Cryptic speciation in allotetraploids: Lessons from the <i>Botrychium matricariifolium</i> complex

Williams, Evelyn W.; Farrar, Donald R.; Henson, Don

doi:10.3732/ajb.1500281

Cited by 15 publications

(15 citation statements)

References 52 publications

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“…Polyploidy is a major speciation process in plants (Stebbins, 1950;Soltis and Soltis, 2009;Rothfels and Otto, 2016), particularly within ferns, which have rates of polyploid speciation approximately twice those of angiosperms (Otto and Whitton, 2000;Wood et al, 2009). The fern genus Botrychium (Ophioglossaceae) is a classic example where recurrent inter-specific hybridization between diploid progenitors has been postulated to have formed an allopolyploid complex (Gilman et al, 2015;Williams et al, 2016; for other examples in ferns see, e.g. Myriopteris, Grusz et al 2009;Dryopteris, Sessa et al, 2012;Cystopteris, Rothfels et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…These data enabled the reconstruction of the bi-parental origin of allopolyploids and the proposal of new hybridization hypotheses (Stensvold et al, 2002;Zika and Farrar, 2009;Gilman et al, 2015). This genetic fingerprinting has since been complemented by other molecular tools, such as amplified fragment length polymorphism (AFLP) or microsatellites, to provide new insights on the genetic diversity within specific allopolyploid complexes (Williams and Waller, 2012;Ellis, 2014;Williams et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…The genus comprises an estimated 48 taxa divided among three major clades: Lanceolatum (3 diploids, 14 polyploids), Lunaria (10 diploids, 1 polyloid), and Simplex-Campestre (11 diploids, 9 polyploids;Dauphin et al, 2017). Previous studies additionally revealed various morphologically cryptic taxa (including both diploids and polyploids) and provided a phylogenetic foundation that helped identify diagnostic morphological characters (Stensvold and Farrar, 2017;Williams et al, 2016;Meza-Torres et al, 2017;Farrar and Gilman, 2017). However, despite the recent advances in our understanding of the maternal phylogenetic relationships among Botrychium taxa, phylogenetic information about the paternal lines through nuclear sequencing is lacking.…”

Section: Introductionmentioning

confidence: 99%

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Rapid allopolyploid radiation of moonwort ferns (Botrychium; Ophioglossaceae) revealed by PacBio sequencing of homologous and homeologous nuclear regions

Dauphin

Grant

Farrar

et al. 2018

Molecular Phylogenetics and Evolution

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Polyploidy is a major speciation process in vascular plants, and is postulated to be particularly important in shaping the diversity of extant ferns. However, limitations in the availability of bi-parental markers for ferns have greatly limited phylogenetic investigation of polyploidy in this group. With a large number of allopolyploid species, the genus Botrychium is a classic example in ferns where recurrent polyploidy is postulated to have driven frequent speciation events. Here, we use PacBio sequencing and the PURC bioinformatics pipeline to capture all homeologous or allelic copies of four long (∼1 kb) low-copy nuclear regions from a sample of 45 specimens (25 diploids and 20 polyploids) representing 37 Botrychium taxa, and three outgroups. This sample includes most currently recognized Botrychium species in Europe and North America, and the majority of our specimens were genotyped with co-dominant nuclear allozymes to ensure species identification. We analyzed the sequence data using maximum likelihood (ML) and Bayesian inference (BI) concatenated-data ("gene tree") approaches to explore the relationships among Botrychium species. Finally, we estimated divergence times among Botrychium lineages and inferred the multi-labeled polyploid species tree showing the origins of the polyploid taxa, and their relationships to each other and to their diploid progenitors. We found strong support for the monophyly of the major lineages within Botrychium and identified most of the parental donors of the polyploids; these results largely corroborate earlier morphological and allozyme-based investigations. Each polyploid had at least two distinct homeologs, indicating that all sampled polyploids are likely allopolyploids (rather than autopolyploids). Our divergence-time analyses revealed that these allopolyploid lineages originated recently-within the last two million years-and thus that the genus has undergone a recent radiation, correlated with multiple independent allopolyploidizations across the phylogeny. Also, we found strong parental biases in the formation of allopolyploids, with individual diploid species participating multiple times as either the maternal or paternal donor (but not both). Finally, we discuss the role of polyploidy in the evolutionary history of Botrychium and the interspecific reproductive barriers possibly involved in these parental biases.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Rapid allopolyploid radiation of moonwort ferns (Botrychium; Ophioglossaceae) revealed by PacBio sequencing of homologous and homeologous nuclear regions

