] Alexander, D.H., Lange, K., 2011. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12, 1-6.
[5] Allendorf, F.W., Hohenlohe, P.A., Luikart, G., 2010. Genomics and the future of conservation genetics. Nat. Rev. Genet. 11, 697-709.
[6] An, Z., Kutzbach, J.E., Prell, W.L., et al., 2001. Evolution of Asian monsoons and phased uplift of the Himalaya-Tibetan plateau since Late Miocene times. Nature 411, 62-66.
[7] Babbar, R., Tiwari, L.D., Mishra, R.C., et al., 2023. Arabidopsis plants overexpressing additional copies of heat shock protein Hsp101 showed high heat tolerance and endo-gene silencing. Plant Sci. 330, 111639.
[8] Bartrina, I., Jensen, H., Novak, O., et al., 2017. Gain-of-function mutants of the cytokinin receptors AHK2 and AHK3 regulate plant organ size, flowering time and plant longevity. Plant Physiol. 173, 1783-1797.
[9] Bencivenga, S., Serrano-Mislata, A., Bush, M., et al., 2016. Control of oriented tissue growth through repression of organ boundary genes promotes stem morphogenesis. Dev. Cell 39, 198-208.
[10] Bickford, D., Lohman, D.J., Sodhi, N.S., et al., 2007. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22, 148-155.
[11] Bolnick, D.I., Svanback, R., Fordyce, J.A., et al., 2003. The ecology of individuals:incidence and implications of individual specialization. Am. Nat. 161, 1-28.
[12] Brodersen, J., Seehausen, O., 2014. Why evolutionary biologists should get seriously involved in ecological monitoring and applied biodiversity assessment programs. Evol. Appl. 7, 968-983.
[13] Browning, S.R., Browning, B.L., 2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am. J. Hum. Genet. 81, 1084-1097.
[14] Camacho, C., Coulouris, G., Avagyan, V., et al., 2009. BLAST+:architecture and applications. BMC Bioinformatics 10, 1-9.
[15] Cao, Y.N., Zhu, S.S., Chen, J., et al., 2020. Genomic insights into historical population dynamics, local adaptation, and climate change vulnerability of the East Asian Tertiary relict Euptelea (Eupteleaceae). Evol. Appl. 13, 2038-2055.
[16] Chen, H., Patterson, N., Reich, D., 2010. Population differentiation as a test for selective sweeps. Genome Res. 20, 393-402.
[17] Chen, J.M., Zhao, S.Y., Liao, Y.Y., et al., 2015. Chloroplast DNA phylogeographic analysis reveals significant spatial genetic structure of the relictual tree Davidia involucrata (Davidiaceae). Conserv. Genet. 16, 583-593.
[18] Chen, S., Zhou, Y., Chen, Y., et al., 2018. fastp:an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884-i890.
[19] Chen, J., Hao, Z., Guang, X., et al., 2019. Liriodendron genome sheds light on angiosperm phylogeny and species-pair differentiation. Nat. Plants 5, 18-25.
[20] Chen, Y., Ma, T., Zhang, L., et al., 2020. Genomic analyses of a "living fossil":The endangered dove-tree. Mol. Ecol. Resour. 20, 756-769.
[21] Chen, X., MacGregor, D.R., Stefanato, F.L., et al., 2023. A VEL3 histone deacetylase complex establishes a maternal epigenetic state controlling progeny seed dormancy. Nat. Commun. 14, 2220.
[22] Cingolani, P., Platts, A., Wang, L.L., et al., 2012. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff:SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80-92.
[23] Crandall, K.A., Bininda-Emonds, O.R., Mace, G.M., et al., 2000. Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15, 290-295.
[24] Cuevas-Velazquez, C.L., Vellosillo, T., Guadalupe, K., et al., 2021. Intrinsically disordered protein biosensor tracks the physical-chemical effects of osmotic stress on cells. Nat. Commun. 12, 5438.
[25] Danecek, P., Auton, A., Abecasis, G., et al., 2011. The variant call format and VCFtools. Bioinformatics 27, 2156-2158.
[26] Emms, D., Kelly, S., 2019. OrthoFinder2:fast and accurate phylogenomic orthology analysis from gene sequences. Genome Biol. 20, 238.
[27] Excoffier, L., Marchi, N., Marques, D.A., et al., 2021. fastsimcoal2:demographic inference under complex evolutionary scenarios. Bioinformatics 37, 4882-4885.
[28] Eyde, R.H., 1997. Fossil record and ecology of Nyssa (Cornaceae) Bot. Rev. 63, 97-123.
[29] Feckler, A., Zubrod, J.P., Thielsch, A., et al., 2014. Cryptic species diversity:an overlooked factor in environmental management? J. Appl. Ecol. 51, 958-967.
