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Phylogenetic relationships within the genus Ramalina based on a maximum likelihood analysis of concatenated ITS, IGS, RPB1 and RPB2 sequences. Bootstrap values ≥ 75% are given above the internodes; these branches are depicted with thickened lines. Clades marked with capital letters are discussed in the text. Clades highlighted in grey are samples from the ingroup, the R. siliquosa complex. For chemotype abbreviations of samples from the R. siliquosa complex, see Table 2. Chemotype numbers for the R. americana and R. culbersoniorum samples follow the numbering systems of Culberson et al. (1990) and LaGreca (1999). The dashed line indicates the branch connecting the two parts of the tree, which was divided because of space considerations. Scale = nucleotide substitution rate.
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Lichens of the Ramalina siliquosa complex dominate seashore cliffs in Europe and South-East Asia, but their taxonomy has been vigorously debated for over a century. On many cliffs, they exhibit a bewildering zonation of chemotypes that resembles the classic zonation of organisms that occupy the littoral zone below. Do the chemotypes represent separ...
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... Our combined data set contained 2507 aligned positions, of which 886 were variable within the ingroup. Of these variable characters, 169 occurred in the ITS region, 184 in the IGS, 233 in the RPB2 and 300 in the RPB1. The total proportion of gaps and indeterminable characters in the alignment was 52.77%. The ML tree (Fig. 2) had a final ML optimization likelihood value of −14969.549914. Clades with thickened lines are supported by Maximum Likelihood Bootstrap (MLBS) values ≥ 75%; those denoted by capital letters are discussed in the text. The following taxa and clades have branch lengths much longer than other branches in the ML tree: Ramalina denticulata, ...
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... ML tree (Fig. 2) shows the 59 ingroup samples forming three well-supported clades (A, C and G), none of which are direct phylogenetic sisters. Most of the backbone branches of the reconstructed tree have low support (MLBS < 75%), except for one strongly supported clade (H) comprising all Ramalina species included in this study that produce medullary ...
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... Ramalina siliquosa complex Our ML analysis (Fig. 2) provides strong evidence that the European members of the Ramalina siliquosa complex comprise two distinct evolutionary lineages ('phylogenetic species' sensu Mishler (1996)), supporting a two-species classification (Table 2): R. siliquosa (Huds.) A. L. Sm. s. str. (clade C; 96% MLBS), including the hypoprotocetraric, protocetraric ...
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... ß-orcinol depsidones). Unlike in Europe, the chemotypes in South-East Asia do not display zonation on cliffs (H. Kashiwadani & K. Moon, personal observation). South-East Asian material has been identified until now as R. siliquosa but is slightly different morphologically. Based on our ML analysis of 20 R. siliquosa specimens from Japan and Korea (Fig. 2, clade A; 96% MLBS), the South-East Asian populations belong to a separate species which we originally thought was new to science. A review of the literature, however, revealed a little-known variety of R. scopulorum (Ach.) Ach., var. semicuspidata Räsänen (Räsänen 1940), which was elevated to species level by Sheard (1978a) in a short ...
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... samples representing 36 other taxa, mainly from North America and Europe, were added to our four-locus data set. As in previous studies (e.g. Pérez-Vargas & Pérez-Ortega 2014;Gasparyan et al. 2017; references therein), the relationships among many of the Ramalina taxa included in our broader phylogeny remain unresolved (Fig. 2). This lack of resolution indicates that the evolutionary history of the genus may be too complex to be adequately captured by a dichotomously branching phylogeny based on only a few loci. A number of clades, however, were reconstructed with MLBS values ≥ 75%. For example, clade J (85% MLBS) includes all south-eastern United States ...
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... environment' as the evolutionary mechanism producing the seven European sibling chemospecies he recognized in the Ramalina siliquosa complex ( Table 2). The present study has demonstrated, however, that only two species exist in Europe (R. cuspidata and R. siliquosa) and, furthermore, they are not sibling species. Neither the majority-rule (Fig. 2) nor the single-gene trees (not shown) support a sister relationship for R. cuspidata and R. siliquosa s. str. In fact, the majority-rule tree indicates that the epiphytic, fistulose species R. roesleri is sister to R. siliquosa (80% MLBS) and that this pair (clade B; 80% MLBS), in turn, is sister to two other fistulose species, R. ...
