Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: A case study using the lichen-forming genus Peltigera section Polydactylon
[en] Synteny can be maintained for certain genomic regions across broad phylogenetic groups. In these homologous genomic regions, sites that are under relaxed purifying selection, such as intergenic regions, could be used broadly as markers for population genetic and phylogenetic studies on species complexes. To explore the potential of this approach, we found 125 Collinear Orthologous Regions (COR) ranging from 1 to >10 kb across nine genomes representing the Lecanoromycetes and Eurotiomycetes (Pezizomycotina, Ascomycota). Twenty-six of these COR were found in all 24 eurotiomycete genomes surveyed for this study. Given the high abundance and availability of fungal genomes we believe this approach could be adopted for other large groups of fungi outside the Pezizomycotina. As a proof of concept, we selected three Collinear Orthologous Regions (COR1b, COR3, and COR16), based on synteny analyses of several genomes representing three classes of Ascomycota: Eurotiomycetes, Lecanoromycetes, and Lichinomycetes. COR16, for example, was found across these three classes of fungi. Here we compare the resolving power of these three new markers with five loci commonly used in phylogenetic studies of fungi, using section Polydactylon of the cyanolichen-forming genus Peltigera (Lecanoromycetes) – a clade with several challenging species complexes. Sequence data were subjected to three species discovery and two validating methods. COR markers substantially increased phylogenetic resolution and confidence, and highly contributed to species delimitation. The level of phylogenetic signal provided by each of the COR markers was higher than the commonly used fungal barcode ITS. High cryptic diversity was revealed by all methods. As redefined here, most species represent lineages that have relatively narrower, and more homogeneous biogeographical ranges than previously understood. The scabrosoid clade consists of ten species, seven of which are new. For the dolichorhizoid clade, twenty-two new species were discovered for a total of twenty-nine species in this clade.
Magain, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Miadlikowska, Jolanta
Mueller, Olaf
Gajdeczka, Michael
Truong, Camille
Salamov, Asaf A.
Dubchak, Inna
Grigoriev, Igor V.
Goffinet, Bernard
Sérusiaux, Emmanuël ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et de la conservation - aCREA-Ulg
Lutzoni, François
Language :
English
Title :
Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: A case study using the lichen-forming genus Peltigera section Polydactylon
Publication date :
December 2017
Journal title :
Molecular Phylogenetics and Evolution
ISSN :
1055-7903
eISSN :
1095-9513
Publisher :
Academic Press, San Diego, United States - California
Special issue title :
25th Anniversary Issue of Molecular Phylogenetics and Evolution
Altermann, S., Leavitt, S.D., Goward, T., Nelsen, M.P., Lumbsch, H.T., How do you solve a problem like Letharia? A new look at cryptic species in lichen-forming fungi using Bayesian clustering and SNPs from multilocus sequence data. PLoS One, 9(5), 2014, e97556.
Blackwell, M., The Fungi: 1, 2, 3, …, 5.1 million species?. Am. J. Bot. 98 (2011), 426–438.
Carstens, B.C., Pelletier, T.A., Reid, N.M., Satler, J.D., How to fail at species delimitation. Mol. Ecol. 22 (2013), 4369–4383.
Crespo, A., Kauff, F., Divakar, P.K., del Prado, R., Pérez-Ortega, S., de Paz, G.A., Ferencova, Z., Blanco, O., Roca-Valiente, B., Núñez-Zapata, J., Cubas, P., Argüello, A., Elix, J.A., Esslinger, T.L., Hawksworth, D.L., Millanes, A.M., Molina, M.C., Wedin, M., Ahti, T., Aptroot, A., Barreno, E., Bungartz, F., Calvelo, S., Candan, M., Cole, M.J., Ertz, D., Goffinet, B., Lindblom, L., Lücking, R., Lutzoni, F., Mattsson, J.E., Messuti, M.I., Miadlikowska, J., Piercey-Normore, M.D., Rico, V.J., Sipman, H., Schmitt, I., Spribille, T., Thell, A., Thor, G., Upreti, D.K., Lumbsch, H.T., Phylogenetic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence. Taxon 59 (2010), 1735–1753.
