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DEPARTAMENTO DE BIOLOGÍA VEGETAL II FACULTAD DE FARMACIA UNIVERSIDAD COMPLUTENSE DE MADRID PhD dissertation SPECIES, PHYLOGEOGRAPHY AND EXTROLITE PRODUCTION IN BRYORIA AND PSEUDEPHEBE (PARMELIACEAE) Carlos Galán Boluda Madrid, July 6th 2017 Study conducted under the supervision of: Dr. Víctor Jiménez Rico Dr. David L. Hawksworth Index • Introduction • Objectives • Materials and Methods • Chapters: • 1. Pseudephebe species are cryptic with an environmentally modified morphology. • 2. Molecular studies reveal a new species of Bryoria in Chile. • 3. Bryoria fuscescens s. l. show a mismatch between haplotypes and chemotypes. • 4. Fluorescence microscopy as a tool for the visualization of lichen substances within Bryoria thalli. • 5. Characterization of microsatellite loci in lichen-forming fungi of Bryoria section Implexae. • 6. Towards an integrative taxonomy of Bryoria sect. Implexae. • 7. Phylogeography and evolution of Bryoria fuscescens s. str. • Conclusions Introduction Mycobiont = Lichen taxonomy Photobiont Ascomycota Chlorophyta Basidiomycota Cyanobacteria “Glomeromycota” Heterokontophyta Small animals Lichenicolous fungi Cystobasidiomycetes Other algae yeasts Proteobacteria and other bacteria Tundra community, Norway Introduction At least 15 independent origins of lichenized fungi Dikarya Lecanoromycetes Usnea trichodeoides, Tanzania Introduction Parmeliaceae Divakar et al. 2015 Pseudephebe Nodobryoria Bryocaulon Alectoria Bryoria Introduction Intermediate specimens between species in: Pseudephebe Pseudephebe minuscula Pseudephebe pubescens Brodo & Hawksworth 1977 section Implexae Bryoria Velmala et al. 2014 Main Objectives • Perform an integrative taxonomical study of Bryoria section Implexae and Pseudephebe. • Study the extrolite composition, location and taxonomical utility in Bryoria and Pseudephebe. • Study the interaction between Bryoria fuscescens and the environment. • Understand the evolutive processes that are producing the phenotypical variability observed in Bryoria fuscescens s. str. Materials and Methods Sampled areas Pseudephebe: aprox. 120 specimens Bryoria: aprox. 2.100 specimens Materials and Methods Example of three sampled regions Norway Norway Portugal Materials and Methods Main data Main analyses Distribution Phenograms: “R”. Phenotypical Recombination detection: RDP, GENECONV, Chimaera, Morphological characters Maxchi, Bootscan, SiScan, PhylPro, 3Seq. Chemical characters Phylogenetic reconstruction: RAxML, MrBayes, MAFFT, Molecular Partitionfinder, Mega, jModeltest, Beast, Figtree, CADM test. 7 standard DNA markers (6 +1) Divergence time estimation: Beast. 5 new DNA markers Species delimitation programs: ABGD, GMYC, PTP, 18 microsatellite markers BP&P, DISSECT. Genepool detection: PCoA, DAPC, haplotype network, Main lab. techniques STRUCTURE. Genetic diversity: “R”, ADZE, GenAlEx, KGTESTS, Fluorescence microscopy Arlequin. Thin layer chromatography Population dynamics: Beast. PCR Spatial analyses: Migrate-n, ibd. Sequencing Potential distribution: Maxent. 545 pyrosequencing Bryoria: Pseudephebe: Chapter 1 Pseudephebe species are cryptic with an environmentally modified morphology Chapter 1 Pseudephebe species concept 120 specimens Pseudocyphellae Bryoria mariensis Pseudephebe pubescens P. minuscula 37 specimens + 25 outgroup Phylogenetic tree using: nuITS, RPB1 & MCM7 Characters not reported in bibliography Not three phenotipic groups can be obtained Chapter 1 Pseudephebe species concept 26.5 Mya 4.3 Mya 9.5 Mya 1.25 Mya ML and bayesian phylogenetic tree from the concatenated matrix of ITS, RPB1 and MCM7. Chapter 1 Pseudephebe species concept New species concept: P. minuscula Syn: Bryoria mariensis P. pubescens ML and Bayesian phylogenetic tree from the concatenated matrix of ITS, RPB1 and MCM7. Species delimitation programs Chapter 1 Pseudephebe species concept Pseudocyphellae P. pubescens No discriminatory characters between species P. minuscula P. minuscula and P. pubescens are cryptic species Chapter 2 Molecular studies reveal a new species of Bryoria in Chile Chapter 2 Bryoria araucana sp. nov. - Morphological study - Thin layer chromatography Maximum likelihood tree - nuITS, mtSSU, MCM7 Bayesian tree B. glabra / fuscescens Bryoria aff. trichodes or B. sect. Implexae Chapter 2 Bryoria araucana sp. nov. B. araucana sp. nov. B. glabra Bryoria sect. Bryoria is polyphyletic Chapter 2 Bryoria araucana sp. nov. Boluda et al. 2015 Chapter 3 Bryoria fuscescens s. l. show a mismatch between haplotypes and chemotypes Typical lichen community