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... evidence for allopatric sibling speciation, driven by geographical isolation. A similar scenario might explain why the South-East Asian species revealed in the present study, Ramalina semicuspidata, is morphologically similar to the European R. siliquosa complex; however, phylogenetic evidence for an intercontinental dispersal event is lacking (Fig. 2). By contrast, sympatric speciation, the process by which sibling species co-occur in the same habitats, is reportedly much less common than allopatric speciation (Futuyma & Kirkpatrick 2017). This is because morphologically similar, co-occurring sister species cannot coexist over time: one either gets outcompeted or adapts to a ...
Citations
... Therefore, we suggest that in the absence of evidence definitively linking the other four specimens in the Taylor Herbarium to FH 00780177, they are best treated as syntypes rather than as duplicates of the lectotype. In addition, although studies have demonstrated cryptic species in lichens (e.g., Singh & al., 2015;Del-Prado & al., 2016), this is not the case for R. menziesii (Sork & Werth, 2014;LaGreca & al., 2020). An attempt was not made to sequence the lectotype due to the Harvard University Herbaria's destructive sampling policy that precludes sampling of "type collections, from historical specimens, or from taxa represented in the herbaria with less than three collections, except in rare instances". ...
A lectotype is designated for the name of the iconic and well-known macrolichen Ramalina menziesii Taylor from among a suite of largely overlooked syntypes deposited in the Thomas Taylor Herbarium at the Farlow Herbarium, Harvard University. Lectotypes are also selected for the synonyms of R. menziesii: Chlorodictyon foliosum, Ramalina reticulata (≡ Lichen reticulatus Noehd., nom. illeg.) and R. retiformis. The place of publication of L. reticulatus Noehd. is discussed in detail. The case highlights the surprising degree to which the application of names for taxa that have been extensively studied and are widely known outside a narrow specialist field, can remain unresolved.
... L. atrobrunnea 1 '2.3', and L. atrobrunnea s. lat. 1 '4.1' (Fig. 2). The mixed utility of secondary metabolites as diagnostic characters has been demonstrated in other lichens, with some cases showing chemically polymorphic species (Mark et al. 2016;Boluda et al. 2019;LaGreca et al. 2020) and others showing secondary metabolites coinciding with distinct lineages (Schmitt & Lumbsch 2004;Fehrer et al. 2008). ...
Species of lichen-forming fungi (LFF) display an array of geographical distribution patterns. Among the broadly distributed lichen-forming fungal species, the degree of reproductive isolation and genetic substructure among populations varies widely, in some cases masking unrecognized diversity or meaningful biogeographical patterns. Lecidea atrobrunnea (Raymond ex Lam. & DC.) Schaer. s. lat. (Lecideaceae) is a widespread species complex that has been studied for over two centuries since its initial description. The diversity of the L. atrobrunnea group is highest in western North America, where a dizzying array of morphologies and chemistry can occur at local scales. Here we investigate whether the assumed cosmopolitan distribution of L. atrobrunnea s. lat. is an artifact of taxonomic limitations and masks biogeo-graphical patterns in this species complex. To address these questions, we compiled sequence data from the standard fungal barcoding marker (ITS) for over 100 specimens within this complex, in addition to genome-scale data from a subset of these representing over 1600 single-copy nuclear genes spanning over 3 Mb of the genome. Our study corroborates the perspective that the morphologically and chemically variable Lecidea atrobrunnea group reflects a complex of distinct species-level lineages, with 42-83 candidate species inferred from the ITS region and high levels of diversity inferred from a subset of specimens using genome-scale data. However, both phenotype-and molecular-based species boundaries remained unsettled, with the most common nominal taxa recovered as highly poly-phyletic and with conflict among different molecular species delimitation approaches. Our study also highlights the potential for geographically restricted species, with fascinating biogeographical patterns, challenging, in part, the assumed cosmopolitan distribution of L. atrobrunnea s. lat. This study provides valuable direction for future research that will be crucial in understanding diversification and establishing a robust taxonomy for this well-known species complex.
