On the relative abundance of autopolyploids and allopolyploids

New Phytologist, Journal Year: 2015, Volume and Issue: 210(2), P. 391 - 398

Published: Oct. 6, 2015

The prevalence of autopolyploids in angiosperms has long been a subject debate. Müntzing (1936) and Darlington (1937) concluded that were common important evolutionary entities. However, Clausen et al. (1945) Stebbins (1947) subsequently considered them rare, part because the criteria upon which interpretations autopolyploidy rendered not rigorous. This position was reiterated by Grant (1981) decades later, although evidence mounting autopolyploid taxa might be natural populations (Lewis, 1980). As cytological genetic data have accumulated, it become increasingly apparent latter view is likely to correct (Soltis al., 2004b, 2007, 2010). still appears majority polyploids are allopolyploids (Parisod 2010; Soltis 2010), even though Ramsey & Schemske (1998, p. 467) conclude 'the rate formation may often higher than allopolyploid formation.' In this letter we survey literature assess whether indeed prevailing cytotype nature. Using our new estimates for incidence allopolyploidy, discuss some dynamics driving their frequencies Finally, suggest avenues future research on polyploidy build results other recent progress field. Polyploidy enjoyed renaissance over past decade 2014b). Advances plant genomics revealed history throughout evolution (Cui 2006; Barker 2008, 2009; Shi Jiao 2011, 2012, 2014; Arrigo Barker, 2012; Vekemans Kagale Cannon 2015; Edger 2015). Among contemporary species, wealth phylogenetic analyzed with tools (Mayrose 2010, 2015) estimate frequency, incidence, diversification polyploid species (Otto Whitton, 2000; Meyers Levin, Wood Mayrose Scarpino 2014a). Despite progress, these analyses addressed relative contributions autopolylpoidy allopolyploidy evolution. Although researchers speciation rare (Clausen 1945; Stebbins, 1947), current consensus probably more element diversity historic views suggest. Autopolyploid underestimated, perhaps greatly, taxonomists do recognize as 2007). These taxonomically cryptic cytotypes comprise substantial fraction diversity. A precise census frequency importance remains unavailable. We surveyed systematic evaluate within genera. Phylogenetic, cytological, integrated develop an empirical taxa. from 47 vascular genera representing 4003 (Supporting Information Table S1, Methods S1). assembled initial phylogenies at least 30% represented. Following survey, cross-referenced those chromosome counts (Wood Rice additional nature genus (e.g. allozyme, microsatellite, or amplified fragment length polymorphism (AFLP) studies). combination sets yielded 43 > represented four 50 available data. collected nearly 300 publications (Methods S1) used assign ploidy level (diploid vs polyploid) (autopolyploid allopolyploid). inferred multiple base count each (2009). Polyploids also frequently identified methods, such isozyme microsatellite evidence, included set (Table Note account origins species. Thus, estimated rather number did unnamed meet various concepts. Given itself reproductive barrier, most would fulfill requirements biological concept. divided into based reports survey. continuum parental divergences yields corresponding distribution natures true autopolyploids, 'hybrid autopolyploids', 'segmental allopolyploids', (Stebbins, 1950), distinguish gradations. Across genera, found 76% diploids 24% (Fig. 1a). similar previous 2011) largely different set. Our confirmed 2007; Parisod 2010) prevalent indicated taxonomy alone. all 13% whereas 11% allopolyploids. near parity contrasts expectation predominant 1947; Grant, 1981), but consistent many overlooked Husband 2013). Notably, named unnamed, represent c. very unpublished Flora California reported (2007). estimate, J. B. C. (unpublished) 334 2647 contained (Husband Assuming single taxon, 11.2% autopolyploids. taxa, consistency suggests values robust. Differences taxonomic practice appear primary source perception 1b). More 87% recognized only 12% named. Much difference attributable fact distinct morphological features 1947). concepts 2007), they relegated cytotypes. finds recommendation (2007), should provide accurate accounting further elucidate processes proportion constitutes continuous across sampled 1c). there whose either allopolyploid, mixture On average, 50% autos allos. mean had 95% confidence interval 43% 56%, standard deviation 21%. requires opportunities hybridization, vary widely degree interspecific hybridization (Whitney differential production success ploidal types varies phylogeny. Whether differences proportions reflects production, persistence, clear present study, avenue research. How flowering exist nature? Current 350 000 another 10–20% general (Joppa 2011). 53.2% 1b; 1). numbers representative angiosperms, 51 000–61 relied recognition literature, unknown magnitude. will challenging traits alone, naming does where autos, unnamed. relatively restricted geographically ecologically, lack confounds biogeographic genomic compiled (Goff 2011; Boyle 2013; Matasci Violle Wickett 2015), individuals levels properly recognized. For represents cytotypes, users databases. Genome duplication associated physiological shifts (Chao 2013) could distort biogeographic, functional genomic, ecological analyses. Applying names improve large disparity rates. (1998) rates per generation basis unreduced gamete range When gametes come fertile diploids, autotetraploid 2.16 × 10−5 h (1.22 10−3) allotetraploids, refers rate, assuming plants outcrossing. They (Ramsey Schemske, 1998) 0.0272 2.7% required allotetraploid equal. low possible diploid hybrids almost times greater nonhybrids (27.5% 0.6%). case self-fertilization, 7.14 (4.05 10−2) allopolyploids, hybridization. 