New insights into the Usnea cornuta aggregate (Parmeliaceae, lichenized Ascomycota): Molecular analysis reveals high genetic diversity correlated with chemistry

Gerlach, Alice; Toprak, Zeynep; Naciri, Yamama; Caviró, Elena Araujo; Silveira, Rosa Mara Borges da; Clerc, Philippe

doi:10.1016/j.ympev.2018.10.035

Cited by 19 publications

(89 citation statements)

References 108 publications

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“…Strongly supported clades, however, can have a diverse chemistry, such as the decipiens clade, endemic to the Canary Islands and the Madeira archipelago (including Porto Santo), which have species producing either ß-depsidones or depsides. Therefore, worldwide sampling is needed to further evaluate secondary chemistry to give support for deep node segregation, such as in other macrolichen genera ( Xanthoparmelia pulla -group: De Paz et al 2012 ; Usnea cornuta -group: Gerlach et al 2019 ; Cetrelia : Mark et al 2019 ). However, the model of chemical characters as support of evolutionary nodes is not universal as demonstrated by the Bryoria fuscescens group ( Boluda et al 2019 ) and Thamnolia (Onuț-Brännström et al 2017).…”

Section: Discussionmentioning

confidence: 99%

“…Indeed, although it is sensitive to the choice of priors, it can explore the entire space of species trees including evolutionary processes causing discordance, such as ILS (Incomplete Lineage Sorting). The STACEY approach has been successfully applied to species delimitation in several lichen groups ( Boluda et al 2019 ; Gerlach et al 2019 ; Mark et al 2019 ; Lutsak et al 2020 ) and seems to avoid the overestimation of the number of potential species usually encountered with BPP ( Edwards et al 2016 ).…”

Section: Methodsmentioning

confidence: 99%

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The fruticose genera in the Ramalinaceae (Ascomycota, Lecanoromycetes): their diversity and evolutionary history

Spjut¹,

Simon²,

Guissard³

et al. 2020

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We present phylogenetic analyses of the fruticose Ramalinaceae based on extensive collections from many parts of the world, with a special focus on the Vizcaíno deserts in north-western Mexico and the coastal desert in Namibia. We generate a four-locus DNA sequence dataset for accessions of Ramalina and two additional loci for Niebla and Vermilacinia. Four genera are strongly supported: the subcosmopolitan Ramalina, the new genus Namibialina endemic to SW Africa, and a duo formed by Niebla and Vermilacinia, endemic to the New World except the sorediate V. zebrina that disjunctly occurs in Namibia. The latter three genera are restricted to coastal desert and chaparral where vegetation depends on moisture from ocean fog. Ramalina is subcosmopolitan and much more diverse in its ecology. We show that Ramalina and its sister genus Namibialina diverged from each other at c. 48 Myrs, whereas Vermilacinia and Niebla split at c. 30 Myrs. The phylogeny of the fruticose genera remains unresolved to their ancestral crustose genera. Species delimitation within Namibialina and Ramalina is rather straightforward. The phylogeny and taxonomy of Vermilacinia are fully resolved, except for the two youngest clades of corticolous taxa, and support current taxonomy, including four new taxa described here. Secondary metabolite variation in Niebla generally coincides with major clades which are comprised of species complexes with still unresolved phylogenetic relationships. A micro-endemism pattern of allopatric species is strongly suspected for both genera, except for the corticolous taxa within Vermilacinia. Both Niebla and saxicolous Vermilacinia have chemotypes unique to species clades that are largely endemic to the Vizcaíno deserts. The following new taxa are described: Namibialinagen. nov. with N. melanothrix (comb. nov.) as type species, a single new species of Ramalina (R. krogiae) and four new species of Vermilacinia (V. breviloba, V. lacunosa, V. pustulata and V. reticulata). The new combination V. granulans is introduced. Two epithets are re-introduced for European Ramalina species: R. crispans (= R. peruviana auct. eur.) and R. rosacea (= R. bourgeana auct. p.p). A lectotype is designated for Vermilacinia procera. A key to saxicolous species of Vermilacinia is presented.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

The fruticose genera in the Ramalinaceae (Ascomycota, Lecanoromycetes): their diversity and evolutionary history