... Enormous progress has recently been made in the evolutionary and taxonomic knowledge of the genus Ramalina, with the work of Pérez-Ortega et al. (2019), LaGreca et al. (2020) and Spjut et al. (2020). The preliminary evolutionary tree of Sérusiaux et al. (2010) has been broadly confirmed, and the generic boundaries within the fruticose Ramalinaceae are now well established (Spjut et al. 2020): three genera endemic to coastal deserts benefiting from regular fog along the Pacific coasts in the New World (Niebla and Vermilacinia) and the Atlantic coasts of SW Africa (Namibialina and a single Vermilacinia species shared with the New World), and a globally distributed genus with a much larger ecological amplitude (Ramalina). ...
Ramalina arsenii sp. nov. belongs to the R. pollinaria group and is easily recognized by its ITS barcode and several micro-morphological characters that are diagnostic in a European context: small size, less than 3 cm long; soralia developing on the underside of lobe apices; absence of excavate depressions on the lower side. Its ecological niche (i.e. rock outcrops and especially underhangs of slightly calcareous rocks, at low and mid altitudes) is also unique. Ramalina arsenii is frequent and locally abundant in France (Alps, Cantal) and Switzerland (western Alps), and is also known from Germany and the Spanish side of the Pyrenees.
... Lichen fungi thus became part of regularly implemented updates of fungal classifications and this facilitated a seamless transition into the molecular era, with substantial changes in the higher classification of fungi including lichen-formers in the past three decades (Miądlikowska et al. 2006(Miądlikowska et al. , 2014aNelsen et al. , 2011Nelsen et al. , 2020Lumbsch and Huhndorf 2010;Frisch et al. 2014;Chen et al. 2015;Lücking et al. 2017a;Kraichak et al. 2018;Pizarro et al. 2018;Widhelm et al. 2019). Molecular phylogenies were also employed early on to address species delimitation in lichen fungi, first using single-marker approaches focusing on the fungal ITS barcoding marker but also increasingly other approaches such as multi-marker coalescence or phylogenomics, including microsatellites, RADseq and target capture (Franc and Kärnefelt 1998;Lohtander et al. 1998;Thell et al. 2000;Kroken and Taylor 2001;Moncada et al. 2014;Lücking et al. 2017b;Magain et al. 2017;Grewe et al. 2018;Lagostina et al. 2018;LaGreca et al. 2020;Widhelm et al. 2021;Lücking et al. 2021b). These studies have also generated new interest in the application of theoretical species concepts to species-level taxonomy in lichen fungi (Grube and Kroken 2000;Buschbom and Mueller 2006;Crespo and Pérez-Ortega 2009;Crespo and Lumbsch 2010;Lumbsch and Leavitt 2011;Leavitt et al. 2016a, b;Jørgensen 2019). ...
... As a consequence, even in the absence of molecular data, species are now much more narrowly defined (Lücking 2014). On the other hand, molecular data have also shown that previously separated taxa may indeed represent discrete variation of a single species (Fryday et al. 2017;Boluda et al. 2019;LaGreca et al. 2020). ...
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.
Oceanic islands have been recognized as natural laboratories in which to study a great variety of evolutionary processes. One such process is evolutionary radiations, the diversification of a single ancestor into a number of species that inhabit different environments and differ in the traits that allow them to exploit those environments. The factors that drive evolutionary radiations have been studied for decades in charismatic organisms such as birds or lizards, but are lacking in lichen-forming fungi, despite recent reports of some lineages showing diversification patterns congruent with radiation. Here we propose the Ramalina decipiens group as a model system in which to carry out such studies. This group is currently thought to be comprised of five saxicolous species, all of them endemic to the Macaronesian region (the Azores, Madeira, Selvagens, Canary and Cape Verde islands). Three species are single-island endemics (a rare geographic distribution pattern in lichens), whereas two are widespread and show extreme morphological variation. The latter are suspected to harbor unrecognized species-level lineages. In order to use the Ramalina decipiens group as a model system it is necessary to resolve the group's phylogeny and to clarify its species boundaries. In this study we attempt to do so following an integrative taxonomy approach. We constructed a phylogenetic tree based on six molecular markers, four of which are newly developed and generated competing species hypotheses based on molecular (species discovery strategies based on both single locus and multilocus datasets) and phenotypic data (unsupervised clustering algorithms based on morphology, secondary chemistry and geographic origin). We found that taxonomic diversity in the Ramalina decipiens group has been highly underestimated in previous studies. In consequence, we describe six new species, most of them single-island endemics and provide a key to the group. Phylogenetic relationships among species have been reconstructed with almost full support which, coupled with the endemic character of the group, makes it an excellent system for the study of island radiations in lichen-forming fungi.
