Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes

doi:10.1016/j.pld.2026.02.005

Plant Diversity ›› 2026, Vol. 48 ›› Issue (04): 747-765.DOI: 10.1016/j.pld.2026.02.005

• Articles • Previous Articles Next Articles

Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes

Gulbar Yisilam^a,b,c, Yu-Zhu Gao^a,b, Zuan Wei^a,b, Hans Peter Comes^d, Zheng Li^e, Pan Li^f,g, Xin-Min Tian^a,b

a. Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Ministry of Education) & Guangxi Key Laboratory of Landscape Resources Conservation and Sustainable Utilization in Lijiang River Basin, Guangxi Normal University, Guilin 541006, China;
b. University Engineering Research Center of Bioinformation and Genetic Improvement of Specialty Crops, Guangxi, Guilin 541006, China;
c. Laboratory of Systematic & Evolutionary Botany and Biodiversity, College of Life Sciences, Zhejiang University, Hangzhou 310058, China;
d. Department of Environment & Biodiversity, University of Salzburg, Salzburg, Austria;
e. Department of Biology, Miami University, Oxford, OH 45056, USA;
f. Key Laboratory of Biodiversity and Environment on the Qinghai-Tibetan Plateau, Ministry of Education, School of Ecology and Environment, Xizang University, Lhasa 850000, China;
g. Motuo Biodiversity Observation and Research Station of Xizang Autonomous Region, Motuo 860700, China

Received:2025-12-27 Revised:2026-02-03 Accepted:2026-02-06 Online:2026-02-16 Published:2026-07-25
Contact: Pan Li,E-mail:panli_zju@126.com;Xin-Min Tian,E-mail:tianxm333333@foxmail.com
Supported by:
This work was supported by the Key Research and Development Program of Guangxi Province of China (GuikeAB25069162, GuikeAB25069252), the National Natural Science Foundation of China (31760102, 32360058, 32570239), the Central Government Guides Local Science and Technology Development Projects (2023ZYZX1224), and Science and Technology Projects of Xizang Autonomous Region, China (XZ202402ZD0005). We would like to thank the University of Arizona Herbarium (ARIZ) and the Wisconsin State Herbarium (WIS) for providing Lycium specimens.

Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes

Gulbar Yisilam^a,b,c, Yu-Zhu Gao^a,b, Zuan Wei^a,b, Hans Peter Comes^d, Zheng Li^e, Pan Li^f,g, Xin-Min Tian^a,b

a. Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Ministry of Education) & Guangxi Key Laboratory of Landscape Resources Conservation and Sustainable Utilization in Lijiang River Basin, Guangxi Normal University, Guilin 541006, China;
b. University Engineering Research Center of Bioinformation and Genetic Improvement of Specialty Crops, Guangxi, Guilin 541006, China;
c. Laboratory of Systematic & Evolutionary Botany and Biodiversity, College of Life Sciences, Zhejiang University, Hangzhou 310058, China;
d. Department of Environment & Biodiversity, University of Salzburg, Salzburg, Austria;
e. Department of Biology, Miami University, Oxford, OH 45056, USA;
f. Key Laboratory of Biodiversity and Environment on the Qinghai-Tibetan Plateau, Ministry of Education, School of Ecology and Environment, Xizang University, Lhasa 850000, China;
g. Motuo Biodiversity Observation and Research Station of Xizang Autonomous Region, Motuo 860700, China

通讯作者: Pan Li,E-mail:panli_zju@126.com;Xin-Min Tian,E-mail:tianxm333333@foxmail.com
基金资助:
This work was supported by the Key Research and Development Program of Guangxi Province of China (GuikeAB25069162, GuikeAB25069252), the National Natural Science Foundation of China (31760102, 32360058, 32570239), the Central Government Guides Local Science and Technology Development Projects (2023ZYZX1224), and Science and Technology Projects of Xizang Autonomous Region, China (XZ202402ZD0005). We would like to thank the University of Arizona Herbarium (ARIZ) and the Wisconsin State Herbarium (WIS) for providing Lycium specimens.

Abstract

Abstract: The genus Lycium is of considerable medicinal and economic importance and has a discontinuous intercontinental distribution. However, its evolutionary history remains obscured by morphological convergence, hybridization, and incomplete lineage sorting (ILS). Here, we conducted the first phylogenomic study of Lycium, integrating three independent genomic compartments, single-copy nuclear genes, mitochondrial genomes, and published plastid data to reconstruct its history and dissect the roles of incomplete lineage sorting, hybridization, and long-distance dispersal in its evolution. Both concatenation and coalescence methods based on nuclear genes yielded a congruent, well-resolved phylogeny, strongly supporting the monophyly of Lycium and recovering five major clades with a North American lineage as sisters to all the others. This phylogeny reveals significant conflicts with the traditional morphology. Our analyses clarify the primary cause of two distinct types of conflict. First, the pervasive tripartite (nuclear-plastid-mitochondrial) topological discordance is primarily linked to historical hybridization and introgression events, as demonstrated by strong gene-flow signals and detailed network models. In contrast, the discordance observed among gene trees appears to be predominantly influenced by incomplete lineage sorting, with some nodes exhibiting peaks exceeding 60%, indicative of rapid radiation during the Miocene epoch. Divergence dating and ancestral area reconstruction support a North American origin in the early Miocene (∼21.84 Ma), followed by sequential long-distance dispersal to South America across the Pacific, Africa, and Eurasia. Collectively, our results establish a process-based framework for Lycium’s complex evolutionary history, highlighting the interplay of rapid radiation, quantified ILS, modeled hybridization, and bird-mediated dispersal in shaping its intercontinental distribution.

