Phylogeny of Cyttaria Inferred from Nuclear and Mitochondrial Sequence and Morphological Data

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Phylogeny of Cyttaria Inferred from Nuclear and Mitochondrial Sequence and Morphological Data Mycologia, 102(6), 2010, pp. 1398–1416. DOI: 10.3852/10-046 # 2010 by The Mycological Society of America, Lawrence, KS 66044-8897 Phylogeny of Cyttaria inferred from nuclear and mitochondrial sequence and morphological data Kristin R. Peterson1 sort into clades according to their associations with Donald H. Pfister subgenera Lophozonia and Nothofagus. Department of Organismic and Evolutionary Biology, Key words: Encoelioideae, Leotiomycetes, Notho- Harvard University, 22 Divinity Avenue, Cambridge, fagus, southern hemisphere Massachusetts 02138 INTRODUCTION Abstract: Cyttaria species (Leotiomycetes, Cyttar- Species belonging to Cyttaria (Leotiomycetes, Cyttar- iales) are obligate, biotrophic associates of Nothofagus iales) have interested evolutionary biologists since (Hamamelididae, Nothofagaceae), the southern Darwin (1839), who collected on his Beagle voyage beech. As such Cyttaria species are restricted to the their spherical, honeycombed fruit bodies in south- southern hemisphere, inhabiting southern South ern South America (FIG. 1). His collections of these America (Argentina and Chile) and southeastern obligate, biotrophic associates of tree species belong- Australasia (southeastern Australia including Tasma- ing to genus Nothofagus (Hamamelididae, Nothofa- nia, and New Zealand). The relationship of Cyttaria gaceae) became the first two Cyttaria species to be to other Leotiomycetes and the relationships among described (Berkeley 1842, Darwin 1839). Hooker species of Cyttaria were investigated with newly reported to Darwin a third species from Nothofagus generated sequences of partial nucSSU, nucLSU trees in Tasmania (Berkeley 1847, 1848; Darwin and mitSSU rRNA, as well as TEF1 sequence data 1846). Over time Cyttaria species have been shown and morphological data. Results found Cyttaria to be to be restricted to Nothofagus trees in southern South defined as a strongly supported clade. There is America (Argentina and Chile) and southeastern evidence for a close relationship between Cyttaria Australasia (southeastern Australia, including Tasma- and these members of the Helotiales: Cordierites, nia, and New Zealand). certain Encoelia spp., Ionomidotis and to a lesser Cyttaria species are presumed to be weak parasites extent Chlorociboria. Order Cyttariales is supported by (Gamundı´ and Lederkremer 1989) that produce molecular data, as well as by the unique endostro- trunk and branch cankers on Nothofagus trees. Two matic apothecia, lack of chitin and highly specific types of cankers generally are produced (Gamundı´ habit of Cyttaria species. Twelve Cyttaria species are 1971, Rawlings 1956): globose ones that arise from hypothesized, including all 11 currently accepted growth mainly in the transverse axis of the branch and species plus an undescribed species that accommo- longitudinal ones that arise from growth mainly along dates specimens known in New Zealand by the the long axis. misapplied name C. gunnii, as revealed by molecular A typical mature fruit body of a Cyttaria species data. Thus the name C. gunnii sensu stricto is consists of what may appear to be an orange, pitted reserved for specimens occurring on N. cunninghamii ascoma, somewhat similar to a morel or a deeply in Australia, including Tasmania. Morphological data dimpled golf ball. However each fruit body is actually now support the continued recognition of C. composed of sterile fungal tissue, the stroma, in septentrionalis as a species separate from C. gunnii. which apothecia are immersed. The stromata typically Three major clades are identified within Cyttaria: one have a fleshy-gelatinous consistency, but those of in South America hosted by subgenus Nothofagus, some species are gummy or slimy. As the stromata another in South America hosted by subgenera develop, apothecia form