Population genomics of a reindeer lichen species from North American lichen woodlands.
Cladonia stellaris
Apothecia
Quebec
SNPs
Stacks
dispersal
fire
population genomics
reproduction
Journal
American journal of botany
ISSN: 1537-2197
Titre abrégé: Am J Bot
Pays: United States
ID NLM: 0370467
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
22
04
2020
accepted:
28
09
2020
pubmed:
30
1
2021
medline:
16
2
2021
entrez:
29
1
2021
Statut:
ppublish
Résumé
Lichens are one of the main structural components of plant communities in the North American boreal biome. They play a pivotal role in lichen woodlands, a large ecosystem situated north of the closed-crown forest zone, and south of the forest-tundra zone. In Eastern Canada (Quebec), there is a remnant LW found 500 km south of its usual distribution range, in the Parc National des Grands-Jardins, originated mainly because of wildfires. We inferred the origin of the lichen Cladonia stellaris from this LW and assessed its genetic diversity in a postfire succession. We genotyped 122 individuals collected across a latitudinal gradient in Quebec. Using the software Stacks, we compared four different approaches of locus selection and single-nucleotide polymorphism calling. We identified the best fitting approach to investigate population structure and estimate genetic diversity of C. stellaris. Populations in southern Quebec are not genetically different from those of northern LWs. The species consists of at least four phylogenetic lineages with elevated levels of genetic diversity and low co-ancestry. In Parc National des Grands-Jardins, we reported high values of genetic diversity not related with time since fire disturbance and low genetic differentiation among populations with different fire histories. This first population genomic study of C. stellaris is an important step forward to understand the origin and biogeographic patterns of lichen woodlands in North America. Our findings also contribute to the understanding of the effect of postfire succession on the genetic structure of the species.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
159-171Informations de copyright
© 2021 Botanical Society of America.
Références
Ahti, T. 1959. Studies on the caribou lichen stands of Newfoundland. Annales Botanici Societalis Zoologicae Botanicae Fennicae ‘Vanamo’ 30: 1-44.
Ahti, T. 1961. Taxonomic Studies on Reindeer Lichens (Cladonia, Subgenus Cladina). Suomalaisen Kirjallisuuden Kirjapaino, Helsinki, Finland.
Allen, J. L., S. K. McKenzie, R. S. Sleith, and S. E. Alter. 2018. First genome-wide analysis of the endangered, endemic lichen Cetradonia linearis reveals isolation by distance and strong population structure. American Journal of Botany 105: 1556-1567.
Alors, D., F. D. Grande, P. Cubas, A. Crespo, I. Schmitt, M. C. Molina, and P. K. Divakar. 2017. Panmixia and dispersal from the Mediterranean Basin to Macaronesian Islands of a macrolichen species. Scientific Reports 7: 1-9.
Anderson, E., and E. D. Rudolph. 1956. An analysis of variation in a variable population of Cladonia. Evolution 10: 147-156.
Andrews, S. 2010. fastqc: a quality control tool for high throughput sequence data (Version 0.11.3). Website: http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
Armaleo, D., O. Muller, F. Lutzoni, O. S. Andresson, G. Blanc, H. B. Bode, F. R. Collart, et al. 2019. The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata. BMC Genomics 20: 605.
Asselin, H., and S. Payette. 2005. Late Holocene opening of the forest tundra landscape in northern Quebec, Canada. Global Ecology and Biogeography 14: 307-313.
Athukorala, S. N. P., J. Doering, and M. D. Piercey-Normore. 2016. Morphological and genetic polymorphism in two North American reindeer lichens: Cladonia arbuscula and C. rangiferina. Ceylon Journal of Science (Biological Sciences) 44: 55-65.
Athukorala, S. N. P., R. Pino-Bodas, S. Stenroos, T. Ahti, and M. D. Piercey-Normore. 2016. Phylogenetic relationships among reindeer lichens of North America. Lichenologist 48: 209-227.
Auclair, A. N. D., and A. N. Rencz. 1982. Concentration, mass, and distribution of nutrients in a subarctic Picea mariana-Cladonia alpestris ecosystem. Canadian Journal of Forest Research 12: 947-968.
Bailey, R., and P. James. 1979. Birds and dispersal of lichen propagules. Lichenologist 11: 105-106.