of B. fuscescens s.l. in Spain Chapter 3 Bryoria fuscescens mismatch 45 morphologically invariable B. fuscescens specimens from three close localities Each specimen was divided into four regions: - Base - Branches (without soralia) - Soralia TLC & nuITS - Tips Chapter 3 Bryoria fuscescens mismatch nuITS phylogenetic tree nuITS Haplotype network showing the chemotypes Locality Haplotype Chemotype Specimen1 Specimen2 Fumarprotocetraric Norstictic Psoromic And Fumarprotocetraric acid Base psoromic Branch acid acid Tips acid Soralia Chapter 4 Fluorescence microscopy as a tool for the visualization of lichen substances within Bryoria thalli Autofluorescence of psoromic acid crystalls Chapter 4 Fluorescence microscopy Norstictic acid Fumarprotocetraric acid Pseudocyphellae Pd+ red Pseudocyphellae K+ red Chlorophyll Fumarprotocetraric acid UV 450-490 nm Chapter 4 Fluorescence microscopy White light UV 450-490 nm Atranorine Atranorine Pseudocyphellae Chlorophyll Usnic acid Salazinic acid Parmelia sulcata UV 450-490 nm Chapter 4 Fluorescence microscopy Psoromic acid Fast crystallization Apothecia of Pseudocyphellae of Bryoria bicolor (no extrolites) direction Bryoria capillaris Crystallization Fluorescence microscopy is a good tool to locate and sometimes identify extrolites inside the lichen thallus Slow crystallization Chapter 5 Characterization of microsatellite loci in lichen-forming fungi of Bryoria section Implexae Microsatellites PCR products Chapter 5 Mirosatellites development Obtaining the microsatellites and FRBi markers Bryoria sect. Implexae Spanish specimens 454 Pyrosequencing 6.329 putative Swiss specimens MSATCOMMANDER 533.962 reads (Scanning for microsatellites) (average length 812 bp) microsatellites Finnish specimens Unfavorable primers Duplicates 30 morphologically variable specimens Bryoria sect. 44 putative 58 putative 397 putative Implexae specimens microsatellites microsatellites microsatellites PCR conditions Invariable microsatellites Algae and other Trebouxia microsatellites NCBI microsatellites Trebouxia 18 microsatellites cultures 36 flanking 5 flanking regions regions Unfavorable primers Invariable regions Chapter 6 Towards an integrative taxonomy of Bryoria sect. Implexae B. fuscescens B. implexa B. capillaris Chapter 6 Bryoria sect. Implexae taxonomy Main key characters: - Extrolites - Soralia - Pseudocyphellae - Thallus colour - Branching angles Velmala et al. 2014 Chapter 6 Bryoria sect. Implexae taxonomy 142 specimens from: - Morphology (incl. lichenicolous) - Chemistry - DNA sequences nuITS, IGS, GAPDH FRBi15, FRBi16 (not showed) - Microsatellites Velmala et al. 2014 Chapter 6 Bryoria sect. Implexae taxonomy Phenetic analyses Extrolites Extrolites + morphology The species concept in Bryoria sect. Implexae, established mainly using septentrional specimens, break down when meridional specimens are studied. Chapter 6 Bryoria sect. Implexae taxonomy ML and Bayesian tree form the concatenated matrix (ITS, IGS & GAPDH) Bryoria fuscescens agg. Bryoria sect. Implexae WD Tree backbone well supported NA Ko G Chapter 6 ML and Bayesian tree form the concatenated matrix (ITS, IGS & GAPDH) NA WD Ko G NA Ko Tree backbone well supported G Chapter 6 Extrolite composition WD NA Ko G WD Chapter 6 WD DISSECT NA Ko G Chapter 6 WD Haplotype network NA gaps missing 95% connection limit Ko G Chapter 6 WD NA Principal coordinate analyses using microsatellites Ko G Chapter 6 STRUCTURE using microsatellites WD NA Ko G Chapter 6 WD NA Ko Divergence time estimation G Chapter 6 Past population dynamics WD NA X = Million years ago Ko Y = Population size G Chapter 6 Proposed species concept Bryoria fuscescens Syn: B. capillaris, B. implexa, B. kuemmerleana, B. vrangiana. WD Cryptic Bryoria pseudofuscescens 1 Mya of divergence Syn: B. friabilis, B. inactiva, B. pikei. Bryoria kockiana Syn: B. sp. NA Ko Bryoria glabra G Chapter 6 WD NA Ko G Chapter 7 Phylogeography and evolution of Bryoria fuscescens Chapter 7 Bryoria phylogeography Bryoria morphospecies growing together What is producing that phenotypes? Chapter 7 Bryoria phylogeography Phenotype-capillaris Bryoria fuscescens s. str. Phenotype-fuscescens - Usually pale - Usually dark - With barbatolic acid - Without barbatolic acid - Soralia rare - Soralia frequent - Angles usually acute - Angles variable Cortical UV autofluorescence Cortical UV autofluorescence Chapter 7 Bryoria phylogeography 1.359 specimens 1.400 specimens, 64 populations, 18 microsatellites 14 microsatellites No missing data 35 specimens used for a phylogenetical reconstruction (3 standard loci, and 5 new loci) Chapter 7 Bryoria phylogeography AMOVA Allelic richness Higher diversity within populations than among. Similar diversity in trunks and twigs. Chapter 7 Bryoria phylogeography Scandinavia: Alps: High diversity Iberia: Low diversity Carpathians: Great Britain: Chapter 7 Bryoria phylogeography - Less clonallity than expected - Saxicolous populations are genetically poor. Pops. 1-13 not showed - Apotheciated populations are not significantly
