Mycological Progress

, 15:26 | Cite as

Clitopilus reticulosporus, a new species with unique spore ornamentation, its phylogenetic affinities and implications on the spore evolution theory

  • Luis N. MorgadoEmail author
  • Machiel E. Noordeloos
  • Anton Hausknecht
Original Article


Clitopilus reticulosporus (Entolomataceae, Agaricales) growing on rotting wood is described as a new species based on collections from Austria and Hungary. Multi-gene phylogenetic analysis of ITS, rpb2, LSU and mtSSU confirms the placement of C. reticulosporus in the Clitopilus-Rhodocybe clade in the Entolomataceae. It is nested within the subclade containing the species with clitopiloid spores (Clitopilus s. str.). Scanning electron microscopy studies demonstrate that the spores of this species have a peculiar reticulate ornamentation resembling an intermediate form between the clitopiloid type with longitudinal ribs, and the rhodocyboid type with irregular bumps and ridges. However, our ancestral character reconstruction suggests that (1) this character state is not an intermediate form and (2) the discovery of this new character state does not have a direct implication on the Entolomataceae spore evolution theory. Our phylogenetic reconstruction uncovered, at least, three distinct lineages in the Clitopilus s. str. clade, and suggest that sect. Clitopilus is monophyletic, while sect. Schyphoides and sect. Pleurotelloides are not.


Entolomataceae Rhodocybe Phylogeny Pleurotoid Ancestral character reconstruction Spore evolution 



The authors wish to thank Hermann Voglmayr for providing the SEM pictures of the spores, and Irmgard Krisai-Greilhuber for providing the Latin diagnosis. Thom Kuyper critically read an earlier draft of this paper, for which we are very grateful. The authors are thankful to Jesus Aguirre-Gutiérrez for the help in R.

Supplementary material

11557_2016_1165_MOESM1_ESM.pdf (1.6 mb)
Figure S1 Graphic display of the raw probabilities and the trend line of each spore state per node (relative to the Fig. 3) without (left) and with (right) information about the reticulate spore type in the Rhodocybe-Clitopilus clade. Based on the 4 runs of BI and ACS reconstruction with RJMCMC model, both with 25 % burn in. Legend: red: bumpy spores; green: longitudinally ridged; blue: smooth spores; purple: reticulate spores. Node 1: a, f; Node 2: b, g; Node 3: c, h; Node 4: d, i; Node 5: e, j. (PDF 1.59 MB)
11557_2016_1165_MOESM2_ESM.pdf (10 kb)
Table S2 ACS probability using MLML method per node (specified in Fig. 1), with and without knowledge of the new spore character state – reticulated spore, with probability changes highlighted in bold. (PDF 10.4 kb)


  1. Baroni TJ (1981) A revision of the genus Rhodocybe Maire (Agaricales). Beihefte zur Nova Hedwigia 67. J. Cramer, GermanyGoogle Scholar
  2. Co-David D, Langeveld D, Noordeloos ME (2009) Molecular phylogeny and spore evolution of Entolomataceae. Persoonia 23:147–176CrossRefPubMedPubMedCentralGoogle Scholar
  3. Hartley AJ, Mattos-Shipley K, Collins CM, Kilaru S, Forster GD, Bailey AM (2009) Investigating pleuromutilin-producing Clitopilus species and related basidiomycetes. FEMS Microbiol Lett 297:24–30CrossRefPubMedGoogle Scholar
  4. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647--1649Google Scholar
  5. Kluting KL, Baroni TJ, Bergemann SE (2014) Toward a stable classification of genera within the Entolomataceae: a phylogenetic re-evaluation of the Rhodocybe-Clitopilus clade. Mycologia 106:1127–1142. doi: 10.3852/13-270 CrossRefPubMedGoogle Scholar
  6. Moncalvo J-M, Vilgalys R, Redhead SA et al (2002) One hundred and seventeen clades of euagarics. Mol Phylogenet Evol 23:357–400CrossRefPubMedGoogle Scholar
  7. Moncalvo J-M, Baroni TJ, Bhatt RP, Stephenson SL (2004) Rhodocybe paurii, a new species from the Indian Himalaya. Mycologia 96:859–865CrossRefPubMedGoogle Scholar
  8. Moreno G, Contu M, Ortega A, Platas G, Peláez F (2007) Molecular phylogenetic studies show Omphalina giovanellae represents a new section of Clitopilus (Agaricomycetes). Mycol Res 111:1399–1405CrossRefPubMedGoogle Scholar
  9. Morgado LN, Noordeloos ME, Lamoureux Y, Geml J (2013) Multi-gene phylogenetic analyses reveal species limits, phylogeographic patterns, and evolutionary histories of key morphological traits in Entoloma (Agaricales, Basidiomycota). 159–178Google Scholar
  10. Pagel M (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst Biol 48:612–622CrossRefGoogle Scholar
  11. Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53:673–684CrossRefPubMedGoogle Scholar
  12. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL
  13. Ronquist F, Teslenko M, Mark P, Ayres D, Darling A et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedPubMedCentralGoogle Scholar
  14. Singer R (1986) The Agaricales in modern taxonomy, 4th edn. Koeltz Scientific Books, Germany, pp 669–705Google Scholar
  15. Wickham H (2009) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New YorkGoogle Scholar
  16. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at AustinGoogle Scholar

Copyright information

© German Mycological Society and Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Luis N. Morgado
    • 1
    • 2
    Email author
  • Machiel E. Noordeloos
    • 1
  • Anton Hausknecht
    • 3
  1. 1.Botany DepartmentNaturalis Biodiversity CenterLeidenThe Netherlands
  2. 2.Section for Genetics and Evolutionary Biology (Evogene), Department of BiosciencesUniversity of OsloOsloNorway
  3. 3.Faculty Centre of BiodiversityUniversity of ViennaWienAustria

Personalised recommendations