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Decrypting the Hebeloma Crustuliniforme Complex: European Species of Hebeloma Section Denudata Subsection Denudata (Agaricales)

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Decrypting the Hebeloma Crustuliniforme Complex: European Species of Hebeloma Section Denudata Subsection Denudata (Agaricales) Persoonia 35, 2015: 101–147 www.ingentaconnect.com/content/nhn/pimj RESEARCH ARTICLE http://dx.doi.org/10.3767/003158515X687704 Decrypting the Hebeloma crustuliniforme complex: European species of Hebeloma section Denudata subsection Denudata (Agaricales) U. Eberhardt 1,2, H.J. Beker 3, J. Vesterholt 4 Key words Abstract Hebeloma subsection Denudata includes the type of H. section Denudata, Hebeloma crustuliniforme, as well as the majority of the taxa commonly included in the Hebeloma crustuliniforme complex. Complementing Hebeloma eburneum the work of D.K. Aanen and co­workers, and using refined morphological and molecular methods we were able to Hebeloma helodes recognize further individual taxa within the section. Fifteen species occurring in Europe are assigned to H. subsect. Hebeloma lutense Denudata. Of these, we describe eight species as new, namely H. aanenii, H. aurantioumbrinum, H. geminatum, Hebeloma minus H. louiseae, H. luteicystidiatum, H. pallidolabiatum, H. perexiguum and H. salicicola. Naucoria bellotiana, a species Hebeloma pusillum very similar to H. alpinum is recombined into Hebeloma. A key to Hebeloma subsect. Denudata is provided. We MCM7 demonstrate that within this subsection there is good overall consistency between morphological, phylogenetic and mitochondrial SSU biological species concepts. In contrast to current opinion, in this group there is little species overlap, particularly Salix when also considering species frequencies, between arctic and alpine floras on one hand and temperate on the other. Article info Received: 16 May 2014; Accepted: 20 October 2014; Published: 27 February 2015. INTRODUCTION It is tempting to consider ICGs as biological species and they may well represent biological species, but as Aanen & Kuyper Hebeloma is a genus of ectomycorrhizal fungi occurring in many (1999) point out, the production of basidiospores in the dikary- different habitats in the northern hemisphere (Marmeisse et al. otic mycelia generated in the intercompatibility tests could not 1999) and indeed worldwide, with the possible exception of be tested, therefore we do not know what the implications of regions, where Fagales are not endogenous, such as Northern the observed intercompatibility in nature are. In general, on the South America (Tedersoo et al. 2010) or Africa. However, as population level, partial intercompatibility may correspond to typical nursery fungi, Hebeloma spp. are likely to have been incomplete speciation (Aanen & Kuyper 1999). Almost all of a introduced through human activity (see Sulzbacher et al. 2013). quite high number of strains stemming from 110 collections Hebeloma crustuliniforme is one of the most often recorded could be unambiguously assigned to a single ICG, thus support- (Vesterholt et al. 2014) species of the genus Hebeloma, but it ing the notion that distinct biological taxa have already formed is widely recognised that what has in the past been referred in this species aggregate. to as H. crustuliniforme is among the most notorious species Aanen & Kuyper (1999) linked this finding of partial compatibi­ complexes that have long defied recognition of individual taxa. lity between some ICGs with the difficulty of morphologically In Vesterholt et al. (2014) we proposed an epitype for H. crus- separating ICGs into morpho-species, suggesting that partial tuliniforme so as to tie this name to a particular taxon within intercompatibility might contribute to the failure to form distinct this complex, which we then suggested should be referred to morphological and ecological syndromes. Accordingly, Aanen as H. crustuliniforme (Bull.) Quél. emend. Vesterh., U. Eberh. and co-workers (Aanen 1999, Aanen et al. 2000, Aanen & & Beker to avoid confusion with earlier applied concepts of the Kuyper 2004) adopted wide species concepts, i.e. H. crustu- taxon. As we stated at the time, this was the first step towards linifome including H. alpinum with six ICGs and H. pusillum unravelling this complex of species within sect. Denudata. (four ICGs), partially overlapping with H. helodes (at least six More than 10 years ago, D.K. Aanen and others (Aanen & ICGs). In the later work (Aanen & Kuyper 2004) H. helodes and Kuyper 1999, 2004, Aanen et al. 2000) carried out a profound H. pusillum