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    The Lichenologist 48(5): 343–346 (2016) © British Lichen Society, 2016 doi:10.1017/S0024282916000360 A Liber Amicorum: Irwin Brodo FIG. 1. Irwin Brodo in Newfoundland, Canada, 2007. This issue of The Lichenologist is dedicated to career in lichenology began. The absence Irwin (Ernie) Brodo (Fig. 1) on the occasion of a lichenologist at Cornell prompted of his 80th birthday. Ernie to seek the assistance of Mason Hale at Ernie has been a mainstay in North the Smithsonian Institution to complete American lichenology for over 50 years. He ecological studies on lichens, but he was was born on November 7, 1935 in New York largely self-taught during this time. With City, where he obtained an undergraduate his interest in lichens piqued, Ernie headed degree in biology at the City College of to Michigan State University (MSU) to New York (now part of the City University of complete a doctorate under the supervision New York) in 1957. In 1959, he received a of Henry Imshaug. He received his master’s degree from Cornell University in Ph.D. in 1965 for a series of ecological and Ithaca, New York, where his distinguished floristic studies on the lichens of Long Island. Downloaded from http:/www.cambridge.org/core. Duke University Libraries, on 03 Oct 2016 at 15:15:24, subject to the Cambridge Core terms of use, available at http:/www.cambridge.org/core/terms. http://dx.doi.org/10.1017/S0024282916000360 344 THE LICHENOLOGIST Vol. 48 A B C D E F FIG. 2. Irwin Brodo. A, in the field with Jennifer Staniforth in the Yukon Territory, Canada; B, in the laboratory with Chicita Culberson at Duke University, USA; C, atop Mount Washington with notable north-eastern American cryptogamists, New Hampshire, USA; D, in the field in Israel; E, identifying specimens in Australia; F, in front of the new Canadian Museum of Nature Building with the first author in 2006, Québec, Canada.
  • Effect of Patch Size on Species Richness and Distribution of Sub-Alpine Saxicolous Lichens

    Effect of Patch Size on Species Richness and Distribution of Sub-Alpine Saxicolous Lichens

    Effect of patch size on species richness and distribution of sub-alpine saxicolous lichens Abraham Adida1, Melody Griffith2, Margot Kirby3, and Amanda Lin3 1University of California, Santa Cruz; 2University of California, Davis; 3University of California, Los Angeles ABSTRACT Understanding how communities respond to environmental pressures is important for conservation planning and management. In this observational study, we examined the SLOSS debate and the ecological concept of nestedness in respect to how saxicolous lichen communities in sub-alpine habitats are structured. We analyzed the effects of patch size on the species richness and distribution of saxicolous lichen. We surveyed 242 granitic rocks in the White Mountains, California, and collected data on the different taxa found. Our results showed that there was greater species richness per m2 on small rocks, supporting the “Several Small” side of the SLOSS debate. Additionally, we found that there was a high degree of nestedness in our study system. Saxicolous lichen provide a manageable scale to test community-level ecological concepts and allow us to better define the boundaries of their applications. Keywords: saxicolous lichen, community ecology, SLOSS, nestedness, sub-alpine INTRODUCTION addresses species richness within a confined habitat, but overlooks species composition Investigation into how ecological concepts and distribution across habitats, and is can be used to determine community therefore often supplemented with the responses to environmental pressures may ecological concept of nestedness. help inform conservation planning and Nestedness is a measure of structure in the management of biotic assemblages (Will- distribution of species across habitats. wolf et al. 2006).⁠ Application of these models Systems with high nestedness would can vary among taxa and defining their demonstrate that species-poor habitats boundaries can increase confidence in their contain a subset of the taxa in species-rich use.