Integrated phylogenomic analyses unveil reticulate evolution in Parthenocissus (Vitaceae), highlighting speciation dynamics in the Himalayan-Hengduan Mountains.
Parthenocissus
Himalayan-Hengduan Mountains region
biogeography
comprehensive approach
phylogenetic discordance
reticulation
speciation reversal
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
04 2023
04 2023
Historique:
received:
09
08
2022
accepted:
19
10
2022
pubmed:
29
10
2022
medline:
21
3
2023
entrez:
28
10
2022
Statut:
ppublish
Résumé
Hybridization caused by frequent environmental changes can lead both to species diversification (speciation) and to speciation reversal (despeciation), but the latter has rarely been demonstrated. Parthenocissus, a genus with its trifoliolate lineage in the Himalayan-Hengduan Mountains (HHM) region showing perplexing phylogenetic relationships, provides an opportunity for investigating speciation dynamics based on integrated evidence. We investigated phylogenetic discordance and reticulate evolution in Parthenocissus based on rigorous analyses of plastome and transcriptome data. We focused on reticulations in the trifoliolate lineage in the HHM region using a population-level genome resequencing dataset, incorporating evidence from morphology, distribution, and elevation. Comprehensive analyses confirmed multiple introgressions within Parthenocissus in a robust temporal-spatial framework. Around the HHM region, at least three hybridization hot spots were identified, one of which showed evidence of ongoing speciation reversal. We present a solid case study using an integrative methodological approach to investigate reticulate evolutionary history and its underlying mechanisms in plants. It demonstrates an example of speciation reversal through frequent hybridizations in the HHM region, which provides new perspectives on speciation dynamics in mountainous areas with strong topographic and environmental heterogeneity.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
888-903Informations de copyright
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation. This article has been partially contributed to by US Government employees and their work is in the public domain in the USA.
Références
Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, Boughman J, Brelsford A, Buerkle CA, Buggs R et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26: 229-246.
Andersen MJ, McCullough JM, Gyllenhaal EF, Mapel XM, Haryoko T, Jønsson KA, Joseph L. 2021. Complex histories of gene flow and a mitochondrial capture event in a nonsister pair of birds. Molecular Ecology 30: 2087-2103.
Antonelli A, Kissling WD, Flantua SGA, Bermúdez MA, Mulch A, Muellner-Riehl AN, Kreft H, Linder HP, Badgley C, Fjeldså J et al. 2018. Geological and climatic influences on mountain biodiversity. Nature Geoscience 11: 718-725.
Ané C, Larget B, Baum DA, Smith SD, Rokas A. 2007. Bayesian estimation of concordance among gene trees. Molecular Biology and Evolution 24: 412-426.
Arcila D, Ortí G, Vari R, Armbruster JW, Stiassny MLJ, Ko KD, Sabaj MH, Lundberg J, Revell LJ, Betancur RR. 2017. Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. Nature Ecology and Evolution 1: 0020.
Barraclough TG, Nee S. 2001. Phylogenetics and speciation. Trends in Ecology & Evolution 16: 391-399.
Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological) 57: 289-300.
Blackmon H, Adams RA. 2015. EvobiR: tools for comparative analyses and teaching evolutionary biology. Zenodo. doi: 10.5281/zenodo.30938.
Blair C, Ané C. 2020. Phylogenetic trees and networks can serve as powerful and complementary approaches for analysis of genomic data. Systematic Biology 69: 593-601.
Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114-2120.
Brizicky GK. 1965. The genera of Vitaceae in the southeastern United States. Journal of the Arnold Arboretum 46: 48-67.
Budenhagen C, Lemmon AR, Lemmon EM, Bruhl J, Cappa J, Clement WL, Donoghue M, Edwards EJ, Hipp AL, Kortyna M et al. 2016. Anchored phylogenomics of angiosperms I: assessing the robustness of phylogenetic estimates. bioRxiv. doi: 10.1101/086298.
Cai LM, Xi ZX, Lemmon EM, Lemmon AR, Mast A, Buddenhagen CE, Liu L, Davis CC. 2021. The perfect storm: gene tree estimation error, incomplete lineage sorting, and ancient gene flow explain the most recalcitrant ancient angiosperm clade, Malpighiales. Systematic Biology 70: 491-507.
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972-1973.
Chen IJ, Manchester SR. 2007. Seed morphology of modern and fossil Ampelocissus (Vitaceae) and implications for phytogeography. American Journal of Botany 94: 1534-1553.
Chen IJ. 2009. Biogeographic history of Vitaceae inferred from morphological phylogeny and the fossil record of seeds. PhD thesis, University of Florida, Gainesville, FL, USA.