0.17% yield equal formation. Is frequent enough formation? Very little known about ranges wild 1998). If partially sympatric and/or local conditions allowing contact rarely met, then mixed B, vice versa. example, if 1% species' 2.7%, 100 1.35%, 200 greater. Of course, much < 1%. Accordingly, seems It tempting two good portion ranges, achieved. factors, mating system, play role allopolyploidy. selfing increase, (or outcrossing any type) must go down. transpecific value achieved, especially somewhat preferences. models indicate boon establishment persistence (Rausch Morgan, 2005). Modest spatial differentiation limited dispersal, combined increased enhance (Baack, Thus usually far exceed selfing. discussion thus assumed occurs uniformly apparently absent others. Ellstrand (1996) reviewed regional biosystematic floras Europe, North America, Hawaiian islands hybrids. percentages ranged high 16% (British Isles) 6% (Hawaii). Whitney (2010) expanded study include United States one Australia. Globally, hybrids, 84% not. coexisting congeners unable foster viable potential hybridize typically divergent niche prevents co-occurrence. Most relevant discussion, absence rarity vast 3200 indicates exceeds production. genesis unchanging variable, fertility relationship B constant time. case. closer get time ancestor, hybrid be. Hybrid declines sterility by-product stochastic, nonadaptive chromosomal changes (Levin, Coyne 2004; Lowry 2008; Fierst Hansen, Matute Moyle Nakazato, Presgraves, Sherman Larcombe less prone producing gametes, progeny There conflicting contention literature. Consistent expectation, studies (Chapman Burke, Paun 2009) produced homoploid result crosses between closely related Buggs (2008) actually random draw divergence. (Buggs 2009, came conclusion after re-assessing Chapman Burke (2007) (2009) purposes unclear divergence formed congeneric cross. varying incompatibilities resolve novelty, combinations face challenges persistence. At least, among subsequent restricts narrower window arguments made assume via triploid bridge, process involves successive generations (Harlan DeWet, 1975; Allopolyploid bridge ubiquitous time, argued earlier. fewer expected According (1998), accounts outcrossers. occurred nature, significant advantage. course deep five-fold 20-fold. approaches insight advantage differential, lineages lineages, else being An accrue population occur genome doubling, when genomes present, provides immediate vehicle transcending niches. Greater progenitor neopolyploid increases proximity opportunity mate neopolyploids, key factor (Fowler 1984; Rodriguez, 1996; 2002; Oswald Nuismer, addition, lead competition progenitors competitive advantage, correlatively growth, essential survive demographic environmental stochasticity. ability exploit novel habitats manifested, abundance recently deglaciated areas (Brochmann 2004). seem adept colonizing beyond tolerances (te Beest 2012). neoautoploids lower fertilities neoalloploids 2002). Allopolyploids endure change better former marshal resources through reorganization flexibility gene expression cope stresses (Doyle Leitch Leitch, Jackson Chen, survival union same products (Paun nascent cannot particular type change, others survive, persist. Aegilops (Meimberg 2009), Asplenium (Werth 1985), Mimulus (Vallejo-Marín Senecio (Abbott 2007) Tragopogon 2004a), bode well longevity. [Correction added online publication 6 October 2015: preceding sentence text 'Galax (Servick 2015)' deleted.] Whereas directly measure failure can consider variable taxon vulnerability, namely geographical size. Taxa vulnerable extinction narrow distributions (Gaston Fuller, Birand 2012), small (Dynesius Jansson, 2014). Small sizes sensitivity stochasticity, heightened inbreeding, reduced (Mayr, 1963; Anacker Strauss, Taxon vulnerability breadths (Morin Lechowicz, Slatyer Are extirpation aforementioned criteria, apt shorter duration taxa? few direction polyploids. briefly ponder magnitude difference. Let us diverging, lives 20 million years, 5 years 10 years. Since diverging time-frame expect 80 Even five greater, 40 Yet, representation. To achieve parity, 40-fold lineage diversification. 'fitness' quite surprising, believe conservative. pair 50:1, easily 100-fold. Better needed how phylogeny contribute shown that, approximate terms numbers. now mechanistic explanation why appreciate, (2007, holistic approach, populations, ultimately form novel, long-lived outcrossers exceeded always sympatry today (assuming allopatric parapatric speciation), move towards splitting. Logic substitute data; lacking aspects expectations 2011), biases inclusive tropical woody useful. size continue systematists relationships groups. agree call global angiosperm (Galbraith address gaps need (De Storme Mason, comprehensive assessment internal needed. establish sympatry, determine cross-compatible congener. New gained extending model (Suda Herben, reasonably fruitful extend work meiosis (Hollister Wright selection meiotic machinery differentially influence Research genetics Geelen, 2013a,b) show promise advancements area. Mining molecular insights penchant branching Hopefully, spur efforts investigate product vantage points renewed vigor. authors thank K. Dlugosch, S. Jorgensen, X. Qi, E. Sessa three anonymous reviewers thoughtful comments manuscript. funded SNSF Ambizione grant (PZ00P3_148224) N.A. NSF-IOS-1339156 M.S.B. M.S.B., D.A.L. planned designed A.E.B. Z.L. conducted N.A., wrote Please note: Wiley Blackwell responsible content functionality supporting information supplied authors. Any queries (other missing material) directed Phytologist Central Office. publisher content) author article.

