Background <p>Phylogenetic research in <i>Tulipa</i> (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 <i>Amana</i>, <i>Erythronium</i>, and <i>Tulipa</i>, 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.</p> Results <p>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 (<i>Notholirion campanulatum</i>), 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 <i>Amana</i>, <i>Erythronium</i>, and <i>Tulipa</i>, were further investigated by applying D-statistics and QuIBL.</p> Conclusions <p>We failed to reconstruct a reliable and unambiguous evolutionary history among <i>Amana</i>, <i>Erythronium</i>, and <i>Tulipa</i> due to especially pervasive ILS and reticulate evolution, likely caused either by obscured minority phylogenetic signal or differing signals among genomic compartments. However, within <i>Tulipa</i> we confirmed the monophyly of most subgenera, with the exception of two species in the small subgenus <i>Orithyia</i>, of which <i>Tulipa heterophylla</i> was recovered as sister to the remainder of the genus, whereas <i>T</i>. <i>sinkiangensis</i> clustered within subgenus <i>Tulipa</i>. In contrast, most traditional sections of <i>Tulipa</i> were found to be non-monophyletic.</p>

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Incomplete lineage sorting and introgression among genera and species of Liliaceae tribe Tulipeae: insights from phylogenomics

  • Zhihui Zhang,
  • Meizhen Wang,
  • Zhaoping Yang,
  • Hans Peter Comes,
  • Xin Zhong,
  • Ryan A. Folk,
  • Yigang Song,
  • Dana A. York,
  • Kenneth M. Cameron,
  • Pan Li

摘要

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.