The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications
The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major...
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doaj-fdc1946c0f3848bf92d578ace0124ea82020-11-24T22:24:03ZengFrontiers Media S.A.Frontiers in Ecology and Evolution2296-701X2018-08-01610.3389/fevo.2018.00117389545The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome DuplicationsPierre Baduel0Sian Bray1Mario Vallejo-Marin2Filip Kolář3Filip Kolář4Levi Yant5Levi Yant6Institut de Biologie de l'École Normale Supérieure, Paris, FranceDepartment of Cell and Developmental Biology, John Innes Centre, Norwich, United KingdomBiological and Environmental Sciences, University of Stirling, Stirling, United KingdomDepartment of Botany, University of Innsbruck, Innsbruck, AustriaDepartment of Botany, Faculty of Science, Charles University in Prague, Prague, CzechiaDepartment of Cell and Developmental Biology, John Innes Centre, Norwich, United KingdomSchool of Life Sciences and Future Food Beacon, University of Nottingham, Nottingham, United KingdomThe duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short- and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as “sponges” accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew.https://www.frontiersin.org/article/10.3389/fevo.2018.00117/fullpolyploidyselectionpopulation geneticsevolutionautopolyploidygenome duplication |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Pierre Baduel Sian Bray Mario Vallejo-Marin Filip Kolář Filip Kolář Levi Yant Levi Yant |
spellingShingle |
Pierre Baduel Sian Bray Mario Vallejo-Marin Filip Kolář Filip Kolář Levi Yant Levi Yant The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications Frontiers in Ecology and Evolution polyploidy selection population genetics evolution autopolyploidy genome duplication |
author_facet |
Pierre Baduel Sian Bray Mario Vallejo-Marin Filip Kolář Filip Kolář Levi Yant Levi Yant |
author_sort |
Pierre Baduel |
title |
The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications |
title_short |
The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications |
title_full |
The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications |
title_fullStr |
The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications |
title_full_unstemmed |
The “Polyploid Hop”: Shifting Challenges and Opportunities Over the Evolutionary Lifespan of Genome Duplications |
title_sort |
“polyploid hop”: shifting challenges and opportunities over the evolutionary lifespan of genome duplications |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Ecology and Evolution |
issn |
2296-701X |
publishDate |
2018-08-01 |
description |
The duplication of an entire genome is no small affair. Whole genome duplication (WGD) is a dramatic mutation with long-lasting effects, yet it occurs repeatedly in all eukaryotic kingdoms. Plants are particularly rich in documented WGDs, with recent and ancient polyploidization events in all major extant lineages. However, challenges immediately following WGD, such as the maintenance of stable chromosome segregation or detrimental ecological interactions with diploid progenitors, commonly do not permit establishment of nascent polyploids. Despite these immediate issues some lineages nevertheless persist and thrive. In fact, ecological modeling commonly supports patterns of adaptive niche differentiation in polyploids, with young polyploids often invading new niches and leaving their diploid progenitors behind. In line with these observations of polyploid evolutionary success, recent work documents instant physiological consequences of WGD associated with increased dehydration stress tolerance in first-generation autotetraploids. Furthermore, population genetic theory predicts both short- and long-term benefits of polyploidy and new empirical data suggests that established polyploids may act as “sponges” accumulating adaptive allelic diversity. In addition to their increased genetic variability, introgression with other tetraploid lineages, diploid progenitors, or even other species, further increases the available pool of genetic variants to polyploids. Despite this, the evolutionary advantages of polyploidy are still questioned, and the debate over the idea of polyploidy as an evolutionary dead-end carries on. Here we broadly synthesize the newest empirical data moving this debate forward. Altogether, evidence suggests that if early barriers are overcome, WGD can offer instantaneous fitness advantages opening the way to a transformed fitness landscape by sampling a higher diversity of alleles, including some already preadapted to their local environment. This occurs in the context of intragenomic, population genomic, and physiological modifications that can, on occasion, offer an evolutionary edge. Yet in the long run, early advantages can turn into long-term hindrances, and without ecological drivers such as novel ecological niche availability or agricultural propagation, a restabilization of the genome via diploidization will begin the cycle anew. |
topic |
polyploidy selection population genetics evolution autopolyploidy genome duplication |
url |
https://www.frontiersin.org/article/10.3389/fevo.2018.00117/full |
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