Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition

The transition of traits between genetically related lineages is a fascinating topic that provides clues to understanding the drivers of speciation and diversification. Much can be learned about this process from phylogeny-based trait evolution. However, such inference is often plagued by genome-wid...

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Main Authors: Zengzhu Zhang, Gang Liu, Minjie Li
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2024-01-01
Series:Plant Diversity
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2468265923001038
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author Zengzhu Zhang
Gang Liu
Minjie Li
author_facet Zengzhu Zhang
Gang Liu
Minjie Li
author_sort Zengzhu Zhang
collection DOAJ
description The transition of traits between genetically related lineages is a fascinating topic that provides clues to understanding the drivers of speciation and diversification. Much can be learned about this process from phylogeny-based trait evolution. However, such inference is often plagued by genome-wide gene-tree discordance (GTD), mostly due to incomplete lineage sorting (ILS) and/or introgressive hybridization, especially when the genes underlying the traits appear discordant. Here, by collecting transcriptomes, whole chloroplast genomes (cpDNA), and population genetic datasets, we used the coalescent model to turn GTD into a source of information for ILS and employed hemiplasy to explain specific cases of apparent “phylogenetic discordance” between different morphological traits and probable species phylogeny in the Allium subg. Cyathophora. Both concatenation and coalescence methods consistently showed the same phylogenetic topology for species tree inference based on single-copy genes (SCGs), as supported by the KS distribution. However, GTD was high across the genomes of subg. Cyathophora: ∼27%–38.9% of the SCG trees were in conflict with the species tree. Plasmid and nuclear incongruence was also present. Our coalescent simulations indicated that such GTD was mainly a product of ILS. Our hemiplasy risk factor calculations supported that random fixation of ancient polymorphisms in different populations during successive speciation events along the subg. Cyathophora phylogeny may have caused the character transition, as well as the anomalous cpDNA tree. Our study exemplifies how phylogenetic noise can be transformed into evolutionary information for understanding character state transitions along species phylogenies.
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spelling doaj.art-7a55ed81bb304b3693c35cbe906840c22024-02-04T04:45:50ZengKeAi Communications Co., Ltd.Plant Diversity2468-26592024-01-014612838Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transitionZengzhu Zhang0Gang Liu1Minjie Li2State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Ecology, Lanzhou University, Lanzhou 730000, Gansu, PR ChinaState Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Ecology, Lanzhou University, Lanzhou 730000, Gansu, PR ChinaCorresponding author.; State Key Laboratory of Herbage Improvement and Grassland Agro-Ecosystems, College of Ecology, Lanzhou University, Lanzhou 730000, Gansu, PR ChinaThe transition of traits between genetically related lineages is a fascinating topic that provides clues to understanding the drivers of speciation and diversification. Much can be learned about this process from phylogeny-based trait evolution. However, such inference is often plagued by genome-wide gene-tree discordance (GTD), mostly due to incomplete lineage sorting (ILS) and/or introgressive hybridization, especially when the genes underlying the traits appear discordant. Here, by collecting transcriptomes, whole chloroplast genomes (cpDNA), and population genetic datasets, we used the coalescent model to turn GTD into a source of information for ILS and employed hemiplasy to explain specific cases of apparent “phylogenetic discordance” between different morphological traits and probable species phylogeny in the Allium subg. Cyathophora. Both concatenation and coalescence methods consistently showed the same phylogenetic topology for species tree inference based on single-copy genes (SCGs), as supported by the KS distribution. However, GTD was high across the genomes of subg. Cyathophora: ∼27%–38.9% of the SCG trees were in conflict with the species tree. Plasmid and nuclear incongruence was also present. Our coalescent simulations indicated that such GTD was mainly a product of ILS. Our hemiplasy risk factor calculations supported that random fixation of ancient polymorphisms in different populations during successive speciation events along the subg. Cyathophora phylogeny may have caused the character transition, as well as the anomalous cpDNA tree. Our study exemplifies how phylogenetic noise can be transformed into evolutionary information for understanding character state transitions along species phylogenies.http://www.sciencedirect.com/science/article/pii/S2468265923001038HemiplasyMultispecies coalescenceLineage sortingGene tree discordancePhylotranscriptomicsAllium subg. Cyathophora
spellingShingle Zengzhu Zhang
Gang Liu
Minjie Li
Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition
Plant Diversity
Hemiplasy
Multispecies coalescence
Lineage sorting
Gene tree discordance
Phylotranscriptomics
Allium subg. Cyathophora
title Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition
title_full Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition
title_fullStr Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition
title_full_unstemmed Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition
title_short Phylotranscriptomic discordance is best explained by incomplete lineage sorting within Allium subgenus Cyathophora and thus hemiplasy accounts for interspecific trait transition
title_sort phylotranscriptomic discordance is best explained by incomplete lineage sorting within allium subgenus cyathophora and thus hemiplasy accounts for interspecific trait transition
topic Hemiplasy
Multispecies coalescence
Lineage sorting
Gene tree discordance
Phylotranscriptomics
Allium subg. Cyathophora
url http://www.sciencedirect.com/science/article/pii/S2468265923001038
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AT gangliu phylotranscriptomicdiscordanceisbestexplainedbyincompletelineagesortingwithinalliumsubgenuscyathophoraandthushemiplasyaccountsforinterspecifictraittransition
AT minjieli phylotranscriptomicdiscordanceisbestexplainedbyincompletelineagesortingwithinalliumsubgenuscyathophoraandthushemiplasyaccountsforinterspecifictraittransition