Key words: Phylogenomics, Reticulate evolution, Biogeography, Incomplete lineage sorting, Hybridization, Mitogenome

摘要： The genus Lycium is of considerable medicinal and economic importance and has a discontinuous intercontinental distribution. However, its evolutionary history remains obscured by morphological convergence, hybridization, and incomplete lineage sorting (ILS). Here, we conducted the first phylogenomic study of Lycium, integrating three independent genomic compartments, single-copy nuclear genes, mitochondrial genomes, and published plastid data to reconstruct its history and dissect the roles of incomplete lineage sorting, hybridization, and long-distance dispersal in its evolution. Both concatenation and coalescence methods based on nuclear genes yielded a congruent, well-resolved phylogeny, strongly supporting the monophyly of Lycium and recovering five major clades with a North American lineage as sisters to all the others. This phylogeny reveals significant conflicts with the traditional morphology. Our analyses clarify the primary cause of two distinct types of conflict. First, the pervasive tripartite (nuclear-plastid-mitochondrial) topological discordance is primarily linked to historical hybridization and introgression events, as demonstrated by strong gene-flow signals and detailed network models. In contrast, the discordance observed among gene trees appears to be predominantly influenced by incomplete lineage sorting, with some nodes exhibiting peaks exceeding 60%, indicative of rapid radiation during the Miocene epoch. Divergence dating and ancestral area reconstruction support a North American origin in the early Miocene (∼21.84 Ma), followed by sequential long-distance dispersal to South America across the Pacific, Africa, and Eurasia. Collectively, our results establish a process-based framework for Lycium’s complex evolutionary history, highlighting the interplay of rapid radiation, quantified ILS, modeled hybridization, and bird-mediated dispersal in shaping its intercontinental distribution.

关键词: Phylogenomics, Reticulate evolution, Biogeography, Incomplete lineage sorting, Hybridization, Mitogenome

Gulbar Yisilam, Yu-Zhu Gao, Zuan Wei, Hans Peter Comes, Zheng Li, Pan Li, Xin-Min Tian. Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes[J]. Plant Diversity, 2026, 48(04): 747-765.

