Göran Thor

Basidiomycete yeasts in the cortex of ascomycete macrolichens

Lichens assemble in three parts Lichen growth forms cannot be recapitulated in the laboratory by culturing the plant and fungal partners together. Spribille et al. have discovered that the classical binary view of lichens is too simple. Instead, North American beard-like lichens are constituted of not two but three symbiotic partners: an ascomycetous fungus, a photosynthetic alga, and, unexpectedly, a basidiomycetous yeast. The yeast cells form the characteristic cortex of the lichen thallus and may be important for its shape. The yeasts are ubiquitous and essential partners for most lichens and not the result of lichens being colonized or parasitized by other organisms. Science, this issue p. 488 Complete functioning lichen thalli have three partners: alga and ascomycete, plus a basidiomycete yeast. For over 140 years, lichens have been regarded as a symbiosis between a single fungus, usually an ascomycete, and a photosynthesizing partner. Other fungi have long been known to occur as occasional parasites or endophytes, but the one lichen–one fungus paradigm has seldom been questioned. Here we show that many common lichens are composed of the known ascomycete, the photosynthesizing partner, and, unexpectedly, specific basidiomycete yeasts. These yeasts are embedded in the cortex, and their abundance correlates with previously unexplained variations in phenotype. Basidiomycete lineages maintain close associations with specific lichen species over large geographical distances and have been found on six continents. The structurally important lichen cortex, long treated as a zone of differentiated ascomycete cells, appears to consistently contain two unrelated fungi.

Factors of Importance to Some Lichen Species of Deciduous Broad-Leaved Woods in Southern Sweden

Morphological, anatomical, chemical and ecological evidence show that the South African lichen Roccellina capensis (Nyl. ex Stizenb.) Tehler has developed a dispersal strategy with either sexually dispersed individuals, or vegetatively dispersed, sorediate individuals, hence a putative species-pair. The concept ‘species-pair’ is well-known and widely used in lichenology. It refers to closely related, morphologically indistinguishable lichens that differ from each other by their dispersal strategies only. The so-called ‘ primary species ’ produces fruiting bodies and sexual spores, while its counterpart, the ‘ secondary species ’ is vegetatively dispersed by soredia, isidia or fragmentation. Our study uses molecular information to investigate if R. capensis should be treated as a species-pair or not. The internal transcribed spacer (ITS) of the nuclear ribosomal DNA was sequenced for 17 specimens of R. capensis in order to test if sexual and asexual (sorediate) specimens would group into two distinct, monophyletic groups. Such grouping would support their recognition as separate taxa in a species-pair. We also investigated whether the randomly amplified polymorphic DNA (RAPD) method would be a suitable procedure in population studies of lichens. The analysis of the ITS region produced a single most parsimonious tree. The sexual and asexual specimens were grouped according to their geographical distribution, rather than according to their dispersal strategy. This result clearly shows that the sexual and asexual specimens of R. capensis do not represent a species-pair. The RAPD data set produced an almost completely unresolved tree due to several homoplasious characters, possibly a result of algal contamination.

Reproductive mode and genetic variation suggest a North American origin of European Letharia vulpina.

Our data on the intercontinental population biology of Letharia vulpina show an unexpected shift from a recombining North American population with unique haplotypes to genetically depauperate Swedish and Italian populations, each with many representatives of a single repeated haplotype. Analysis of eight loci in 47 individuals supported recombination in North American populations and showed almost no variation among European populations. We infer that a genetic bottleneck caused by limited long‐distance dispersal accounts for the lack of genetic variation found in marginal populations. This lack of variation in the European populations makes it impossible to use population genetic means to distinguish clonal reproduction from self‐fertilization or even outcrossing, but phenotype indicates that reproduction in the marginal populations is by clonal spread, via soredia and isidioid soredia.

Evolution of complex symbiotic relationships in a morphologically derived family of lichen-forming fungi.

We studied the evolutionary history of the Parmeliaceae (Lecanoromycetes, Ascomycota), one of the largest families of lichen-forming fungi with complex and variable morphologies, also including several lichenicolous fungi. We assembled a six-locus data set including nuclear, mitochondrial and low-copy protein-coding genes from 293 operational taxonomic units (OTUs). The lichenicolous lifestyle originated independently three times in lichenized ancestors within Parmeliaceae, and a new generic name is introduced for one of these fungi. In all cases, the independent origins occurred c. 24 million yr ago. Further, we show that the Paleocene, Eocene and Oligocene were key periods when diversification of major lineages within Parmeliaceae occurred, with subsequent radiations occurring primarily during the Oligocene and Miocene. Our phylogenetic hypothesis supports the independent origin of lichenicolous fungi associated with climatic shifts at the Oligocene-Miocene boundary. Moreover, diversification bursts at different times may be crucial factors driving the diversification of Parmeliaceae. Additionally, our study provides novel insight into evolutionary relationships in this large and diverse family of lichen-forming ascomycetes.

