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Net-diversification rate through time plots of the two subclasses and families with more than 500 species in these two main subclasses of lichen-forming fungi. Solid lines are the mean net-diversification rates and the grey areas depict the 95% probability densities. Vertical dash lines indicate 66 MYA. LM = Lecanoromycetidae, OP = Ostropomycetidae. Red color = lineages that are mostly macrolichens, blue color = microlichen lineages.
Source publication
Historical mass extinction events had major impacts on biodiversity patterns. The most recent and intensively studied event is the Cretaceous – Paleogene (K-Pg) boundary (ca. 66 million years ago [MYA]). However, the factors that may have impacted diversification dynamics vary across lineages. We investigated the macroevolutionary dynamics with a s...
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Citations
... The earliest known lichen fossils date back to the Early Devonian period (415 Ma) (Honegger et al., 2013a(Honegger et al., , 2013b, but the exact date of the first appearance of lichens is uncertain (e.g., Nelsen et al., 2020). Reports of lichen fossils are extremely rare because their remains are easily decomposed; consequently, most studies of their evolutionary history and response to the paleoenvironment have relied on a molecular clock approach (Printzen and Lumbsch, 2000;Gaya et al., 2015;Kraichak et al., 2015;Huang et al., 2019;Nelsen et al., 2020). ...
... 2 However, the evolutionary history of lichen-forming fungi is poorly understood, because of the sparse fossil record, and has been primarily reconstructed based on molecular dating analyses. [6][7][8][9] Although these approaches proposed a framework to illustrate how the lichen symbiosis may have evolved, fossil evidence is indispensable in testing and supplementing the current understandings especially when the earlier fossil was discovered. ...
... It has been proposed that the diversification of most modern macrolichens did not occur before the Cretaceous-Paleogene (K-Pg) boundary 65 Mya. 6,9,12 This is contrasted by the finding of the oldest Jurassic macrolichen, Daohugouthallus ciliiferus. 13 Given this lack of evidence for macrolichen fossils prior to the K-Pg boundary, the significance of the Jurassic lichen D. ciliiferus is crucial for understanding the evolutionary history of macrolichens. ...
... The diversification of major macrolichen lineages after the Cretaceous-Paleogene (K-Pg) boundary was mainly concentrated within Lecanoromycetes. 2,6,12 Noticeably, the divergence time of Lecanoromycetes, was estimated at 300-250 Mya based on molecular clock analyses, 7,9,23 coinciding with the period after the end-Permian extinction. Considering the diverse Permian forests that were in existence around the world during that period, 35 this provided a potential ecological setting for the evolution of early epiphytic macrolichens; however, there are no fossils to support such an assumption. ...
Lichens are well known as pioneer organisms or stress-tolerant extremophiles, potentially playing a core role in the early formation of terrestrial ecosystems. Epiphytic macrolichens are known to contribute to the water- and nutrient cycles in forest ecosystem. But due to the scarcity of fossil record, the evolutionary history of epiphytic macrolichens is poorly documented. Based on new fossil of Jurassic Daohugouthallus ciliiferus, we demonstrate the hitherto oldest known macrolichen inhabited a gymnosperm branch. We applied energy dispersive X-ray spectroscopy and geometric morphometric analysis to complementarily verify lichen affinity of D. ciliiferus and quantitatively assess the potential relationships with extant lichenized lineages, providing new approaches for study of this lichen adpression fossil. Considering the results, and the inferred age of D. ciliiferus, a new family, Daohugouthallaceae, is established. This work updates current knowledge to the early evolution of epiphytic macrolichens and reveals more complex lichen-plant interactions in a Jurassic forest ecosystem.
... The notion that Huang et al. (2019) did not report increased diversification rates after the K-Pg-boundary for largely foliicolous families within Lecanoromycetes (Gomphillaceae, Pilocarpaceae, Porinaceae) may be due to the fact that species richness in these families was incompletely assessed, as only sampling bias for the included genera, but not for missing genera, was considered. For instance, Gomphillaceae were represented by four out of 27 genera (one species each), with a mean proportional subsampling of 0.0209, resulting in an inferred richness of 191 species, less than half (45%) of the actual number. ...
... The analysis was done in BEAST 1.7.5 (Drummond et al., 2012), with an external calibration as follows. Divergence time estimates for the split between Gomphillaceae and Graphidaceae were obtained from Beimforde et al. (2014;130 Mya), Kraichak et al. (2018;190 Mya), and Huang et al. (2019;190 Mya). Using the split between subfamily Fissurinoideae and subfamilies Redonographoideae plus Graphidoideae in Kraichak et al. (2018;175 Mya), we also derived indirect estimates for the Gomphillaceae-Graphidaceae split from Lücking et al. (2013;165 Mya) and Nelsen et al. (2020;135 Mya). ...
