Mónica A.G. Otálora

Fragment quality and matrix affect epiphytic performance in a Mediterranean forest landscape

Destruction and fragmentation of habitats represent one of the most important threats for biodiversity. Here, we examined the effects of fragmentation in Mediterranean forests on the epiphytic lichen Lobaria pulmonaria (Lobariaceae). We tested the hypothesis that not only the level of fragmentation affects L. pulmonaria populations, but also the quality of the habitat and the nature of the surrounding matrix affect them. The presence and abundance of the lichen was recorded on 2039 trees in a total of 31 stands. We recorded habitat quality and landscape variables at three hierarchical levels: tree, plot, and patch. We found that L. pulmonaria tends to occur in trees with larger diameters in two types of surveyed forests. In Quercus pyrenaica patches, the mean diameter of colonized trees was smaller, suggesting the importance of bark roughness. Factors affecting the presence and cover of the lichen in each type of forest were different. There was a strong positive influence of distance from a river in beech forests, whereas proximity to forest edge positively affected in oak forests. The influence of the surrounding matrix was also an important factor explaining the epiphytic lichen abundance.

Phylogeography and divergence date estimates of a lichen species complex with a disjunct distribution pattern

Disjunct species distributions may result from a combination of geologic events and long-distance dispersal. The foliose lichen species complex Leptogium furfuraceum-L. pseudofurfuraceum has an intercontinental disjunction pattern. Populations of this species complex are found in western North America, southern South America, Africa, and southern Europe. We conducted a phylogenetic study to reconstruct the biogeographic history of this species complex using two ribosomal genes (ITS and LSU) and a protein-coding gene (partial RPB2). Results indicated that the complex comprises four geographically restricted genetic lineages. A sister relationship was found between populations from the same hemispheres, incongruent with previous data derived from morphological characteristics and geographical classification schemes. Incorporating Bayesian ancestral area reconstruction and Bayesian divergence time estimation, we proposed an evolutionary hypothesis for the species complex. The results suggested that processes of biotic expansion via transoceanic dispersal were responsible for the species divergence and distribution patterns observed today. This study also expands the view that cryptic speciation is not a rare phenomenon among fungi and lichens.

A revised generic classification of the jelly lichens, Collemataceae

Phylogenetic studies have shown the need for a revised circumscription of generic boundaries in the jelly lichens (Collemataceae). Using a four-marker dataset from a recently published phylogeny of Collemataceae, we tested the monophyly of ten morphologically well-characterized groups. To achieve this, we performed Bayesian and maximum likelihood analyses. The monophyly of the ten morphological groups was confirmed. In order to reconcile molecular and morphological data into a formal classification, we here propose new generic delimitations in Collemataceae. Collema and Leptogium are re-circumscribed and six old generic names are resurrected to accommodate the Collema Crispum-group (Blennothallia), the Collema Tenax-group (Enchylium), the Collema Cristatum-group (Lathagrium), the Collema Occultatum-group (Rostania), the former small Leptogium species (Scytinium), and Leptogium diffractum (Pseudoleptogium). In addition, two new genera are described to accommodate Collema multipartitum (Callome) and the Collema Italicum-group (Paracollema). The presence/absence of a eucortex, which was earlier used as the cardinal character to define genera in the family, is still useful, but only in combination with other traits such as thallus habit (size), lobe size, ascospore characteristics, thallus anatomical structure, and habitat preference. A key to the genera is provided. Lectotypes are designated for Collema marginale Hoffm., Synechoblastus nigrescens (Huds.) Trevis., Eucollema (Cromb.) Horw., Collema section Enchylium Ach., Collema section Lathagrium Ach., Collema sect. Mallotium Ach., Collema section Scytinium Ach., Collemodium Nyl. ex Lamy, and Homodium Nyl. ex Olivier.

Multiple origins of high reciprocal symbiotic specificity at an intercontinental spatial scale among gelatinous lichens (Collemataceae, Lecanoromycetes)

Because the number of fungal species (mycobionts) exceeds the number of algae and cyanobacteria (photobionts) found in lichens by more than two orders of magnitude, reciprocal one-to-one specificity between one fungal species and one photobiont across their entire distribution is not expected in this symbiotic system, and has not previously been observed. The specificity of the cyanobacterium Nostoc found in lichens was evaluated at a broad geographical scale within one of the main families of lichen-forming fungi (Collemataceae) that associate exclusively with this photobiont. A phylogenetic study was conducted using rbcLXS sequences from Nostoc sampled from 79 thalli (representing 24 species within the Collemataceae), and 163 Nostoc sequences gathered from GenBank. Although most of the lichen-forming fungal species belonging to the Collemataceae exhibited the expected generalist pattern of association with multiple distinct lineages of Nostoc, five independent cases of one-to-one reciprocal specificity at the species level, including two that span intercontinental distributions, were discovered. Each of the five distinct monophyletic Nostoc groups, associated with these five highly specific mycobiont species, represent independent transitions from a generalist state during the evolution of both partners, which might be explained by transitions to asexual fungal reproduction, involving vertical photobiont transmission, and narrowing of ecological niches.