Chen ZD, Ren H, Wen J. 2007. Vitaceae. In: Wu ZY, Hong DY, Raven PH, eds. Flora of China. Beijing, China; St Louis, MO, USA: Science Press; Missouri Botanical Garden, 173-222.
Chernomor O, Von Haeseler A, Minh BQ. 2016. Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65: 997-1008.
Chifman J, Kubatko L. 2014. Quartet inference from SNP data under the coalescent model. Bioinformatics 30: 3317-3324.
Cristina Acosta M, Premoli AC. 2010. Evidence of chloroplast capture in South American Nothofagus (subgenus Nothofagus, Nothofagaceae). Molecular Phylogenetics and Evolution 54: 235-242.
Dong SS, Wang YL, Xia NH, Liu Y, Liu M, Lian L, Li N, Li LF, Lang XA, Gong YQ et al. 2021. Plastid and nuclear phylogenomic incongruences and biogeographic implications of Magnolia s.l. (Magnoliaceae). Journal of Systematics and Evolution 60: 1-15.
Drew BT, Sytsma KJ. 2013. The South American radiation of Lepechinia (Lamiaceae): phylogenetics, divergence times and evolution of dioecy. Botanical Journal of the Linnean Society 171: 171-190.
Durand EY, Patterson N, Reich D, Slatkin M. 2011. Testing for ancient admixture between closely related populations. Molecular Biology and Evolution 28: 2239-2252.
Earl DA, VonHoldt BM. 2012. Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genetics Resources 4: 359-361.
Edelman NB, Frandsen PB, Miyagi M, Clavijo B, Davey J, Dikow RB, García-accinelli G, Van Belleghem SM, Patterson N, Neafsey DE et al. 2019. Genomic architecture and introgression shape a butterfly radiation. Science 366: 594-599.
Emms DM, Kelly S. 2015. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology 16: 157.
Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology 14: 2611-2620.
Favre A, Päckert M, Pauls SU, Jähnig SC, Uhl D, Michalak I, Muellner-Riehl AN. 2015. The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biological Reviews 90: 236-253.
Ferreira MS, Jones MR, Callahan CM, Farelo L, Tolesa Z, Suchentrunk F, Boursot P, Mills LS, Alves PC, Good JM et al. 2021. The legacy of recurrent introgression during the radiation of hares. Systematic Biology 70: 593-607.
Gao J, Wang BH, Mao JF, Ingvarsson P, Zeng QY, Wang XR. 2012. Demography and speciation history of the homoploid hybrid pine Pinus densata on the Tibetan Plateau. Molecular Ecology 21: 4811-4827.
GBIF.org. 2016. GBIF occurrence download. doi: 10.15468/dl.5tcbur.
Gilman RT, Behm JE. 2011. Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation. Evolution 65: 2592-2605.
Gompert Z, Buerkle CA. 2016. What, if anything, are hybrids: enduring truths and challenges associated with population structure and gene flow. Evolutionary Applications 9: 909-923.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644-652.
Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai WW, Fritz MHY et al. 2010. A draft sequence of the Neandertal genome. Science 328: 710-722.
Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M et al. 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8: 1494-1512.
Harrell FE Jr. 2021. Hmisc: Harrell miscellaneous. R package v.4.6-0. [WWW document] URL https://CRAN.R-project.org/package=Hmisc [accessed 24 September 2022].
Hejase HA, Liu KJ. 2016. A scalability study of phylogenetic network inference methods using empirical datasets and simulations involving a single reticulation. BMC Bioinformatics 17: 422.
Hoang DT, Chernomor O, Von Haeseler A, Minh BQ, Vinh LS. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518-522.
Hu HH, Ye JF, Liu B, Mao LF, Smith SA, Barrett RL, Soltis PS, Soltis DE, Chen ZD, Lu LM. 2022. Temporal and spatial comparisons of angiosperm diversity between eastern Asia and North America. National Science Review 9: nwab199.
Huang DI, Hefer CA, Kolosova N, Douglas CJ, Cronk QCB. 2014. Whole plastome sequencing reveals deep plastid divergence and cytonuclear discordance between closely related balsam poplars, Populus balsamifera and P. trichocarpa (Salicaceae). New Phytologist 204: 693-703.
Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution 23: 254-267.
Jacobsen F, Omland KE. 2011. Increasing evidence of the role of gene flow in animal evolution: hybrid speciation in the yellow-rumped warbler complex. Molecular Ecology 20: 2236-2239.
