Phylogenomic analyses in Phrymaceae reveal extensive gene tree discordance in relationships among major clades

Premise Phylogenomic datasets using genomes and transcriptomes provide rich opportunities beyond resolving bifurcating phylogenetic relationships. Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a well‐supported phylogeny as a basis for a stable taxonomy and f...

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Veröffentlicht in:American journal of botany 2022-06, Vol.109 (6), p.1035-1046
Hauptverfasser: Morales‐Briones, Diego F., Lin, Nan, Huang, Eileen Y., Grossenbacher, Dena L., Sobel, James M., Gilmore, Caroline D., Tank, David C., Yang, Ya
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container_end_page 1046
container_issue 6
container_start_page 1035
container_title American journal of botany
container_volume 109
creator Morales‐Briones, Diego F.
Lin, Nan
Huang, Eileen Y.
Grossenbacher, Dena L.
Sobel, James M.
Gilmore, Caroline D.
Tank, David C.
Yang, Ya
description Premise Phylogenomic datasets using genomes and transcriptomes provide rich opportunities beyond resolving bifurcating phylogenetic relationships. Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a well‐supported phylogeny as a basis for a stable taxonomy and for macroevolutionary comparisons. Methods We sampled 24 genomes and transcriptomes in Phrymaceae and closely related families, including eight newly sequenced transcriptomes. We reconstructed the phylogeny using IQ‐TREE and ASTRAL, evaluated gene tree discordance using PhyParts, Quartet Sampling, and a cloudogram, and carried out reticulation analyses using PhyloNet and HyDe. We searched for whole genome duplication (WGD) events using chromosome numbers, synonymous distances, and gene duplication events as evidence. Results Most gene trees support the monophyly of Phrymaceae and each of its tribes. Most gene trees also support tribe Mimuleae being sister to Phrymeae + Diplaceae + Leucocarpeae, with extensive gene tree discordance among the latter three. Despite the discordance, the monophyly of Mimulus s.l. is rejected, and no individual reticulation event among the Phrymaceae tribes is well‐supported. Reticulation likely occurred among Erythranthe bicolor and closely related species. No ancient WGD was detected in Phrymaceae. Instead, small‐scale duplications are among potential drivers of macroevolutionary diversification of Phrymaceae. Conclusions We show that analysis of reticulate evolution is sensitive to taxon sampling and methods used. We also demonstrate that phylogenomic datasets using genomes and transcriptomes present rich opportunities to investigate gene family evolution and genome duplication events involved in lineage diversification and adaptation.
doi_str_mv 10.1002/ajb2.1860
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Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a well‐supported phylogeny as a basis for a stable taxonomy and for macroevolutionary comparisons. Methods We sampled 24 genomes and transcriptomes in Phrymaceae and closely related families, including eight newly sequenced transcriptomes. We reconstructed the phylogeny using IQ‐TREE and ASTRAL, evaluated gene tree discordance using PhyParts, Quartet Sampling, and a cloudogram, and carried out reticulation analyses using PhyloNet and HyDe. We searched for whole genome duplication (WGD) events using chromosome numbers, synonymous distances, and gene duplication events as evidence. Results Most gene trees support the monophyly of Phrymaceae and each of its tribes. Most gene trees also support tribe Mimuleae being sister to Phrymeae + Diplaceae + Leucocarpeae, with extensive gene tree discordance among the latter three. Despite the discordance, the monophyly of Mimulus s.l. is rejected, and no individual reticulation event among the Phrymaceae tribes is well‐supported. Reticulation likely occurred among Erythranthe bicolor and closely related species. No ancient WGD was detected in Phrymaceae. Instead, small‐scale duplications are among potential drivers of macroevolutionary diversification of Phrymaceae. Conclusions We show that analysis of reticulate evolution is sensitive to taxon sampling and methods used. We also demonstrate that phylogenomic datasets using genomes and transcriptomes present rich opportunities to investigate gene family evolution and genome duplication events involved in lineage diversification and adaptation.