Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes

Next-generation sequencing technologies have facilitated new phylogenomic approaches to help clarify previously intractable relationships while simultaneously highlighting the pervasive nature of incongruence within and among genomes that can complicate definitive taxonomic conclusions. Salvia L., w...

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Main Authors: Jeffrey P. Rose, Ricardo Kriebel, Larissa Kahan, Alexa DiNicola, Jesús G. González-Gallegos, Ferhat Celep, Emily M. Lemmon, Alan R. Lemmon, Kenneth J. Sytsma, Bryan T. Drew
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.767478/full
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author Jeffrey P. Rose
Jeffrey P. Rose
Ricardo Kriebel
Larissa Kahan
Alexa DiNicola
Jesús G. González-Gallegos
Ferhat Celep
Emily M. Lemmon
Alan R. Lemmon
Kenneth J. Sytsma
Bryan T. Drew
author_facet Jeffrey P. Rose
Jeffrey P. Rose
Ricardo Kriebel
Larissa Kahan
Alexa DiNicola
Jesús G. González-Gallegos
Ferhat Celep
Emily M. Lemmon
Alan R. Lemmon
Kenneth J. Sytsma
Bryan T. Drew
author_sort Jeffrey P. Rose
collection DOAJ
description Next-generation sequencing technologies have facilitated new phylogenomic approaches to help clarify previously intractable relationships while simultaneously highlighting the pervasive nature of incongruence within and among genomes that can complicate definitive taxonomic conclusions. Salvia L., with ∼1,000 species, makes up nearly 15% of the species diversity in the mint family and has attracted great interest from biologists across subdisciplines. Despite the great progress that has been achieved in discerning the placement of Salvia within Lamiaceae and in clarifying its infrageneric relationships through plastid, nuclear ribosomal, and nuclear single-copy genes, the incomplete resolution has left open major questions regarding the phylogenetic relationships among and within the subgenera, as well as to what extent the infrageneric relationships differ across genomes. We expanded a previously published anchored hybrid enrichment dataset of 35 exemplars of Salvia to 179 terminals. We also reconstructed nearly complete plastomes for these samples from off-target reads. We used these data to examine the concordance and discordance among the nuclear loci and between the nuclear and plastid genomes in detail, elucidating both broad-scale and species-level relationships within Salvia. We found that despite the widespread gene tree discordance, nuclear phylogenies reconstructed using concatenated, coalescent, and network-based approaches recover a common backbone topology. Moreover, all subgenera, except for Audibertia, are strongly supported as monophyletic in all analyses. The plastome genealogy is largely resolved and is congruent with the nuclear backbone. However, multiple analyses suggest that incomplete lineage sorting does not fully explain the gene tree discordance. Instead, horizontal gene flow has been important in both the deep and more recent history of Salvia. Our results provide a robust species tree of Salvia across phylogenetic scales and genomes. Future comparative analyses in the genus will need to account for the impacts of hybridization/introgression and incomplete lineage sorting in topology and divergence time estimation.
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spelling doaj.art-0a0c55871d0c45e08b0be2f80c35dcac2022-12-21T18:31:51ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-11-011210.3389/fpls.2021.767478767478Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across GenomesJeffrey P. Rose0Jeffrey P. Rose1Ricardo Kriebel2Larissa Kahan3Alexa DiNicola4Jesús G. González-Gallegos5Ferhat Celep6Emily M. Lemmon7Alan R. Lemmon8Kenneth J. Sytsma9Bryan T. Drew10Department of Biology, University of Nebraska at Kearney, Kearney, NE, United StatesDepartment of Botany, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Botany, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Botany, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Botany, University of Wisconsin–Madison, Madison, WI, United StatesCONACYT, Instituto Politeìcnico Nacional, CIIDIR – Durango, Durango, MexicoDepartment of Biology, Faculty of Arts and Sciences, Kırıkkale University, Yahşihan, TurkeyDepartment of Biological Science, Florida State University, Tallahassee, FL, United StatesDepartment of Scientific Computing, Florida State University, Tallahassee, FL, United StatesDepartment of Botany, University of Wisconsin–Madison, Madison, WI, United StatesDepartment of Biology, University of Nebraska at Kearney, Kearney, NE, United StatesNext-generation sequencing technologies have facilitated new phylogenomic approaches to help clarify previously intractable relationships while simultaneously highlighting the pervasive nature of incongruence within and among genomes that can complicate definitive taxonomic conclusions. Salvia L., with ∼1,000 species, makes up nearly 15% of the species diversity in the mint family and has attracted great interest from biologists across subdisciplines. Despite the great progress that has been achieved in discerning the placement of Salvia within Lamiaceae and in clarifying its infrageneric relationships through plastid, nuclear ribosomal, and nuclear single-copy genes, the incomplete resolution has left open major questions regarding the phylogenetic relationships among and within the subgenera, as well as to what extent the infrageneric relationships differ across genomes. We expanded a previously published anchored hybrid enrichment dataset of 35 exemplars of Salvia to 179 terminals. We also reconstructed nearly complete plastomes for these samples from off-target reads. We used these data to examine the concordance and discordance among the nuclear loci and between the nuclear and plastid genomes in detail, elucidating both broad-scale and species-level relationships within Salvia. We found that despite the widespread gene tree discordance, nuclear phylogenies reconstructed using concatenated, coalescent, and network-based approaches recover a common backbone topology. Moreover, all subgenera, except for Audibertia, are strongly supported as monophyletic in all analyses. The plastome genealogy is largely resolved and is congruent with the nuclear backbone. However, multiple analyses suggest that incomplete lineage sorting does not fully explain the gene tree discordance. Instead, horizontal gene flow has been important in both the deep and more recent history of Salvia. Our results provide a robust species tree of Salvia across phylogenetic scales and genomes. Future comparative analyses in the genus will need to account for the impacts of hybridization/introgression and incomplete lineage sorting in topology and divergence time estimation.https://www.frontiersin.org/articles/10.3389/fpls.2021.767478/fullanchored hybrid enrichmentcyto-nuclear discordancedistance metricsincongruenceLamiaceaeRobinson–Foulds distance
spellingShingle Jeffrey P. Rose
Jeffrey P. Rose
Ricardo Kriebel
Larissa Kahan
Alexa DiNicola
Jesús G. González-Gallegos
Ferhat Celep
Emily M. Lemmon
Alan R. Lemmon
Kenneth J. Sytsma
Bryan T. Drew
Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
Frontiers in Plant Science
anchored hybrid enrichment
cyto-nuclear discordance
distance metrics
incongruence
Lamiaceae
Robinson–Foulds distance
title Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
title_full Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
title_fullStr Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
title_full_unstemmed Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
title_short Sage Insights Into the Phylogeny of Salvia: Dealing With Sources of Discordance Within and Across Genomes
title_sort sage insights into the phylogeny of salvia dealing with sources of discordance within and across genomes
topic anchored hybrid enrichment
cyto-nuclear discordance
distance metrics
incongruence
Lamiaceae
Robinson–Foulds distance
url https://www.frontiersin.org/articles/10.3389/fpls.2021.767478/full
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