... In previous studies, the divergence time between Gomphillaceae and Graphidaceae had been estimated at between 190 and 130 Mya, between the Early and Late Jurassic and Early Cretaceous (Rivas Plata, 2011;Lücking et al., 2013;Beimforde et al., 2014;Kraichak et al., 2018;Huang et al., 2019;Nelsen et al., 2020). Using 160 Mya as prior, our analysis resulted in an estimated for this split of around 130 Mya, similar to the most recent finding by Nelsen et al. (2020) and the earliest estimate in the broad analysis by Beimforde et al. (2014). ...
We present the first broad molecular-phylogenetic revision of the lichenized family Gomphillaceae, based on 408 newly generated sequences of the mitochondrial SSU rDNA and nuclear LSU rDNA, representing 342 OTUs. The phylogenetic analysis of 20 out of the 28 currently accepted genera resulted in 48 clades. Twelve genera were resolved as monophyletic: Actinoplaca, Arthotheliopsis, Bullatina, Caleniopsis, Corticifraga, Gomphillus, Gyalectidium, Gyalidea, Jamesiella, Rolueckia, Rubrotricha, and Taitaia. Two genera resulted paraphyletic, namely Aulaxina (including Caleniopsis) and Asterothyrium (including Linhartia). Six genera were in part highly polyphyletic: Aderkomyces, Calenia, Echinoplaca, Gyalideopsis, Psorotheciopsis, and Tricharia. While ascoma morphology and anatomy has traditionally been considered as main character complex to distinguish genera, our study supported the notion that the characteristic asexual anamorph of Gomphillaceae, the so-called hyphophores, are diagnostic for most of the newly recognized clades. As a result, we recognize 26 new genus-level clades, three of which have names available (Microxyphiomyces, Psathyromyces, Spinomyces) and 23 that will require formal description as new genera. We also tested monophyly for 53 species-level names for which two or more specimens were sequenced: 27 were supported as monophyletic and representing a single species, 13 as monophyletic but with an internal topology suggesting cryptic speciation, four as paraphyletic, and nine as polyphyletic. These data suggest that species richness in the family is higher than indicated by the number of accepted names (currently 425); they also confirm that recently refined species concepts reflect species richness better than the broad concepts applied in Santesson's monograph. A divergence time analysis revealed that foliicolous Gomphillaceae diversified after the K–Pg-boundary and largely during the Miocene, a notion supported by limited data available for other common foliicolous lineages such as Chroodiscus (Graphidaceae), Pilocarpaceae, and Porinaceae. This contradicts recent studies suggesting that only macrofoliose Lecanoromycetes exhibit increased diversification rates in the Cenozoic.
... 2 However, the evolutionary history of lichen-forming fungi is poorly understood, because of the sparse fossil record, and has been primarily reconstructed based on molecular dating analyses. [6][7][8][9] Although these approaches proposed a framework to illustrate how the lichen symbiosis may have evolved, fossil evidence is indispensable in testing and supplementing the current understandings especially when the earlier fossil was discovered. ...
... It has been proposed that the diversification of most modern macrolichens did not occur before the Cretaceous-Paleogene (K-Pg) boundary 65 Mya. 6,9,12 This is contrasted by the finding of the oldest Jurassic macrolichen, Daohugouthallus ciliiferus. 13 Given this lack of evidence for macrolichen fossils prior to the K-Pg boundary, the significance of the Jurassic lichen D. ciliiferus is crucial for understanding the evolutionary history of macrolichens. ...
... The diversification of major macrolichen lineages after the Cretaceous-Paleogene (K-Pg) boundary was mainly concentrated within Lecanoromycetes. 2,6,12 Noticeably, the divergence time of Lecanoromycetes, was estimated at 300-250 Mya based on molecular clock analyses, 7,9,23 coinciding with the period after the end-Permian extinction. Considering the diverse Permian forests that were in existence around the world during that period, 35 this provided a potential ecological setting for the evolution of early epiphytic macrolichens; however, there are no fossils to support such an assumption. ...
... Recent studies disagree on the origin of lichenized fungi with one claiming lichenized fungi evolved after the emergence of vascular plants, about 250 Mya (Nelsen et al. 2020), and the other proposing a much earlier origin around 480 Mya (Lutzoni et al. 2018). Regardless of the origin timing, the lichenized fungal diversity we see today is believed to be the result of multiple accelerated diversification events between 100 and 40 million years ago, with most of them being associated with the Cretaceous-Paleogene (K-Pg) boundary and only some diversification events occurring before (Prieto and Wedin 2013;Huang et al. 2019). The subfamily Lobarioideae in the order Peltigerales, the first group of lichenized fungi studied with target capture data, diversified after the Cretaceous-Paleogene mass extinction event, but showed evidence for rapid radiation and potential hybridization events that made resolution of some generic relationships difficult (Widhelm et al. 2019). ...
