Genome-scale data reveal the role of hybridization in lichen-forming fungi (original) (raw)
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The New phytologist, 2015
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, div...
Molecular Phylogenetics and Evolution, 2011
A growing body of evidence indicates that in some cases morphology-based species circumscription of lichenized fungi misrepresents the number of existing species. The cosmopolitan ''rock posy'' lichen (Rhizoplaca melanophthalma) species-complex includes a number of morphologically distinct species that are both geographically and ecologically widespread, providing a model system to evaluate speciation in lichen-forming ascomycetes. In this study, we assembled multiple lines of evidence from nuclear DNA sequence data, morphology, and biochemistry for species delimitation in the R. melanophthalma species-complex. We identify a total of ten candidate species in this study, four of which were previously recognized as distinct taxa and six previously unrecognized lineages found within what has been thus far considered a single species. Candidate species are supported using inferences from multiple empirical operational criteria. Multiple instances of sympatry support the view that these lineages merit recognition as distinct taxa. Generally, we found little corroboration between morphological and chemical characters, and previously unidentified lineages were morphologically polymorphic. However, secondary metabolite data supported one cryptic saxicolous lineage, characterized by orsellinic-derived gyrophoric and lecanoric acids, which we consider to be taxonomically significant. Our study of the R. melanophthalma species-complex indicates that the genus Rhizoplaca, as presently circumscribed, is more diverse in western North American than originally perceived, and we present our analyses as a working example of species delimitation in morphologically cryptic and recently diverged lichenized fungi.
Multiple Origins of Lichen Symbioses in Fungi Suggested by SSU rDNA Phylogeny
Science, 1995
The crustose lichen L&eanora disperss. lichen symbioses, associations between fungi and algae, have originated multiple times during fungal evolution. At least one successful establishment of symbiosis led to the more than 6000 species of the order l ecanorales, represented here by L. dispersa. The white-rimmed c ups (between 0.3 and 0.7 millimeter in diameter) emerging from the rock substrate produce the meiotic spores of th is fungal symbiont. See Phylogenetic hypotheses provide a context for examining the evolution of heterotrophic lifestyles. The lichen lifestyle, which is the symbiotic association of fungi with algae, is found in varIous representatives of Dicaryomycotina, both Ascomycetes and Basidiomycetes. A highly resolved parsimony analysis of small subunit ribosomal DNA (SSU rONA) sequences suggests at least five Independent origins of the lichen habit in disparate groups of Ascomycetes and Basidiomycetes. Because lichen associations arose from parasitic, mycDfThizal. or free-living saprobic fungi, neither mutualism nor parasitism should be construed as endpoints in symbiont evolution.
Molecular Phylogenetics and Evolution, 2011
A molecular phylogeny of combined mtSSU, nuLSU, and RPB2 data revealed previously unrecognized levels of parallel evolution and phenotypic divergence in the lichen family Graphidaceae. Five clades were supported within the family: the Fissurina, Ocellularia, Graphis, Topeliopsis, and Thelotrema clades, containing 33 of the 42 currently accepted genera within the family. The results for the first time provide a fully resolved phylogeny of this family and confirm the synonymy of Graphidaceae and Thelotremataceae. Ancestral character state reconstruction using likelihood, Bayesian, and parsimony approaches indicate that lirellate ascomata evolved independently in each of the five clades. Carbonized ascomata evolved independently in at least four of the five clades. An unexpected result was the independent evolution of columella structures in the Fissurina and Ocellularia clades. Besides these more general findings, we document several cases in which evolution of several traits in parallel resulted in striking look-alikes within unrelated lineages, such as Topeliopsis muscigena and Chapsa meridensis in the Topeliopsis and Thelotrema clades, Leptotrema wightii, Myriotrema laeviusculum, and Leucodecton phaeosporum in the Ocellularia and Thelotrema clades, Ocellularia stylothecia and Melanotrema meiosporum in the Fissurina and Ocellularia clades, and Myriotrema pycnoporellum, Myriotrema clandestinum and Wirthiotrema glaucopallens in the Fissurina, Ocellularia, and Topeliopsis clades. Pagel's test of independent character evolution suggested that at least for some of the traits involved in these cases, ecological constraints may have caused their evolution in parallel. The most intriguing find is the correlation between gall-forming thalli and vertical columns of calcium oxalate crystals, suggesting that these crystals do not function as light distributors, as previously assumed, but instead stabilize the thalli which are usually hollow beneath, similar to a dome-shaped structure. Ancestral character state reconstruction together with an approach to visualize the phenotype of putative ancestral lineages suggested the alpha-Graphidaceae to resemble some of the extant species currently classified in Myriotrema s.lat., with pore-like ascomata, and nonamyloid ascospores with lens-shaped lumina.