[30] Feng, L., Xu, Z.Y., Wang, L., 2019. Genetic diversity and demographic analysis of an endangered tree species Diplopanax stachyanthus in subtropical China:implications for conservation and management. Conserv. Genet. 20, 315-327.
[31] Fick, S.E., Hijmans, R.J., 2017. WorldClim 2:new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302-4315.
[32] Frankham, R., Ballou, J. D., & Briscoe, D. A., 2010. Introduction to Conservation Genetics (2nd ed.). Cambridge University Press, UK.
[33] Frichot, E., Francois, O., 2015. LEA:An R package for landscape and ecological association studies. Methods Ecol. Evol. 6, 925-929.
[34] Funk, W.C., McKay, J.K., Hohenlohe, P.A., et al., 2012. Harnessing genomics for delineating conservation units. Trends Ecol. Evol. 27, 489-496.
[35] He, Z.C., Li, J.Q., Wang, H.C., 2004. Karyomorphology of Davidia involucrata and Camptotheca acuminata, with special reference to their systematic positions. Bot. J. Linn. Soc. 144, 193-198.
[36] Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature 405, 907-913.
[37] Hewitt, G.M., 2004. Genetic consequences of climatic oscillations in the Quaternary. Phil. Trans. R. Soc. Lond. B-Biol. Sci. 359, 183-195.
[38] Hu, H., Yang, Y., Li, A., et al., 2022. Genomic divergence of Stellera chamaejasme through local selection across the Qinghai-Tibet Plateau and northern China. Mol. Ecol. 31, 4782-4796.
[39] Jorger, K.M., Schrodl, M., 2013. How to describe a cryptic species? Practical challenges of molecular taxonomy. Front. Zool. 10, 1-27.
[40] Kang, M., Fu, R., Zhang, P., et al., 2021. A chromosome-level Camptotheca acuminata genome assembly provides insights into the evolutionary origin of camptothecin biosynthesis. Nat. Commun. 12, 3531.
[41] Keightley, P.D., Jackson, B.C., 2018. Inferring the probability of the derived vs. the ancestral allelic state at a polymorphic site. Genetics 209, 897-906.
[42] Letunic, I., Bork, P., 2007. Interactive Tree Of Life (iTOL):an online tool for phylogenetic tree display and annotation. Bioinformatics 23, 127-128.
[43] Li, H., Durbin, R., 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760.
[44] Li, H., Durbin, R., 2011. Inference of human population history from individual whole-genome sequences. Nature 475, 493-496.
[45] Li, H., Handsaker, B., Wysoker, A., et al., 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079.
[46] Li, X., Li, Z., He, C., et al., 2012. Genetic diversity of the endangered Davidia involucrata by AFLP analysis. Acta Hort. Sin. 39, 992-998.
[47] Li, J.L., Zhong, L.L., Wang, J., et al., 2021. Genomic insights into speciation history and local adaptation of an alpine aspen in the Qinghai-Tibet Plateau and adjacent highlands. J. Syst. Evol. 59, 1220-1231.
[48] Liu, Q., Vetukuri, R.R., Xu, W., et al., 2019. Transcriptomic responses of dove tree (Davidia involucrata Baill.) to heat stress at the seedling stage. Forests 10, 656.
[49] Liu, P.L., Zhang, X., Mao, J.F., et al., 2020. The Tetracentron genome provides insight into the early evolution of eudicots and the formation of vessel elements. Genome Biol. 21, 1-30.
[50] Luo, S., He, Y., Ning, G., et al., 2011. Genetic diversity and genetic structure of different populations of the endangered species Davidia involucrata in China detected by inter-simple sequence repeat analysis. Trees 25, 1063-1071.
[51] Lynch, M., Conery, J., Burger, R., 1995. Mutation accumulation and the extinction of small populations. Am. Nat. 146, 489-518.
[52] Ma, Q., Du, Y. J., Chen, N., et al., 2015. Phylogeography of Davidia involucrata (Davidiaceae) inferred from cpDNA haplotypes and nSSR data. Syst. Bot. 40, 796-810.
[53] Malinova, I., Kunz, H.H., Alseekh, S., et al., 2014. Reduction of the cytosolic phosphoglucomutase in Arabidopsis reveals impact on plant growth, seed and root development, and carbohydrate partitioning. PloS One 9, e112468.
[54] Manchester, S.R., Chen, Z.D., An-Ming, L.U., et al., 2009. Eastern Asian endemic seed plant genera and their paleogeographic history throughout the Northern Hemisphere. J. Syst. Evol. 47, 1-42.
[55] Mao, K., Liu, J., 2012. Current 'relicts' more dynamic in history than previously thought. New Phytol. 196, 329-331.
