A worldwide phylogeography of the whiteworm lichens <i>Thamnolia</i> reveals three lineages with distinct habitats and evolutionary histories

Onuţ-Brännström, Ioana; Tibell, Leif; Johannesson, Hanna

doi:10.1002/ece3.2917

Cited by 26 publications

(36 citation statements)

References 56 publications

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“…The three Pseudephebe species show no substantial differentiation with regard to photobiont use, based on haplotype distribution, Fst values and the specialization parameter d' for both ITS and RPL10A. This scenario aligns with previous reports of closely related lichenized fungi sharing the photobiont pool partially or completely (Beck et al 1998;Hestmark et al 2016;Onuţ-Brännström et al 2017;Singh et al 2017;Dal Grande et al 2018;Ossowska et al 2019) and opposes to cases in which ecological speciation drove photobiont differentiation, as in the Lichina-Rivularia symbiosis (Ortiz-Álvarez et al 2015). This is reflected in the most prevalent haplotypes 1 (ITS) and 2 (RPL10A) that are shared by the three mycobiont species across continents and regions spanning different climatic conditions.…”

Section: Discussionsupporting

confidence: 87%

Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi)

et al. 2020

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Lichens are present in most terrestrial ecosystems on Earth and colonize extreme habitats, where vascular plants are unable to thrive, due to unique properties of the fungal-algal symbiosis. Here, we explored the phylogeographic structure of green algae engaged in symbiosis with species in the genus Pseudephebe (Parmeliaceae). These often form deep brown to blackish fruticose thalli on acidic rocks, and have partially overlapping distributions: P. minuscula is bipolar and co-occurs with P. pubescens in Europe. Based on a broad sampling, including the Arctic and Antarctica, we focused on photobionts (1) to identify genetic lineages and their phylogenetic assignment, (2) to infer the haplotype distribution in relation with geography and the mycobiont's identity, and (3) to evaluate spatial genetic structure and polymorphism. Results revealed three Trebouxia clade S lineages (Trebouxia S02, T. suecica and T. angustilobata) associated to Pseudephebe species, with predominant haplotypes distributed throughout the entire geographic distribution, and some, less frequent, shared between widely distant localities. Photobiont switching was evident in the Mediterranean region, and algal co-occurrence was frequent in both mycobionts, which shared the same set of photobionts; this could explain, at least partially, their overlapping distribution. Furthermore, genetic structure was influenced by geography given the substantial percentages of genetic variation (ca. 25-50%) explained by the different delimited eco−/biogeographic regions. In Continental Antarctica, mycobionts showed a high specialization towards the photobionts, which are probably endemic of this climatically extreme region. Taken together, our findings provide further insight about the processes shaping lichen biogeography.

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Section: Discussionsupporting

confidence: 87%

Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi)

et al. 2020

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“…In certain cases, differential levels of resolution between ITS and more variable markers is being resolved by recognizing infraspecific taxa, such as in the lichenforming ascomycete Thamnolia (Onuţ-Brännström et al 2017;Ioana et al 2018;Jørgensen 2019); in other cases, e.g. the various IGS-defined clades of the ubiquitous basidiomycete Schizophyllum commune (James et al 2001), no formal taxonomy has been implemented.…”

Section: Lack Of Resolution Of the Its And Use Of Secondary Barcodesmentioning

confidence: 99%

Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding?