Crespo, A., Lumbsch, H.T., Mattsson, J.E., Blanco, O., Divakar, P.K., Articus, K., Wiklund, E., Bawingan, P.A., Wedin, M., Testing morphology-based hypotheses of phylogenetic relationships in Parmeliaceae (Ascomycota) using three ribosomal markers and the nuclear RPB1 gene. Mol. Phylogenet. Evol. 44 (2007), 812–824.
De Queiroz, K., Species concepts and species delimitation. Syst. Biol. 56 (2007), 879–886.
De Queiroz, K., The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. Howard, Daniel J., Berlocher, Stewart H., (eds.) Endless Forms: Species and Speciation, 1998, Oxford University Press, 57–75.
Deng, W., Nickle, D.C., Learn, G.H., Maust, B., Mullins, J.I., ViroBLAST: a stand-alone BLAST web server for flexible queries of multiple databases and user's datasets. Bioinformatics 23 (2007), 2334–2336.
Drummond, A.J., Rambaut, A., BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol., 7, 2007, 214.
Ebersberger, I., de Matos Simoes, R., Kupczok, A., Gube, M., Kothe, E., Voigt, K., Haeseler, von A., A consistent phylogenetic backbone for the fungi. Mol. Biol. Evol. 29 (2012), 1319–1334.
Ence, D.D., Carstens, B.C., SpedeSTEM: a rapid and accurate method for species delimitation. Mol. Ecol. Resour. 11 (2011), 473–480.
Fitzpatrick, D.A., Logue, M.E., Stajich, J.E., Butler, G., A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol., 6, 2006, 99.
Frazer, K.A., Pachter, L., Poliakov, A., Rubin, E.M., Dubchak, I., Vista: computational tools for comparative genomics. Nucleic Acids Res. 32 (2004), W273–W279.
Grigoriev, I.V., Nordberg, H., Shabalov, I., Aerts, A., Cantor, M., Goodstein, D., Kuo, A., Minovitsky, S., Nikitin, R., Ohm, R.A., Otillar, R., Poliakov, A., Ratnere, I., Riley, R., Smirnova, T., Rokhsar, D., Dubchak, I., The genome portal of the department of energy joint genome institute. Nucleic Acids Res., 2011, gkr947.
Hane, J.K., Rouxel, T., Howlett, B.J., Kema, G.H.J., Goodwin, S.B., Oliver, R.P., A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol., 12, 2011, R45.
Harris, R.S., Improved pairwise alignment of genomic DNA. Ph.D. Thesis, 2007, The Pennsylvania State University.
Hawksworth, D.L., The fungal dimension of biodiversity: Magnitude, significance, and conservation. Mycol. Res. 95 (1991), 641–655.
Hawksworth, D.L., The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycol. Res. 105 (2001), 1422–1432.
Hodkinson, B.P., Allen, J.L., Forrest, L.L., Goffinet, B., Sérusiaux, E., Andresson, O.S., Miao, V., Bellenger, J.-P., Lutzoni, F., Lichen-symbiotic cyanobacteria associated with Peltigera have an alternative vanadium-dependent nitrogen fixation system. Eur. J. Phycol. 49 (2014), 11–19.
Hofstetter, V., Miadlikowska, J., Kauff, F., Lutzoni, F., Phylogenetic comparison of protein-coding versus ribosomal RNA-coding sequence data: a case study of the Lecanoromycetes (Ascomycota). Mol. Phylogenet. Evol. 44:1 (2007), 412–426.
Holtan-Hartwig, J., 1993. The Lichen Genus Peltigera, Exclusive of the P. canina Group, in Norway. Botanical Garden and Museum-University of Oslo.