Disentangling the Collema-Leptogium complex through a molecular phylogenetic study of the Collemataceae (Peltigerales, lichen-forming Ascomycota)

Family Collemataceae (Peltigerales, Ascomycota) includes species of cyanolichens with foliose to fruticose or crustose thalli, with simple or septate ascospores. The current classification divides this family into two groups on the basis of ascospore types. The objective of this study was to evaluate the phylogenetic relationships within this family. Combined DNA sequence data from the nuclear large subunit and mitochondrial small subunit ribosomal RNA genes were used to evaluate monophyly of the family and the relationships between the largest genera of this family. The results revealed that this family is not monophyletic. Genera Staurolemma and Physma, currently classified within the Collemataceae, were found nested within the Pannariaceae. The second result of this study confirms that the genera Collema and Leptogium, both part of the Collemataceae s. str., are not monophyletic and that the presence of a thallus cortex is not a synapomorphy for Leptogium. The main taxonomic conclusion is that families Collemataceae and Pannariaceae were recir-cumscribed in light of molecular findings with the latter family now including Staurolemma and Physma. Genera Collema and Leptogium form a single mixed monophyletic group. Inferred ancestral character states within the Collema-Leptogium complex revealed that the ancestor of this family had a thallus without cortex and that a cortex evolved at least twice relatively early in the evolution of the Collemataceae s. str. These independent gains of a thallus cortex seems to be associated with a transition from colonizing bare rocks and soils in semi-arid and exposed habitats to epiphytism in shady humid forests.

Multiple-scale environmental modulation of lichen reproduction

It is necessary to understand how environmental changes affect plant fitness to predict survival of a species, but this knowledge is scarce for lichens and complicated by their formation of sexual and asexual reproductive structures. Are the presence and number of reproductive structures in Lobaria pulmonaria, a threatened lichen, dependent on thallus size, and is their formation sequential? Does any size-dependence and sequential formation vary along a climate gradient? Generalized linear mixed models were used to explore the effect of environmental predictors on the size and presence/abundance of each reproductive structure and to determine the probability of a given-sized thallus to develop any reproductive structure. The largest individuals are more likely to develop reproductive structures, and the lichen uses a mixed strategy of early asexual reproduction and late sexual. Macro and microclimatic variables also influenced reproductive capacity. Relationships among climate conditions and lichen size and reproductive capacity can compromise the future viability of the species in the most southern populations of Europe.

Cardinal characters on a slippery slope - A re-evaluation of phylogeny, character evolution, and evolutionary rates in the jelly lichens (Collemataceae s. str.)

Recent molecular systematic studies have indicated that the traits currently used for generic delimitation in the jelly lichens (Collemataceae s. str.), may not characterize monophyletic groups. Here we reconstruct the phylogeny of Collemataceae using Bayesian and maximum likelihood analyses based on mitochondrial (mtSSU rDNA) and nuclear (nuLSU rDNA, Beta-tubulin and MCM7) markers of 70 Collemataceae species. We studied the evolution of four morphological and ecological characters traditionally used to delimit genera and infra-generic groups. Finally, we tested if differences in branch-lengths between clades are due to differences in rates of molecular evolution. Eleven strongly supported groups were recovered in the resulting well-resolved and well-supported phylogeny. The presence/absence of a eucortex, which is currently used as the cardinal character to define genera in the group, does not characterize monophyletic groups corresponding to the genera as currently circumscribed. Ancestral state reconstruction indicates that the most recent common ancestor of the jelly lichens most likely was saxicolous/terricolous, lacked a tomentum, and had transversally septate ascospores. Although the cortex state could not be reconstructed for the ancestor of the family, our observations indicate that a lack of cortex may have an evolutionary advantage in saxicolous/terricolous species in semi-arid environments, as non-corticate species tends to be larger and occur in higher frequency and abundance in such regions, compared to corticate species. A significant evidence for faster evolutionary rates was found in a lineage mainly including taxa that occur in the wet tropics and humid temperate regions, compared to other lineages. We suggest that this can explain the greater diversity of Collemataceae in tropical and humid areas.

