Are polyploids really evolutionary dead‐ends (again)? A critical reappraisal of Mayrose<i>et al</i>. (2011)

Soltis, Douglas E.; Segovia-Salcedo, M. Claudia; Jordon‐Thaden, Ingrid E.; Majure, Lucas C.; Miles, Nicolas M.; Mavrodiev, Evgeny V.; Mei, Wenbin; Cortez, Maria Beatriz de Souza; Soltis, Pamela S.; Gitzendanner, Matthew A.

doi:10.1111/nph.12756

Cited by 159 publications

(180 citation statements)

References 122 publications

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“…Polyploidy has both costs and benefits, and under stable environmental conditions, polyploidy is considered to be disadvantageous due to the reduced fitness of polyploid individuals caused by their reproductive isolation and lower fertility (Comai, 2005). The lower speciation/diversification rates and higher extinction rates observed in neopolyploids compared with diploids (Mayrose et al, 2011) could be due to sampling errors and methodological shortcomings (Soltis et al, 2014) or may also be a consequence of the outweighing costs of polyploidy associated genomic and phenotypic instability, as well as the reproductive disadvantages under normal conditions. However, the adaptive advantages of polyploidy caused by enhanced genetic repertoire (resulting from increased heterozygosity, the buffering effect of gene redundancy on mutations, neofunctionalization, differential expression, or epigenetic reprogramming of duplicated genes) and reproductive plasticity (facilitation of reproduction through selffertilization or asexual means) would be expected to confer a competitive advantage to polyploid species under extreme and unstable environmental conditions (Comai, 2005;Fawcett and Van de Peer, 2010).…”

Section: Discussionmentioning

confidence: 99%

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

et al. 2014

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The Brassicaceae (Cruciferae) family, owing to its remarkable species, genetic, and physiological diversity as well as its significant economic potential, has become a model for polyploidy and evolutionary studies. Utilizing extensive transcriptome pyrosequencing of diverse taxa, we established a resolved phylogeny of a subset of crucifer species. We elucidated the frequency, age, and phylogenetic position of polyploidy and lineage separation events that have marked the evolutionary history of the Brassicaceae. Besides the well-known ancient a (47 million years ago [Mya]) and b (124 Mya) paleopolyploidy events, several species were shown to have undergone a further more recent (;7 to 12 Mya) round of genome multiplication. We identified eight whole-genome duplications corresponding to at least five independent neo/mesopolyploidy events. Although the Brassicaceae family evolved from other eudicots at the beginning of the Cenozoic era of the Earth (60 Mya), major diversification occurred only during the Neogene period (0 to 23 Mya). Remarkably, the widespread species divergence, major polyploidy, and lineage separation events during Brassicaceae evolution are clustered in time around epoch transitions characterized by prolonged unstable climatic conditions. The synchronized diversification of Brassicaceae species suggests that polyploid events may have conferred higher adaptability and increased tolerance toward the drastically changing global environment, thus facilitating species radiation.

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Section: Discussionmentioning

confidence: 99%

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

et al. 2014

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“…In particular, WGDs have greatly contributed to plant evolution and speciation (Wood et al, 2009;Jiao et al, 2011). However, to what extent WGD leads to the origin of novel adaptive traits and fosters species radiation remains controversial (Ohno, 1970;Arrigo and Barker, 2012;Soltis et al, 2014). Comprehensive understanding of the molecular and evolutionary processes underlying the preservation and diversification of duplicated genes may thus be central to an integrative consideration of organismal diversity (McGrath and Lynch, 2012;Nei, 2013).…”

Section: Introductionmentioning

confidence: 99%

Repeated Whole-Genome Duplication, Karyotype Reshuffling, and Biased Retention of Stress-Responding Genes in Buckler Mustard

et al. 2015

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Whole-genome duplication (WGD) is usually followed by gene loss and karyotype repatterning. Despite evidence of new adaptive traits associated with WGD, the underpinnings and evolutionary significance of such genome fractionation remain elusive. Here, we use Buckler mustard (Biscutella laevigata) to infer processes that have driven the retention of duplicated genes after recurrent WGDs. In addition to the b-and a-WGD events shared by all Brassicaceae, cytogenetic and transcriptome analyses revealed two younger WGD events that occurred at times of environmental changes in the clade of Buckler mustard (Biscutelleae): a mesopolyploidy event from the late Miocene that was followed by considerable karyotype reshuffling and chromosome number reduction and a neopolyploidy event during the Pleistocene. Although a considerable number of the older duplicates presented signatures of retention under positive selection, the majority of retained duplicates arising from the younger mesopolyploidy WGD event matched predictions of the gene balance hypothesis and showed evidence of strong purifying selection as well as enrichment in gene categories responding to abiotic stressors. Retention of large stretches of chromosomes for both genomic copies supported the hypothesis that cycles of WGD and biased fractionation shaped the genome of this stress-tolerant polypolyloid, promoting the adaptive recruitment of stress-responding genes in the face of environmental challenges.

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“…This expected reduction in genetic diversity has led to some authors to propose that polyploidisation should be an evolutionary dead end (e.g. Stebbins 1950), and recent work suggests that polyploid lineages have lower rates of speciation than diploid lineages (Mayrose et al 2011;Arrigo and Barker 2012; but see Soltis et al 2014a). Yet, the successful establishment of some polyploid lineages indicates that the severity of the challenges associated with the origin of polyploids, including the loss of genetic diversity due to small population sizes at their origin, can sometimes be circumvented.…”

Section: Introductionmentioning

confidence: 99%

Partial interfertility between independently originated populations of the neo-allopolyploid Mimulus peregrinus

et al. 2017

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The reduction in genetic diversity in polyploid lineages, formed from whole-genome duplication of a few individuals, can affect their long-term evolutionary potential. Because most polyploids originate multiple times, secondary contact and gene exchange among independently formed polyploids can create novel genetic combinations and reduce the severity of genetic bottlenecks. However, independently originated polyploids may be reproductively isolated from each other due to genetic and chromosomal differences predating the polyploidisation event, or evolving subsequently in the dynamic genomes of young polyploid populations. Here we conducted experimental crosses to investigate the phenotype and interfertility between two independently originated populations of the allopolyploid Mimulus peregrinus (Phrymaceae). We found that individuals from the two populations are phenotypically distinct, but that inter-and intrapopulation crosses are not statistically different. Interpopulation crosses produce viable and fertile offspring, although our results suggest the existence of partial reproductive barriers in the form of reduced pollen viability. We found no difference in pollen viability between F1 and F2 generations. In contrast, we detected a reduction in floral and vegetative size, and in the proportion of plants that flowered, between F1 and F2 generations for both intra-and interpopulation crosses. Together, our results indicate that populations of independent origin can partially exchange genes, producing variable offspring, and that the phenotype of M. peregrinus may be unstable in the early generations. Natural selection on genetically based variation may be required for the evolution of more stable and fertile individuals of this nascent allopolyploid.

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Are polyploids really evolutionary dead‐ends (again)? A critical reappraisal of Mayroseet al. (2011)

Cited by 159 publications

References 122 publications

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

Polyploid Evolution of the Brassicaceae during the Cenozoic Era

Repeated Whole-Genome Duplication, Karyotype Reshuffling, and Biased Retention of Stress-Responding Genes in Buckler Mustard

Partial interfertility between independently originated populations of the neo-allopolyploid Mimulus peregrinus

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