Huelsenbeck, J.P., Andolfatto, P., Huelsenbeck, E.T., Structurama: Bayesian inference of population structure. Evolut. Bioinf. Online, 7, 2011, 55.
Jeffroy, O., Brinkmann, H., Delsuc, F., Philippe, H., Phylogenomics: the beginning of incongruence?. Trends Genet. 22 (2006), 225–231.
Kirk, P.M., Cannon, P.F., Minter, D.W., Stalpers, J.A., Dictionary of the Fungi. 2008, CABI, Wallingford, U.K.
Kubatko, L.S., Carstens, B.C., Knowles, L.L., STEM: species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics 25 (2009), 971–973.
Kuramae, E.E., Robert, V., Snel, B., Weiß, M., Boekhout, T., Phylogenomics reveal a robust fungal tree of life. FEMS Yeast Res. 6 (2006), 1213–1220.
Lanfear, R., Calcott, B., Ho, S.Y., Guindon, S., PartitionFinder, S., Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29 (2012), 1695–1701.
Leavitt, S.D., Fankhauser, J.D., Leavitt, D.H., Porter, L.D., Johnson, L.A., Clair, L.L.St., Complex patterns of speciation in cosmopolitan “rock posy” lichens–discovering and delimiting cryptic fungal species in the lichen-forming Rhizoplaca melanophthalma species-complex (Lecanoraceae, Ascomycota). Mol. Phylogenet. Evol. 59 (2011), 587–602.
Leavitt, S.D., Johnson, L.A., Goward, T., Clair, L.L.St., Species delimitation in taxonomically difficult lichen-forming fungi: An example from morphologically and chemically diverse Xanthoparmelia (Parmeliaceae) in North America. Mol. Phylogenet. Evol. 60 (2011), 317–332.
Leavitt, S.D., Grewe, F., Widhelm, T., Muggia, L., Wray, B., Lumbsch, H.T., Resolving evolutionary relationships in lichen-forming fungi using diverse phylogenomic datasets and analytical approaches. Sci. Rep., 6, 2016.
Liu, Y., Steenkamp, E.T., Brinkmann, H., Forget, L., Philippe, H., Lang, B.F., Phylogenomic analyses predict sistergroup relationship of nucleariids and fungi and paraphyly of zygomycetes with significant support. BMC Evol. Biol., 9, 2009, 1.
Lücking, R., Dal-Forno, M., Sikaroodi, M., Gillevet, P.M., Bungartz, F., Moncada, B., Yánez-Ayabaca, A., Chaves, J.L., Coca, L.F., Lawrey, J.D., A single macrolichen constitutes hundreds of unrecognized species. Proc. Natl. Acad. Sci. 111 (2014), 11091–11096.
Lumbsch, H.T., Leavitt, S.D., Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity 50 (2011), 59–72.
Maddison, D., Maddison, W., 2005. MacClade v. 4.08.
Magain, N., Forrest, L.L., Sérusiaux, E., Goffinet, B., Microsatellite primers in the Peltigera dolichorhiza complex (lichenized ascomycete, Peltigerales). Am. J. Bot. 97 (2010), e102–e104.
Magain, N., Sérusiaux, E., Zhurbenko, M.P., Lutzoni, F., Miadlikowska, J., Disentangling the Peltigera polydactylon species complex by recognizing two new taxa, P. polydactylon subsp. udeghe and P. seneca. Herzogia 29 (2016), 514–528.
Magain, N., Miadlikowska, J., Goffinet, B., Sérusiaux, E., Lutzoni, F., Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Syst. Biol. 66 (2017), 74–99.
Martínez, I., Burgaz, A.R., Vitikainen, O., Escudero, A., Distribution patterns in the genus Peltigera Willd. Lichenologist 35 (2003), 301–323.
Mason-Gamer, R.J., Kellogg, E.A., Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst. Biol. 45:4 (1996), 524–545.