</description><identifier>ISSN: 0002-9122</identifier><identifier>EISSN: 1537-2197</identifier><identifier>DOI: 10.1002/ajb2.1860</identifier><identifier>PMID: 35462411</identifier><language>eng</language><publisher>United States: Botanical Society of America, Inc</publisher><subject>Chromosomes ; Datasets ; Diplacus ; Discordance ; Ecology ; Erythranthe ; Evolution ; Gene duplication ; Genomes ; Lamiales ; Mimulus ; Phrymaceae ; Phylogeny ; Reproduction (copying) ; reticulate evolution ; Sampling ; Taxonomy ; transcriptome ; Transcriptomes ; whole genome duplication</subject><ispartof>American journal of botany, 2022-06, Vol.109 (6), p.1035-1046</ispartof><rights>2022 The Authors. published by Wiley Periodicals LLC on behalf of Botanical Society of America.</rights><rights>2022 The Authors. American Journal of Botany published by Wiley Periodicals LLC on behalf of Botanical Society of America.</rights><rights>Copyright Botanical Society of America, Inc. 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Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a well‐supported phylogeny as a basis for a stable taxonomy and for macroevolutionary comparisons. Methods We sampled 24 genomes and transcriptomes in Phrymaceae and closely related families, including eight newly sequenced transcriptomes. We reconstructed the phylogeny using IQ‐TREE and ASTRAL, evaluated gene tree discordance using PhyParts, Quartet Sampling, and a cloudogram, and carried out reticulation analyses using PhyloNet and HyDe. We searched for whole genome duplication (WGD) events using chromosome numbers, synonymous distances, and gene duplication events as evidence. Results Most gene trees support the monophyly of Phrymaceae and each of its tribes. Most gene trees also support tribe Mimuleae being sister to Phrymeae + Diplaceae + Leucocarpeae, with extensive gene tree discordance among the latter three. Despite the discordance, the monophyly of Mimulus s.l. is rejected, and no individual reticulation event among the Phrymaceae tribes is well‐supported. Reticulation likely occurred among Erythranthe bicolor and closely related species. No ancient WGD was detected in Phrymaceae. Instead, small‐scale duplications are among potential drivers of macroevolutionary diversification of Phrymaceae. Conclusions We show that analysis of reticulate evolution is sensitive to taxon sampling and methods used. We also demonstrate that phylogenomic datasets using genomes and transcriptomes present rich opportunities to investigate gene family evolution and genome duplication events involved in lineage diversification and adaptation.</description><subject>Chromosomes</subject><subject>Datasets</subject><subject>Diplacus</subject><subject>Discordance</subject><subject>Ecology</subject><subject>Erythranthe</subject><subject>Evolution</subject><subject>Gene duplication</subject><subject>Genomes</subject><subject>Lamiales</subject><subject>Mimulus</subject><subject>Phrymaceae</subject><subject>Phylogeny</subject><subject>Reproduction (copying)</subject><subject>reticulate evolution</subject><subject>Sampling</subject><subject>Taxonomy</subject><subject>transcriptome</subject><subject>Transcriptomes</subject><subject>whole genome duplication</subject><issn>0002-9122</issn><issn>1537-2197</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kU1v1DAQhi0EotvCgT-ALHGhh7S24yT2Bamt-FQleoCzNXEmu1459mJnF_LvSdhSARKn0WgeP5rxS8gLzi44Y-IStq244Kpmj8iKV2VTCK6bx2TF5mGhuRAn5DTn7dxqqcVTclJWshaS8xUJd5vJxzWGODhLIYCfMmbqAr3bpGkAi4A04QHBU_wxYsjugHTmkY4JkXYu25g6CBaXRwk9jC6GvHG7TGGIYU0H2MZErYcO8zPypAef8fl9PSNf3739cvOhuP38_uPN1W1hpSxZwVmvpOYalZCya6q2YZUCkKJHDh1HrYVsrUStNCil2rpXldQdttJiVZVQnpE3R-9u3w7YWQxjAm92yQ2QJhPBmb8nwW3MOh6MLoUq62YWvL4XpPhtj3k0w3wpeg8B4z4bUVcVZ0JVfEZf_YNu4z7NP7lQquSN5FrP1PmRsinmnLB_WIYzs6RolhTNkuLMvvxz-wfyd2wzcHkEvjuP0_9N5urTtfil_AlKVahu</recordid><startdate>202206</startdate><enddate>202206</enddate><creator>Morales‐Briones, Diego F.</creator><creator>Lin, Nan</creator><creator>Huang, Eileen Y.</creator><creator>Grossenbacher, Dena L.</creator><creator>Sobel, James M.</creator><creator>Gilmore, Caroline D.</creator><creator>Tank, David C.