The role of deep hybridization in fern speciation: Examples from the Thelypteridaceae

Premise Hybridization is recognized as an important mechanism in fern speciation, with many allopolyploids known among congeners, as well as evidence of ancient genome duplications. Several contemporary instances of deep (intergeneric) hybridization have been noted, invariably resulting in sterile p...

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Veröffentlicht in:American journal of botany 2024-08, Vol.111 (8), p.e16388-n/a
Hauptverfasser: Tseng, Yu‐Hsin, Kuo, Li‐Yaung, Borokini, Israel, Fawcett, Susan
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creator Tseng, Yu‐Hsin
Kuo, Li‐Yaung
Borokini, Israel
Fawcett, Susan
description Premise Hybridization is recognized as an important mechanism in fern speciation, with many allopolyploids known among congeners, as well as evidence of ancient genome duplications. Several contemporary instances of deep (intergeneric) hybridization have been noted, invariably resulting in sterile progeny. We chose the christelloid lineage of the family Thelypteridaceae, recognized for its high frequency of both intra‐ and intergeneric hybrids, to investigate recent hybrid speciation between deeply diverged lineages. We also seek to understand the ecological and evolutionary outcomes of resulting lineages across the landscape. Methods By phasing captured reads within a phylogenomic data set of GoFlag 408 nuclear loci using HybPhaser, we investigated candidate hybrids to identify parental lineages. We estimated divergence ages by inferring a dated phylogeny using fossil calibrations with treePL. We investigated ecological niche conservatism between one confirmed intergeneric allotetraploid and its diploid progenitors using the centroid, overlap, unfilling, and expansion (COUE) framework. Results We provide evidence for at least six instances of intergeneric hybrid speciation within the christelloid clade and estimate up to 45 million years of divergence between progenitors. The niche quantification analysis showed moderate niche overlap between an allopolyploid species and its progenitors, with significant divergence from the niche of one progenitor and conservatism to the other. Conclusions The examples provided here highlight the overlooked role that allopolyploidization following intergeneric hybridization may play in fern diversification and range and niche expansions. Applying this approach to other fern taxa may reveal a similar pattern of deep hybridization resulting in highly successful novel lineages.
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Several contemporary instances of deep (intergeneric) hybridization have been noted, invariably resulting in sterile progeny. We chose the christelloid lineage of the family Thelypteridaceae, recognized for its high frequency of both intra‐ and intergeneric hybrids, to investigate recent hybrid speciation between deeply diverged lineages. We also seek to understand the ecological and evolutionary outcomes of resulting lineages across the landscape. Methods By phasing captured reads within a phylogenomic data set of GoFlag 408 nuclear loci using HybPhaser, we investigated candidate hybrids to identify parental lineages. We estimated divergence ages by inferring a dated phylogeny using fossil calibrations with treePL. We investigated ecological niche conservatism between one confirmed intergeneric allotetraploid and its diploid progenitors using the centroid, overlap, unfilling, and expansion (COUE) framework. Results We provide evidence for at least six instances of intergeneric hybrid speciation within the christelloid clade and estimate up to 45 million years of divergence between progenitors. The niche quantification analysis showed moderate niche overlap between an allopolyploid species and its progenitors, with significant divergence from the niche of one progenitor and conservatism to the other. Conclusions The examples provided here highlight the overlooked role that allopolyploidization following intergeneric hybridization may play in fern diversification and range and niche expansions. Applying this approach to other fern taxa may reveal a similar pattern of deep hybridization resulting in highly successful novel lineages.