Bergeron, Y., and M. Dubuc. 1989. Succession in the southern part of the Canadian boreal forest. Vegetation 79: 51-63.
Bergeron, Y., S. Gauthier, V. Kafka, P. Lefort, and D. Lesieur. 2001. Natural fire frequency for the eastern Canadian boreal forest: consequences for sustainable forestry. Canadian Journal of Forest Research 31: 384-391.
Bergerud, A. T. 1971. Abundance of forage on the winter range of newfoundland caribou. The Canadian Field Naturalist 85: 39-52.
Boch, S., D. Prati, S. Werth, J. Rüetschi, and M. Fischer. 2011. Lichen endozoochory by snails. PLoS One 6: 2-6.
Bowler, P. A., and P. W. Rundel. 1975. Reproductive strategies in lichens. Botanical Journal of the Linnean Society 70: 325-340.
Brodo, I. M., S. D. Sharnoff, and S. Sharnoff. 2001. Lichen of North America. New Haven and London: Yale University Press.
Coxson, D. S., and J. Marsh. 2001. Lichen chronosequences (postfire and postharvest) in lodgepole pine (Pinus contorta) forests of northern interior British Columbia. Canadian Journal of Botany 79: 1449-1464.
Degtjarenko, P., T. Tõrra, T. Mandel, L. Marmor, A. Saag, C. Scheidegger, and T. Randlane. 2018. Unconstrained gene flow between populations of a widespread epiphytic lichen Usnea subfloridana (Parmeliaceae, Ascomycota) in Estonia. Fungal Biology 122: 731-737.
DeGrandpré, L., D. Gagnon, and Y. Bergeron. 1993. Changes in the understory of Canadian boreal forest after fire. Journal of Vegetable Science 4: 803-810.
Del-Prado, R., P. K. Divakar, H. T. Lumbsch, and A. Crespo. 2016. Hidden genetic diversity in an asexually reproducing lichen forming fungal group. PLoS One 11: 1-18.
Ene, I., and R. Bennett. 2014. The cryptic sexual strategies of human fungal pathogens. Nature Reviews Microbiology 12: 239-251.
Freeland, J. R., S. D. Petersen, and H. Kirk. 2011. Molecular Ecology (2nd Edition). John Wiley and Sons, West Sussex, United Kingdom.
Gauslaa, Y. 1997. Population structure of the epiphytic lichen Usnea longissima in a boreal Picea abies canopy. Lichenologist 29: 455-469.
Gauthier, L., R. Nault, and M. Crête. 1989. Variations saisonnières du régime alimentaire des caribous du troupeau de la rivière George, Québec nordique. Le Naturaliste canadien 116: 101-112.
Girard, F., S. Payette, and A. Delwaide. 2017. Patterns of early postfire succession of alpine, subalpine and lichen-woodland vegetation: 21 years of monitoring from permanent plots. Forests 8: 1-14.
Gjerde, I., H. H. Blom, L. Lindblom, M. Saetersdal, and F. H. Schei. 2012. Community assembly in epiphytic lichens in early stages of colonization. Ecology 93: 749-759.
Grewe, F., J. P. Huang, S. D. Leavitt, and H. T. Lumbsch. 2017. Reference-based RADseq resolves robust relationships among closely related species of lichen-forming fungi using metagenomic DNA. Scientific Reports 7: 1-11.
Grewe, F., E. Lagostina, H. Wu, C. Printzen, and H. T. Lumbsch. 2018. Population genomic analyses of RAD sequences resolves the phylogenetic relationship of the lichen-forming fungal species Usnea antarctica and Usnea aurantiacoatra. MycoKeys 43: 91-113.
Heinken, T. 1999. Dispersal patterns of terricolous lichens by thallus fragments. Lichenologist 31: 603-612.
Héon, J., D. Arseneault, and M. A. Parisien. 2014. Resistance of the boreal forest to high burn rates. Proceedings of the National Academy of Science of the United States of America 38: 13888-13893.
Högberg, N., S. Kroken, G. Thor, and J. W. Taylor. 2002. Reproductive mode and genetic variation suggest a North American origin of European Letharia vulpina. Molecular Ecology 11: 1191-1196.
Hustich, I. 1957. On the phytogeography of the subarctic Hudson Bay lowland. Acta Geographica 16: 1-48.
Jasinski, J. and S. Payette. 2005. The creation of alternative stable states in the southern boreal forest, Quebec, Canada. Ecological Monographs 75: 561-583.