were merged. study of the H. crustuliniforme complex, using three different Molecular studies showed that three of the ICGs of the H. crus- approaches, sporocarp morphology, molecular studies and tuliniforme complex were molecularly quite distinct from the intercompatibility tests, testing for dikaryotization between other 17 ICGs. This supported a view published initially by Boek- pairs of monokaryotic strains. They found 20 intercompatibility hout (1982), then molecularly supported (Aanen et al. 2000, groups (ICGs) within the complex. A small number of strains Boyle et al. 2006), suggesting that there are indeed two dis- were intercompatible with some strains of other ICGs or could tinct groups within this complex, one species complex around not be unambiguously assigned to a unique ICG. H. velutipes (syn. H. leucosarx acc. Grilli 2007) and another 1 Staatliches Museum für Naturkunde Stuttgart, Rosenstein 1, D-70191 Stutt- in sect. Denudata, around H. crustuliniforme. It has found its gart, Germany; corresponding author e-mail: [email protected]. way into the classification system by Vesterholt (2005), which 2 Ghent University, Dpt. Biology, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium. recognized two distinct sections Velutipes and Denudata, each 3 Rue Père de Deken 19, B-1040 Bruxelles, Belgium. including taxa that were formerly considered representatives 4 Natural History Museum of Denmark, Gothersgade 130, DK-1123 Copen- of the H. crustuliniforme complex. hagen K., Denmark. Deceased. © 2015 Naturalis Biodiversity Center & Centraalbureau voor Schimmelcultures You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. 102 Persoonia – Volume 35, 2015 The focus of the present study is on H. sect. Denudata and two species, rare mismatches between morphological and mo- particularly on members of the H. crustuliniforme complex lecular evidence and gaps in the molecular data matrix when and related taxa assigned to subsect. Denudata (described older specimen could not be sequenced for certain loci – that more fully below) of which H. crustuliniforme is the type. The there is good overall consistency between morphological, mo- delimitation of H. subsect. Denudata adopted in this paper is lecular and seemingly also biological species circumscriptions. based on morphological characters. Within the scope of this Implications of earlier taxonomic decisions (Aanen 1999, Aanen paper we do not demonstrate the molecular delimitation of & Kuyper 2004) with regard to the H. crustuliniforme complex H. subsect. Denudata. A separate publication (Eberhardt et al. and results based on environmental sequencing studies in prep.) will be concerned with the classification of subsections (reviewed by Timling & Taylor 2012) supported the view that of H. sect. Denudata and species from these other subsections. agarics, including Hebeloma spp., of the arctic or alpine regions With regard to species delimitation, we follow de Queiroz are essentially the same as temperate taxa at the species level. (2007) unified species concept that treats different criteria According to the results presented here for the H. crustulini- such as morphological distinctness, monophyly, evolutionary forme complex and H. subsect. Denudata, this assumption is distance or intercompatibility as independent lines of evidence debatable. Though taxa of both biomes are doubtlessly closely for recognizing separately evolving lineages, i.e. species. This related, qualitative and quantitative differences can be observed implies that not all lines of evidence necessarily support a spe- between the arctic/alpine flora as opposed to floras of lower cies or the assignment of a particular specimen to a species, latitudes and altitudes. particularly in young species or species with a recent history of range changes. Hybridization and deep coalescence are Materials AND METHODS additional processes, which may prevent representatives from the same biological species from forming monophyletic clades The majority of collections cited in species descriptions and in phylogenetic analyses. In practice, we recognize species that used for molecular studies are included in the private herbarium are morphologically distinct and/or which form a monophyletic of H.J. Beker. Some collections were obtained from other collec- group in phylogenetic analysis of one or several loci, which tors and their private collections. Additional collections were is not contradicted by supported monophyletic groupings in obtained from public herbaria. The latter are referred to by phylogenetic results of any other
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