Mayr, E., Speciation phenomena in birds. Am. Nat. 1940 (1940), 249–278.
McDonald, T.R., Mueller, O., Dietrich, F.S., Lutzoni, F., High-throughput genome sequencing of lichenizing fungi to assess gene loss in the ammonium transporter/ammonia permease gene family. BMC Genomics, 14, 2013, 1.
Miadlikowska, J., Lutzoni, F., Phylogenetic revision of the genus Peltigera (lichen-forming ascomycota) based on morphological, chemical, and large subunit nuclear ribosomal DNA data. Int. J. Plant Sci. 161 (2000), 925–958.
Miadlikowska, J., Richardson, D., Magain, N., Ball, B., Anderson, F., Cameron, R., Lendemer, J., Truong, C., Lutzoni, F., Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes). Am. J. Bot. 101 (2014), 1141–1156.
Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE). IEEE, pp. 1–8.
Nylander, J., MrModeltest v2. Program Distributed by the Author, vol. 2, 2004, Evolutionary Biology Centre, Uppsala University.
Nylander, J.A., Wilgenbusch, J.C., Warren, D.L., Swofford, D.L., AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in bayesian phylogenetics. Bioinformatics 24 (2008), 581–583.
O'Brien, B.L., Parrent, J.L., Jackson, J.A., Moncalvo, J.M., Vilgalys, R., Fungal community analysis by large-scale sequencing of enviromental samples. Appl. Environ. Microbiol. 71 (2005), 5544–5550.
Oliver, J.C., Miadlikowska, J., Arnold, A.E., Maddison, D.R., Lutzoni, F., 2013. Hypha: A Mesquite Package for Support Value Integration. Version 1.0.
Paradis, E., Claude, J., Strimmer, K., APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20 (2004), 289–290.
Parnmen, S., Rangsiruji, A., Mongkolsuk, P., Boonpragob, K., Nutakki, A., Lumbsch, H.T., Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PLoS One, 7(12), 2012, e52245.
Peterson, B.K., Weber, J.N., Kay, E.H., Fisher, H.S., Hoekstra, H.E., Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE, 7, 2012, e37135.
Pritchard, J.K., Stephens, M., Donnelly, P., Inference of population structure using multi-locus genotype data. Genetics 155 (2000), 945–959.
Purvis, O.W., James, P.W., Studies on the lichens of the Azores. Part 1-Caldeira do Faial. ARQUIPÉLAGO. Ciências Biol. Mar.= Life Mar. Sci. 11 (1993), 1–15.
R Development Core Team, 2002. R: A Language and Environment for Statistical Computing.
Rambaut, A., Charleston, M., 2008. Treeedit: phylogenetic tree editor v. 1.0 alpha 10. See < http://evolve.zoo.ox.ac.uk/software/TreeEdit/main.html>.
Rambaut, A., Drummond, A., 2007. Tracer v1. 5.
Reeb, V., Lutzoni, F., Roux, C., Contribution of RPB2 to multilocus phylogenetic studies of the euascomycetes (Pezizomycotina, Fungi) with special emphasis on the lichen-forming Acarosporaceae and evolution of polyspory. Mol. Phylogenet. Evol. 32:3 (2004), 1036–1060.
Reid, N.M., Carstens, B.C., Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed yule-coalescent model. BMC Evol. Biol., 12, 2012, 196.
Robbertse, B., Reeves, J.B., Schoch, C.L., Spatafora, J.W., A phylogenomic analysis of the Ascomycota. Fungal Genet. Biol. 43 (2006), 715–725.
Rodriguez, F., Oliver, J., Marin, A., Medina, J.R., The general stochastic model of nucleotide substitution. J. Theor. Biol. 142 (1990), 485–501.
Rokas, A., Williams, B.L., King, N., Carroll, S.B., Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425 (2003), 798–804.