References

[1] Bernardello, L.M., 1986. Revision taxonomica de las especies sudamericanas de Lycium (Solanaceae). Bol. Acad. Nac. Cienc. Cordoba 57, 173-356.
[2] Bezanson, J., Edelman, A., Karpinski, S., et al., 2017. Julia: a fresh approach to numerical computing. Siam Rev. 59, 65-98. https://doi.org/10.1137/141000671.
[3] Bi, C., Shen, F., Han, F., et al., 2024. PMAT: an efficient plant mitogenome assembly toolkit using low-coverage HiFi sequencing data. Hortic. Res. 11, uhae023. https://doi.org/10.1093/hr/uhae023.
[4] Bolger, A.M., Lohse, M., Usadel, B., et al., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. https://doi.org/10.1093/bioinformatics/btu170.
[5] Borowiec, M.L., 2016. AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ 4, e1660. https://doi.org/10.7717/peerj.1660.
[6] Brassac, J., Blattner, F.R., 2015. Species-level phylogeny and polyploid relationships in Hordeum (Poaceae) inferred by next-generation sequencing and in silico cloning of multiple nuclear loci. Syst. Biol. 64, 792-808. https://doi.org/10.1093/sysbio/syv035.
[7] Cai, L., Xi, Z., Lemmon, E. M., et al., 2021. The perfect storm: gene tree estimation error, incomplete lineage sorting, and ancient gene flow explain the most recalcitrant ancient angiosperm clade, Malpighiales. Syst. Biol. 70, 491-507. https://doi.org/10.1093/sysbio/syaa083.
[8] Calvino, C.I., Teruel, F.E., Downie, S.R., et al., 2016. The role of the Southern Hemisphere in the evolutionary history of Apiaceae, a mostly north temperate plant family. J. Biogeogr. 43, 398-409. https://doi.org/10.1111/jbi.12650.
[9] Cao, Y.L., Li, Y.l., Fan, Y.F., et al., 2021. Wolfberry genomes and the evolution of Lycium (Solanaceae). Commun. Biol. 4, 671. https://doi.org/10.1038/s42003-021-02152-8.
[10] Capella-Gutierrez, S., Silla-Martinez, J.M., Gabaldon, T., 2009. TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972-1973. https://doi.org/10.1093/bioinformatics/btp348.
[11] Chen, K., Liu, Y.C., Huang, Y., et al., 2025. Reassessing the phylogenetic relationships of Pseudosorghum and Saccharinae (Poaceae) using plastome and nuclear ribosomal sequences. Plant Divers. 47, 382-393. https://doi.org/10.1016/j.pld.2025.03.002.
[12] Chen, S., Zhou, Y., Chen, Y., et al., 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884-i890. https://doi.org/10.1093/bioinformatics/bty560.
[13] Chen, Y., Ye, W., Zhang, Y., et al., 2015. High speed BLASTN: an accelerated MegaBLAST search tool. Nucleic Acids Res. 43, 7762-7768. https://doi.org/10.1093/nar/gkv784.
[14] Chiang-Cabrera, F., 1981. A taxonomic study of the North American species of Lycium (Solanaceae). Ph.D. dissertation, The University of Texas, Austin.
[15] Degnan, J.H., Rosenberg, N.A., 2006. Discordance of species trees with their most likely gene trees. PLoS Genetics 2, e68. https://doi.org/10.1371/journal.pgen.0020068.
[16] Degnan, J.H., Rosenberg, N.A., 2009. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332-340. https://doi.org/10.1016/j.tree.2009.01.009.
[17] Delsuc, F., Brinkmann, H., Philippe, H., 2005. Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet. 6, 361-375. https://doi.org/10.1038/nrg1603.
[18] Dobrogojski, J., Adamiec, M., Lucinski, R., 2020. The chloroplast genome: a review. Acta. Physiol. Plant 42, 98. https://doi.org/10.1007/s11738-020-03089-x.
[19] Dong, S., Wang, L., Xia, H., et al., 2021. Plastid and nuclear phylogenomic incongruences and biogeographic implications of Magnolia s.l. (Magnoliaceae). J. Syst. Evol. 60, 1-15. https://doi.org/10.1111/jse.12727.
[20] Dong, W., Liu, Y., Li, E., et al., 2022. Phylogenomics and biogeography of Catalpa (Bignoniaceae) reveal incomplete lineage sorting and three dispersal events. Mol. Phylogenet. Evol. 166, 107330. https://doi.org/10.1016/j.ympev.2021.107330.
[21] Drummond, A.J., Ho, S.Y., Phillips, M.J., et al., 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88. https://doi.org/10.1371/journal.pbio.0040088.
[22] Drummond, A.J., Suchard, M.A., Xie, D., et al., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969-1973. https://doi.org/10.1093/molbev/mss075.
[23] Duan, L., Harris, A.J., Su, C., et al., 2020. Chloroplast phylogenomics reveals the intercontinental biogeographic history of the liquorice genus (Leguminosae: Glycyrrhiza). Front. Plant Sci. 11, 793. https://doi.org/10.3389/fpls.2020.00793.
[24] Duchene, D.A., Bragg, J.G., Duchene, S., et al., 2018. Analysis of phylogenomic tree space resolves relationships among marsupial families. Syst. biol. 67, 400-412. https://doi.org/10.1093/sysbio/syx076.
[25] Edelman, N.B., Frandsen, P.B., Miyagi, M., et al., 2019. Genomic architecture and introgression shape a butterfly radiation. Science 366, 594-599. https://doi.org/10.1126/science.aaw2090.
[26] El Zaatari, S., 2018. The central Levantine corridor: the Paleolithic of Lebanon. Quatern. Int. 466, 33-47. https://doi.org/10.1016/j.quaint.2017.06.047.
[27] Emadzade, K., Horandl, E., 2011. Northern Hemisphere origin, transoceanic dispersal, and diversification of Ranunculeae DC. (Ranunculaceae) in the Cenozoic. J. Biogeogr. 38, 517-530. https://doi.org/10.1111/j.1365-2699.2010.02404.x.
[28] Emms, D.M., Kelly, S., 2019. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238. https://doi.org/10.1186/s13059-019-1832-y.
[29] Feng, S., Bai, M., Rivas-Gonzalez, I., et al., 2022. Incomplete lineage sorting and phenotypic evolution in marsupials. Cell 185, 1646-1660. https://doi.org/10.1016/j.cell.2022.03.034.
[30] Fu, L., Niu, B., Zhu, Z., et al., 2012. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150-3152. https://doi.org/10.1093/bioinformatics/bts565.