[56] McKenna, A., Hanna, M., Banks, E., et al., 2010. The Genome Analysis Toolkit:a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.
[57] Moritz, C., 1994. Defining 'evolutionarily significant units' for conservation. Trends Ecol. Evol. 9, 373-375.
[58] Mou, W., Kao, Y.T., Michard, E., et al., 2020. Ethylene-independent signaling by the ethylene precursor ACC in Arabidopsis ovular pollen tube attraction. Nat. Commun. 11, 4082.
[59] Mourrain, P., Beclin, C., Elmayan, T., et al., 2000. Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533-542.
[60] Mu, W., Wei, J., Yang, T., et al., 2020. The draft genome assembly of the critically endangered Nyssa yunnanensis, a plant species with extremely small populations endemic to Yunnan Province, China. Gigabyte 1-12.
[61] Naciri, Y., Linder, H.P., 2015. Species delimitation and relationships:the dance of the seven veils. Taxon 64, 3-16.
[62] Oksanen, J., Blanchet, F., Kindt, R., et al., 2017. Vegan:community ecology package. https://cran.r-project.org/web/packages/vegan/index.html.
[63] Palsboell, P.J., Berube, M., Allendorf, F.W., 2007. Identification of management units using population genetic data. Trends Ecol. Evol. 22, 11-16.
[64] Pante, E., Puillandre, N., Viricel, A., et al., 2015. Species are hypotheses:avoid connectivity assessments based on pillars of sand. Mol. Ecol. 24, 525-544.
[65] Pauls, S.U., Nowak, C., Balint, M., et al., 2013. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 22, 925-946.
[66] Petit, R.J., El Mousadik, A., Pons, O., 1998. Identifying populations for conservation on the basis of genetic markers. Conserv. Biol. 12, 844-855.
[67] Petit, R.J., Aguinagalde, I., de Beaulieu, J.L., et al., 2003. Glacial refugia:hotspots but not melting pots of genetic diversity. Science 300, 1563-1565.
[68] Pfenninger, M., Schwenk, K., 2007. Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evol. Biol.7, 1-6.
[69] Price, MN, Dehal, et al., 2010. FastTree 2-Approximately Maximum-Likelihood trees for large alignments. PloS One 5, e9490.
[70] Purcell, S., Neale, B., Todd-Brown, K., et al., 2007. PLINK:a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575.
[71] Qi, X.S., Chen, C., Comes, H.P., et al., 2012. Molecular data and ecological niche modelling reveal a highly dynamic evolutionary history of the East Asian Tertiary relict Cercidiphyllum (Cercidiphyllaceae). New Phytol. 196, 617-630.
[72] Qiu, Y.X., Fu, C.X., Comes, H.P., 2011. Plant molecular phylogeography in China and adjacent regions:tracing the genetic imprints of Quaternary climate and environmental change in the world's most diverse temperate flora. Mol. Phylogenet. Evol. 59, 225-244.
[73] Robinson, J., Kyriazis, C.C., Yuan, S.C., et al., 2023. Deleterious variation in natural populations and implications for conservation genetics. Annu. Rev. Anim. Biosci. 11, 93-114.
[74] Sang, Y., Long, Z., Dan, X., et al., 2022. Genomic insights into local adaptation and future climate-induced vulnerability of a keystone forest tree in East Asia. Nat. Commun. 13, 6541.
[75] Scheffers, B.R., Joppa, L.N., Pimm, S.L., et al., 2012. What we know and don't know about Earth's missing biodiversity. Trends Ecol. Evol. 27, 501-510.
[76] Schluter, D., 2000. The ecology of adaptive radiation Oxford Univ. Press Inc., New York, pp. 1-288.
[77] Seehausen, O., 2009. Speciation affects ecosystems. Nature 458, 1122-1123.
[78] Shang, H.Y., Li, Z.H., Dong, M., et al., 2015. Evolutionary origin and demographic history of an ancient conifer (Juniperus microsperma) in the Qinghai-Tibetan Plateau. Sci. Rep. 5, 10216.
[79] Shen, Y., Xia, H., Tu, Z., et al., 2022. Genetic divergence and local adaptation of Liriodendron driven by heterogeneous environments. Mol. Ecol. 31, 916-933.
[80] Song, C., Bao, M., 2006. Genetic diversity of RAPD mark for natural Davidia involucrata populations. Front. For. China 1, 95-99.
[81] Stamatakis, A., 2014. RAxML version 8:a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30,1312-1313.
[82] Staneloni, R.J., Rodriguez-Batiller, M.J., Legisa, D., et al., 2009. Bell-like homeodomain selectively regulates the high-irradiance response of phytochrome A. Proc. Natl. Acad. Sci. U.S.A. 106, 13624-13629.