Collema fasciculare belongs in Arctomiaceae

The phylogenetic placement of Collema fasciculare (L.) F. H. Wigg, the most deviating species within Collema (Collemataceae, Lecanoromycetidae), was studied using maximum likelihood and Bayesian analysis of three molecular loci (mitochondrial SSU rDNA, and the protein-coding, nuclear RPB1 and MCM7 genes). Collema fasciculare belongs to Arctomiaceae (Ostropomycetidae) forming a strongly supported monophyletic group with members of Arctomia. The spores, paraphyses, asci and hymenial reactions in Collema fasciculare are similar to other Arctomia, but the ascoma ontogeny is somewhat different. Also C. leptosporum Malme, another species in the Fasciculare group, shows similarities with Arctomia regarding spores and asci. Arctomia is morphologically heterogeneous and the genus is in need of revision. Until then, the species of the Fasciculare group fit best in Arctomia s. lat. and the combinations Arctomia fascicularis (L.) Otálora & Wedin, Arctomia leptospora (Malme) Otálora & Wedin, Arctomia papuanarum (Degel.) Otálora & Wedin and Arctomia uviformis (Hue) Otálora & Wedin are proposed.

Does the Reproductive Strategy Affect the Transmission and Genetic Diversity of Bionts in Cyanolichens? A Case Study Using Two Closely Related Species

Observed levels of population genetic diversity are often associated with differences in species dispersal and reproductive strategies. In symbiotic organisms, the genetic diversity level of each biont should also be highly influenced by biont transmission. In this study, we evaluated the influence of the reproductive strategies of cyanolichen species on the current levels of population genetic diversity of bionts. To eliminate any phylogenetic noise, we selected two closely related species within the genus Degelia, which only differ in their reproductive systems. We sampled all known populations of both species in central Spain and genotyped the fungal and cyanobacterial components of lichen samples using DNA sequences as molecular markers. We applied population genetics approaches to evaluate the genetic diversity and population genetic structure of the symbiotic components of both lichen species. Our results indicate that fungal and cyanobiont genetic diversity is highly influenced by the reproductive systems of lichen fungus. We detected higher bionts genetic diversity values in the sexual species Degelia plumbea. By contrast, the levels of fungal and cyanobiont genetic diversity in the asexual species Degelia atlantica were extremely low (almost clonal), and the species shows a high specificity towards its cyanobiont. Our results indicate that reproduction by vegetative propagules, in species of the genus Degelia, favors vertical transmission and clonality, which affects the species’ capacity for resources and competition, thereby limiting the species to restricted niches.

Phylogenetic study of Catapyrenium s. str. (Verrucariaceae, lichen-forming Ascomycota) and related genus Placidiopsis

The current classification of what used to be called Catapyrenium comprises eight genera belonging to distinct lineages in the Verrucariaceae. Previous phylogenetic studies have shown that the redefined genus Catapyrenium (Catapyrenium s. str.) is monophyletic and sister of Placidiopsis within the Staurothele group, but this relationship was based on only two species from each genus. We conducted a phylogenetic study of Catapyrenium and Placidiopsis as currently delimited to evaluate the monophyly of each genus and infer infrageneric relationships. An initial family level phylogenetic analysis based on the nuLSU locus and implementing a backbone constraint tree (with both weighted maximum parsimony and bootstrap maximum likelihood approaches) was performed to infer phylogenetic placements of Catapyrenium and Placidiopsis taxa not included in previous molecular systematic studies. The results of this analysis were used to define the ingroup for a second phylogenetic analysis based on nuITS and nuLSU and centered on Catapyrenium s. str. and Placidiopsis. Placidiopsis was found to be monophyletic, whereas Catapyrenium s. str. was not. Catapyrenium dactylinum was found to be closely related to Placopyrenium caeruleopulvinum and Placopyrenium stanfordii, all of which were closely related to Placocarpus schaereri and Verrucula. In addition we found genus Placopyrenium to be polyphyletic. The resulting trees confirmed that Catapyrenium s. str. (excluding C. dactylinum) and Placidiopsis constitute two sister monophyletic entities. The data do not support Placidiopsis cinerascens and P. tenella as two distinct species because no characters can be used to distinguish them. Thus P. tenella is here reduced to synonymy with P. cinerascens.