Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics
Abstract Background Phylogenetic research in Tulipa (Liliaceae), a genus of significant economic and horticultural value, has relied on limited nuclear (mostly nuclear ribosomal internal transcribed spacer, nrITS) and plastid DNA sequences, resulting in low-resolution phylogenetic trees and uncertai...
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2025-04-01
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| author | Zhihui Zhang Meizhen Wang Zhaoping Yang Hans Peter Comes Xin Zhong Ryan A. Folk Yigang Song Dana A. York Kenneth M. Cameron Pan Li |
| author_facet | Zhihui Zhang Meizhen Wang Zhaoping Yang Hans Peter Comes Xin Zhong Ryan A. Folk Yigang Song Dana A. York Kenneth M. Cameron Pan Li |
| author_sort | Zhihui Zhang |
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| description | Abstract Background Phylogenetic research in Tulipa (Liliaceae), a genus of significant economic and horticultural value, has relied on limited nuclear (mostly nuclear ribosomal internal transcribed spacer, nrITS) and plastid DNA sequences, resulting in low-resolution phylogenetic trees and uncertain intrageneric classifications. The genus, noted for its large genome, presents discordant relationships among Amana, Erythronium, and Tulipa, likely due to incomplete lineage sorting (ILS) and/or reticulate evolution. Thus, phylogenomic approaches are needed to clarify these relationships and the conflicting signals within the tribe Tulipeae. Results We newly sequenced 50 transcriptomes of 46 species of tribe Tulipeae (including multiple accessions of all four genera) and one outgroup species of the sister tribe Lilieae (Notholirion campanulatum), and downloaded 15 previously published transcriptomes of tribe Tulipeae to supplement the sampling. One plastid dataset (74 plastid protein-coding genes, PCGs) and one nuclear dataset (2594 nuclear orthologous genes, OGs) were constructed, with the latter used for species tree inference based on maximum likelihood (ML) and multi-species coalescent (MSC) methods. To investigate causes of gene tree discordance, “site con/discordance factors” (sCF and sDF1/sDF2) were calculated first, after which phylogenetic nodes displaying high or imbalanced sDF1/2 were selected for phylogenetic network analyses and polytomy tests to determine whether ILS or reticulate evolution best explain incongruence. Key relationships not resolved by this technique, especially those among Amana, Erythronium, and Tulipa, were further investigated by applying D-statistics and QuIBL. Conclusions We failed to reconstruct a reliable and unambiguous evolutionary history among Amana, Erythronium, and Tulipa due to especially pervasive ILS and reticulate evolution, likely caused either by obscured minority phylogenetic signal or differing signals among genomic compartments. However, within Tulipa we confirmed the monophyly of most subgenera, with the exception of two species in the small subgenus Orithyia, of which Tulipa heterophylla was recovered as sister to the remainder of the genus, whereas T. sinkiangensis clustered within subgenus Tulipa. In contrast, most traditional sections of Tulipa were found to be non-monophyletic. |
| format | Article |
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| spelling | doaj-art-fa2e3972fad749f68088ba4a85ad94fc2025-08-20T01:47:30ZengBMCBMC Biology1741-70072025-04-0123112210.1186/s12915-025-02204-zIncomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomicsZhihui Zhang0Meizhen Wang1Zhaoping Yang2Hans Peter Comes3Xin Zhong4Ryan A. Folk5Yigang Song6Dana A. York7Kenneth M. Cameron8Pan Li9Systematic & Evolutionary Botany and Biodiversity Group, State Key Laboratory for Vegetation Structure, Function and Construction, College of Life Sciences, Zhejiang UniversityCollege of Biology and Environmental Engineering, Zhejiang Shuren UniversityCollege of Life Sciences and Technologies, Tarim UniversityDepartment of Environment & Biodiversity, University of SalzburgShanghai Chenshan Botanical GardenDepartment of Biological Sciences, Mississippi State UniversityShanghai Chenshan Botanical GardenCalifornia Academy of SciencesDepartment of Botany, University of WisconsinSystematic & Evolutionary Botany and Biodiversity Group, State Key Laboratory for Vegetation Structure, Function and Construction, College of Life Sciences, Zhejiang UniversityAbstract Background Phylogenetic research in Tulipa (Liliaceae), a genus of significant economic and horticultural value, has relied on limited nuclear (mostly nuclear ribosomal internal transcribed spacer, nrITS) and plastid DNA sequences, resulting in low-resolution phylogenetic trees and uncertain intrageneric classifications. The genus, noted for its large genome, presents discordant relationships among Amana, Erythronium, and Tulipa, likely due to incomplete lineage sorting (ILS) and/or reticulate evolution. Thus, phylogenomic approaches are needed to clarify these relationships and the conflicting signals within the tribe Tulipeae. Results We newly sequenced 50 transcriptomes of 46 species of tribe Tulipeae (including multiple accessions of all four genera) and one outgroup species of the sister tribe Lilieae (Notholirion campanulatum), and downloaded 15 previously published transcriptomes of tribe Tulipeae to supplement the sampling. One plastid dataset (74 plastid protein-coding genes, PCGs) and one nuclear dataset (2594 nuclear orthologous genes, OGs) were constructed, with the latter used for species tree inference based on maximum likelihood (ML) and multi-species coalescent (MSC) methods. To investigate causes of gene tree discordance, “site con/discordance factors” (sCF and sDF1/sDF2) were calculated first, after which phylogenetic nodes displaying high or imbalanced sDF1/2 were selected for phylogenetic network analyses and polytomy tests to determine whether ILS or reticulate evolution best explain incongruence. Key relationships not resolved by this technique, especially those among Amana, Erythronium, and Tulipa, were further investigated by applying D-statistics and QuIBL. Conclusions We failed to reconstruct a reliable and unambiguous evolutionary history among Amana, Erythronium, and Tulipa due to especially pervasive ILS and reticulate evolution, likely caused either by obscured minority phylogenetic signal or differing signals among genomic compartments. However, within Tulipa we confirmed the monophyly of most subgenera, with the exception of two species in the small subgenus Orithyia, of which Tulipa heterophylla was recovered as sister to the remainder of the genus, whereas T. sinkiangensis clustered within subgenus Tulipa. In contrast, most traditional sections of Tulipa were found to be non-monophyletic.https://doi.org/10.1186/s12915-025-02204-zPhylogenyIncomplete lineage sorting (ILS)IntrogressionReticulate evolutionTulipeaeTranscriptome sequencing |
| spellingShingle | Zhihui Zhang Meizhen Wang Zhaoping Yang Hans Peter Comes Xin Zhong Ryan A. Folk Yigang Song Dana A. York Kenneth M. Cameron Pan Li Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics BMC Biology Phylogeny Incomplete lineage sorting (ILS) Introgression Reticulate evolution Tulipeae Transcriptome sequencing |
| title | Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics |
| title_full | Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics |
| title_fullStr | Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics |
| title_full_unstemmed | Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics |
| title_short | Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics |
| title_sort | incomplete lineage sorting and introgression among genera and species of liliaceae tribe tulipeae insights from phylogenomics |
| topic | Phylogeny Incomplete lineage sorting (ILS) Introgression Reticulate evolution Tulipeae Transcriptome sequencing |
| url | https://doi.org/10.1186/s12915-025-02204-z |
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