Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae)
Abstract Background Gene tree incongruence is a well-documented, but the biological and analytical factors driving phylogenetic discordance remains incompletely understood. In this study, we investigated how different factors contribute to incongruence among gene trees in Fagaceae. Results Each data...
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2025-07-01
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| Online Access: | https://doi.org/10.1186/s12870-025-06963-3 |
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| author | Zhao Shen Biao-Feng Zhou Yi-Ye Liang Jing-Shu Wang Run-Xian Yu Yong Shi Shao-Jun Ling Wen-Ji Luo Qiong-Qiong Lin Jing-Wei Niu Liang-Jing Qiao Paul S. Manos Baosheng Wang |
| author_facet | Zhao Shen Biao-Feng Zhou Yi-Ye Liang Jing-Shu Wang Run-Xian Yu Yong Shi Shao-Jun Ling Wen-Ji Luo Qiong-Qiong Lin Jing-Wei Niu Liang-Jing Qiao Paul S. Manos Baosheng Wang |
| author_sort | Zhao Shen |
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| description | Abstract Background Gene tree incongruence is a well-documented, but the biological and analytical factors driving phylogenetic discordance remains incompletely understood. In this study, we investigated how different factors contribute to incongruence among gene trees in Fagaceae. Results Each dataset produced highly supported topologies, with Fagus and Trigonobalanus consistently placed as early-diverging lineages within the Fagaceae family. However, the cpDNA and mtDNA divided the remaining Fagaceae species into New World and Old World clades, a pattern that sharply contrasted with the phylogenetic relationships inferred from nuclear genome data. These discrepancies between the cytoplasmic and nuclear gene trees likely result from ancient interspecific hybridization within Fagaceae. The decomposition analyses revealed that gene tree estimation error, incomplete lineage sorting, and gene flow accounted for 21.19%, 9.84%, and 7.76% of gene tree variation, respectively. We further revealed that 58.1–59.5% of genes exhibited consistent phylogenetic signals (“consistent genes”), while 40.5–41.9% of genes displayed conflicting signals (“inconsistent genes”). Consistent genes showed stronger phylogenetic signals and were more likely to recover the species tree topology than inconsistent genes. However, consistent and inconsistent genes did not significantly differ in terms of sequence- and tree-based characteristics. By excluding a subset of inconsistent genes, the study significantly reduced inconsistencies between concatenation- and coalescent-based approaches. Conclusions This study illustrates how diverse factors contribute to gene tree incongruence, offering new insights into the evolutionary history of Fagaceae. |
| format | Article |
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| institution | DOAJ |
| issn | 1471-2229 |
| language | English |
| publishDate | 2025-07-01 |
| publisher | BMC |
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| series | BMC Plant Biology |
| spelling | doaj-art-e8142f65364347a686e5ea4d6d41fc162025-08-20T03:04:27ZengBMCBMC Plant Biology1471-22292025-07-0125111610.1186/s12870-025-06963-3Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae)Zhao Shen0Biao-Feng Zhou1Yi-Ye Liang2Jing-Shu Wang3Run-Xian Yu4Yong Shi5Shao-Jun Ling6Wen-Ji Luo7Qiong-Qiong Lin8Jing-Wei Niu9Liang-Jing Qiao10Paul S. Manos11Baosheng Wang12Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesSchool of Life Sciences, State Key Laboratory of Biocontrol and Guangdong Provincial Key Laboratory of Plant Resources, Sun Yat-Sen UniversityGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesDepartment of Biology, Duke UniversityGuangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of SciencesAbstract Background Gene tree incongruence is a well-documented, but the biological and analytical factors driving phylogenetic discordance remains incompletely understood. In this study, we investigated how different factors contribute to incongruence among gene trees in Fagaceae. Results Each dataset produced highly supported topologies, with Fagus and Trigonobalanus consistently placed as early-diverging lineages within the Fagaceae family. However, the cpDNA and mtDNA divided the remaining Fagaceae species into New World and Old World clades, a pattern that sharply contrasted with the phylogenetic relationships inferred from nuclear genome data. These discrepancies between the cytoplasmic and nuclear gene trees likely result from ancient interspecific hybridization within Fagaceae. The decomposition analyses revealed that gene tree estimation error, incomplete lineage sorting, and gene flow accounted for 21.19%, 9.84%, and 7.76% of gene tree variation, respectively. We further revealed that 58.1–59.5% of genes exhibited consistent phylogenetic signals (“consistent genes”), while 40.5–41.9% of genes displayed conflicting signals (“inconsistent genes”). Consistent genes showed stronger phylogenetic signals and were more likely to recover the species tree topology than inconsistent genes. However, consistent and inconsistent genes did not significantly differ in terms of sequence- and tree-based characteristics. By excluding a subset of inconsistent genes, the study significantly reduced inconsistencies between concatenation- and coalescent-based approaches. Conclusions This study illustrates how diverse factors contribute to gene tree incongruence, offering new insights into the evolutionary history of Fagaceae.https://doi.org/10.1186/s12870-025-06963-3Gene tree discordanceHybridizationIncomplete lineage sortingGene tree estimation errorFagaceae |
| spellingShingle | Zhao Shen Biao-Feng Zhou Yi-Ye Liang Jing-Shu Wang Run-Xian Yu Yong Shi Shao-Jun Ling Wen-Ji Luo Qiong-Qiong Lin Jing-Wei Niu Liang-Jing Qiao Paul S. Manos Baosheng Wang Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae) BMC Plant Biology Gene tree discordance Hybridization Incomplete lineage sorting Gene tree estimation error Fagaceae |
| title | Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae) |
| title_full | Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae) |
| title_fullStr | Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae) |
| title_full_unstemmed | Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae) |
| title_short | Teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family (Fagaceae) |
| title_sort | teasing apart the sources of phylogenetic tree discordance across three genomes in the oak family fagaceae |
| topic | Gene tree discordance Hybridization Incomplete lineage sorting Gene tree estimation error Fagaceae |
| url | https://doi.org/10.1186/s12870-025-06963-3 |
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