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Phylogeny of Fomitopsis Pinicola: a Species Complex

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Phylogeny of Fomitopsis Pinicola: a Species Complex Mycologia, 108(5), 2016, pp. 925–938. DOI: 10.3852/14-225R1 # 2016 by The Mycological Society of America, Lawrence, KS 66044-8897 Phylogeny of Fomitopsis pinicola: a species complex John-Erich Haight1 concepts. Morphological data currently available for Institute of Arctic Biology and the Biology and Wildlife F. pinicola do not delimit these species, and three of Department, University of Alaska, Fairbanks, Alaska 99775 the species are not specific to either hardwood or soft- USDA-FS Northern Research Station, One Gifford Pinchot wood trees. Originally described from Europe, F. pini- Drive, Madison, Wisconsin 53726 cola appears to be restricted to Eurasia. Based on Gary A. Laursen DNA data obtained from an isotype, one well-defined Institute of Arctic Biology and the Biology and Wildlife and widespread clade found only in North America Department, University of Alaska, Fairbanks, Alaska 99775 represents the recently described Fomitopsis ochracea. Jessie A. Glaeser The remaining two North American clades represent USDA-FS Northern Research Station, One Gifford Pinchot previously undescribed species. Drive, Madison, Wisconsin 53726 Key words: Bayesian, coalescent, maximum likeli- D. Lee Taylor2 hood, phylogenetic species, polyporoid clade, spe- Institute of Arctic Biology and the Biology and Wildlife cies tree Department, University of Alaska, Fairbanks, Alaska 99775 INTRODUCTION Abstract: The variable phenotypic appearance of Fomitopsis pini- Fungal species with a broad distribution may cola (Sw. n: Fr.) P. Karst as well as its collection on a exhibit considerable genetic variation over their geo- variety of host species (Mounce 1929) covering a broad graphic ranges. Variation may develop among popula- geographic range (Spaulding 1961, Anonymous 1979, tions based on geographic isolation, lack of migration, Quiniones 1980, Schmid-Heckel 1988, Teng 1996, Fil- and genetic drift, though this genetic variation may not siñska 1997, Hermansson 1997, Pande and Rao 1998, always be evident when examining phenotypic charac- Chen 2002, Cho and Shin 2004, Legon et al. 2005, ters. Fomitopsis pinicola is an abundant saprotrophic Kobayashi 2007) has led to speculation that cryptic spe- fungus found on decaying logs throughout temperate cies may be present. Fries (1821) described two spe- regions of the Northern Hemisphere. Phylogenetic cies, Polyporous marginata being lighter in color and studies have addressed the relationship of F. pinicola ungulate, and Polyporus pinicola with a cap color tend- to other wood-rotting fungi, but pan-continental varia- ing to black and cinnamon. The host range of P. mar- tion within F. pinicola has not been addressed using ginata included Fagus, Betula, Pinus, and Pyrus, while molecular data. While forms found growing on hard- wood and softwood hosts exhibit variation in habit that of P. pinicola included Abies, and Betula. Saccardo and appearance, it is unknown if these forms are (1888) described a third species, Fomes ungulates, hav- genetically distinct. In this study, we generated DNA ing a cap with thick, concentric reddish-ochre colored sequences of the nuc rDNA internal transcribed furrows, which was collected on conifers in the Italian spacers (ITS), the TEF1 gene encoding translation Alps. Mounce (1929) found various forms and colors elongation factor 1-a, and the RPB2 gene encoding of sporocarps on Tsuga in the United States. Her the second largest subunit of RNA polymerase II for extensive collections and work with crosses of single collections across all major geographic regions where spore isolates lead her to agree with Hedgecock this fungus occurs, with a primary focus on North (1914), Lloyd (1915), Murrill (1908), and Overholts America. We used Bayesian and maximum likelihood (1915) that the three species described by Saccardo analyses and evaluated the gene trees within the spe- were forms of the same species. Mounce discovered cies tree using coalescent methods to elucidate evolu- that, both within and between North America and Eur- tionarily independent lineages. We find that F. ope, monosporous mycelia of F. pinicola isolated from pinicola sensu lato encompasses four well-supported, sporophores collected on deciduous hosts were mutu- congruent clades: a European clade, southwestern US ally fertile with monosporous mycelia isolated from clade, and two sympatric northern North American sporophores from coniferous hosts. She concluded clades. Each clade represents distinct species accord- that F. marginalis and F. pinicola were the same species ing to phylogenetic and population-genetic species and that European and American forms of the fungus were identical to each other. Further work with mono- Submitted 