Abstract
The Gyromitra gigas species complex includes six morphologically similar taxa, several of which have a long history of segregation, synonymization, and rearrangement among different genera. These taxa occur throughout Asia, Europe, and North America and include G. gigas, G. khanspurensis, G. korfii, G. montana, G. pseudogigas, and G. ticiniana. ITS and LSU sequences from 66 specimens, including type specimens for all six taxa, were included in phylogenetic analyses to establish species boundaries and resolve species relationships. Sequence similarity comparisons were also conducted between the two molecular markers and between the ITS1 and ITS2 regions. Although ITS exhibited sufficient variability to discriminate among species in the G. gigas species complex, LSU displayed very low variability rendering it completely useless as a molecular marker for separating taxa in this group. The ITS1 region was twice as informative as the ITS2 region and can be used as a barcode marker to identify these species. Gyromitra gigas and G. montana occur as a well-supported clade of sister species and can be distinguished based on ascospore morphology. Gyromitra korfii and G. ticiniana also form a highly supported clade and are considered distinct species based on geography. Gyromitra littiniana is confirmed to be synonymous with G. ticiniana based on molecular data. Gyromitra khanspurensis and G. pseudogigas, which also form a highly supported clade, are considered separate species early in the process of speciation that differ significantly in ascomata and ascospore morphology. A key to species based on morphology and geography is provided.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data and materials have been deposited in publicly accessible holdings.
References
Abarenkov K, Tedersoo L, Nilsson RH, Vellak K, Saar I, Veldre V, Parmasto E, Prous M, Aan A, Ots M, Kurina O, Ostonen I, Jõgeva J, Halapuu S, Põldmaa K, Toots M, Truu J, Larsson KH, Kõljalg U (2010) PlutoF—a web based workbench for ecological and taxonomic research, with an online implementation for fungal ITS sequences. Evol Bioinformatics Online 6:189–196. https://doi.org/10.4137/EBO.S6271
Abbott SP, Currah RS (1997) The Helvellaceae: systematic revision and occurrence in northern and northwestern North America. Mycotaxon 62:1–125
Alfaro ME, Zoller S, Lutzoni F (2003) Bayes or bootstrap. A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20:255–266. https://doi.org/10.1093/molbev/msg028
Carbone M, Van Vooren N, Klener V, Alvarado P (2018) Preliminary phylogenetic and morphological studies in the Gyromitra gigas lineage (Pezizales): Epitypification of Gyromitra gigas and G. ticiniana. Ascomycete.org 10(5):187–199. https://doi.org/10.25664/art-0241
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Donadini J-C (1984) Étude des discomycètes IV. Le genre Discina (1). Mycol Helvet 1(4):251–266
Donadini J-C (1986) Le genre Discina (Gyromitra) (2). Les espèces connues – Variabilité des caractères taxonomiques –Scanning (Ascomycetes, Pezizales). Bull Société linnéenne Prov 38:161–187
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):962–1083. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Ginns JH (1975) Discina korfii. Fungi Candenses 69. Biosystematics Research Institute, Ottawa
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259
Groves JW, Hoare SC (1953) The Helvellaceae of the Ottawa District. Canadian Field-Nat 67(3):95–102
Guindon S, Gascuel O (2003) A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704. https://doi.org/10.1080/10635150390235520
Harmaja H (1969) A wider and more natural concept of the genus Gyromitra. Karstenia 9:9–12
Harmaja H (1973) Amendments of the limits of the genera Gyromitra and Pseudorhizina, with the description of a new species, Gyromitra montana. Karstenia 13:48–58
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192. https://doi.org/10.1093/sysbio/42.2.182
Huelsenbeck JP, Ronquist FR (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Huelsenbeck JP, Ronquist FR (2005) Bayesian analysis of molecular evolution using MrBayes. In: Nielsen R (ed) Statistical methods in molecular ecology. Springer Publishing Co, New York, pp 186–226
Krisai-Greilhuber I, Chen Y, Jabeen S, Madrid H, Marincowitz S, Razaq A, Ševčíková H, Voglmayr H, Yazici K, Aptroot A, Aslan A, Boekhout T, Borovička J, Crous PW, Ilyas S, Jami F, Jiang Y-L, Khalid AN, Kolecka A, Konvalinková T, Norphanphoun C, Shaheen S, Wang Y, Wingfield MJ, Wu S-P, Wu Y-M, Yu J-Y (2017) Fungal systematics and evolution: FUSE 3. Sydowia 69:229–264. https://doi.org/10.12905/0380.sydowia69-2017-0229
Krombholtz JV (v) (1834) Naturgetreue Abbildungen und Beschreibungen der essbaren, schädlichen und verdächtigen Schwämme. Vol 3. Prag, Calve
Kuo M (2005) Morels. Ann Arbor, The University of Michigan Press
Larget B, Simon DL (1999) Markov chain Monte Carlo algorithms for the Bayesian analysis of phylogenetic trees. Mol Biol Evol 16(6):750–759. https://doi.org/10.1093/oxfordjournals.molbev.a026160
Littini G (1988) Gyromitra ticiniana sp. nov. Pagine di Botanica 12:17–20