... The Peltigerales also show diversification of clades during the Cretaceous-Paleogene (K-Pg) boundary around 66 Mya and most of the cladogenic events in our reconstructions occur after this. Mass extinctions associated with K-Pg boundary may have reduced competition and provided an opportunity for surviving lineages to radiate (Renne et al. 2013;Huang et al. 2019). These results should be interpreted with caution, however, as we used secondary calibrations and less than four percent of the total diversity in Peltigerales, but the comparison between the complete and minimal datasets provided useful information. ...
Rapid radiations in Fungi are only beginning to be studied with phylogenomic data. The evolutionary history of the lichenized fungal order Peltigerales has not been well resolved, particularly for the Collematineae. Here, we used concatenation and coalescent-based species tree methods to reconstruct the phylogeny of the Peltigerales based on sequences of 125 nuclear single-copy exon sequences among 60 samples, representing 58 species. Despite uneven, lineage-specific missing data and significant topological incongruence of individual exon trees, the resulting phylogenies were concordant and successfully resolved the phylogenetic relationships of the Peltigerales. Relationships in the Collematineae were defined by short branches and lower nodal support than in other parts of the tree, due in part to conflicting signal in exon trees, suggesting rapid diversification events in the early evolution of the suborder. Using tree distance measures, we were able to identify a minimum subset of exons that could reconstruct phylogenetic relationships in Peltigerales with higher support than the 125-exon dataset. Comparisons between the minimum and complete datasets in species tree inferences, bipartition analyses, and divergence time estimations displayed similar results, although the minimum dataset was characterized by higher levels of error in estimations of divergence times. Contrasting our inferences from the complete and minimum datasets to those derived from few nuclear and mitochondrial loci reveal that our topology is concordant with topologies reconstructed using the nuclear large subunit and mitochondrial small subunit ribosomal DNA markers, but the target capture datasets had much higher support values. We demonstrated how target capture approaches can effectively decipher ancient rapid radiations in cases where well resolved individual exon trees are sufficiently sampled and how to identify subsets of loci that are appropriate for fungal order-level phylogenetics.
... In contrast, clade 'S' likely occupied forested habitats (partially or exclusively), and expanded during the Early Cenozoic into a regime comprised of taxa occupying cooler and drier climates-coinciding with the continued development of cool, temperate habitats in the Late Cretaceous-Early Cenozoic (Saward 1992;Deconto et al. 1999;Beerling and Woodward 2001). This clade subsequently diversified in nonforested habitats during the Paleocene-Miocene, coinciding with the diversification of several Trebouxia-associated lineages of LFF (such as the cetrarioid core, Xanthoparmelia and Rhizoplaca) that are common in these habitats Kraichak et al. 2015;Leavitt et al. 2016;Huang et al. 2019;Nelsen et al. 2020b). Clade 'I' is inferred to have partially or extensively relied on forested habitats, and isolated lineages underwent a Cenozoic transition into ...
Lichens are classic models of symbiosis, and one of the most frequent nutritional modes among fungi. The ecologically and geographically widespread lichen-forming algal (LFA) genus Trebouxia is one of the best-studied groups of LFA and associates with over 7000 fungal species. Despite its importance, little is known about its diversification. We synthesized twenty years of publicly-available data by characterizing the ecological preferences of this group and testing for time-variant shifts in climatic regimes over a distribution of trees. We found evidence for limited shifts among regimes, but that disparate lineages convergently evolved similar ecological tolerances. Early Trebouxia lineages were largely forest specialists or habitat generalists that occupied a regime whose extant members occur in moderate climates. Trebouxia then convergently diversified in non-forested habitats and expanded into regimes whose modern representatives occupy wet-warm and cool-dry climates. We rejected models in which climatic diversification slowed through time, suggesting climatic diversification is inconsistent with that expected under an adaptive radiation. In addition, we found that climatic and vegetative regime shifts broadly coincided with the evolution of biomes and associated or similar taxa. Together, our work illustrates how this keystone symbiont from an iconic symbiosis evolved to occupy diverse habitats across the globe.
... Lecanoromycetes, closest to the Lecanora crown (sensuPrieto and Wedin 2013: table 3;Beimforde et al. 2014;Samarakoon et al. 2016;Huang et al. 2019). The mean divergence time of the clade including all accessions of the fruticose Ramalinaceae plus their crustose sister taxon (Cliostomum s. str., including the genus type C. corrugatum) is 55.53 Myrs [95% highest posterior density (HPD) interval: 40.23-72.29] ...