26 Aug 2014; accepted for publication 21 Jun 2016. sporous pairings lead to the discovery of two interster- 1 Corresponding author. E-mail: [email protected] 2 Current address: Department of Biology, University of New Mexico, ile populations in North America (Mounce and Albuquerque, New Mexico 87131. Macrae 1938). Describing them as separate species 925 926 MYCOLOGIA was rejected when both populations were found to provide much greater insight into fungal speciation. form fertile spores when crossed with isolates from The present study of F. pinicola illustrates this potential. Europe. Though inhabiting a large geographic range, Although principles of the biological species con- European populations of F. pinicola were found to be cept and the phylogenetic species concept were also members of one intersterility group (Högberg considered, our study centered on coalescent theory, et al. 1999). using a Bayesian hierarchical model (Liu and Pearl A recently described species, F. ochracea, originally 2007) to estimate the phylogeny of the species collected in Alberta, Canada on Populus tremuloides complex in F. pinicola. We tested the hypothesis that (Ryvarden and Stokland 2008), was delimited from F. F. pinicola constitutes a species complex using comple- pinicola based largely on pore color and spore mor- mentary methods: phylogenetic and recently devel- phology. Ryvarden and Stokland (2008) reported that oped coalescent population genetic methods. In the pore surface of F. ochracea did not exhibit a change doing so, we also sought to test whether distinct species from cream to citrus yellow when bruised, as seen in F. within the F. pinicola complex correspond to geograph- pinicola, and that the basidiospores were globose to ic regions, host plants, or sporocarp color forms. This broadly ellipsoid, rather than cylindrical. They noted paper focuses primarily on evolutionary questions, that the smooth ochraceous pileus of F. ochracea is easi- and a parallel paper will address taxonomic ly separated from that of F. pinicola. They also obtained descriptions. a sequence from the holotype and compared it to sequences of several F. pinicola from North America MATERIALS AND METHODS but did not make formal comparisons to other collections. Sample collections.—To encompass the largest possible genetic In this study we evaluated the use of sequence data diversity, fresh fruiting bodies collected by us were augment- from three nuclear and two mitochondrial loci to ed with data collected from herbarium specimens and cul- assess whether F. pinicola comprises a species complex. tures, which allowed us to increase the geographical range Species boundaries in a species complex can be deter- of the dataset. Sporophores were collected from decaying softwood and hardwood substrates in various habitat types mined by various criteria depending on the species including circumpolar subarctic boreal forests, coastal tem- concept in use. Molecular techniques have given rise perate rainforests, northern mixed hardwood forests, and to the phylogenetic species concept, and promising southern coniferous forests at high elevations (TABLE I). statistical-molecular species delimitation methods include genealogical concordance and coalescent spe- Herbaria and culture collections.—Dried specimens of F. pinicola cies delimitation. Coalescent theory is a branch of pop- were sampled from the Gary A. Laursen Herbarium, Univer- ulation genetics that models genetic drift backward sity of Washington, formerly located at the University of through time, tracing polymorphism in a gene back Alaska, Fairbanks; the Center for Forest Mycology Research to a most recent common ancestral allele. This process Herbarium, US Forest Service, Madison, Wisconsin; the models divergence between alleles from the present, US National Fungus Collections (BPI), Beltsville, Maryland; when genes are sampled, back to the time when allelic the National Herbarium of the Netherlands, University of genes diverged (Degnan and Salter 2005). At this point Leiden Branch, Leiden, the Netherlands; and the Royal Ontario Museum Fungarium, Ontario, Canada. Fungal cul- all lineages of the gene have coalesced and the result- tures were obtained from private and public culture collec- ing product is a gene genealogy. This process accom- tions including the Center for Forest Mycology Research modates incomplete lineage sorting that can be Culture Collection, US Forest Service, Madison, Wisconsin. problematic in conventional phylogenetic analyses An attempt to include the type specimen of F. pinicola in and has been successful in delimiting cryptic species this study was unsuccessful as the type exists as an illustration in lichens (Leavitt et al. 2011, 2012a, 2012b) but has only and no biological specimen is known (Ryvarden 1991). not been applied widely in the fungi.
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