Spjut¹,

Simon²,

Guissard³

et al. 2020

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“…To assess the morphology, anatomy, and medullary chemistry of the sequenced specimens, we examined them using established protocols (Clerc 1987(Clerc , 2007Gerlach et al 2017Gerlach et al , 2019Halonen et al 1998Halonen et al , 1999Herrera-Campos 2016;Mark et al 2016;Ohmura 2001Ohmura , 2012Randlane et al 2009;Truong & Clerc 2016;Truong et al 2013b). For morphological and anatomical observations, we used a LEICA Zoom 2000 dissecting microscope.…”

Section: Methodsmentioning

confidence: 99%

“…In a detailed analysis of all available ITS barcoding data for this hyperdiverse genus (in the definition by Lücking et al 2017a), Lücking et al (2020c) demonstrated numerous shortcomings in sequence data pertaining to Usnea: first and foremost taxonomic and geographic gaps, but also substantial issues with sequence identifications and voucher information. In addition, species identification in Usnea is challenging, as many presumably widespread taxa represent complexes of partly unrelated lineages and much work remains to be done to fully resolve the taxonomy of this genus (Seymour et al 2007;Wirtz et al 2008Wirtz et al , 2012Lumbsch & Wirtz 2011;Saag et al 2011;Shen et al 2012;Truong & Clerc 2012Truong et al 2013a, b;Clerc 2016;Mark et al 2016;Gerlach et al 2017Gerlach et al , 2019Gerlach et al , 2020Clerc & Otte 2018;Grewe et al 2018;Lagostina et al 2018;Dorey et al 2019;Temu et al 2019;Lücking et al 2020c).…”

Section: Introductionmentioning

confidence: 99%

“…Here we use Colombia as an example to illustrate the potential and the limitations of ITS-barcoding in the genus Usnea focusing on tropical species. South America has been identified as one of the better sampled regions in terms of molecular data for this genus (Lücking et al 2020c), and a number of taxonomic and phylogenetic revisions have been published for this region in the past decade (Truong et al 2011(Truong et al , 2013Truong & Clerc 2016;Gerlach et al 2017Gerlach et al , 2019Gerlach et al , 2020Bungartz et al 2018). For Colombia, 63 species were listed in the Catalog of Lichens of Colombia (Sipman & Aguirre-C. 2016), a number subsequently adjusted to 60, with six name changes (Lücking et al 2020d).…”

Section: Introductionmentioning

confidence: 99%

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Testing DNA barcoding in Usnea (Parmeliaceae) in Colombia using the internal transcribed spacer (ITS)

Moncada¹,

Sipman²,

Lücking³

2020

Plant and Fungal Systematics

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We tested the functionality of ITS-based DNA barcoding in lichen fungi using Colombian samples of the genus Usnea as an example. New ITS sequences were generated for 15 samples from five localities in two different ecoregions, representing varying morphologies and medullary chemistries. We employed five strategies to identify the samples: (1) BLASTn on the NCBI BLAST site with the original identifications of the best matching reference sequences; (2) as previous, but with revised identifications of the reference sequences based on a separately published revision of ITS sequences published for the genus; (3) local BLASTn in BioEdit using a separately published, revised and curated set of ITS reference sequences for the genus; (4) multiple alignment based phylogenetic analysis within the framework of all available ITS sequences for Usnea s.str.; and (5) integrative taxonomy, combining molecular phylogeny and comparative analysis of phenotype and chemical data. Using the latter approach as reference, we found that NCBI BLASTn with original identifications performed poorly, resulting in an identification success rate of only 7% (a single sample). NCBI BLASTn with revised identifications more than tripled identification success (23%), but was still unsatisfactory. Local BLASTn in BioEdit using the revised, curated reference data further doubled identification success (47%), but remained inadequate. Multiple alignment-based phylogenetic analysis achieved an identification success rate of 80% compared to the result from integrative taxonomy. Based on these results, we conclude that ITS-based DNA barcoding of the genus Usnea under the current circumstances performs poorly, but can be substantially improved using three strategies: (1) update identifications of reference sequences in primary repositories such as GenBank or alternatively use a curated reference data set; (2) perform local BLAST with a curated reference data set focusing on the target genus only, combined with multiple alignment-based phylogenetic analysis as a verification step; and (3) close substantial geographic and taxonomic gaps in the existing reference data. Our analyses suggest that if a near-complete reference data set with correct identifications existed for the genus, then standard BLAST approaches could achieve high levels of identification success close to 100%. As part of our DNA barcoding exercise, which generated the first 15 ITS sequences for Colombian samples of the genus Usnea, we confirm the presence of U. aranea and U. wasmuthii in Colombia and we report for the first time U. tenuicorticata for the country.