[31] Fukuda, T., Yokoyama, J., Ohashi, H., 2001. Phylogeny and biogeography of the genus Lycium (Solanaceae): inferences from chloroplast DNA sequences. Mol. Phylogenet. Evol. 19, 246-258. https://doi.org/10.1006/mpev.2001.0921.
[32] Gong, H., Rehman, F., Ma, Y., et al., 2022. Germplasm resources and strategy for genetic breeding of Lycium species: a review. Front. Plant Sci. 13, 802936.https://doi.org/10.3389/fpls.2022.802936.
[33] Grabherr, M.G., Haas, B.J., Yassour, M., et al., 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644-652. https://doi.org/10.1038/nbt.1883.
[34] Greiner, S., Lehwark, P., Bock, R., 2019. OrganellarGenomeDRAW (OGDRAW) version 1.3.1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Res. 47, 59-64. https://doi.org/10.1093/nar/gkz238.
[35] Gu, W., Zhang, T., Liu, S.Y., et al., 2024. Phylogenomics, reticulation, and biogeographical history of Elaeagnaceae. Plant Divers. 4, 683-697. https://doi.org/10.1016/j.pld.2024.07.001.
[36] Guo, J.F., Zhao, W., Andersson, B., et al., 2023. Genomic clines across the species boundary between a hybrid pine and its progenitor in the eastern Tibetan Plateau. Plant Commun. 4, 100574. https://doi.org/10.1016/j.xplc.2023.100574.
[37] Guo, Z.T., Ruddiman, W.F., Hao, Q.Z., et al., 2002. Onset of Asian desertification by 22 Myr ago inferred from loess deposits in China. Nature 416, 159-163. https://doi.org/10.1038/416159a.
[38] Haas, B.J., Papanicolaou, A., Yassour, M., et al., 2013. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8, 1494-1512. https://doi.org/10.1038/nprot.2013.084.
[39] Hitchcock, C.Leo., 1932. A monographic study of the genus Lycium of the western hemisphere .. St. Louis: Washington University. 19, 179-374.
[40] Hoang, D.T., Chernomor, O., von Haeseler, A., et al., 2018. UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518-522. https://doi.org/10.1093/molbev/msx281.
[41] Hodel, R.G.J., Zimmer, E., Wen, J., 2021. A phylogenomic approach resolves the backbone of Prunus (Rosaceae) and identifies signals of hybridization and allopolyploidy. Mol. Phylogenet. Evol. 160, 107118. https://doi.org/10.1016/j.ympev.2021.107118.
[42] Hodel, R.G.J., Zimmer, E.A., Liu, B.B., et al., 2022. Synthesis of nuclear and chloroplast data combined with network analyses supports the polyploid origin of the apple tribe and the hybrid origin of the Maleae-Gillenieae clade. Front. Plant Sci. 12, 820997. https://doi.org/10.3389/fpls.2021.820997.
[43] Hoorn, C., Wesselingh, F.P., ter Steege, H., et al., 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330, 927-931. https://doi.org/10.1126/science.1194585.
[44] Hu, H., Sun, P., Yang, Y., et al., 2023. Genome-scale angiosperm phylogenies based on nuclear, plastome, and mitochondrial datasets. J. Integr. Plant Biol. 65, 1479-1489. https://doi.org/10.1111/jipb.13455.
[45] Huang, J., Xu, W., Zhai, J., et al., 2023. Nuclear phylogeny and insights into whole-genome duplications and reproductive development of Solanaceae plants. Plant Commun. 4, 100595. https://doi.org/10.1016/j.xplc.2023.100595.
[46] Huson, D.H., Scornavacca, C., 2012. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst. Biol. 61, 1061-1067. https://doi.org/10.1093/sysbio/sys062.
[47] Johnson, M.G., Gardner, E.M., Liu, Y., et al., 2016. HybPiper: extracting coding sequence and introns for phylogenetics from high-throughput sequencing reads using target enrichment. Appl. Plant Sci. 4, 1600016. https://doi.org/10.3732/apps.1600016.
[48] Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. https://doi.org/10.1093/molbev/mst010.
[49] Ke, X., Morales-Briones, D.F., Wang, H., et al., 2021. Nuclear and plastid phylogenomic analyses provide insights into the reticulate evolution, species delimitation, and biogeography of the Sino-Japanese disjunctive Diabelia (Caprifoliaceae). J. Syst. Evol. 60, 1331-1343. https://doi.org/10.1111/jse.12815.
[50] Kearse, M., Moir, R., Wilson, A., et al., 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649. https://doi.org/10.1093/bioinformatics/bts199.
[51] Kurtz, S., Choudhuri, J.V., Ohlebusch, E., et al., 2001. REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res. 29, 4633-4642. https://doi.org/10.1093/nar/29.22.4633.
[52] Lanfear, R., Frandsen, P.B., Wright, A.M., et al., 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772-773. https://doi.org/10.1093/molbev/msw260.
[53] Levin, R.A., Miller, J.S., 2005. Relationships within tribe Lycieae (Solanaceae): paraphyly of Lycium and multiple origins of gender dimorphism. Am. J. Bot. 92, 2044-2053. https://eurekamag.com/research/003/882/003882754.php.
[54] Levin, R.A., Shak, J.R., Bernardello, G., et al., 2007. Evolutionary relationships in tribe Lycieae (Solanaceae). Acta Hort. 745, 225-239 https://doi.org/10.17660/ActaHortic.2007.745.9.
[55] Levin, R.A., Whelan, A., Miller, J.S., 2009. The utility of nuclear conserved ortholog set II (COSII) genomic regions for species-level phylogenetic inference in Lycium (Solanaceae). Mol. Phylogenet. Evol. 53, 881-890. https://doi.org/10.1016/j.ympev.2009.08.016.
[56] Li, J., Ni, Y., Lu, Q., et al., 2025. PMGA: a plant mitochondrial genome annotator. Plant Commun. 10, 101191. https://doi.org/10.1016/j.xplc.2024.101191.
[57] Li, M., Ohi-Toma, T., Gao, Y., et al., 2017. Molecular phylogenetics and historical biogeography of Sorbus sensu stricto (Rosaceae). Mol. Phylogenet. Evol. 111, 76-86. https://doi.org/10.1016/j.ympev.2017.03.018.
[58] Li, P., Li, Z., Sun, Q., et al., 2024. Protective effect and mechanism of Lycium ruthenicum Murray anthocyanins against retinal damage induced by blue light exposure. J. Food. Sci. 89, 5113-5129. https://doi.org/10.1111/1750-3841.17184.