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: Namibialina gen. 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.
... Similarly, the ecological and geographic preferences of a lichen are also shaped by thallus growth form (which is determined by the LFF), which may also confer competitive advantages that increase fitness. Consistent with this is the enhanced diversification observed in several macrolichen lineages of LFF (44). Together, these evolutionary shifts in photobiont association and growth form may affect the evolutionary trajectories of these lineages and their ecological contributions. ...
... Macrolichens first evolved during the Late Jurassic-Early Cretaceous, with most transitions occurring through the Cenozoic. This agrees with a taxonomically ambiguous lichen fossil from the Lower Cretaceous, consistent with a foliose growth form (94), Eocene macrolichen (Lecanoromycetidae) fossils (45), and previous ASR (44). The evolution of macrolichens likely enhanced contributions to many processes through increased substrate surface roughness and texture, which would have increased capture of aeolian dust, water interception, and retention, contributions to C and mineral cycling, and lichen-animal interactions, while also reducing albedo (28,29,95). ...
Significance
Symbioses are evolutionarily and ecologically widespread, yet we lack a robust understanding of their origins, losses, and macroevolutionary consequences. We traced the evolution of partner choice and phenotype in lichens—a classic model of symbiosis—and revealed shifts among symbiont groups and phenotypic evolution. Symbiont switches broadly coincided with the convergent acquisition of similar partners by divergent clades. Fungi abandoned the lichen habit far earlier than previously understood, and subsequently reacquired it with algae that have frequently facilitated independent fungal transitions to lichenization. Finally, diversification in lichenized fungi was not strictly modulated by partner choice or phenotype, and differed from other fungi, suggesting complex and variable dynamics within lichen fungi and across fungal nutritional modes.
... A major extinction is characterised by a loss of biodiversity, followed by a re-diversification of the survivors [77]. This process pertains not only to multi-cellular fossilforming organisms, but also to organisms for which there is no good fossil record, as evidenced by studies of microbialites [78] and of lichen-forming fungi [79]. In order to assess whether the observed AAI gap between 74 and 76% among members of the family Weeksellaceae would correspond to this gap in ANI values due to the Permian extinction, we charted AAI data for each strain comparison against average nucleotide identity blastn (ANIb) data for the same set of strains (data available on request), and found that a quadratic fit could be used to derive a formula that calculates the expected AAI from the ANIb (Fig. S2, part A). ...
The genus Chryseobacterium in the family Weeksellaceae is known to be polyphyletic. Amino acid identity (AAI) values were calculated from whole-genome sequences of species of the genus Chryseobacterium, and their distribution was found to be multi-modal. These naturally-occurring non-continuities were leveraged to standardise genus assignment of these species. We speculate that this multi-modal distribution is a consequence of loss of biodiversity during major extinction events, leading to the concept that a bacterial genus corresponds to a set of species that diversified since the Permian extinction. Transfer of nine species ( Chryseobacterium arachidiradicis , Chryseobacterium bovis , Chryseobacterium caeni , Chryseobacterium hispanicum , Chryseobacterium hominis , Chryseobacterium hungaricum , Chryseobacterium molle , Chryseobacterium pallidum and Chryseobacterium zeae ) to the genus Epilithonimonas and eleven ( Chryseobacterium anthropi , Chryseobacterium antarcticum , Chryseobacterium carnis , Chryseobacterium chaponense , Chryseobacterium haifense, Chryseobacterium jeonii , Chryseobacterium montanum , Chryseobacterium palustre , Chryseobacterium solincola , Chryseobacterium treverense and Chryseobacterium yonginense ) to the genus Kaistella is proposed. Two novel species are described: Kaistella daneshvariae sp. nov. and Epilithonimonas vandammei sp. nov. Evidence is presented to support the assignment of Planobacterium taklimakanense to a genus apart from Chryseobacterium, to which Planobacterium salipaludis comb nov. also belongs. The novel genus Halpernia is proposed, to contain the type species Halpernia frigidisoli comb. nov., along with Halpernia humi comb. nov., and Halpernia marina comb. nov.
... A major extinction is characterised by a loss of biodiversity, followed by a re-diversification of the survivors [77]. This process pertains not only to multi-cellular fossilforming organisms, but also to organisms for which there is no good fossil record, as evidenced by studies of microbialites [78] and of lichen-forming fungi [79]. In order to assess whether the observed AAI gap between 74 and 76% among members of the family Weeksellaceae would correspond to this gap in ANI values due to the Permian extinction, we charted AAI data for each strain comparison against average nucleotide identity blastn (ANIb) data for the same set of strains (data available on request), and found that a quadratic fit could be used to derive a formula that calculates the expected AAI from the ANIb (Fig. S2, part A). ...