McKnight KH (1968) Artifacts on spores of Discineae induced by common reagents. Mycologia 60(3):723–727
McKnight KH (1969) A note on Discina. Mycologia 61(3):614–630. https://doi.org/10.1080/00275514.1969.12018775
McKnight KH (1971) On two species of false morels (Gyromitra) in Utah. Great Basin Nat 31(2):35–47
McKnight KH (1973) Two misunderstood species of Gyromitra (false morels) in North America. Michigan Botanist 12:147–162
Methven AS, Zelski SE, Miller AN (2013) A molecular phylogenetic assessment of the genus Gyromitra in North America. Mycologia 105(5):1306–1314. https://doi.org/10.3852/12-397
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov 2010, New Orleans, Louisiana pp 1–8
Miller AN, Matlak A, Raudabaugh D, Pärtel K, Tamm H, Methven AS, Voitk A (2015) The genus Gyromitra in NL. Omphalina 6(3):4–15
MyCoPortal (2020) http://mycoportal.org/portal/index.php. Accessed on July 23
Osmundson TW, Robert VA, Schoch CL, Baker LJ, Smith A, Robich G, Mizzan L, Garbelotto MM (2013) Filling gaps in biodiversity knowledge for macrofungi: contributions and assessment of an herbarium collection DNA barcode sequencing project. PLoS One 8(4):e62419. https://doi.org/10.1371/journal.pone.0062419
Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808. https://doi.org/10.1080/10635150490522304
Raitviir A (1970) Once more on Neogyromitra caroliniana. Botaanika-alased Tõõd 9:364–373
Rehner SA, Samuels GL (1995) Molecular systematics of the Hypocreales: a teleomorph gene phylogeny and the status of their anamorphs. Can J Bot 73(Suppl 1):S816–S823
Riva A (1998) Gyromitra ticiniana Litini. una specie precoce sosia macroscopico della Gyromitra gigas. I Funghi 45:37–44
Riva A (2010) Gyromitra littiniana sp. nov. Descrizione di un ascomycete stipitato a crescita precoce nei boschi di latifoglie eliofile e sosia di Gyromitra gigas. Schweizerische Zeitschrift für Pilzkunde 88(6):230–233
Rodríguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic model of nucleotide substitutions. J Theor Biol 142:485–501. https://doi.org/10.1016/s0022-5193(05)80104-3
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109(16):6241–6246. https://doi.org/10.1073/pnas.1117018109
Smith AH (1949) Mushrooms in their natural habitats. Sawyer Inc, Portland
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stamatakis A, Hoover P, Rougemont J (2008) A fast bootstrapping algorithm for the RAxML web-servers. Syst Biol 57:758–771. https://doi.org/10.1080/10635150802429642
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164
Thiers B (2013) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden Virtual Herbarium. http://sweetgum.nybg.org/ih. Accessed 1 July 2020
Van Vooren N, Moreau P-A (2009a) Essai taxinomique sur le genre Gyromitra Fr. sensu lato (Pezizales). 1. Introduction et systématique. Ascomycete.org 1(1):3–6. https://doi.org/10.25664/art-0001
Van Vooren N, Moreau P-A (2009b) Essai taxinomique sur le genre Gyromitra Fr. sensu lato (Pezizales). 2. Le genre Gyromitra Fr., sous-genre Gyromitra. Ascomycete.org 1(1):7–14. https://doi.org/10.25664/art-0002
Van Vooren N, Moreau P-A (2009c) Essai taxinomique sur le genre Gyromitra Fr. sensu lato (Pezizales). 3. Le genre Gyromitra Fr., sous-genre Discina. Ascomycete.org 1(2):3–13. https://doi.org/10.25664/art-0003
Vilgalys R, Hester M (1990) Rapid identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
Wang X-C, Zhuang W-Y (2019) A three-locus phylogeny of Gyromitra (Discinaceae, Pezizales) and discovery of two cryptic species. Mycologia 111(1):69–77. https://doi.org/10.1080/00275514.2018.1515456
Weber NS (1988) A morel hunter’s companion: a guide to the true and false morels of Michigan. Two Peninsula Press, Lansing
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA (ed) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322
Acknowledgements
The authors wish to thank the curators and collections managers for the loan of specimens at the following fungaria: BPI, CUP, ILLS, LUG, O, OSC, OULU, NY, TAAM, WTU, and YSU. We also thank Andrus Voitk, Michael Kuo, and Nina Filippova for the loan of specimens.
Author information
Authors and Affiliations
Contributions
Andrew N. Miller was responsible for the study conception and design. Andrew N. Miller, Angela Yoon, and Øyvind Stensholt generated molecular sequence data. Gro Gulden, Nicolas Van Vooren, Esteri Ohenoja, and Andrew S. Methven provided voucher specimens. Molecular analyses were performed by Andrew N. Miller. Morphological analyses were performed by Andrew S. Methven. The first draft of the manuscript was written by Andrew N. Miller. Andrew S. Methven edited the manuscript and all authors commented on subsequent versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Not applicable
Consent to participate
Not applicable
Consent for publication
Not applicable
Additional information
Section Editor: Roland Kirschner
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Miller, A.N., Yoon, A., Gulden, G. et al. Studies in Gyromitra I: the Gyromitra gigas species complex. Mycol Progress 19, 1459–1473 (2020). https://doi.org/10.1007/s11557-020-01639-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-020-01639-8