[59] Lin, X.H., Xie, S.Y., Ma, D.K., et al., 2025. Phylogenomic insights into Adenophora and its allies (Campanulaceae): revisiting generic delimitation and hybridization dynamics. Plant Divers. 47, 576-592. https://doi.org/10.1016/j.pld.2025.05.010.
[60] Liu, B., Ma, Y., Ren, C., et al., 2021. Capturing single-copy nuclear genes, organellar genomes, and nuclear ribosomal DNA from deep genome skimming data for plant phylogenetics: a case study in Vitaceae. J. Syst. Evol. 59, 1124-1138. https://doi.org/10.1111/jse.12806.
[61] Liu, C., Yang, Z., Yang, L., et al., 2018. The complete plastome of Panax stipuleanatus: comparative and phylogenetic analyses of the genus Panax (Araliaceae). Plant Divers. 40, 265-276. https://doi.org/10.1016/j.pld.2018.11.001.
[62] Liu, Q., Duan, W., Hao, G., et al., 2014. Evolutionary history and underlying adaptation of alpine plants on the Qinghai-Tibet Plateau. J. Syst. Evol. 52, 241-249. https://doi.org/10.1111/jse.12094.
[63] Liu, S.Y., Yang, Y.Y., Tian, Q., et al., 2025. An integrative framework reveals widespread gene flow during the early radiation of oaks and relatives in Quercoideae (Fagaceae). J. Integr. Plant Biol. 67, 1119-1141. https://doi.org/10.1111/jipb.13773.
[64] Liu, X., Deng, P., Chen, Z., et al., 2022b. Systematics of Mukdenia and Oresitrophe (Saxifragaceae): insights from genome skimming data. J. Syst. Evol. 61, 99-114. https://doi.org/10.1111/jse.12833.
[65] Liu, X., Wang, Z., Wang, W., et al., 2022a. Origin and evolutionary history of Populus (Salicaceae): further insights based on time divergence and biogeographic analysis. Front. Plant Sci. 13, 1031087. https://doi.org/10.3389/fpls.2022.1031087.
[66] Liu, Y., Xu, X., Dimitrov, D., et al., 2023. An updated floristic map of the world. Nat. Commun. 14, 2990. https://doi.org/10.1038/s41467-023-38375-y.
[67] Ma, F., Liang, Y., Meng, F., et al., 2025. The LbNAM2-LbZDS module enhances drought resistance in wolfberry (Lycium barbarum) by participating in ABA biosynthesis. Plant J. 121, e70077. https://doi.org/10.1111/tpj.70077.
[68] Ma, S., Zhang, M.L., 2012. Phylogeography and conservation genetics of the relic Gymnocarpos przewalskii (Caryophyllaceae) restricted to northwestern China. Conserv. Genet. 13, 1531-1541. https://doi.org/10.1007/s10592-012-0397-z.
[69] Ma, Z.Y., Nie, Z.L., Ren, C., et al., 2021. Phylogenomic relationships and character evolution of the grape family (Vitaceae). Mol. Phylogenet. Evol. 154, 106948. https://doi.org/10.1016/j.ympev.2020.106948.
[70] Malinsky, M., Matschiner, M., Svardal, H., 2021. Dsuite-fast D-statistics and related admixture evidence from VCF files. Mol. Ecol. Resour. 21, 584-595. https://doi.org/10.1111/1755-0998.13265.
[71] McLay, T.G.B., Fowler, R.M., Fahey, P.S., et al., 2023. Phylogenomics reveals extreme gene tree discordance in a lineage of dominant trees: hybridization, introgression, and incomplete lineage sorting blur deep evolutionary relationships despite clear species groupings in Eucalyptus subgenus Eudesmia. Mol. Phylogenet. Evol. 187, 107869. https://doi.org/10.1016/j.ympev.2023.107869.
[72] McLoughlin, S., 2001. The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism. Aust. J. Bot. 49, 271. https://doi.org/10.1071/BT00023.
[73] Meheretu, Y., Mikula, O., Frynta, D., et al., 2024. Phylogeny, biogeography, and integrative taxonomic revision of the Afro-Arabian rodent genus Ochromyscus (Muridae: Murinae: Praomyini). Zool. J. Linn. Soc. 202, 1-15. https://doi.org/10.1093/zoolinnean/zlad158.
[74] Meng, H., Gao, X., Huang, J., et al., 2015. Plant phylogeography in arid Northwest China: retrospectives and perspectives. J. Syst. Evol. 53, 33-46. https://doi.org/10.1111/jse.12088.
[75] Messeder, J.V.S., Carlo, T.A., Zhang, G., et al., 2024. A highly resolved nuclear phylogeny uncovers strong phylogenetic conservatism and correlated evolution of fruit color and size in Solanum L. New Phytol. 243, 765-780. https://doi.org/10.1111/nph.19849.
[76] Miller, J.S., 2002. Phylogenetic relationships and the evolution of gender dimorphism in Lycium (Solanaceae). Syst. Bot. 27, 416-428. https://doi.org/10.2307/3093881.
[77] Miller, J.S., Kamath, A., Damashek, J., et al., 2011. Out of America to Africa or Asia: inference of dispersal histories using nuclear and plastid DNA and the S-Rnase self-incompatibility locus. Mol. Biol. Evol. 28, 793-801. https://doi.org/10.1093/molbev/msq253.
[78] Miller, J.S., Venable, D.L., 2000. Polyploidy and the evolution of gender dimorphism in plants. Science 289, 2335-2338. https://doi.org/10.1126/science.289.5488.2335.
[79] Milton, J.J., Affenzeller, M., Abbott, R., et al., 2022. Plant speciation in the Namib Desert: potential origin of a widespread derivative species from a narrow endemic. Plant Ecol. Divers. 15, 329-353. https://doi.org/10.1080/17550874.2022.2130018.
[80] Minh, B.Q., Schmidt, H.A., Chernomor, O., et al., 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530-1534. https://doi.org/10.1093/molbev/msaa015.
[81] Minne, L., Spies, J.J., Venter, H.J.T., et al., 1994. Breeding systems in some representatives of the genus Lycium (Solanaceae). Bothalia. 24, 107-110. https://doi.org/10.4102/abc.v24i1.759.
[82] Morales-Briones, D.F., Liston, A., Tank, D.C., 2018. Phylogenomic analyses reveal a deep history of hybridization and polyploidy in the Neotropical genus Lachemilla (Rosaceae). New Phytol. 218, 1668-1684. https://doi.org/10.1111/nph.15099.