Language: Английский

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The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization

Nature Ecology & Evolution, Journal Year: 2020, Volume and Issue: 4(6), P. 841 - 852

Published: March 30, 2020

Abstract Sturgeons seem to be frozen in time. The archaic characteristics of this ancient fish lineage place it a key phylogenetic position at the base ~30,000 modern teleost species. Moreover, sturgeons are notoriously polyploid, providing unique opportunities investigate evolution polyploid genomes. We assembled high-quality chromosome-level reference genome for sterlet, Acipenser ruthenus . Our analysis revealed very low protein rate that is least as slow other deep branches vertebrate tree, such coelacanth. uncovered whole-genome duplication occurred Jurassic, early entire sturgeon lineage. Following polyploidization, rediploidization included loss whole chromosomes segmental deduplication process. While known adaptive processes helped conserve high degree structural and functional tetraploidy over more than 180 million years, reduction redundancy seems have been remarkably random.

Language: Английский

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Post-polyploid diploidization and diversification through dysploid changes

Current Opinion in Plant Biology, Journal Year: 2018, Volume and Issue: 42, P. 55 - 65

Published: March 19, 2018

Language: Английский

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Introgressiomics: a new approach for using crop wild relatives in breeding for adaptation to climate change

Euphytica, Journal Year: 2017, Volume and Issue: 213(7)

Published: July 1, 2017

Language: Английский

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Homoeologous Exchanges, Segmental Allopolyploidy, and Polyploid Genome Evolution

Frontiers in Genetics, Journal Year: 2020, Volume and Issue: 11

Published: Aug. 28, 2020

Polyploidy is a major force in plant evolution and speciation. In newly formed allopolyploids, pairing between related chromosomes from different subgenomes (homoeologous chromosomes) during meiosis common. The initial stages of allopolyploid formation are characterized by spectrum saltational genomic regulatory alterations that responsible for evolutionary novelty. Here we highlight the possible effects roles recombination homoeologous early stabilization. Homoeologous exchanges (HEs) have been reported young allopolyploids across angiosperms. Although all lineages undergo karyotype change via chromosome rearrangements over time, generations after predicted to show an accelerated rate change. HEs can also cause changes allele dosage, genome-wide methylation patterns, downstream phenotypes, hence be speciation genome stabilization events. Additionally, propose fixation duplication – deletion events resulting could lead production genomes which appear mix autopolyploid segments, sometimes termed "segmental allopolyploids". We discuss implications these findings our understanding relationship instability novel polyploids evolution.

