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Tylopilus Griseiolivaceus Sp. Nov. and T. Leucomycelinus (Boletaceae) Revisited from the Dominican Republic Within a Comprehensive Phylogeny of Tylopilus S

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Tylopilus Griseiolivaceus Sp. Nov. and T. Leucomycelinus (Boletaceae) Revisited from the Dominican Republic Within a Comprehensive Phylogeny of Tylopilus S Mycological Progress (2019) 18:1039–1056 https://doi.org/10.1007/s11557-019-01513-2 ORIGINAL ARTICLE Tylopilus griseiolivaceus sp. nov. and T. leucomycelinus (Boletaceae) revisited from the Dominican Republic within a comprehensive phylogeny of Tylopilus s. str. Matteo Gelardi1 & Claudio Angelini2,3 & Federica Costanzo1 & Francesco Dovana4 & Beatriz Ortiz-Santana5 & Alfredo Vizzini4 Received: 2 July 2019 /Revised: 31 July 2019 /Accepted: 2 August 2019 # German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract The genus Tylopilus s. str. in the Dominican Republic is investigated. Tylopilus griseiolivaceus is introduced as a novel species based on material recorded in a neotropical montane pine woodland but also known to occur in temperate coniferous forests in southeastern USA. The Central American species T. leucomycelinus is also re-evaluated and its geographical range expanded. A detailed morphological description is provided for both species and accompanied by colour images of fresh basidiomes in habitat, line drawings of the main anatomical features and molecular support relying on a multilocus phylogenetic inference (nrITS, nrLSU (28S), rpb2 datasets). In addition, DNA was successfully isolated from the type material of T. leucomycelinus and compared with the genetic material obtained from additional neotropical samples. The taxonomic placement, ecological require- ments and distribution patterns of T. griseiolivaceus and T. leucomycelinus are investigated/reviewed and their relationships with closely allied taxa in Tylopilus s. str. are elucidated and discussed. Epitypification of T. leucomycelinus is proposed herein. Keywords Boletales . Tylopilus . Molecular phylogeny . Greater Antilles . Neotropical boletes . Taxonomy Introduction 2008). It was one of the earlier boletoid genera to be separated from Boletus Fr. s.l. as intended in the Friesian system and its Tylopilus P. Karst., typified by T. felleus (Bull.) P. Karst., is a establishment is dated back to the second half of the nine- cosmopolitan and ubiquitous genus that is mainly character- teenth century (Karsten 1881). Up to very recent times, ized by pileate-stipitate basidiomes with non-glutinous sur- Tylopilus has been conceived in a very broad sense, including faces, pinkish flesh to vinaceous brown spore print, smooth a very large array of species with a wide range of different basidiospores and ectomycorrhizal (ECM) nutritional mode morphological, chemical and ecological features (Singer (Horak 1968; Pegler and Young 1981; Singer 1986; Watling 1947, 1986; Heinemann 1951;Hongo1960; Horak 1968, 2011; Snell and Dick 1970; Smith and Thiers 1971; Corner 1972;Thiers1975; Grund and Harrison 1976; Wolfe Jr 1979, Editorial Responsibility: Zhu-Liang Yang 1986; Singer et al. 1983, 1991; Imazeki et al. 1988; Both 1993; Wolfe Jr and Bougher 1993; Watling and Turnbull * Alfredo Vizzini [email protected] 1994; Watling and Li 1999; Bessette et al. 2000;Mao2009). However, molecular phylogenetic approaches carried out in 1 Anguillara Sabazia, Italy the last 20 years have clearly and repeatedly demonstrated that 2 Pordenone, Italy such an assemblage of species into a single genus should be disregarded, since Tylopilus s.l. appears to be definitely poly- 3 Dr. Rafael Ma. Moscoso National Botanical Garden, Av. República de Colombia, Santo Domingo, Dominican Republic phyletic, consisting of several independent phylogenetic line- ages (Binder and Hibbett 2006; Drehmel et al. 2008;Lietal. 4 Department of Life Science and Systems Biology, University of Turin, Viale P.A. Mattioli 25, I-10125 Torino, Italy 2011, 2014; Halling et al. 2012a, b;Nuhnetal.2013;Wuetal. 2014, 2016; Magnago et al. 2017). A number of different 5 USDA Forest Service, Northern Research Station, Center for Forest Mycology Research, One Gifford Pinchot Drive, genera have thus been erected to accommodate species previ- Madison, WI 53726, USA ously placed in this genus, such as Zangia Yan C. Li & Zhu L. 1040 Mycol Progress (2019) 18:1039–1056 Yang, Sutorius Halling, Nuhn & Fechner, Australopilus similarly only a limited number of taxa have till now been Halling & Fechner, Harrya Halling, Nuhn & Osmundson, reported from the underexplored areas of central and southern Pseudoaustroboletus Yan C. Li & Zhu L. Yang and Chiua South America (Palfner 2005;Barbosa-Silvaetal.2017; YanC.Li&ZhuL.Yang(Lietal.2011, 2014; Halling Magnago et al. 2017). The situation appears to be not much et al. 2012a, b;Wuetal.2016). Currently, the circumscription dissimilar in the islands of the Caribbean, where the genus is of