</creator><creator>Yang, Ya</creator><general>Botanical Society of America, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6221-0984</orcidid><orcidid>https://orcid.org/0000-0003-1535-5739</orcidid></search><sort><creationdate>202206</creationdate><title>Phylogenomic analyses in Phrymaceae reveal extensive gene tree discordance in relationships among major clades</title><author>Morales‐Briones, Diego F. ; Lin, Nan ; Huang, Eileen Y. ; Grossenbacher, Dena L. ; Sobel, James M. ; Gilmore, Caroline D. ; Tank, David C. ; Yang, Ya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4430-10f84919e8244d75b7058aa42fe1ad1e9924bc4e989a888b6f8549deb4ce553a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Chromosomes</topic><topic>Datasets</topic><topic>Diplacus</topic><topic>Discordance</topic><topic>Ecology</topic><topic>Erythranthe</topic><topic>Evolution</topic><topic>Gene duplication</topic><topic>Genomes</topic><topic>Lamiales</topic><topic>Mimulus</topic><topic>Phrymaceae</topic><topic>Phylogeny</topic><topic>Reproduction (copying)</topic><topic>reticulate evolution</topic><topic>Sampling</topic><topic>Taxonomy</topic><topic>transcriptome</topic><topic>Transcriptomes</topic><topic>whole genome duplication</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Morales‐Briones, Diego F.</creatorcontrib><creatorcontrib>Lin, Nan</creatorcontrib><creatorcontrib>Huang, Eileen Y.</creatorcontrib><creatorcontrib>Grossenbacher, Dena L.</creatorcontrib><creatorcontrib>Sobel, James M.</creatorcontrib><creatorcontrib>Gilmore, Caroline D.</creatorcontrib><creatorcontrib>Tank, David C.</creatorcontrib><creatorcontrib>Yang, Ya</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>American journal of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Morales‐Briones, Diego F.</au><au>Lin, Nan</au><au>Huang, Eileen Y.</au><au>Grossenbacher, Dena L.</au><au>Sobel, James M.</au><au>Gilmore, Caroline D.</au><au>Tank, David C.</au><au>Yang, Ya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phylogenomic analyses in Phrymaceae reveal extensive gene tree discordance in relationships among major clades</atitle><jtitle>American journal of botany</jtitle><addtitle>Am J Bot</addtitle><date>2022-06</date><risdate>2022</risdate><volume>109</volume><issue>6</issue><spage>1035</spage><epage>1046</epage><pages>1035-1046</pages><issn>0002-9122</issn><eissn>1537-2197</eissn><abstract>Premise Phylogenomic datasets using genomes and transcriptomes provide rich opportunities beyond resolving bifurcating phylogenetic relationships. Monkeyflower (Phrymaceae) is a model system for evolutionary ecology. However, it lacks a well‐supported phylogeny as a basis for a stable taxonomy and for macroevolutionary comparisons. Methods We sampled 24 genomes and transcriptomes in Phrymaceae and closely related families, including eight newly sequenced transcriptomes. We reconstructed the phylogeny using IQ‐TREE and ASTRAL, evaluated gene tree discordance using PhyParts, Quartet Sampling, and a cloudogram, and carried out reticulation analyses using PhyloNet and HyDe. We searched for whole genome duplication (WGD) events using chromosome numbers, synonymous distances, and gene duplication events as evidence. Results Most gene trees support the monophyly of Phrymaceae and each of its tribes. Most gene trees also support tribe Mimuleae being sister to Phrymeae + Diplaceae + Leucocarpeae, with extensive gene tree discordance among the latter three. Despite the discordance, the monophyly of Mimulus s.l. is rejected, and no individual reticulation event among the Phrymaceae tribes is well‐supported. Reticulation likely occurred among Erythranthe bicolor and closely related species. No ancient WGD was detected in Phrymaceae. Instead, small‐scale duplications are among potential drivers of macroevolutionary diversification of Phrymaceae. Conclusions We show that analysis of reticulate evolution is sensitive to taxon sampling and methods used. We also demonstrate that phylogenomic datasets using genomes and transcriptomes present rich opportunities to investigate gene family evolution and genome duplication events involved in lineage diversification and adaptation.</abstract><cop>United States</cop><pub>Botanical Society of America, Inc</pub><pmid>35462411</pmid><doi>10.1002/ajb2.1860</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-6221-0984</orcidid><orcidid>https://orcid.org/0000-0003-1535-5739</orcidid><oa>free_for_read</oa></addata></record>
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subjects Chromosomes
Datasets
Diplacus
Discordance
Ecology
Erythranthe
Evolution
Gene duplication
Genomes
Lamiales
Mimulus
Phrymaceae
Phylogeny
Reproduction (copying)
reticulate evolution
Sampling
Taxonomy
transcriptome
Transcriptomes
whole genome duplication
title Phylogenomic analyses in Phrymaceae reveal extensive gene tree discordance in relationships among major clades
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