[83] Pease, J.B., Brown, J.W., Walker, J.F., et al., 2018. Quartet Sampling distinguishes lack of support from conflicting support in the green plant tree of life. Am. J. Bot. 105, 385-403. https://doi.org/10.1002/ajb2.1016.
[84] Pease, J.B., Hahn, M.W., 2015. Detection and polarization of introgression in a five-taxon phylogeny. Syst. Biol. 64, 651-662. https://doi.org/10.1093/sysbio/syv023.
[85] Perez-Escobar, O.A., Zizka, A., Bermudez, M.A., et al., 2022. The Andes through time: evolution and distribution of Andean floras. Trends Plant Sci. 27, 364-378. https://doi.org/10.1016/j.tplants.2021.09.010.
[86] Pezzi, P.H., Wheeler, L.C., Freitas, L.B., et al., 2024. Incomplete lineage sorting and hybridization underlie tree discordance in Petunia and related genera (Petunieae, Solanaceae). Mol. Phylogenet. Evol. 198, 108136. https://doi.org/10.1016/j.ympev.2024.108136.
[87] Portik, D.M., Papenfuss, T.J., 2015. Historical biogeography resolves the origins of endemic Arabian toad lineages (Anura: Bufonidae): evidence for ancient vicariance and dispersal events with the Horn of Africa and South Asia. BMC Evol. Biol. 15, 152. https://doi.org/10.1186/s12862-015-0417-y.
[88] Qin, Y.Q., Zhang, M.H., Yang, C.Y., et al., 2024. Phylogenomics and divergence pattern of Polygonatum (Asparagaceae: Polygonateae) in the north temperate region. Mol. Phylogenet. Evol. 190, 107962. https://doi.org/10.1016/j.ympev.2023.107962.
[89] Qiu, Y.L., Lee, J., Bernasconi-Quadroni, F., et al., 1999. The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402, 404-407. https://doi.org/10.1038/46536.
[90] Rabosky, D.L., Grundler, M., Anderson, C., et al., 2014. BAMMtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods Ecol. Evol. 5, 701-707. https://doi.org/10.1111/2041-210X.12199.
[91] 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. 66, 477-498. https://doi.org/10.1093/sysbio/syx037.
[92] Rambaut, A., Drummond, A.J., Xie, D., et al., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901-904. https://doi.org/10.1093/sysbio/syy032.
[93] Raven, P.H., 1963. Amphitropical relationships in the floras of North and South America. Q. Rev. Biol. 38, 151-177. https://doi.org/10.1086/403797.
[94] Raven, P.H., Axelrod, D.I., 1974. Angiosperm biogeography and past continental movements. Ann. Missouri Bot. Gard. 61, 539-673. https://doi.org/10.2307/2395021.
[95] Revell, L.J., 2024. Phytools 2.0: an updated R ecosystem for phylogenetic comparative methods (and other things). PeerJ 12, e16505. https://doi.org/10.7717/peerj.16505.
[96] Rhodes, J.A., Banos, H., Mitchell, J.D., et al., 2021. MSCquartets 1.0: quartet methods for species trees and networks under the multispecies coalescent model in R. Bioinformatics 37, 1766-1768. https://doi:10.1093/bioinformatics/btaa868.
[97] Sarkinen, T., Bohs, L., Olmstead, R.G., et al., 2013. A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol. Biol. 13, 214. https://doi.org/10.1186/1471-2148-13-214.
[98] Schumer, M., Cui, R., Rosenthal, G.G., 2015. Reproductive isolation of hybrid populations driven by genetic incompatibilities. PLoS Genet. 11, e1005041. https://doi.org/10.1371/journal.pgen.1005041.
[99] Schumer, M., Rosenthal, G.G., Andolfatto, P., 2014. How common is homoploid hybrid speciation? Evolution 68, 1553-1560. https://doi.org/10.1111/evo.12399.
[100] Shi, X.J., Zhang, M.L., 2015. Phylogeographical structure inferred from cpDNA sequence variation of Zygophyllum xanthoxylon across north-west China. J. Plant. Res. 128, 269-282. https://doi.org/10.1007/s10265-014-0699-y.
[101] Simpson, M.G., Johnson, L.A., Villaverde, T., et al., 2017. American amphitropical disjuncts: perspectives from vascular plant analyses and prospects for future research. Am. J. Bot. 104, 1600-1650. https://doi.org/10.3732/ajb.1700308.
[102] Smith, S.A., Brown, J.W., Walker, J.F., 2018. So many genes, so little time: a practical approach to divergence-time estimation in the genomic era. PloS one 13, e0197433. https://doi.org/10.1371/journal.pone.0197433.
[103] Smith, S.A., Moore, M.J., Brown, J.W., et al., 2015. Analysis of phylogenomic datasets reveals conflict, concordance, and gene duplications with examples from animals and plants. BMC Evol. Biol. 15, 1-15. https://doi.org/10.1186/s12862-015-0423-0.
[104] Solis-Lemus, C., Ane, C., 2016. Inferring phylogenetic networks with maximum pseudolikelihood under incomplete lineage sorting. PLoS Genet. 12, e1005896 https://doi.org/10.1371/journal.pgen.1005896.
[105] Solis-Lemus, C., Bastide, P., Ane, C., 2017. PhyloNetworks: a package for phylogenetic networks. Mol. Biol. Evol. 34, 3292-3298. https://doi.org/10.1093/molbev/msx235.
[106] Stadler, T., 2009. On incomplete sampling under birth-death models and connections to the sampling-based coalescent. J. Theor. Biol. 261, 58-66. https://doi.org/10.1016/j.jtbi.2009.07.018.
[107] Stubbs, R.L., Folk, R.A., Xiang, C.L., et al., 2020. A phylogenomic perspective on evolution and discordance in the alpine-arctic plant clade Micranthes (Saxifragaceae). Front. Plant Sci. 10, 1773. https://doi.org/10.3389/fpls.2019.01773.
[108] Su, Z., Zhang, M., Cohen, J.I., 2012. Phylogeographic and demographic effects of Quaternary climate oscillations in Hexinia polydichotoma (Asteraceae) in Tarim Basin and adjacent areas. Plant Syst. Evol. 298, 1767-1776. https://doi.org/10.1007/s00606-012-0677-6.
[109] Symon, D.E., 1991. Gondwanan elements of the Solanaceae, In: J. G. Hawks, R. N. Lester, M. Nee, and N. Eserada, (Eds.), Solanaceae III: Taxonomy - Chemistry - Evolution. Royal Botanic Garden, Kew and the Linnean Society of London, Richmond, pp. 139-150.
[110] Tamura, K., Stecher, G., Kumar, S., 2021. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022-3027. https://doi.org/10.1093/molbev/msab120.