Johnson, E. A., and K. Miyanishi. 1999. Subarctic lichen woodlands. In R. C. Anderson, J. S. Fralish, and J. M. Baskin [eds.], Savannas, Barrens, and Rock Outcrop Plant Communities of North America, 421-436.Cambridge University Press, New York, USA.
Jombart, T., Z. N. Kamvar, R. Lustrik,C. Collins, M. P. Beugin, B. Knaus, and F. Calboli. 2016. adegenet: Exploratory analysis of genetic and genomic data (version 2.0.1). Computer program and documentation distributed by the author. Website: https://cran.r-project.org/web/packages/adegenet/index.html.
Kenkel, N. C., D. J. Walker, P. R. Watson, R. T. Caners, and R. A. Lastra. 1997. Vegetation dynamics in boreal forest ecosystems. Coenoses 12: 97-108.
Kershaw, K. A. 1978. The role of lichens in boreal tundra transition areas. The Bryologist 81: 294-306.
Kershaw, K. A., and W. R. Rouse. 1976. The impact of fire on forest and tundra ecosystems. Final Report 1975. Arctic Land Use Research. Program Report 75-76-63.
Kück, U., and S. Pöggeler. 2009. Cryptic sex in fungi. Fungal Biology Reviews 23: 86-90.
Lafleur, B., S. Zouaoui, N. J. Fenton, P. Drapeau, and Y. Bergeron. 2016. Short-term response of Cladonia lichen communities to logging and fire in boreal forests. Forest Ecology and Management 372: 44-52.
Langmead, B., and S. L. Salzberg. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9: 357-359.
Li, H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. Computer program and documentation distributed by the author. Website: https://arxiv.org/abs/1303.3997.
Li, H., and R. Durbin. 2009. Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25: 1754-1760.
Maikawa, E., and K. A. Kershaw. 1976. Studies on lichen dominated systems. XIX. The postfire Québec’s closed-crown forest zone. American Journal of Plant Science 4: 749-765.
Malinsky, M., E. Trucchi, D. J. Lawson, and D. Falush. 2018. RADpainter and fineRADstructure: Population inference from RADseq data. Molecular Biology and Evolution 35: 1284-1290.
Mascher, M., S. Wu, P. St. Amand, N. Stein, and J. Poland. 2013. Application of Genotyping-by-Sequencing on Semiconductor Sequencing Platforms: A Comparison of Genetic and Reference-Based Marker Ordering in Barley. PLoS One 8: e76925.
Morneau, C., and S. Payette. 1989. Postfire lichen-spruce woodland recovery at the limit of the boreal forest in northern Quebec. Canadian Journal of Botany 67: 2770-2782.
Pan, J., B. Wang, Z. Y. Pei, and J. Gao. 2015. Optimization of the genotyping-by-sequencing strategy for population genomic analysis in conifers. Molecular Ecology 15: 771-722.
Paris, J. R., J. R. Stevens, and J. M. Catchen. 2017. Lost in parameter space: A road map for stacks. Methods in Ecology and Evolution 8: 1360-1373.
Park, S., S. Jang, S. Oh, J. A. Kim, and J. Hur. 2014. An easy, rapid, and cost-effective method for DNA extraction from various lichen taxa and specimens suitable for analysis of fungal and algal strains. Mycobiology 42: 311-320.
Payette, S. 1992. Fire as a controlling process in the North American boreal forest. In H. H. Shugart, R. Leemans, and G. B. Bonan [eds.], A Systems Analysis of the Global Boreal Forest, 144-165.Cambridge University Press, Cambridge, United Kingdom.
Payette, S., N. Bhiry, A. Delwaide, and M. Simard. 2000. Origin of the lichen woodland at its southern range limit in eastern Canada: the catastrophic impact of insect defoliators and fire on the spruce-moss forest. Canadian Journal of Forest Research 30: 288-305.
Payette, S., and A. Delwaide. 2018. Tamm review: The North-American lichen woodland. Forest Ecology and Management 417: 167-183.
Payette, S., M. Fortin, and I. Gamache. 2001. The subarctic forest-tundra: the structure of a biome in a changing climate. BioScience 51: 709-718.
Payette, S., C. Morneau, L. Sirois, and M. Desponts. 1989. Recent fire history of the northern Quebec biomes. Ecology 70: 656-673.