Journal of Systematics and Evolution, 2019
Blastenia is a widely distributed lichen genus in Teloschistaceae. We reconstructed its phylogeny in order to test species delimitation and to find evolutionary drivers forming recent Blastenia diversity. The origin of Blastenia is dated to the early Tertiary period, but later diversification events are distinctly younger. We recognized 24 species (plus 2 subspecies) within 6 infrageneric groups. Each species strongly prefers a single type of substrate (17 species occur on organic substrates, 7 on siliceous rock), and most infrageneric groups also show a clear substrate preference. All infrageneric groups tend to have the Mediterranean and Macaronesian distribution, but some epiphytic species have much larger geographic ranges and some evolved after a long-distance dispersal outside the region. Chlorinated and nonchlorinated anthraquinone chemosyndromes co-occur in apothecia of most species, but the chemotype has been secondarily reduced in some lineages. One infrageneric group has a marked reduction in apothecial size, associated with a substrate shift to twigs. Only seven species have vegetative diaspores; they also produce apothecia but have smaller ascospores. Genome sizes (22-35 Mb in Blastenia) are significantly higher in epilithic species. Within-species genetic variation is low in widely distributed species but high in some epilithic species with small geographical ranges.
PLoS ONE, 2013
Parmelioid lichens form a species-rich group of predominantly foliose and fruticose lichenized fungi encompassing a broad range of morphological and chemical diversity. Using a multilocus approach, we reconstructed a phylogeny including 323 OTUs of parmelioid lichens and employed ancestral character reconstruction methods to understand the phenotypical evolution within this speciose group of lichen-forming fungi. Specifically, we were interested in the evolution of growth form, epicortex structure, and cortical chemistry. Since previous studies have shown that results may differ depending on the reconstruction method used, here we employed both maximum-parsimony and maximum-likelihood approaches to reconstruct ancestral character states. We have also implemented binary and multistate coding of characters and performed parallel analyses with both coding types to assess for potential codingbased biases. We reconstructed the ancestral states for nine well-supported major clades in the parmelioid group, two higher-level sister groups and the ancestral character state for all parmelioid lichens. We found that different methods for coding phenotypical characters and different ancestral character state reconstruction methods mostly resulted in identical reconstructions but yield conflicting inferences of ancestral states, in some cases. However, we found support for the ancestor of parmelioid lichens having been a foliose lichen with a non-pored epicortex and pseudocyphellae. Our data suggest that some traits exhibit patterns of evolution consistent with adaptive radiation.
Fungal Diversity
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 w...
Scientific Reports, 2015
Renewed interests in macroevolutionary dynamics have led to the proliferation of studies on diversification processes in large taxonomic groups, such as angiosperms, mammals and birds. However, such a study has yet to be conducted in lichenized fungi – an extremely successful and diverse group of fungi. Analysing the most comprehensive time-calibrated phylogenies with a new analytical method, we illustrated drastically different diversification dynamics between two hyper-diverse families of lichenized fungi, Graphidaceae and Parmeliaceae, which represent more than a fourth of the total species diversity of lichenized fungi. Despite adopting a similar nutrition mode and having a similar number of species, Graphidaceae exhibited a lower speciation rate, while Parmeliaceae showed a sharp increase in speciation rate that corresponded with the aridification during the Oligocene-Miocene transition, suggesting their adaptive radiation into a novel arid habitat.