</description><identifier>ISSN: 0002-9122</identifier><identifier>ISSN: 1537-2197</identifier><identifier>EISSN: 1537-2197</identifier><identifier>DOI: 10.1002/ajb2.16388</identifier><identifier>PMID: 39135339</identifier><language>eng</language><publisher>United States: Botanical Society of America, Inc</publisher><subject>allopolyploidy ; allotetraploidy ; botany ; Centroids ; Christella ; Congeners ; data collection ; Diploids ; diploidy ; Divergence ; Ecological niches ; family ; Ferns ; Ferns - classification ; Ferns - genetics ; ferns and fern allies ; fossils ; Genetic Speciation ; genome ; hybrid speciation ; Hybridization ; Hybridization, Genetic ; Hybrids ; intergeneric hybrid ; Intergeneric hybridization ; landscapes ; niche conservatism ; Niche overlap ; Niches ; Pattern analysis ; Phylogeny ; Polyploidy ; progeny ; reticulate evolution ; Speciation ; species ; Thelypteridaceae</subject><ispartof>American journal of botany, 2024-08, Vol.111 (8), p.e16388-n/a</ispartof><rights>2024 The Author(s). published by Wiley Periodicals LLC on behalf of Botanical Society of America.</rights><rights>2024 The Author(s). 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Several contemporary instances of deep (intergeneric) hybridization have been noted, invariably resulting in sterile progeny. We chose the christelloid lineage of the family Thelypteridaceae, recognized for its high frequency of both intra‐ and intergeneric hybrids, to investigate recent hybrid speciation between deeply diverged lineages. We also seek to understand the ecological and evolutionary outcomes of resulting lineages across the landscape. Methods By phasing captured reads within a phylogenomic data set of GoFlag 408 nuclear loci using HybPhaser, we investigated candidate hybrids to identify parental lineages. We estimated divergence ages by inferring a dated phylogeny using fossil calibrations with treePL. We investigated ecological niche conservatism between one confirmed intergeneric allotetraploid and its diploid progenitors using the centroid, overlap, unfilling, and expansion (COUE) framework. Results We provide evidence for at least six instances of intergeneric hybrid speciation within the christelloid clade and estimate up to 45 million years of divergence between progenitors. The niche quantification analysis showed moderate niche overlap between an allopolyploid species and its progenitors, with significant divergence from the niche of one progenitor and conservatism to the other. Conclusions The examples provided here highlight the overlooked role that allopolyploidization following intergeneric hybridization may play in fern diversification and range and niche expansions. 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Several contemporary instances of deep (intergeneric) hybridization have been noted, invariably resulting in sterile progeny. We chose the christelloid lineage of the family Thelypteridaceae, recognized for its high frequency of both intra‐ and intergeneric hybrids, to investigate recent hybrid speciation between deeply diverged lineages. We also seek to understand the ecological and evolutionary outcomes of resulting lineages across the landscape. Methods By phasing captured reads within a phylogenomic data set of GoFlag 408 nuclear loci using HybPhaser, we investigated candidate hybrids to identify parental lineages. We estimated divergence ages by inferring a dated phylogeny using fossil calibrations with treePL. We investigated ecological niche conservatism between one confirmed intergeneric allotetraploid and its diploid progenitors using the centroid, overlap, unfilling, and expansion (COUE) framework. Results We provide evidence for at least six instances of intergeneric hybrid speciation within the christelloid clade and estimate up to 45 million years of divergence between progenitors. The niche quantification analysis showed moderate niche overlap between an allopolyploid species and its progenitors, with significant divergence from the niche of one progenitor and conservatism to the other. Conclusions The examples provided here highlight the overlooked role that allopolyploidization following intergeneric hybridization may play in fern diversification and range and niche expansions. 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source MEDLINE; Wiley Online Library Journals Frontfile Complete
subjects allopolyploidy
allotetraploidy
botany
Centroids
Christella
Congeners
data collection
Diploids
diploidy
Divergence
Ecological niches
family
Ferns
Ferns - classification
Ferns - genetics
ferns and fern allies
fossils
Genetic Speciation
genome
hybrid speciation
Hybridization
Hybridization, Genetic
Hybrids
intergeneric hybrid
Intergeneric hybridization
landscapes
niche conservatism
Niche overlap
Niches
Pattern analysis
Phylogeny
Polyploidy
progeny
reticulate evolution
Speciation
species
Thelypteridaceae
title The role of deep hybridization in fern speciation: Examples from the Thelypteridaceae
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