Tylopilus s.str. as a monophyletic lineage belonging to the nearly absent. As a matter of fact, only a couple of Tylopilus subfamily Boletoideae Singer (Wu et al. 2014, 2016)isre- species have been reported to occur in the Dominican stricted to sect. Tylopilus (= sect. Fellei Singer) and sect. Republic to date, viz. T. chromapes (Frost) A.H. Sm. & Oxydabiles Singer pro parte as outlined by Singer (1986) Thiers and T. balloui (Peck) Singer (Ortiz-Santana et al. and Singer et al. (1991), encompassing species featuring 2007). However, the former has recently been reassigned to brownish, brown-olive to violet-purple colours, reticulate or a separate genus Harrya (Halling et al. 2012b) within the smooth stipe, white context and basal mycelium, tissues un- subfamily Zangioideae G. Wu, Y.C. Li & Zhu L. Yang (Wu changeable or reddening-darkening, occasionally greenish et al. 2014) based on morphological and molecular phyloge- blue to sea green on bruising, bitter to rarely mild taste and netic evidence, whereas the latter resulted from a misidentifi- dextrinoid cystidia (Binder and Hibbett 2006;Nuhnetal. cation of T. leucomycelinus (Singer & M.H. Ivory) R. Flores 2013;Wuetal.2014, 2016; Gelardi et al. 2015; & Simonini with the North American taxon (see below). Chakraborty et al. 2018; Liang et al. 2018;Chaietal.2019). As part of an ongoing project aiming at recording and Furthermore, two additional morphologically homogeneous analysing the boletes of the Dominican Republic, and well-delimited species groups, the T. balloui (Peck) T. griseiolivaceus is presented as a new species and a modern Singer complex (characterized by yellow-orange to orange- re-description and epitypification of T. leucomycelinus is pro- red or reddish brown colours, smooth stipe, negative reaction vided. In addition, DNA was successfully extracted from the with ammonia, mild taste, short phaseoliform-allantoid to type material of T. leucomycelinus and inferred to match with subovoid basidiospores and trichoderm to ixotrichoderm sequences obtained from samples recently recorded in Belize, pileipellis) and T. potamogeton Singer complex (sect. Guatemala and the Dominican Republic. Potamogetones Singer) (sharing tomentose pileus and stipe, non-staining context, bluing surfaces with ammonia, bitter taste and ECM association with caesalpinoid legumes) should Materials and methods also be retained within Tylopilus s. str. (Osmundson 2009; Nuhn et al. 2013;Wuetal.2014, 2016; Gelardi et al. 2015; Collection site and sampling Magnago et al. 2017; Chakraborty et al. 2018). However, due to the considerable morphological plasticity of Tylopilus,its Specimens examined were collected in Belize, Dominican taxonomic and phylogenetic boundaries have only partially Republic and Honduras, and are deposited in BRH, CFMR, been assessed and the infrageneric classification still remains F and JBSD (acronyms from Thiers 2019), while “ANGE” unclear. and “MG” refer to the personal herbarium of Claudio Angelini In America, the diversity of Tylopilus s.l. has a long tradi- and Matteo Gelardi, respectively. Herbarium numbers are cit- tion of study, having been widely explored over the past two ed for all collections from which morphological features were centuries, especially in the temperate belt of southeastern examined. Author citations follow the Index Fungorum, Canada and eastern USA (Frost 1874; Peck 1889; Murrill Authors of Fungal Names (www.indexfungorum.org/ 1909, 1914, 1948; Coker and Beers 1943; Singer 1947; authorsoffungalnames.htm). Novel names and typifications Snell and Dick 1970; Smith and Thiers 1971; Grund and are registered with MycoBank (http://www.mycobank.org/). Harrison 1976;WolfeJr1981, 1983, 1986;WolfeJrand Halling 1989; Both 1993; Baroni and Both 1998; Bessette Morphological studies et al. 2000, 2016) as well as in the adjacent neotropical forests of mainland Central America and Northern South America Macroscopic descriptions and ecological information such as (Singer 1978, 1989;Singeretal.1983, 1991;Halling1989; habitat notations, time of fruiting and associated plant com- Wolfe Jr and Bougher 1993; Flores Arzù and Simonini 2000; munities accompanied the detailed field notes of the fresh Henkel 1999, 2001; Halling and Mueller 2001, 2005;Amtoft basidiomes. In the field, latitude, longitude, and elevation et al. 2002;Fulgenzietal.2007; Ortiz-Santana et al. 2007; were determined with a Global Positioning System (GPS) Fulgenzi 2009;OsmundsonandHalling2010), owing to the receiver. Colour terms in capital letters (e.g. White, Plate large number of species being distributed in these regions. By LIII) are from Ridgway (1912). Photographs of collections contrast, the genus is apparently very scarcely represented were taken in the natural habitat using a Nikon Coolpix along the Pacific Northwest with just a few species occurring 8400 camera. Microscopic anatomical features were observed (Thiers 1975; Arora 1986; Siegel
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