Fernández-López et al. IMA Fungus (2019) 10:2 https://doi.org/10.1186/s43008-019-0010-x IMA Fungus RESEARCH Open Access Addressing the diversity of Xylodon raduloides complex through integrative taxonomy Javier Fernández-López1, M. Teresa Telleria1, Margarita Dueñas1, Andrew W. Wilson2, Mahajabeen Padamsee3, Peter K. Buchanan3, Gregory M. Mueller4 and María P. Martín1* Abstract In this study, the taxonomic diversity of the Xylodon raduloides species complex (Hymenochaetales, Basidiomycota)is examined. Specimens were studied using an integrative taxonomic approach that includes molecular phylogenetic and morphological analyses, and environmental niche comparisons. Four different species were found inside the Xylodon raduloides complex, with a biogeographic distribution pattern bound by geographic regions: Europe, North America, Patagonia, and Australia–New Zealand. Molecular, morphological, and environmental evidences delimit two lineages within this complex: a Northern Hemisphere clade with longer basidiospores and wider ranges in temperature and precipitation tolerance, and a Southern Hemisphere clade with smaller and more spherical basidiospores, and an isothermal and more humid climate preference. The integrative taxonomic approach used in this study demonstrates congruence between data sets and shows how morphological and environmental characteristics contribute to the differentiation of fungal species complexes. By combining various sources of taxonomic information, three new species are described: Xylodon laurentianus, X. novozelandicus, and X. patagonicus. Keywords: Basidiomycota, Biogeography, Corticioid fungi, Environmental niche, Hymenochaetales, Morphological traits, Multilocus phylogeny, New taxa INTRODUCTION environments around the world (Hallenberg 1991). For Corticioid fungi represent a polyphyletic group delimited these reasons, corticioid fungi offer unique opportunities by effused and resupinate basidiomes that usually grow to study speciation and the geographic patterns that re- on dead wood. One descriptor for these fungi is “paint sult from this process. on wood” which accurately characterizes their thin crust The idea that fungi are free from dispersal barriers had of reproductive structures, which are among the most a long tradition, so global distributions were accepted as elementary in Agaricomycetes. Although traditional clas- normal (Lumbsch et al. 2008). Cosmopolitanism or a sification grouped these fungi in a single family, molecu- high similarity index in corticioid fungi distribution pat- lar phylogenetic analyses have identified up to 50 terns have been reported in many studies (Gilbertson different families in at least 11 orders (Larsson 2007). 1980, Ghobad-Nejhad 2011). However, molecular studies Studying the biodiversity of corticioid fungi presents have demonstrated distinct biogeographic patterns re- an opportunity to explore their phylogeny. First, despite lated to hidden biodiversity (Taylor et al. 2006, Knight & their apparent macromorphological homogeneity, ac- Goddard 2015). In this context, the “everything is every- cording to Mueller et al. (2007), there are more than where” hypothesis (Baas Becking 1934) for all fungal 1800 described species, making them a highly diverse groups has given way to the argument that geographic group. Second, they have colonized a broad range of range inferred for a fungal species strongly depends on the nature of the characters used for its delimitation * Correspondence: [email protected] (Taylor et al. 2000). 1Departamento de Micología, Real Jardín Botánico-CSIC, Plaza de Murillo 2, Species concepts in fungi remain an important discus- 28014 Madrid, Spain sion topic (Taylor et al. 2000, Öpik et al. 2016). The Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Fernández-López et al. IMA Fungus (2019) 10:2 Page 2 of 20 same species concept is not always applicable across all important role in ecosystem services due to their ability fungal taxa due to the multiple evolutionary processes to alter wood structure and create habitat for other that can lead to fungal speciation (e.g. horizontal gene groups of organisms. As noted by Hibbett et al. (2014), transfer, hybridization, etc.; Giraud et al. 2008). During it is one of the largest genera of wood-rotting fungi, with the last two decades, molecular tools have transformed 162 current legitimate names (Robert et al. 2005; Robert the study of fungal biodiversity. Among all the regions