et al. 2020

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True fungi (Fungi) and fungus-like organisms (e.g. Mycetozoa, Oomycota) constitute the second largest group of organisms based on global richness estimates, with around 3 million predicted species. Compared to plants and animals, fungi have simple body plans with often morphologically and ecologically obscure structures. This poses challenges for accurate and precise identifications. Here we provide a conceptual framework for the identification of fungi, encouraging the approach of integrative (polyphasic) taxonomy for species delimitation, i.e. the combination of genealogy (phylogeny), phenotype (including autecology), and reproductive biology (when feasible). This allows objective evaluation of diagnostic characters, either phenotypic or molecular or both. Verification of identifications is crucial but often neglected. Because of clade-specific evolutionary histories, there is currently no single tool for the identification of fungi, although DNA barcoding using the internal transcribed spacer (ITS) remains a first diagnosis, particularly in metabarcoding studies. Secondary DNA barcodes are increasingly implemented for groups where ITS does not provide sufficient precision. Issues of pairwise sequence similarity-based identifications and OTU clustering are discussed, and multiple sequence alignment-based phylogenetic approaches with subsequent verification are recommended as more accurate alternatives. In metabarcoding approaches, the trade-off between speed and accuracy and precision of molecular identifications must be carefully considered. Intragenomic variation of the ITS and other barcoding markers should be properly documented, as phylotype diversity is not necessarily a proxy of species richness. Important strategies to improve molecular identification of fungi are: (1) broadly document intraspecific and intragenomic variation of barcoding markers; (2) substantially expand sequence repositories, focusing on undersampled clades and missing taxa; (3) improve curation of sequence labels in primary repositories and substantially increase the number of sequences based on verified material; (4) link sequence data to digital information of voucher specimens including imagery. In parallel, technological improvements to genome sequencing offer promising alternatives to DNA barcoding in the future. Despite the prevalence of DNA-based fungal taxonomy, phenotype-based approaches remain an important strategy to catalog the global diversity of fungi and establish initial species hypotheses.

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“…In our recent study, which was based on the analyses of six nuclear markers (genes or noncoding regions) of a worldwide sample of Thamnolia (including the Nelsen & Gargas (2009) dataset), we showed the existence of three well-supported lineages with different chemistries and geographical distributions (Fig. 1) (Onut-Brännström et al 2017). One lineage (‘Lineage C’, ibid .)…”

Section: Introductionmentioning

confidence: 93%

“…They mainly occur in alpine and arctic environments where extensive colonies are often formed. Even if signs of past or infrequent recombination have been found (Onut-Brännström et al 2017), Thamnolia has never been found fruiting and it is believed to disperse exclusively by thallus fragments (Andrei et al 2006–2007) or mitospores formed in pycnidia (Lord et al . 2013).…”

Section: Introductionmentioning

confidence: 99%

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Thamnolia tundrae sp. nov., a cryptic species and putative glacial relict

2018

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The lichen species of the genus Thamnolia, with their striking wormlike thalli and frequent occurrence in arctic and tundra environments, have often been debated with regard to the use of chemistry in lichen taxonomy. Phylogenetic studies have arrived at different conclusions as to the recognition of species in the genus, but in a recent study based on the analyses of six nuclear markers (genes or noncoding regions) of a worldwide sample of Thamnolia, we showed the existence of three well-supported lineages with two different chemistries and geographical distributions. Here, we present two analyses based on ITS and three markers, respectively, which were extended from the study mentioned above to include type specimens and additional Thamnolia strains and taxa. In these analyses the same three clades were retrieved. A putative DEAD-box helicase is used here for the first time as an informative phylogenetic marker to provide taxonomic resolution at species level. The distribution of morphological and chemical characters across the phylogeny was analyzed and it was concluded that three morphologically cryptic, but genetically well supported, species occur: T. vermicularis s. str., T. subuliformis s. str. and T. tundrae sp. nov. Thamnolia vermicularis s. str. contains individuals with uniform secondary chemistry (producing thamnolic acid) and a rather limited distribution in the European Alps, Tatra Mts and the Western Carpathians, a distribution which might result from glacial survival in an adjacent refugium/refugia. Thamnolia subuliformis s. str. is widely distributed in all hemispheres and the samples contain two chemotypes (either with thamnolic or squamatic acids). Thamnolia tundrae is described as new; it produces baeomycesic and squamatic acids, and has a distribution limited to the arctic tundra of Eurasia extending to the Aleutian Islands in North America. It may have survived the latest glaciation in coastal refugia near its present distribution. Thus, secondary chemistry alone is not suitable for characterizing species in Thamnolia, secondary chemistry and geographical origin are informative, and the ITS region can be confidently used for species recognition. Nomenclatural notes are given on several other names that have been used in Thamnolia.

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A worldwide phylogeography of the whiteworm lichens Thamnolia reveals three lineages with distinct habitats and evolutionary histories

Cited by 26 publications

References 56 publications

Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi)

Amphitropical variation of the algal partners of Pseudephebe (Parmeliaceae, lichenized fungi)

Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding?

Thamnolia tundrae sp. nov., a cryptic species and putative glacial relict

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