The role of species’ interactions in structuring biological communities remains unclear. Mutualistic symbioses, involving close positive interactions between two distinct organismal lineages, provide an excellent means to explore the roles of both evolutionary and ecological processes in determining how positive interactions affect community structure. In this study, we investigate patterns of co-diversification between fungi and algae for a range of New Zealand lichens at the community, genus, and species levels and explore explanations for possible patterns related to spatial scale and pattern, taxonomic diversity of the lichens considered, and the level sampling replication.We assembled six independent datasets to compare patterns in phylogenetic congruence with varied spatial extent of sampling, taxonomic diversity and level of specimen replication. For each dataset, we used the DNA sequences from the ITS regions of both the fungal and algal genomes from lichen specimens to produce genetic distance matrices. Phylogenetic congruence between fungi and algae was quantified using distance-based redundancy analysis and we used geographic distance matrices in Moran’s eigenvector mapping and variance partitioning to evaluate the effects of spatial variation on the quantification of phylogenetic congruence. Phylogenetic congruence was highly significant for all datasets and a large proportion of variance in both algal and fungal genetic distances was explained by partner genetic variation. Spatial variables, primarily at large and intermediate scales, were also important for explaining genetic diversity patterns in all datasets. Interestingly, spatial structuring was stronger for fungal than algal genetic variation. As the spatial extent of the samples increased, so too did the proportion of explained variation that was shared between the spatial variables and the partners’ genetic variation. Different lichen taxa showed some variation in their phylogenetic congruence and spatial genetic patterns and where greater sample replication was used, the amount of variation explained by partner genetic variation increased. Our results suggest that the phylogenetic congruence pattern, at least at small spatial scales, is likely due to reciprocal co-adaptation or co-dispersal. However, the detection of these patterns varies among different lichen taxa, across spatial scales and with different levels of sample replication. This work provides insight into the complexities faced in determining how evolutionary and ecological processes may interact to generate diversity in symbiotic association patterns at the population and community levels. Further, it highlights the critical importance of considering sample replication, taxonomic diversity and spatial scale in designing studies of co-diversification.
Systematic Biology, 2009
Fungi associated with photosynthetic organisms are major determinants of terrestrial biomass, nutrient cycling, and ecosystem productivity from the poles to the equator. Whereas most fungi are known because of their fruit bodies (e.g., saprotrophs), symptoms (e.g., pathogens), or emergent properties as symbionts (e.g., lichens), the majority of fungal diversity is thought to occur among species that rarely manifest their presence with visual cues on their substrate (e.g., the apparently hyperdiverse fungal endophytes associated with foliage of plants). Fungal endophytes are ubiquitous among all lineages of land plants and live within overtly healthy tissues without causing disease, but the evolutionary origins of these highly diverse symbionts have not been explored. Here, we show that a key to understanding both the evolution of endophytism and the diversification of the most species-rich phylum of Fungi (Ascomycota) lies in endophyte-like fungi that can be isolated from the interior of apparently healthy lichens. These "endolichenic" fungi are distinct from lichen mycobionts or any other previously recognized fungal associates of lichens, represent the same major lineages of Ascomycota as do endophytes, largely parallel the high diversity of endophytes from the arctic to the tropics, and preferentially associate with green algal photobionts in lichen thalli. Using phylogenetic analyses that incorporate these newly recovered fungi and ancestral state reconstructions that take into account phylogenetic uncertainty, we show that endolichenism is an incubator for the evolution of endophytism. In turn, endophytism is evolutionarily transient, with endophytic lineages frequently transitioning to and from pathogenicity. Although symbiotrophic lineages frequently give rise to free-living saprotrophs, reversions to symbiosis are rare. Together, these results provide the basis for estimating trophic transition networks in the Ascomycota and provide a first set of hypotheses regarding the evolution of symbiotrophy and saprotrophy in the most species-rich fungal phylum.