[83] Sun, J.F., Gong, Y.B., Renner, S.S., et al., 2008. Multifunctional bracts in the dove tree Davidia involucrata (Nyssaceae:Cornales):rain protection and pollinator attraction. Am. Nat. 171, 119-124.
[84] Tang, C.Q., Dong, Y.F., Herrando-Moraira, S., et al., 2017. Potential effects of climate change on geographic distribution of the Tertiary relict tree species Davidia involucrata in China. Sci. Rep. 7, 43822.
[85] Torres-Cambas, Y., Ferreira, S., Cordero-Rivera, A., et al., 2017. Identification of evolutionarily significant units in the Cuban endemic damselfly Hypolestes trinitatis (Odonata:Hypolestidae). Conserv. Genet. 18, 1229-1234.
[86] Treffon, P., Rossi, J., Gabellini, G., et al., 2022. Proteome profiling of a S-Nitrosoglutathione reductase (GSNOR) null mutant reveals that aldo-keto reductases form a new class of enzymes involved in nitric oxide homeostasis. FASEB J. 36, 1.
[87] Velinov, V., Vaseva, I., Zehirov, G., et al., 2020. Overexpression of the NMig1 gene encoding a NudC domain protein enhances root growth and abiotic stress tolerance in Arabidopsis thaliana. Front. Plant Sci. 11, 815.
[88] Wang, L., Abbott, R.J., Zheng, W., et al., 2009. History and evolution of alpine plants endemic to the Qinghai-Tibetan Plateau:Aconitum gymnandrum (Ranunculaceae). Mol. Ecol. 18, 709-721.
[89] Wang, Z.W., Chen, S.T., Nie, Z.L., et al., 2015. Climatic factors drive population divergence and demography:insights based on the phylogeography of a riparian plant species endemic to the Hengduan Mountains and adjacent regions. PLoS One 10, e0145014.
[90] Wang, Z., Jiang, Y., Bi, H., et al., 2021. Hybrid speciation via inheritance of alternate alleles of parental isolating genes. Mol. Plant. 14, 208-222.
[91] Wu, Y., Yang, J., Yang, Y., et al., 2023. The genome sequence and demographic history of Przewalskia tangutica (Solanaceae), an endangered alpine plant on the Qinghai-Tibet Plateau. DNA Res. 30, dsad005.
[92] Xue, Y., Prado-Martinez, J., Sudmant, P.H., et al., 2015. Mountain gorilla genomes reveal the impact of long-term population decline and inbreeding. Science 348, 242-245.
[93] Yang, X., Kang, M., Yang, Y., et al., 2019. A chromosome-level genome assembly of the Chinese tupelo Nyssa sinensis. Sci. Data 6, 282.
[94] Yang, Y., Zhang, L., Huang, X., et al., 2020. Response of photosynthesis to different concentrations of heavy metals in Davidia involucrata. PLoS One 15, e0228563.
[95] Zachos, J., Pagani, M., Sloan, L., et al., 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686-693.
[96] Zdobnov, E.M., Apweiler, R., 2001. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17, 847-848.
[97] Zhang, Q., Guo, Q., Xu, D., et al., 2000. Influence of climate changes on geographical distribution of Davidia involucrata, a precious and endangered species native to China. Sci. Silvae Sin. 36, 47-52.
[98] Zhang, C., Dong, S.S., Xu, J.Y., et al., 2019. PopLDdecay:a fast and effective tool for linkage disequilibrium decay analysis based on variant call format files. Bioinformatics 35, 1786-1788.
[99] Zhang, X., Sun, Y., Landis, J.B., et al., 2020. Genomic insights into adaptation to heterogeneous environments for the ancient relictual Circaeaster agrestis (Circaeasteraceae, Ranunculales). New Phytol. 228, 285-301.
[100] Zhang, C., Zhao, S., Li, Y.S., et al., 2022. Crystal structures of Arabidopsis thaliana GDP-D-Mannose pyrophosphorylase VITAMIN c DEFECTIVE 1. Front. Plant Sci. 13, 899738.
[101] Zhao, Y.P., Fan, G., Yin, P.P., et al., 2019. Resequencing 545 ginkgo genomes across the world reveals the evolutionary history of the living fossil. Nat. Commun. 10, 4201.
[102] Zhu, S., Chen, J., Zhao, J., et al., 2020. Genomic insights on the contribution of balancing selection and local adaptation to the long-term survival of a widespread living fossil tree, Cercidiphyllum japonicum. New Phytol. 228, 1674-1689.

Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing

Cryptic divergences and repeated hybridizations within the endangered “living fossil” dove tree (Davidia involucrata) revealed by whole genome resequencing

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