Lichen diversity and red-listed lichen species relationships with tree species and diameter in wooded meadows.

This study provides a unique large dataset of total epiphytic lichen diversity (fruticose, foliose and crustose species) and composition on 1,294 trees of 17 tree species in wooded meadows in Sweden and Estonia, the Baltic region. The inventory (25,380 observations and 246 lichen taxa) clearly illustrated that Ulmus minor, Quercus robur and Fraxinus excelsior contributed most significantly to epiphytic lichen richness and number of red-listed species. In Sweden, average single tree α richness was 22.2 on Ulmus (only in Sweden), 21.6 on Quercus (25.0 in Estonia) and 19.8 on Fraxinus (16.7 in Estonia), respectively. Ulmus hosted on average one red-listed species per tree, compared with 0.7 on Fraxinus (0.6 in Estonia), 0.4 on Quercus (0.7 in Estonia) and only 0.05 on Betula (same in Estonia). Lichen species composition and the average number of red-listed lichens were influenced by tree diameter on Fraxinus and Quercus, whilst no such pattern was evident on Ulmus. Randomized species accumulation curves of the dominating tree species illustrated that Fraxinus, Quercus and Ulmus supported α dominated lichen communities where individual trees hosted a substantial part of the total richness. Betula, on the other hand, supported β dominated communities where individual trees tended to be dissimilar and, therefore, more of the total richness existed as species turnover among host trees. Lichen species composition was influenced by tree species, and most notably, lichen species on Ulmus had a strong consistent clumping in ordination graphs, with many rare and red-listed lichens. The broadleaved deciduous trees within the wooded meadows clearly contribute greatly to the biodiversity of the Baltic region.

Estimating Coextinction Risks from Epidemic Tree Death: Affiliate Lichen Communities among Diseased Host Tree Populations of Fraxinus excelsior

At least 10% of the world’s tree species are threatened with extinction and pathogens are increasingly implicated in tree threats. Coextinction and threats to affiliates as a consequence of the loss or decline of their host trees is a poorly understood phenomenon. Ash dieback is an emerging infectious disease causing severe dieback of common ash Fraxinus excelsior throughout Europe. We utilized available empirical data on affiliate epiphytic lichen diversity (174 species and 17,800 observations) among 20 ash dieback infected host tree populations of F. excelsior on the island Gotland in the Baltic Sea, Sweden. From this, we used structured scenario projections scaled with empirical data of ash dieback disease to generate probabilistic models for estimating local and regional lichen coextinction risks. Average coextinction probabilities (Ā) were 0.38 (95% CI ±0.09) for lichens occurring on F. excelsior and 0.14 (95% CI ±0.03) when considering lichen persistence on all tree species. Ā was strongly linked to local disease incidence levels and generally increasing with lichen host specificity to F. excelsior and decreasing population size. Coextinctions reduced affiliate community viability, with significant local reductions in species richness and shifts in lichen species composition. Affiliates were projected to become locally extirpated before their hosts, illuminating the need to also consider host tree declines. Traditionally managed open wooded meadows had the highest incidence of ash dieback disease and significantly higher proportions of affiliate species projected to go extinct, compared with unmanaged closed forests and semi-open grazed sites. Most cothreatened species were not previously red-listed, which suggest that tree epidemics cause many unforeseen threats to species. Our analysis shows that epidemic tree deaths represent an insidious, mostly overlooked, threat to sessile affiliate communities in forested environments. Current conservation and management strategies must account for secondary extinctions associated with epidemic tree death.

Diagnostics for a troubled backbone: testing topological hypotheses of trapelioid lichenized fungi in a large-scale phylogeny of Ostropomycetidae (Lecanoromycetes)