Jansen RK, Kaittanis C, Saski C, Lee S-B, Tomkins J, Alverson AJ, Daniell H. 2006. Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evolutionary Biology 6: 32.
Jiang XL, An M, Zheng SS, Deng M, Su ZH. 2018. Geographical isolation and environmental heterogeneity contribute to the spatial genetic patterns of Quercus kerrii (Fagaceae). Heredity 120: 219-233.
Johnson MG, Gardner EM, Liu Y, Medina R, Goffinet B, Shaw AJ, Zerega NJC, Wickett NJ. 2016. HybPiper: extracting coding sequence and introns for phylogenetics from high-throughput sequencing reads using target enrichment. Applications in Plant Sciences 4: 1600016.
Kalyaanamoorthy S, Minh BQ, Wong TKF, Von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587-589.
Karimi N, Grover CE, Gallagher JP, Wendel JF, Ané C, Baum DA. 2020. Reticulate evolution helps explain apparent homoplasy in floral biology and pollination in baobabs (Adansonia; Bombacoideae; Malvaceae). Systematic Biology 69: 462-478.
Katoh K, Standley DM. 2013. Mafft multiple sequence alignment software v.7: improvements in performance and usability. Molecular Biology and Evolution 30: 772-780.
Kearns AM, Restani M, Szabo I, Schrøder-Nielsen A, Kim JA, Richardson HM, Marzluff JM, Fleischer RC, Johnsen A, Omland KE. 2018. Genomic evidence of speciation reversal in ravens. Nature Communications 9: 906.
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649.
Larget BR, Kotha SK, Dewey CN, Ané C. 2010. BUCKy: gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26: 2910-2911.
Li JL, Milne RI, Ru DF, Miao JB, Tao WJ, Zhang L, Xu JJ, Liu JQ, Mao KS. 2020. Allopatric divergence and hybridization within Cupressus chengiana (Cupressaceae), a threatened conifer in the northern Hengduan Mountains of western China. Molecular Ecology 29: 1250-1266.
Li SH, Ji XP, Harrison T, Deng CL, Wang SQ, Wang LR, Zhu RX. 2020. Uplift of the Hengduan Mountains on the southeastern margin of the Tibetan Plateau in the late Miocene and its paleoenvironmental impact on hominoid diversity. Palaeogeography, Palaeoclimatology, Palaeoecology 553: 109794.
Li WZ, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658-1659.
Linder CR, Rieseberg LH. 2004. Reconstructing patterns of reticulate evolution in plants. American Journal of Botany 91: 1700-1708.
Liu J, Möller M, Provan J, Gao LM, Poudel RC, Li DZ. 2013. Geological and ecological factors drive cryptic speciation of yews in a biodiversity hotspot. New Phytologist 199: 1093-1108.
Liu L, Yu LL. 2010. Phybase: an R package for species tree analysis. Bioinformatics 26: 962-963.
Lu LM, Cox CJ, Mathews S, Wang W, Wen J, Chen ZD. 2018. Optimal data partitioning, multispecies coalescent and Bayesian concordance analyses resolve early divergences of the grape family (Vitaceae). Cladistics 34: 57-77.
Lu LM, Wen J, Chen ZD. 2012. A combined morphological and molecular phylogenetic analysis of Parthenocissus (Vitaceae) and taxonomic implications. Botanical Journal of the Linnean Society 168: 43-63.
Ma ZY, Nie ZL, Ren C, Liu XQ, Zimmer EA, Wen J. 2021. Phylogenomic relationships and character evolution of the grape family (Vitaceae). Molecular Phylogenetics and Evolution 154: 106948.
Manish K, Pandit MK. 2018. Geophysical upheavals and evolutionary diversification of plant species in the Himalaya. PeerJ 6: e5919.
Martin SH, Davey JW, Jiggins CD. 2015. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Molecular Biology and Evolution 32: 244-257.
Meng HH, Su T, Gao XY, Li J, Jiang XL, Sun H, Zhou ZK. 2017. Warm-cold colonization: response of oaks to uplift of the Himalaya-Hengduan Mountains. Molecular Ecology 26: 3276-3294.
Mirarab S, Reaz R, Bayzid MS, Zimmermann T, Swenson SM, Warnow T. 2014. Astral: genome-scale coalescent-based species tree estimation. Bioinformatics 30: 541-548.
Moore MO, Wen J. 2016. Vitaceae. In: Flora of North America Editorial Committee, ed. Flora of North America, North of Mexico, Magnoliophyta: Vitaceae to Garryaceae. New York, NY, USA: Oxford University Press, 3-23.
