Ploidy as a leaky reproductive barrier: mechanisms, rates and evolutionary significance of interploidy gene flow.

adaptation evolution genetic introgression polyploidy speciation whole genome duplication

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
13 Jun 2024
Historique:
received: 01 02 2024
medline: 13 6 2024
pubmed: 13 6 2024
entrez: 13 6 2024
Statut: aheadofprint

Résumé

Whole genome duplication (polyploidization) is a dominant force in sympatric speciation, particularly in plants. Genome doubling instantly poses a barrier to gene flow owing to the strong crossing incompatibilities between individuals differing in ploidy. The strength of the barrier, however, varies from species to species and recent genetic investigations revealed cases of rampant interploidy introgression in multiple ploidy-variable species. Here, we review novel insights into the frequency of interploidy gene flow in natural systems and summarize the underlying mechanisms promoting interploidy gene flow. Field surveys, occasionally complemented by crossing experiments, suggest frequent opportunities for interploidy gene flow, particularly in the direction from diploid to tetraploid, and between (higher) polyploids. However, a scarcity of accompanying population genetic evidence and a virtual lack of integration of these approaches leave the underlying mechanisms and levels of realized interploidy gene flow in nature largely unknown. Finally, we discuss potential consequences of interploidy genome permeability on polyploid speciation and adaptation and highlight novel avenues that have just recently been opened by the very first genomic studies of ploidy-variable species. Standing in stark contrast with rapidly accumulating evidence for evolutionary importance of homoploid introgression, similar cases in ploidy-variable systems are yet to be documented. The genomics era provides novel opportunity to re-evaluate the role of interploidy introgression in speciation and adaptation. To achieve this goal, interdisciplinary studies bordering ecology and population genetics and genomics are needed.

Sections du résumé

BACKGROUND BACKGROUND
Whole genome duplication (polyploidization) is a dominant force in sympatric speciation, particularly in plants. Genome doubling instantly poses a barrier to gene flow owing to the strong crossing incompatibilities between individuals differing in ploidy. The strength of the barrier, however, varies from species to species and recent genetic investigations revealed cases of rampant interploidy introgression in multiple ploidy-variable species.
SCOPE METHODS
Here, we review novel insights into the frequency of interploidy gene flow in natural systems and summarize the underlying mechanisms promoting interploidy gene flow. Field surveys, occasionally complemented by crossing experiments, suggest frequent opportunities for interploidy gene flow, particularly in the direction from diploid to tetraploid, and between (higher) polyploids. However, a scarcity of accompanying population genetic evidence and a virtual lack of integration of these approaches leave the underlying mechanisms and levels of realized interploidy gene flow in nature largely unknown. Finally, we discuss potential consequences of interploidy genome permeability on polyploid speciation and adaptation and highlight novel avenues that have just recently been opened by the very first genomic studies of ploidy-variable species. Standing in stark contrast with rapidly accumulating evidence for evolutionary importance of homoploid introgression, similar cases in ploidy-variable systems are yet to be documented.
CONCLUSIONS CONCLUSIONS
The genomics era provides novel opportunity to re-evaluate the role of interploidy introgression in speciation and adaptation. To achieve this goal, interdisciplinary studies bordering ecology and population genetics and genomics are needed.

Identifiants

pubmed: 38868992
pii: 7692267
doi: 10.1093/aob/mcae096
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.

Auteurs

Paolo Bartolić (P)

Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, CZ-128 01 Prague, Czech Republic.

Emma J Morgan (EJ)

Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, CZ-128 01 Prague, Czech Republic.

Nélida Padilla-García (N)

Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, CZ-128 01 Prague, Czech Republic.
Departamento de Botánica y Fisiología Vegetal, University of Salamanca, 37007 Salamanca, Spain.

Filip Kolář (F)

Department of Botany, Faculty of Science, Charles University in Prague, Benátská 2, CZ-128 01 Prague, Czech Republic.

Classifications MeSH