Scherrer, S., Zippler, U., Honegger, R., Characterisation of the mating-type locus in the genus Xanthoria (lichen-forming ascomycetes, Lecanoromycetes). Fungal Genet. Biol. 42 (2005), 976–988.
Schmull, M., Miadlikowska, J., Pelzer, M., Stocker-Wörgötter, E., Hofstetter, V., Fraker, E., Hodkinson, B.P., Reeb, V., Kuwka, M., Lumbsch, H.T., Kauff, F., Lutzoni, F., Phylogenetic affiliations of members of the heterogeneous lichen-forming fungi of the genus Lecidea sensu Zahlbruckner (Lecanoromycetes, Ascomycota). Mycologia 103 (2011), 983–1003.
Schneider, K., Resl, P., Spribille, T., Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event. Mol. Ecol., 2016, 10.1111/mec.13636.
Schoch, C.L., Crous, P.W., Groenewald, J.Z., Boehm, E.W.A., Burgess, T.I., De Gruyter, J., De Hoog, G.S., Dixon, L.J., Grube, M., Gueidan, C., Harada, Y., A class-wide phylogenetic assessment of Dothideomycetes. Stud. Mycol. 64 (2009), 1–15.
Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W., Griffith, G.W., Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc. Natl. Acad. Sci. 109 (2012), 6241–6246.
Sérusiaux, E., Goffinet, B., Miadlikowska, J., Vitikainen, O., Taxonomy, phylogeny and biogeography of the lichen genus Peltigera in Papua New Guinea. Fungal Diversity, 38, 2009, 185.
Stamatakis, A., RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 (2006), 2688–2690.
Stamatakis, A., Hoover, P., Rougemont, J., A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57 (2008), 758–771.
Steyskal, G.C., The meaning of the term 'sibling species’. Syst. Biol., 21, 1972, 446.
Sukumaran, J., Knowles, L.L., Multispecies coalescent delimits structure, not species. Proc. Natl. Acad. Sci. 114 (2017), 1607–1612.
Swofford, D.L., 2003. PAUP∗. Phylogenetic analysis using parsimony (∗ and other methods). Version 4.
Taylor, J.W., Jacobson, D.J., Kroken, S., Kasuga, T., Geiser, D.M., Hibbett, D.S., Fisher, M.C., Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 31 (2000), 21–32.
Vitikainen, O., Taxonomic revision of Peltigera (lichenized Ascomycotina) in Europe. Acta Bot. Fennica 152 (1994), 1–96.
Wedin, M., Wiklund, E., Jørgensen, P.M., Ekman, S., Slippery when wet: phylogeny and character evolution in the gelatinous cyanobacterial lichens (Peltigerales, Ascomycetes). Mol. Phylogenet. Evol. 53 (2009), 862–871.
Wickham, H., Ggplot2: Elegant Graphics for Data Analysis. 2009, Springer.
Wiemers, M., Fiedler, K., Does the DNA barcoding gap exist? – a case study in blue butterflies (Lepidoptera: Lycaenidae). Front. Zool., 4, 2007, 8.
Xavier, B.B., Miao, V.P., Jonsson, Z.O., Andresson, O.S., Mitochondrial genomes from the lichenized fungi Peltigera membranacea and Peltigera malacea: Features and phylogeny. Fungal Biol. 116 (2012), 802–814.
Yang, Z., PAML: a program package for phylogenetic analysis by maximum likelihood. Bioinformatics 13 (1997), 555–556.
Yang, Z., Rannala, B., Bayesian species delimitation using multilocus sequence data. Proc. Natl. Acad. Sci. 107 (2010), 9264–9269.
Zhang, J., Kapli, P., Pavlidis, P., Stamatakis, A., A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 (2013), 2869–2876.
Zoller, S., Lutzoni, F., Scheidegger, C., Genetic variation within and among populations of the threatened lichen Lobaria pulmonaria in Switzerland and implications for its conservation. Mol. Ecol. 8 (1999), 2049–2059.