Piercey-Normore, M. D., T. Ahti, and T. Goward. 2010. Phylogenetic and haplotype analyses of four segregates within Cladonia arbuscula s.l. Botany 88: 397-408.
Richardson, D. H. S., and C. M. Young. 1977. Lichens and Vertebrates. In M. R. D. Seaward [ed.], Lichen Ecology, 121-144.Academic Press, London, United Kingdom.
Rochette, N. C., and J. M. Catchen. 2017. Deriving genotypes from RAD- seq short-read data using Stacks. Nature Protocols 12: 2640-2659.
Rochette, N. C., A. G. Rivera-Colón, and J. M. Catchen. 2019. Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology 28: 4737-4754.
Ronnås, C., S. Werth, O. Ovaskainen, G. Várkonyi, C. Scheidegger, and T. Snäll. 2017. Discovery of long-distance gamete dispersal in a lichen-forming ascomycete. The New phytologist 216: 216-226.
Seymour, F. A., P. D. Crittenden, and P. S. Dyer. 2005. Sex in the extremes: lichen-forming fungi. Mycologist 19: 51-58.
Shaver, G. R., and F. S. Chapin. 1991. Production: biomass relationships and element cycling in contrasting arctic vegetation types. Ecological Monographs 61: 1-31.
Simard, M., and S. Payette. 2001. Black spruce decline triggered by spruce budworm at the southern limit of lichen woodland in eastern Canada. Canadian Journal of Forest Research 31: 2160-2172.
Singh, G., F. Dal Grande, S. Werth, and C. Scheidegger. 2015. Long-term consequences of disturbances on reproductive strategies of the rare epiphytic lichen Lobaria pulmonaria: Clonality a gift and a curse. FEMS Microbiology Ecology 91: 1-11.
Spalink, D., R. MacKay, and K. J. Sytsma. 2019. Phylogeography, population genetics, and distribution modeling reveal vulnerability of Scirpus longii (Cyperaceae) and the Atlantic Coastal Plain flora to climate change. Molecular Ecology 28: 2046-2061.
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylgogenies. Bioinformatics 30: 1312-1313.
Stenroos, S., R. Pino-Bodas, J. Hyvönen, H. T. Lumbsch, and T. Ahti. 2018. Phylogeny of the family Cladoniaceae (Lecanoromycetes, Ascomycota) based on sequences of multiple loci. Cladistics 35: i-ii, 351-460.
Svihus, B., and Ø. Holand. 2000. Lichen polysaccharides and their relation to reindeer/caribou nutrition. Journal of Range Management 53: 642-648.
Vainio, E. A. 1897. Monographia Cladoniarum universalis. 3. Acta Societatis pro Fauna et Flora Fennica 14: 1-268.
Vézeau, C., and S. Payette. 2016. Gap expansion in old-growth subarctic forests: The climate-pathogen connection. New Phytology 212: 1044-1056.
Walser, J. C., R. Holderegger, F. Gugerli, S. E. Hoebee, and C. Scheidegger. 2005. Microsatellites reveal regional population differentiation and isolation in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology 14: 457-467.
Webb, E. T. 1998. Survival, persistence, and regeneration of the reindeer lichens, Cladina stellaris, C. rangiferina, and C. mitis following clear cut logging and forest fire in northwestern Ontario. Rangifer 10: 19-21.
Werth, S. 2010. Population genetics of lichen-forming fungi-A review. Lichenologist 42: 499-519.
Werth, S., F. Gugerli, R. Holderegger, H. H. Wagner, D. Csencsics, and C. Scheidegger. 2007. Landscape-level gene flow in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology 16: 2807-2815.
Werth, S., H. H. Wagner, R. Holderegger, J. M. Kalwij, and C. Scheidegger. 2006. Effect of disturbances on the genetic diversity of an old-forest associated lichen. Molecular Ecology 15: 911-921.
Yarranton, G. A. 1975. Population growth in Cladonia stellaris (Opiz.) Pouz. and Vezda. New Phytologist 75: 99-110.
Zouaoui, S., C. Boudreault, P. Drapeau, and Y. Bergeron. 2014. Influence of time since fire and micro-habitat availability on terricolous lichen communities in Black Spruce (Picea mariana) boreal forests. Forests 5: 2793-2809.