Trapelioid fungi constitute a widespread group of mostly crust-forming lichen mycobionts that are key to understanding the early evolutionary splits in the Ostropomycetidae, the second-most species-rich subclass of lichenized Ascomycota. The uncertain phylogenetic resolution of the approximately 170 species referred to this group contributes to a poorly resolved backbone for the entire subclass. Based on a data set including 657 newly generated sequences from four ribosomal and four protein-coding gene loci, we tested a series of a priori and new evolutionary hypotheses regarding the relationships of trapelioid clades within Ostropomycetidae. We found strong support for a monophyletic group of nine core trapelioid genera but no statistical support to reject the long-standing hypothesis that trapelioid genera are sister to Baeomycetaceae or Hymeneliaceae. However, we can reject a sister group relationship to Ostropales with high confidence. Our data also shed light on several long-standing questions, recovering Anamylopsoraceae nested within Baeomycetaceae, elucidating two major monophyletic groups within trapelioids (recognized here as Trapeliaceae and Xylographaceae), and rejecting the monophyly of the genus Rimularia. We transfer eleven species of the latter genus to Lambiella and describe the genus Parainoa to accommodate a previously misunderstood species of Trapeliopsis. Past phylogenetic studies in Ostropomycetidae have invoked “divergence order” for drawing taxonomic conclusions on higher level taxa. Our data show that if backbone support is lacking, contrasting solutions may be recovered with different or added data. We accordingly urge caution in concluding evolutionary relationships from unresolved phylogenies.

Crypthonia, a new genus of byssoid Arthoniaceae (lichenised Ascomycota)

Crypthonia with 11 species is described as belonging to the Arthoniaceae. The new genus is characterised by (1) white to pale carneous, maculiform ascomata lacking a distinct exciple, (2) a weakly gelatinised, hydrophobic hymenium of paraphysoids, (3) a discontinuous layer of branched ascogenous hyphae in the hypothecium, (4) small, clavate to broadly clavate asci of the Arthonia-type lacking a hemiamyloid ring structure in the tholus, (5) eight small, hyaline, 1–3-septate, thin-walled ascospores per ascus, (6) loosely attached thalli with a byssoid, coloured hypothallus, and (7) a chemistry of mainly β-orcinol depsidones and tridepsides including psoromic, norstictic, and gyrophoric acids. Rugulosin occurs in C. bella and C. citrina. Crypthonia athertoniensis Frisch & G. Thor, C. bella Frisch & G. Thor, C. brevispora Frisch & G. Thor, C. citrina Frisch & G. Thor, C. olivacea Frisch & G. Thor, C. palaeotropica Frisch & G. Thor, and C. vandenboomii Frisch & G. Thor are described. C. albida (Fée) Frisch & G. Thor, C. biseptata (Aptroot & Wolseley) Frisch & G. Thor, C. mycelioides (Vain.) Frisch & G. Thor, and C. polillensis (Vain.) Frisch & G. Thor are new combinations. The delimitation from similar genera and the position within the Arthoniaceae is discussed.

A large-scale phylogenetic revision of Roccellaceae (Arthoniales) reveals eight new genera

A two-locus phylogenetic hypothesis of the family Roccellaceae is presented based on data from the nuclear ribosomal large subunit (nucLSU) and the second largest subunit of RNA polymerase II (RPB2). This analysis includes 341 sequences (166 newly generated) and 180 specimens representing about 114 species. The genera Lecanactis, Roccellina, Schismatomma and Sigridea were found to be paraphyletic/polyphyletic. In order to make these groups monophyletic, the new genera Crocellina, Diromma, Gyrographa, Gyronactis, Ocellomma, Pseudoschismatomma, Psoronactis and Vigneronia are described. The genus Sagenidium is placed in synonymy with Lecanactis. The new species Enterographa incognita, Gyronactis asiatica and Lecanactis submollis are described. Several species of Opegrapha are transferred to the Roccellaceae. Sorediate morphs are recorded for the first time in the genus Syncesia.

Occurrence patterns of lichens on stumps in young managed forests.

The increasing demand for forest-derived bio-fuel may decrease the amount of dead wood and hence also the amount of available substrate for saproxylic ( = dead-wood dependent) organisms. Cut stumps constitute a large portion of dead wood in managed boreal forests. The lichen flora of such stumps has received little interest. Therefore, we investigated which lichens that occur on stumps in young (4–19 years), managed forests and analyzed how species richness and occurrence of individual species were related to stump and stand characteristics. We performed lichen inventories of 576 Norway spruce stumps in 48 forest stands in two study areas in Central Sweden, recording in total 77 lichen species. Of these, 14 were obligately lignicolous, while the remaining were generalists that also grow on bark, soil or rocks. We tested the effect of characteristics reflecting successional stage, microclimate, substrate patch size, and the species pool in the surrounding area on (1) total lichen species richness, (2) species richness of obligately lignicolous lichens and (3) the occurrence of four obligately lignicolous lichen species. The most important variables were stump age, with more species on old stumps, and study area, with similar total species richness but differences in occupancy for individual species. Responses for total lichen species richness and species richness of obligately lignicolous lichens were overall similar, indicating similar ecological requirements of these two groups. Our results indicate that species richness measurements serve as poor proxies for the responses of individual, obligately lignicolous lichen species.