Language: Английский

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Chromosome evolution in Lepidoptera

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: May 14, 2023

Abstract Chromosomes are a central unit of genome organisation. One tenth all described species on Earth Lepidoptera, butterflies and moths, these generally possess 31 holocentric chromosomes. However, subset lepidopteran display dramatic variation in chromosome counts. By analysing 210 chromosomally-complete genomes, the largest analysis eukaryotic chromosomal-level reference genomes to date, we show that diverse karyotypes extant derived from 32 ancestral linkage groups, which term Merian elements. elements have remained largely intact across 250 million years evolution diversification. Against this stable background, identify eight independent lineages evaded constraint undergone extensive reorganisation - either by numerous fissions or combination fusion fission events. Outside lineages, fusions rare rarer still. Fusions tend involve small, repeat-rich and/or Z chromosome. Together, our results reveal constraints architecture Lepidoptera enable deeper understanding importance chromosomal rearrangements shaping genomes.

Language: Английский

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Comparative genomics reveals the dynamics of chromosome evolution in Lepidoptera

Nature Ecology & Evolution, Journal Year: 2024, Volume and Issue: 8(4), P. 777 - 790

Published: Feb. 21, 2024

Chromosomes are a central unit of genome organization. One-tenth all described species on Earth butterflies and moths, the Lepidoptera, which generally possess 31 chromosomes. However, some display dramatic variation in chromosome number. Here we analyse 210 chromosomally complete lepidopteran genomes show that chromosomes extant lepidopterans derived from 32 ancestral linkage groups, term Merian elements. elements have remained largely intact through 250 million years evolution diversification. Against this stable background, eight lineages undergone extensive reorganization either numerous fissions or combination fusion fission events. Outside these lineages, fusions rare rarer still. Fusions often involve small, repeat-rich sex-linked element. Our results reveal constraints architecture Lepidoptera provide deeper understanding chromosomal rearrangements eukaryotic evolution.

Language: Английский

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Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification

Genome biology, Journal Year: 2017, Volume and Issue: 18(1)

Published: June 14, 2017

The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification are often temporally separated WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 million years ago, fit such a ‘time-lag’ model post-WGD radiation, which occurred alongside major delay in the rediploidization process. Here we propose model, ‘lineage-specific ohnologue resolution’ (LORe), address consequences delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent sister lineages sharing an ancestral event. Using cross-species sequence capture, phylogenomics genome-wide analyses expression divergence, demonstrate impact LORe on salmonid evolution. One-quarter each genome, harbouring at least 4550 ohnologues, has evolved under with occurring multiple occasions >50 post-WGD. We existence regulatory many ohnologues functions lineage-specific physiological adaptations that potentially facilitated radiation. show enriched for different than ‘older’ began diverging ancestor. unappreciated significance as nested component impacts properties genes, whilst providing available solely adaptation. predicted following events, outcomes need not appear ‘explosively’, but can arise gradually over tens millions years, promoting regimes prevailing ecological pressures.

Language: Английский

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Hybridization and hybrid speciation under global change

New Phytologist, Journal Year: 2016, Volume and Issue: 211(4), P. 1170 - 1187

Published: May 23, 2016

Contents 1170 I. II. 1172 III. 1175 IV. 1180 V. 1183 1184 References SUMMARY: An unintended consequence of global change is an increase in opportunities for hybridization among previously isolated lineages. Here we illustrate how can facilitate the breakdown reproductive barriers and formation hybrids, drawing on flora British Isles insight. Although may ameliorate some preventing hybrid establishment, example by providing new ecological niches it will have limited effects environment-independent post-zygotic barriers. For example, genic incompatibilities differences chromosome numbers structure within genomes are unlikely to be affected change. We thus speculate that a larger effect eroding pre-zygotic (eco-geographical isolation phenology) than barriers, shifting relative importance these two classes from what usually seen naturally produced hybrids where largest contributors isolation. long-term fate neo-hybrids still determined, massive impact dynamics distribution biodiversity generates unprecedented opportunity study large unpredicted, often replicated, 'experiments', allowing us peer into birth death evolutionary

Language: Английский

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Lessons on Evolution from the Study of Edaphic Specialization

The Botanical Review, Journal Year: 2017, Volume and Issue: 84(1), P. 39 - 78

Published: Oct. 26, 2017

Language: Английский

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