Variation in heteroploid reproduction and gene flow across a polyploid complex: One size does not fit all

Sutherland, Brittany L.; Galloway, Laura F.

doi:10.1002/ece3.7791

Cited by 7 publications

(3 citation statements)

References 54 publications

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“…In some cases, triploid offspring can produce functional gametes ( Krahulcová and Krahulec 2000 ) that can result in tetraploid offspring ( Peckert and Chrtek 2006 ), but in others there may be complete reproductive isolation between diploids and tetraploids (i.e., triploid-block, Marks 1966 ). In instances where there is a triploid-block but higher level ploidies in the complex exist, gene flow across ploidies can occur between other intermediates (e.g., pentaploids, Peskoller et al 2021 ; Sutherland and Galloway 2021 ). Despite strong evidence of gene flow across ploidies in some animals ( Bogart et al 2020 ; Novikova et al 2020 ), these processes are even further understudied.…”

Section: Introductionmentioning

confidence: 99%

The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs

Booker

Gerhardt

Lemmon

et al. 2021

Molecular Biology and Evolution

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Polyploid speciation has played an important role in evolutionary history across the tree of life, yet there remain large gaps in our understanding of how polyploid species form and persist. While systematic studies have been conducted in numerous polyploid complexes, recent advances in sequencing technology have demonstrated that conclusions from data-limited studies may be spurious and misleading. The North American gray treefrog complex, consisting of the diploid Hyla chrysoscelis and the tetraploid Hyla versicolor, has long been used as a model system in a variety of biological fields, yet all taxonomic studies to date were conducted with only a few loci from nuclear and mitochondrial genomes. Here, we utilized anchored hybrid enrichment and high-throughput sequencing to capture hundreds of loci along with whole mitochondrial genomes to investigate the evolutionary history of this complex. We used several phylogenetic and population genetic methods, including coalescent simulations and testing of polyploid speciation models with Approximate Bayesian Computation (ABC), to determine that H. versicolor was most likely formed via autopolyploidization from a now extinct lineage of H. chrysoscelis. We also uncovered evidence of significant hybridization between diploids and tetraploids where they co-occur, and show that historical hybridization between these groups led to the re-formation of distinct polyploid lineages following the initial whole genome duplication event. Our study indicates that a wide variety of methods and explicit model testing of polyploid histories can greatly facilitate efforts to uncover the evolutionary history of polyploid complexes.

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Section: Introductionmentioning

confidence: 99%

The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs

Booker

Gerhardt

Lemmon

et al. 2021

Molecular Biology and Evolution

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“…Despite the fitness consequences of hybridizing across ploidies, numerous studies have demonstrated pervasive gene flow between autopolyploids and their diploid relatives when their ranges overlap (Arnold et al 2016; Marburger et al 2019; Monnahan et al 2019; Bogart et al 2020; Novikova et al 2020; Shastry et al 2021; Booker et al 2022). Although hybridization across ploidies during formation is often considered a way for neo-polyploids to overcome the massive population bottleneck during formation (Stebbins 1980), admixture following their establishment should be generally disfavored as mixed-ploidy offspring suffer extensive fitness consequences (Ramsey and Schemske 1998)–though this may be mitigated in higher-level ploidies (Peskoller et al 2021; Sutherland and Galloway 2021). However, hybridization to relieve the deleterious load accumulated through range expansion may help to explain why this phenomenon is so pervasive, and why the evolutionary histories of autopolyploids can be so reticulate (e.g.…”

Section: Discussionmentioning

confidence: 99%

The genetic consequences of range expansion and its influence on diploidization in polyploids

Booker,

Schrider

2023

Preprint

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Despite newly formed polyploids being subjected to myriad fitness consequences, the relative prevalence of polyploidy both contemporarily and in ancestral branches of the tree of life suggests alternative advantages that outweigh these consequences. One proposed advantage is that polyploids have an elevated adaptive potential that enables them to colonize novel habitats such as previously glaciated areas. However, previous research conducted in diploids suggests that range expansion comes with a fitness cost as deleterious mutations may fix rapidly on the expansion front. Here, we interrogate the potential consequences of expansion in polyploids by conducting spatially explicit forward-in-time simulations of autopolyploids, allopolyploids, and diploids to investigate how ploidy and inheritance patterns impact the relative ability of polyploids to expand their range. We show that under realistic dominance models, autopolyploids suffer greater fitness reductions than diploids as a result of range expansion due to the fixation of increased mutational load that is masked in the range core. Alternatively, the disomic inheritance of allopolyploids provides a shield to this fixation resulting in minimal fitness consequences under an empirically estimated DFE. In light of this advantage provided by disomy, we investigate how range expansion may influence cytogenetic diploidization through the reversion to disomy in autotetraploids. We show that under both a model of where the mode of inheritance is determined by a small number of loci and a model where inheritance is regulated by chromosomal similarity, disomy evolves more rapidly on the expansion front than in the range core, and that this dynamic inheritance model has additional effects on fitness. Together our results point to a complex interaction between dominance, ploidy, inheritance, and recombination on fitness as a population spreads across a geographic range.

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“…The key reproductive isolation mechanism in the formation of triploids is considered to be the triploid block, which operates in different polyploid systems [22,[57][58][59][60]. The triploid block is caused by malfunction of the endosperm as a result of an imbalance between paternally and maternally imprinted genes during the endosperm development, and often leads to seed abortion [61].…”

Section: Sexuality In Cotoneaster Integerrimus Populationsmentioning

confidence: 99%

Genome Size, Cytotype Diversity and Reproductive Mode Variation of Cotoneaster integerrimus (Rosaceae) from the Balkans

Bogunić

Šiljak-Yakovlev

Mahmutović-Dizdarević

et al. 2021

Plants

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Cotoneaster integerrimus represents a multiploid and facultative apomictic system of widely distributed mountain populations. We used flow cytometry to determine genome size, ploidy level, and reproduction mode variation of the Balkan populations, supplemented by analysis of nuclear microsatellites in order to address: (i) geographic distribution and variation of cytotypes among the populations; (ii) variation of reproduction mode and the frequency of sexuality; (iii) pathways of endosperm formation among the sampled polyploids and their endosperm balance requirements; (iv) genotypic diversity and geographic distribution of clonal lineages of polyploids. The prevalence of apomictic tetraploid cytotype followed by sexual diploids and extremely rare triploids was demonstrated. This prevalence of tetraploids affected the populations’ structure composed from clonal genotypes with varying proportions. The co-occurrence of diploids and tetraploids generated higher cytotype, reproductive mode, and genotypic diversity, but mixed-ploidy sites were extremely rare. The endosperm imbalance facilitates the development and the occurrence of intermediate triploids in mixed-ploidy populations, but also different tetraploid lineages elsewhere with unbalanced endosperm. All these results showed that the South European populations of C. integerrimus have higher levels of cytotype and reproductive diversity compared to the Central European ones. Therefore, the South European populations can be considered as a potential reservoir of regional and global diversity for this species.

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Variation in heteroploid reproduction and gene flow across a polyploid complex: One size does not fit all

Cited by 7 publications

References 54 publications

The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs

The Complex History of Genome Duplication and Hybridization in North American Gray Treefrogs

The genetic consequences of range expansion and its influence on diploidization in polyploids

Genome Size, Cytotype Diversity and Reproductive Mode Variation of Cotoneaster integerrimus (Rosaceae) from the Balkans

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