Dauphin

Grant

Farrar

et al. 2018

Molecular Phylogenetics and Evolution

Self Cite

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“…Additionally, the reconstruction of maternal lineages of Botrychium revealed genetic diversity within the Lunaria clade highlighting the uncertainty of taxonomic assignments (Dauphin et al, 2014;Maccagni et al, 2017;Dauphin et al, 2017). Previous population genetic studies based on isozymes showed a lack of genetic differentiation among morphologically recognized types (Williams et al, 2016), and the low amount of genetic variation detected within Botrychium populations suggests pervasive self-fertilization (Farrar, 1998;Hauk and Haufler, 1999). Furthermore, genetic differentiation among populations and regions was found to be low suggesting that gene flow may occur (Camacho and Liston, 2001;Swartz and Brunsfeld, 2002;Birkeland et al, 2017).…”

Section: An Important Genus Lacking Transcriptomic Resources Is Botrymentioning

confidence: 92%

A transcriptome for the early-branching fernBotrychium lunariaenables fine-grained resolution of population structure

Mossion

Dauphin

Grant

et al. 2020

Preprint

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26Ferns are the second most dominant group of land plants after angiosperms. Extant species occupy an 27 extensive range of habitats and contribute significantly to ecosystem functioning. Despite the 28 importance of ferns, most taxa are poorly covered by genomic resources. The genus Botrychium 29 belongs to one of the earliest divergent lineages of vascular plants and has a global distribution with 30 35 species, half of which are polyploids. Here, we establish a reference transcriptome for Botrychium 31 lunaria, a diploid species with an extremely large genome of 27.5 Gbp. We assembled 25,721 high-32quality transcripts with an average length of 1,332 bp based on deep RNA-sequencing of a single 33 individual. We sequenced an additional 11 transcriptomes of individuals from two populations in 34 Switzerland, including the population of the reference individual. Based on read mapping to reference 35 transcript sequences, we identified 374,510 single nucleotide polymorphisms (SNPs) segregating 36 among individuals for an average density of 14 SNPs per kb. The transcriptome-wide markers 37 provided unprecedented resolution of the population genetic structure revealing substantial variation in 38 heterozygosity among individuals. We also constructed a phylogenomic tree of 73 taxa representating 39 all fern orders to ascertain the placement of the genus Botrychium. The high-quality transcriptomic 40 resources enable powerful population and phylogenomic studies in an important group of ferns. 41 42 43

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“…9) Botrychium matricariifolium is a tetraploid species with a limited sub-Atlantic distribution in Europe and North America. It is the only member of the B. matricariifolium complex in Europe, whose diploid parents are North American B. pallidum and a still unresolved taxon (Williams et al 2016). It is widespread in central Europe and southern Scandinavia, eastwards reaching European Russia, while it is rare in the north of the British Isles, Corsica, Croatia and Montenegro.…”

Section: Azolla Filiculoides (Fig 6)mentioning

confidence: 99%

Distributions of vascular plants in the Czech Republic

Kaplan¹,

Danihelka²,

Koutecký³

et al. 2017

Preslia

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This the fourth part of the series on the distributions of vascular plants in the Czech Republic includes grid maps of 84 taxa of the genera Aldrovanda, Alisma, Asclepias, Azolla, Blechnum, Botrychium, Butomus, Carex, Centaurea, Drosera, Dysphania, Hypochaeris, Illecebrum, Luronium, Ophioglossum, Persicaria, Pilularia, Rubrivena, Sagittaria, Salvinia, Scirpoides, Sideritis, Streptopus, Teesdalia and Thesium. These maps were produced by taxonomic experts based on herbarium specimens, literature and field records. Of the native taxa studied, 40 are on the national Red List. Among them, Carex pseudobrizoides, Hypochaeris glabra and Illecebrum verticillatum are rare species of mainly sandy habitats, which are all now restricted to a few or several sites and are therefore classified as critically threatened. Endangered aquatics and wetland plants are represented by Alisma gramineum, Salvinia natans, three Drosera species, Luronium natans and Pilularia globulifera, of which the latter two are species with sub-Atlantic distributions, reaching in this country their south-eastern and eastern distribution limits, respectively. All eight species of the genus Thesium and most species of Botrychium are endangered, either because they are rare or they are now considerably less common than they were, or combination of both. Two of the species mapped in this paper are now extirpated from this country. Botrychium simplex was last recorded more than 120 years ago, whereas the spontaneous occurrences of Aldrovanda vesiculosa vanished after 1952. However, the latter species has recently been deliberately planted in the wild for conservation purposes. The taxonomically extremely difficult Centaurea sect. Jacea, whose taxonomy and evolution is complicated by polyploidization and frequent hybridization, includes many taxa whose distributions were unclear until recently. Maps

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Cryptic speciation in allotetraploids: Lessons from the Botrychium matricariifolium complex

Cited by 15 publications

References 52 publications

Rapid allopolyploid radiation of moonwort ferns (Botrychium; Ophioglossaceae) revealed by PacBio sequencing of homologous and homeologous nuclear regions

Rapid allopolyploid radiation of moonwort ferns (Botrychium; Ophioglossaceae) revealed by PacBio sequencing of homologous and homeologous nuclear regions

A transcriptome for the early-branching fernBotrychium lunariaenables fine-grained resolution of population structure

Distributions of vascular plants in the Czech Republic

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