Here we provide one of the first detailed studies of lichen and allied fungi diversity in a continental North American city (Edmonton, Alberta, Canada), including an annotated checklist, images of all species, dichotomous keys, and local distribution maps. Edmonton is the northernmost city in North America with a population of over one million, and an industrial and transportation gateway for much of northern Canada. Lichen-based biomonitoring could be a tool to track airborne pollutants resulting from Edmonton’s growing populace and industrial activity. The first step towards such a program is documenting the diversity and distribution of lichens in the city. To accomplish this, we conducted a city-wide, systematic survey of 191 sites focused on epiphytes growing on deciduous boulevard trees. We augmented that survey with surveys of rare trees, opportunistic collections from river valley and ravine habitats, herbarium collections, phylogenetic analyses of a subset of collections, and observations submitted to online nature-reporting applications. We present ITS sequence barcode data for 33 species, phylogenetic analyses for Candelariaceae, Endocarpon, Flavopunctelia, the Lecanora dispersa group, Lecidella, Peltigera, Physconia, and Punctelia, and detailed descriptions of 114 species in 47 genera and 23 families. Two species are hypothesized to be new to North America (Endocarpon aff. unifoliatum, Lecidella albida), twelve more are new to Alberta (Amandinea dakotensis, Bacidia circumspecta, Candelaria pacifica, Candelariella antennaria, Heterodermia japonica, Lecania naegelii, Lecanora sambuci, Lecanora stanislai, Lecidea erythrophaea, Peltigera islandica, Phaeocalicium aff. tremulicola, and the introduced Xanthoria parietina), and five are putative new species to science (Physcia aff. dimidiata, Physcia aff. stellaris, Phaeocalicium sp., Phaeocalicium aff. tremulicola, Lichenaceae sp.). Illustrations are provided for all species to aid in verification and public outreach. Species richness was highest in foliose lichens (48), followed by crustose and calicioid lichens and allied fungi (41), with the lowest richness in fruticose lichens (25). We did a preliminary assessment of the suitability of species for citizen-science biomonitoring by assessing their distribution across the city, perceptibility to the public, identification accuracy, and, for a subset, how consistently species were surveyed by trained novices. Compared to other urban areas where lichen diversity has been studied, Edmonton is relatively species-rich in calicioids and Peltigera. Promising bioindicators may be limited to chlorolichens, including Caloplaca spp., Evernia mesomorpha, Flavopunctelia spp., Phaeophyscia orbicularis, Physcia adscendens, Physcia aipolia group, Physcia aff. stellaris, Usnea spp., and Xanthomendoza fallax. Other genera that may be responsive to pollutants such as Cladonia and Peltigera were almost exclusively restricted to river valley and ravine ecosystems, limiting their application as bioindicators. Some species commonly used as biomonitors elsewhere were too rare, small, poorly developed, or obscured by more common species locally (e.g., Candelaria concolor s.l., Xanthomendoza hasseana). The low overlap with lists of biomonitoring species from other regions of North America illustrates the necessity of grounding monitoring in knowledge of local diversity. Future augmentation of this list should focus on enhanced sampling of downed wood-, conifer-, and rock-dwelling lichens, particularly crustose species. The next step in developing a biomonitoring program will require modelling species’ responses to known air quality and climatic gradients.
This preliminary exploration of marine lichenized fungi (lichens) as bioindicators of water pollution examined the distribution of intertidal lichen communities in the Boston Harbor Islands National Recreation Area with respect to recorded pollution throughout the harbor. We found significant negative associations between pollution measurements and the health of the lichen community based on cover and species richness. We also observed significant differences in species composition between areas of higher pollution and areas of lower pollution, though not enough data are available to establish the pollution sensitivity or tolerance of individual species. We note that difficulties in the collection and identification of marine lichens hamper efforts to use them broadly as bioindicators. This study suggests that marine lichens could prove useful as bioindicators, but more research is needed to understand the differential effects of pollution on individual species as well as to establish practical procedures both for quantifying marine lichen community health and for widespread bioindication using marine lichens. Finally, one species collected during this study, Verrucaria ceuthocarpa, represents a first report for the Boston Harbor Islands National Recreation Area.