[111] Thiv, M., Van der Niet, T., Rutschmann, F., et al., 2011. Old-New World and trans-African disjunctions of Thamnosma (Rutaceae): intercontinental long-distance dispersal and local differentiation in the succulent biome. Am. J. Bot. 98, 76-87. https://doi.org/10.3732/ajb.1000339.
[112] Thureborn, O., Wikstrom, N., Razafimandimbison, S.G., et al., 2024. Plastid phylogenomics and cytonuclear discordance in Rubioideae, Rubiaceae. PLoS One 19, e0302365. https://doi.org/10.1371/journal.pone.0302365.
[113] Tian, B., Zhao, J., Zhang, M., et al., 2021. Lycium ruthenicum anthocyanins attenuate high-fat diet-induced colonic barrier dysfunction and inflammation in mice by modulating the gut microbiota. Mol. Nutr. Food Res. 65, 2000745. https://doi.org/10.1002/mnfr.202000745.
[114] Velichkevich, F.Y., Zastawniak, E., 2003. The Pliocene flora of Kholmech, south-eastern Belarus and its correlation with other Pliocene floras of Europe. Acta Palaeobot. 43, 137-259.
[115] Venter, A.M., Venter, H.J.T., Manning, J.C., 2003. Lycium gariepense (Solanaceae), a new species from South Africa and Namibia. S. Afr. J. Bot. 69, 161-164. https://doi.org/10.1016/S0254-6299(15)30340-9.
[116] Wang, C., Zhao, X., Liu, Z., et al., 2008. Constraints on the early uplift history of the Tibetan Plateau. Proc. Nat. Acad. Sci. U.S.A. 105, 4987-4992. https://doi.org/10.1073/pnas.0703595105.
[117] Wang, J., Kan, S., Liao, X., et al., 2024a. Plant organellar genomes: Much done, much more to do. Trends Plant Sci. 29, 754-769. https://doi.org/10.1016/j.tplants.2023.12.014.
[118] Wang, M., Zhu, M., Qian, J., et al., 2024b. Phylogenomics of mulberries (Morus, Moraceae) inferred from plastomes and single copy nuclear genes. Mol. Phylogenet. Evol. 197, 108093. https://doi.org/10.1016/j.ympev.2024.108093.
[119] Wetters, S., Horn, T., Nick, P., 2018. Goji Who? Morphological and DNA based authentication of a “Superfood”. Front. Plant Sci. 9, 1859. https://doi.org/10.3389/fpls.2018.01859.
[120] Wilf, P., Carvalho, M.R., Gandolfo, M.A., et al., 2017. Eocene lantern fruits from Gondwanan Patagonia and the early origins of Solanaceae. Science 355, 71-75. https://doi.org/10.1126/science.aag2737.
[121] Xiong, M., Peng, J., Zhou, S., et al., 2025. Lycium barbarum L.: a potential botanical drug for preventing and treating retinal cell apoptosis. Front. Pharmacol. 16, 1571554. https://doi.org/10.3389/fphar.2025.1571554.
[122] Xu, X., Kleidon, A., Miller, L., et al., 2010. Late Quaternary glaciation in the Tianshan and implications for palaeoclimatic change: a review. Boreas 39, 215-232. https://doi.org/10.1111/j.1502-3885.2009.00118.x.
[123] Xue, T.T., Janssens, S.B., Liu, B.B., et al., 2024. Phylogenomic conflict analyses of the plastid and mitochondrial genomes via deep genome skimming highlight their independent evolutionary histories: A case study in the cinquefoil genus Potentilla sensu lato (Potentilleae, Rosaceae). Mol. Phylogenet. Evol. 190, 107956. https://doi.org/10.1016/j.ympev.2023.107956.
[124] Yao, R., Heinrich, M., Weckerle, C.S., 2018. The genus Lycium as food and medicine: a botanical, ethnobotanical and historical review. J. Ethnopharmacol. 212, 50-66. https://doi.org/10.1016/j.jep.2017.10.010.
[125] Yao, X., Peng, Y., Xu, L.J., et al., 2011. Phytochemical and biological studies of Lycium medicinal plants. Chem. Biodivers. 8, 976-1010. https://doi.org/10.1002/cbdv.201000018.
[126] Yisilam, G., Cameron, K.M., Zhang, Y., et al., 2025. New insights into the phylogeny and biogeography of goji berries (Lycium, Solanaceae) inferred from plastid data. J. Biogeogr. 52, e15163. https://doi.org/10.1111/jbi.15163.
[127] Yisilam, G., Wang, C.X., Xia, M.Q., et al., 2022. Phylogeography and population genetics analyses reveal evolutionary history of the desert resource plant Lycium ruthenicum (Solanaceae). Front. Plant Sci. 13, 915526. https://doi.org/10.3389/fpls.2022.915526.
[128] Yu, Y., Blair, C., He, X., 2020. RASP 4: ancestral state reconstruction tool for multiple genes and characters. Mol. Biol. Evol. 37, 604-606. https://doi.org/10.1016/j.ympev.2015.03.008.
[129] Zachos, J., Pagani, M., Sloan, L., et al., 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292, 686-693. https://doi.org/10.1126/science.1059412.
[130] Zeng, Y.F., Zhang, J.G., Abuduhamiti, B., et al., 2018. Phylogeographic patterns of the desert poplar in Northwest China shaped by both geology and climatic oscillations. BMC Ecol. Evol. 18, 75. https://doi.org/10.1186/s12862-018-1194-1.
[131] Zhang, C., Rabiee, M., Sayyari, E., et al., 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinf. 19, 15-30. https://doi.org/10.1186/s12859-018-2129-y.
[132] Zhang, L., Zhang, E., Wei, Y., et al., 2024. Phylogenetic analysis and divergence time estimation of Lycium species in China based on the chloroplast genomes. BMC Genomics 25, 569. https://doi.org/10.1186/s12864-024-10487-9.
[133] Zhang, M.L., Fritsch, P.W., 2010. Evolutionary response of Caragana (Fabaceae) to Qinghai-Tibetan Plateau uplift and Asian interior aridification. Plant Syst. Evol. 288, 191-199. https://doi.org/10.1007/s00606-010-0324-z.
[134] Zhang, X., Li, S., Wang, C., et al., 2021. Insights into the aridification history of Central Asian Mountains and international conservation strategy from the endangered wild apple tree. J. Biogeogr. 48, 332-344. https://doi.org/10.1111/jbi.13999.
[135] Zou, Y., Zhu, W., Hou, Y., et al., 2025. The evolutionary dynamics of organellar pan-genomes in Arabidopsis thaliana. Genome Biol. 26, 240. https://doi.org/10.1186/s13059-025-03717-0.

Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes

Phylogenomic conflict in Lycium (Solanaceae): Revealing the roles of hybridization, incomplete lineage sorting, and biogeographic history using nuclear and mitochondrial genomes

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Xin Yan, Enze Li, Xingyong Cui, Liangcheng Zhao, Wenpan Dong. Niche evolution and asymmetric diversification in elm species (Ulmaceae) [J]. Plant Diversity, 2026, 48(04): 704-719.
[2]	Chen-Xuan Yang, Shui-Yin Liu, Qin Tian, Wei Gu, Qing Lu, Robert P. Guralnick, Gregory W. Stull, Heather R. Kates, Ryan A. Folk, Douglas E. Soltis, Pamela S. Soltis, Elliot M. Gardner, Ting-Shuang Yi. Phylogenomic conflict in Moraceae: Evidence for pervasive introgression and incomplete lineage sorting [J]. Plant Diversity, 2026, 48(04): 688-703.
[3]	Zhe Wang, Sheng-Xuan Cai, Jing-Rou Yu, Dan-Dan Li, Xue-Ping Lai, Ling-Ao Yang, Shui-Liang Guo, Jing Yu. Distinct intraspecific trait variations in two moss species: Insights from a latitudinal investigation across 66 coastal islands [J]. Plant Diversity, 2026, 48(03): 567-575.
[4]	Pengpeng Yan, Chang Guo, Xingyong Cui, Enze Li, Yuran Bai, Manuel R. Roncal-Rabanal, Gangmin Zhang, Wenpan Dong. Phylogenomics unravels the early divergence and diversification in Bignoniaceae [J]. Plant Diversity, 2026, 48(02): 307-319.
[5]	Xiao-Gang Fu, Jie Liu, Richard I. Milne, Alex K. Monro, Shui-Yin Liu, Qin Tian, Gregory W. Stull, Amos Kipkoech, Ting-Shuang Yi, De-Zhu Li, Zeng-Yuan Wu. A robust phylogenomic framework supports a revised intrafamilial classification of Urticaceae [J]. Plant Diversity, 2026, 48(02): 289-306.
[6]	Xiaoling Tian, Ningning Zhang, Xiaohua Li, Zhong Zhang, Heng Shu, Chunying Zhang, Yongpeng Ma, Yupeng Geng. Whole genome sequencing analysis reveals strong reproductive isolation between two hybridizing Rhododendron species in subgenus Tsutsusi [J]. Plant Diversity, 2026, 48(01): 212-215.
[7]	Deyi Wang, Vincent S. F. T. Merckx, Hans Jacquemyn, Sofia I. F. Gomes. Mycorrhizal communities in Orchidaceae are likely shaped by plant trophic mode and biogeography but not phylogeny [J]. Plant Diversity, 2026, 48(01): 117-127.
[8]	Jia-Min Xiao, Ming-Yang Li, Jun Wen, Radosław Puchałka, Huan-Yu Wu, Wen-He Li, Zi-Yi Li, Bo-Wen Liu, Yue-Xin Luo, Ru-Dan Lyu, Le-Le Lin, Jian He, Jin Cheng, Lei Xie, Liang-Qian Li. Worldwide phylogeny and integrative taxonomy of Clematis: Insights from phylogenomics [J]. Plant Diversity, 2026, 48(01): 16-40.
[9]	Sining Zhang, Jun Chen, Pan Li. The first haplotype-resolved genome assembly of Prunus s.l. subgenus Laurocerasus (Prunus spinulosa) [J]. Plant Diversity, 2025, 47(06): 991-994.
[10]	Aiying Zhang, Xiaofei Wei, Donghao Wu, Zhonghan Wang, Mingjian Yu, Lingfeng Mao. Fragmentation effects on β-diversity: The role of abundance and intraspecific trait variation in shaping taxonomic, functional, and phylogenetic patterns [J]. Plant Diversity, 2025, 47(06): 981-990.
[11]	Xiaochun Shu, Ruisen Lu, Pat Heslop-Harrison, Trude Schwarzacher, Zhong Wang, Yalong Qin, Ning Wang, Fengjiao Zhang. Unraveling the evolutionary complexity of Lycoris: Insights into chromosomal variation, genome size, and phylogenetic relationships [J]. Plant Diversity, 2025, 47(06): 931-943.
[12]	Jinliang Liu, Mengyuan Chen, Lu Wang, Tengteng Liu, Xinjie Jin, Fei-Hai Yu, Yonghua Zhang. Habitat fragmentation differentially affects invasive and native plant diversity in a human-dominated wetland island system [J]. Plant Diversity, 2025, 47(05): 824-832.
[13]	Zhao-Yang Jing (景昭阳), Ren-Gang Zhang (张仁纲), Yang Liu (刘阳), Ke-Guang Cheng (程可光), De-Tuan Liu (刘德团), Heng Shu (舒恒), Jiali Kong (孔佳莉), Zhong-Hua Liu (刘忠华), Yong-Peng Ma (马永鹏), Ping-Li Liu (刘平丽). Genomic insights into the evolutionary history and conservation of the living fossil Tetracentron sinense [J]. Plant Diversity, 2025, 47(05): 759-771.
[14]	Na-Na Zhang (张娜娜), Gregory W. Stull, Xue-Jie Zhang (张学杰), Shou-Jin Fan (樊守金), Ting-Shuang Yi (伊廷双), Xiao-Jian Qu (曲小健). PlastidHub: An integrated analysis platform for plastid phylogenomics and comparative genomics [J]. Plant Diversity, 2025, 47(04): 544-560.
[15]	Ibrokhimjon Ergashov, Ziyoviddin Yusupov, Alireza Dolatyari, Mina Khorasani, İsmail Eker, Nazgul Turdumatova, Georgy Lazkov, Farruhbek Rasulov, Hang Sun, Tao Deng, Komiljon Tojibaev. New insights into the molecular phylogeny and biogeographical history of Allium subgenus Melanocrommyum (Amaryllidaceae) based on plastome and nuclear sequences [J]. Plant Diversity, 2025, 47(04): 561-575.