Morales-Briones DF, Liston A, Tank DC. 2018. Phylogenomic analyses reveal a deep history of hybridization and polyploidy in the Neotropical genus Lachemilla (Rosaceae). New Phytologist 218: 1668-1684.
Morley RJ. 2003. Interplate dispersal paths for megathermal angiosperms. Perspectives in Plant Ecology, Evolution and Systematics 6: 5-20.
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. 2015. IQ-Tree: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268-274.
Nie JS, Ruetenik G, Gallagher K, Hoke G, Garzione CN, Wang WT, Stockli D, Hu XF, Wang Z, Wang Y et al. 2018. Rapid incision of the Mekong River in the middle Miocene linked to monsoonal precipitation. Nature Geoscience 11: 944-948.
Nie ZL, Sun H, Chen ZD, Meng Y, Manchester SR, Wen J. 2010. Molecular phylogeny and biogeographic diversification of Parthenocissus (Vitaceae) disjunct between Asia and North America. American Journal of Botany 97: 1342-1353.
Niu YT, Jabbour F, Barrett RL, Ye JF, Zhang ZZ, Lu KQ, Lu LM, Chen ZD. 2018. Combining complete chloroplast genome sequences with target loci data and morphology to resolve species limits in Triplostegia (Caprifoliaceae). Molecular Phylogenetics and Evolution 129: 15-26.
Norell MA. 1993. Tree-based approaches to understanding history: comments on ranks, rules, and the quality of the fossil record. American Journal of Science 293 A: 407-417.
Nylander JAA. 2004. MrModeltest, h.2. Program distributed by the author. Uppsala, Sweden: Evolutionary Biology Centre, Uppsala University. [WWW document] URL https://github.com/nylander/MrModeltest2 [accessed 16 July 2022].
Okuyama Y, Fujii N, Wakabayashi M, Kawakita A, Ito M, Watanabe M, Murakami N, Kato M. 2005. Nonuniform concerted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (Saxifragaceae). Molecular Biology and Evolution 22: 285-296.
Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T, Keane JA, Harris SR. 2016. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microbial Genomics 2: e000056.
Pavón-Vázquez CJ, Brennan IG, Keogh JS. 2021. A comprehensive approach to detect hybridization sheds light on the evolution of earth's largest lizards. Systematic Biology 70: 877-890.
Payseur BA, Rieseberg LH. 2016. A genomic perspective on hybridization and speciation. Molecular Ecology 25: 2337-2360.
Pritchard JK, Stephens M, Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, De Bakker PIW, Daly MJ et al. 2007. Plink: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics 81: 559-575.
Rieseberg LH, Soltis DE. 1991. Phylogenetic consequences of cytoplasmic. Evolutionary Trends in Plants 5: 65-84.
Rieseberg LH, Wendel JF. 1993. Introgression and its consequences in plants. In: Harrison RG, ed. Hybrid zones and the evolutionary process. New York, NY, USA: Oxford University Press, 70-100.
Robinson DF, Foulds LR. 1981. Comparison of phylogenetic trees. Mathematical Biosciences 53: 131-147.
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539-542.
Rose JP, Toledo CAP, Lemmon EM, Lemmon AR, Sytsma KJ. 2021. Out of sight, out of mind: widespread nuclear and plastid-nuclear discordance in the flowering plant genus Polemonium (Polemoniaceae) suggests widespread historical gene flow despite limited nuclear signal. Systematic Biology 70: 162-180.
Ru DF, Sun YS, Wang DL, Chen Y, Wang TJ, Hu QJ, Abbott RJ, Liu JQ. 2018. Population genomic analysis reveals that homoploid hybrid speciation can be a lengthy process. Molecular Ecology 27: 4875-4887.
Salichos L, Stamatakis A, Rokas A. 2014. Novel information theory-based measures for quantifying incongruence among phylogenetic trees. Molecular Biology and Evolution 31: 1261-1271.
Seehausen O, Takimoto G, Roy D, Jokela J. 2008. Speciation reversal and biodiversity dynamics with hybridization in changing environments. Molecular Ecology 17: 30-44.
Seehausen O. 2006. Conservation: losing biodiversity by reverse speciation. Current Biology 16: 334-337.
Sheldon ND, Retallack GJ. 2004. Regional paleoprecipitation records from the Late Eocene and Oligocene of North America. Journal of Geology 112: 487-494.
Smith SA, Moore MJ, Brown JW, Yang Y. 2015. Analysis of phylogenomic datasets reveals conflict, concordance, and gene duplications with examples from animals and plants. BMC Evolutionary Biology 15: 1-15.