et al. 2013). During the last ten years, six new Xylodon tested in Schoch et al. (2012), the nuclear ribosomal in- species have been described (Ariyawansa et al. 2015, ternal transcribed spacer DNA region (ITS, the fungal Chen et al. 2018, Crous et al. 2018, Viner et al. 2018), barcode) in most cases has the highest resolving power also 59 combinations made (Hjortstam & Ryvarden for discrimination between closely related species. Even 2009, Riebesehl & Langer 2017, Chen et al. 2018) and so, taxonomic/systematic studies benefit by including two new names were proposed (Hjortstam & Ryvarden other genetic regions (Balasundaram et al. 2015). Fungal 2009, Riebesehl & Langer 2017). species concepts have evolved through time (Cai et al. Xylodon raduloides (Riebesehl & Langer 2017), previ- 2011) and mycologists have benefited from the develop- ously known as Schizopora radula (Hallenberg 1983), ment of genealogical concordance phylogenetic species has been widely reported. It is widespread in Europe, recognition (GCPSR) for describing fungal diversity and the Canary Islands (Hallenberg 1983, 1991, Langer (Taylor et al. 2000). Molecular data have provided a de- 1994, Ryvarden & Gilbertson 1994, Melo et al. 2007, tailed view of previously hidden fungal diversity, enab- Ryvarden & Melo 2014), and is also known from North ling better use of traditional species recognition America (Hallenberg 1983, Langer 1994, Zhou et al. methods in morphology or mating compatibility to un- 2016), South America (Langer 1994, Greslebin & Raj- mask this cryptic fungal diversity (Giraud et al. 2008). chenberg 2003, Gorjón & Hallenberg 2013, Martínez & The implementation of GCPSR has revealed the pres- Nakasone 2014), temperate Asia (Langer 1994, Hallen- ence of hidden diversity in several complexes of corti- berg 1983), and Australasia (McKenzie et al. 2000, Pau- cioid fungi where morphological species recognition lus et al. 2000). approaches failed (e.g. Serpula himantiodes, Carlsen et In a broad phylogenetic study of the genus Schizopora al. 2011). However, with the increase of DNA regions (now included in Xylodon), some degree of genetic isola- used to estimate phylogenies, many researchers have ar- tion between populations of X. raduloides was detected, gued the need to consider processes that could lead to also supported by intercompatibility studies (Paulus et discordance among gene phylogenies, that is, differences al. 2000). The worldwide geographic distribution of X. between gene-trees and species-trees (Edwards 2009; raduloides, along with available molecular data, sug- Heled & Drummond 2010). The use of different models, gested it could be a species complex with the true diver- such as the coalescent theory (Kingman 1982) that al- sity reflecting biogeography. In this study, the diversity lows gene tree heterogeneity, have been successfully ap- and biogeographic relationships in X. raduloides are ad- plied for fungal species delimitation (e.g. Hyphoderma dressed using an integrative taxonomic approach (Dayrat paramacaronesicum, Martín et al. 2018). 2005). Our aim is to achieve a comprehensive under- The search for evidence in addition to molecular phylo- standing of the taxonomic diversity of the complex genetic data has emerged as a goal for species delimitation through the use of multiple sources of evidence (multi- (Wiens 2007). Interest has increased in ecological traits as locus species coalescent phylogeny, morphological char- characters for species identification in many organisms acters, and environmental equivalence analysis). (Rissler & Apodaca 2007). The combination of phyloge- netics and niche modeling methodologies has proven use- ful in studying the mechanisms that shape biogeographic MATERIALS AND METHODS patterns (Raxworthy et al. 2007,Marskeetal.2012). With Taxon sampling and morphological studies the development of GIS-based and cartographic ap- A total of 39 vouchers of Xylodon raduloides (Table 1) proaches, the comparison of environmental niches has were obtained from four fungaria (CFMR, MA-Fungi, been proposed to study such evolutionary processes as NY, and PDD), cultures of the Forest Products Labora- sympatric speciation and niche conservatism (Warren et tory (USDA), and ICMP culture collection (World Data al. 2008, Broennimann et al. 2012, Ahmadzadeh et al. Center for Microorganism 2011). Specimens from Hui- 2013). Due to the paucity of detectable macromorphologi- nay (Los Lagos Region, Chile) were