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Species in lichen-forming fungi: balancing between conceptual and practical considerations, and between phenotype and phylogenomics

2021

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Lichens are symbiotic associations resulting from interactions among fungi (primary and secondary mycobionts), algae and/or cyanobacteria (primary and secondary photobionts), and specific elements of the bacterial microbiome associated with the lichen thallus. The question of what is a species, both concerning the lichen as a whole and its main fungal component, the primary mycobiont, has faced many challenges throughout history and has reached new dimensions with the advent of molecular phylogenetics and phylogenomics. In this paper, we briefly revise the definition of lichens and the scientific and vernacular naming conventions, concluding that the scientific, Latinized name usually associated with lichens invariably refers to the primary mycobiont, whereas the vernacular name encompasses the entire lichen. Although the same lichen mycobiont may produce different phenotypes when associating with different photobionts or growing in axenic culture, this discrete variation does not warrant the application of different scientific names, but must follow the principle "one fungus = one name". Instead, broadly agreed informal designations should be used for such discrete morphologies, such as chloromorph and cyanomorph for lichens formed by the same mycobiont but with either green algae or cyanobacteria. The taxonomic recognition of species in lichen-forming fungi is not different from other fungi and conceptual and nomenclatural approaches follow the same principles. We identify a number of current challenges and provide recommendations to address these. Species delimitation in lichen-forming fungi should not be tailored to particular species concepts but instead be derived from empirical evidence, applying one or several of the following principles in what we call the LPR approach: lineage (L) coherence vs. divergence (phylogenetic component), phenotype (P) coherence vs. divergence (morphological component), and/or reproductive (R) compatibility vs. isolation (biological component). Species hypotheses can be established based on either L or P, then using either P or L (plus R) to corroborate them. The reliability of species hypotheses depends not only on the nature and number of characters but also on the context: the closer the relationship and/or similarity between species, the higher the number of characters and/or specimens that should be analyzed to provide reliable delimitations. Alpha taxonomy should follow scientific evidence and an evolutionary framework but should also offer alternative practical solutions, as long as these are scientifically defendable. Taxa that are delimited phylogenetically but not readily identifiable in the field, or are genuinely cryptic, should not be rejected due to the inaccessibility of proper tools. Instead, they can be provisionally treated as undifferentiated complexes for purposes that do not require precise determinations. The application of infraspecific (gamma) taxonomy should be restricted to cases where there is a biological rationale, i.e., lineages of a species complex that show limited phylogenetic divergence but no evidence of reproductive isolation. Gamma taxonomy should not be used to denote discrete phenotypical variation or ecotypes not warranting the distinction at species level. We revise the species pair concept in lichen-forming fungi, which recognizes sexually and asexually reproducing morphs with the same underlying phenotype as different species. We conclude that in most cases this concept does not hold, but the actual situation is complex and not necessarily correlated with reproductive strategy. In cases where no molecular data are available or where single or multi-marker approaches do not provide resolution, we recommend maintaining species pairs until molecular or phylogenomic data are available. This recommendation is based on the example of the species pair Usnea aurantiacoatra vs. U. antarctica, which can only be resolved with phylogenomic approaches, such as microsatellites or RADseq. Overall, we consider that species delimitation in lichen-forming fungi has advanced dramatically over the past three decades, resulting in a solid framework, but that empirical evidence is still missing for many taxa. Therefore, while phylogenomic approaches focusing on particular examples will be increasingly employed to resolve difficult species complexes, broad screening using single barcoding markers will aid in placing as many taxa as possible into a molecular matrix. We provide a practical protocol how to assess and formally treat taxonomic novelties. While this paper focuses on lichen fungi, many of the aspects discussed herein apply generally to fungal taxonomy. The new combination Arthonia minor (Lücking) Lücking comb. et stat. nov. (Bas.: Arthonia cyanea f. minor Lücking) is proposed.

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New insights into the Usnea cornuta aggregate (Parmeliaceae, lichenized Ascomycota): Molecular analysis reveals high genetic diversity correlated with chemistry

Cited by 19 publications

References 108 publications

The fruticose genera in the Ramalinaceae (Ascomycota, Lecanoromycetes): their diversity and evolutionary history

The fruticose genera in the Ramalinaceae (Ascomycota, Lecanoromycetes): their diversity and evolutionary history

Testing DNA barcoding in Usnea (Parmeliaceae) in Colombia using the internal transcribed spacer (ITS)

Species in lichen-forming fungi: balancing between conceptual and practical considerations, and between phenotype and phylogenomics

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