Soltis PS, Soltis DE. 2009. The role of hybridization in plant speciation. Annual Review of Plant Biology 60: 561-588.
Solís-Lemus C, Ané C. 2016. Inferring phylogenetic networks with maximum pseudolikelihood under incomplete lineage sorting. PLoS Genetics 12: 1-21.
Solís-Lemus C, Bastide P, Ané C. 2017. PhyloNetworks: a package for phylogenetic networks. Molecular Biology and Evolution 34: 3292-3298.
Spicer RA, Farnsworth A, Su T. 2020. Cenozoic topography, monsoons and biodiversity conservation within the Tibetan Region: an evolving story. Plant Diversity 42: 229-254.
Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
Stenz NWM, Larget B, Baum DA, Ané C. 2015. Exploring tree-like and non-tree-like patterns using genome sequences: an example using the inbreeding plant species Arabidopsis thaliana (L.) Heynh. Systematic Biology 64: 809-823.
Swofford DL. 2002. Paup*. Phylogenetic analysis using parsimony (* and other methods), v.4. Sunderland, MA, USA: Sinauer Associates.
Thiers B. 2017. Index Herbariorum a global directory of public herbaria and associated staff. New York Botanical Garden's Virtual Herbarium. [WWW document] URL http://sweetgum.nybg.org/ih [accessed 24 May 2019].
Tiffney BH, Manchester SR. 2001. The use of geological and paleontological evidence in evaluating plant phylogeographic hypotheses in the Northern Hemisphere Tertiary. International Journal of Plant Sciences 162: S3-S17.
Tiffney BH. 1985. The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. Journal of the Arnold Arboretum 66: 243-273.
Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hübner S, Heredia SM, Hahn MA, Caseys C, Bock DG et al. 2016. Hybridization and extinction. Evolutionary Applications 9: 892-908.
vonHoldt BM, Kays R, Pollinger JP, Wayne RK. 2016. Admixture mapping identifies introgressed genomic regions in North American canids. Molecular Ecology 25: 2443-2453.
Wen J, Nie ZL, Ickert-Bond SM. 2016. Intercontinental disjunctions between eastern Asia and western North America in vascular plants highlight the biogeographic importance of the Bering land bridge from late Cretaceous to Neogene. Journal of Systematics and Evolution 54: 469-490.
Wen J, Nie ZL, Soejima A, Meng Y. 2007. Phylogeny of Vitaceae based on the nuclear GAI1 gene sequences. Canadian Journal of Botany 85: 731-745.
Wen J, Zhang JQ, Nie ZL, Zhong Y, Sun H. 2014. Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau. Frontiers in Genetics 5: 4.
Westerhold T, Marwan N, Drury AJ, Liebrand D, Agnini C, Anagnostou E, Barnet JSK, Bohaty SM, De Vleeschouwer D, Florindo F et al. 2020. An astronomically dated record of earth's climate and its predictability over the last 66 million years. Science 369: 1383-1388.
Whittemore AT, Schaal BA. 1991. Interspecific gene flow in sympatric oaks. Proceedings of the National Academy of Sciences, USA 88: 2540-2544.
Wu SD, Wang Y, Wang ZF, Shrestha N, Liu JQ. 2022. Species divergence with gene flow and hybrid speciation on the Qinghai-Tibet Plateau. New Phytologist 234: 392-404.
Wyman SK, Jansen RK, Boore JL. 2004. Automatic annotation of organellar genomes with Dogma. Bioinformatics 20: 3252-3255.
Yang ZH. 2007. Paml 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586-1591.
Yu Y, Dong JR, Liu KJ, Nakhleh L. 2014. Maximum likelihood inference of reticulate evolutionary histories. Proceedings of the National Academy of Sciences, USA 111: 16448-16453.
Yu Y, Harris AJ, Blair C, He XJ. 2015. Rasp (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Molecular Phylogenetics and Evolution 87: 46-49.
Yu Y, Nakhleh L. 2015. A maximum pseudo-likelihood approach for phylogenetic networks. BMC Genomics 16: 1-10.
Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Research 18: 821-829.
Zhang C, Rabiee M, Sayyari E, Mirarab S. 2018. Astral-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19: 15-30.
Zhang L, Thibert-Plante X, Ripa J, Svanbäck R, Brännström Å. 2019. Biodiversity loss through speciation collapse: mechanisms, warning signals, and possible rescue. Evolution 73: 1504-1516.
Zheng YC, Janke A. 2018. Gene flow analysis method, the D-statistic, is robust in a wide parameter space. BMC Bioinformatics 19: 10.