beneath a membrane that Nothofagus and Lophozonia, and a third in South envelopes the fruit body. At maturity this membra- America and Australasia hosted by subgenus Lopho- nous ectostroma peels away to reveal, depending on zonia, thus producing a non-monophyletic grade of the species and the stroma, 1–200 apothecia, each South American species and a monophyletic clade of lined with asci. The eight-spored asci are inoperculate Australasian species, including monophyletic Austra- with Bulgaria inquinans-type ascus apices (Mengoni lian and New Zealand clades. Cyttaria species do not 1986) that possess an annulus that stains blue in iodine. Ascospores are uninucleate (Mengoni 1986), Submitted 2 Mar 2010; accepted for publication 29 Apr 2010. subglobose to ovoid, smooth to rugulose, at first 1 Corresponding author. E-mail: [email protected] hyaline to yellowish but later becoming pigmented, 1398 PETERSON AND PFISTER:PHYLOGENY OF CYTTARIA 1399 FIG. 1. Bayesian tree from the combined molecular dataset showing the monophyly of Cyttaria and its relationship to members of Leotiomycetes. Numbers associated with nodes represent posterior probabilities from BI analyses (above branches) and .50% bootstrap support from P analyses (below branches). The illustration from Darwin (1846) is reproduced courtesy of the library of the Gray Herbarium, Harvard University, Cambridge, Massachusetts. Asterisks are discussed in Peterson et al. (2010). AUS 5 Australia, NZL 5 New Zealand, SSA 5 southern South America. 1400 MYCOLOGIA are actively discharged, producing a dark gray to justify placement in its own order (Carpenter 1976, black spore print. In some species, before forming Eriksson and Hawksworth 1986, Gamundı´ 1971, apothecia, the stromata produce pycnidia in which Gernandt et al. 2001, Kimbrough 1970, Korf 1973, monoblastic, uninucleate (Mengoni 1989), haploid Luttrell 1951, Rifai 1968), from the description of the mitospores, or conidia, are produced in basipetal first Cyttaria species (Berkeley 1842), taxonomists succession from conidiophores. The function of these often have hypothesized relationships of Cyttaria with mitospores has not been confirmed, but they have taxa belonging to Helotiales (Pezizomycotina, Leo- been proposed to be involved in sexual reproduction tiomycetes). In early molecular studies Cyttaria, (Gamundı´ 1971, Minter et al. 1987). represented by a single published sequence (Landvik The 11 currently accepted species of Cyttaria and Eriksson 1994), grouped with other Leotiomy- (Gamundı´ 1971, 1991; Gamundı´ et al. 2004; Rawlings cetes, including members of Erysiphales, Helotiales, 1956) are obligate, biotrophic associates of all 11 Rhytismatales, Thelebolales and Myxotrichaceae species of Nothofagus subgenera Lophozonia and (Leotiomycetes incertae sedis), as well as members Nothofagus. The relationship between Cyttaria species of Pseudeurotiaceae (Ascomycota incertae sedis) and Nothofagus hosts often is cited as a classic (Do¨ring and Triebel 1998, Gernandt et al. 2001, example of cospeciation, and because of this well Landvik and Eriksson 1994, Landvik et al. 1998, known association it is one of the few cases where the Marvanova´ et al. 2002, Mori et al. 2000, Paulin and biogeography of a fungus is commonly mentioned. Harrington 2000, Sugiyama et al. 1999, Winka 2000). This is despite the fact that the associations between In none of these phylogenies is Cyttaria monophyletic species of Cyttaria and Nothofagus usually do not with the Helotiales as a whole. Using unpublished correspond in a simple one to one relationship; Cyttaria sequences generated in this study, other several Cyttaria species may infect the same Nothofa- phylogenetic studies of the Helotiales and Leotiomy- gus species and a single Cyttaria species may infect cetes by Wang et al. (2006a, b) and (Schoch et al. several Nothofagus species (TABLE I). 2009), hypothesized a close relationship among Relationships within Nothofagus.—Nothofagus is one Cyttaria, Chlorociboria (Helotiales, Helotiaceae) and of the few southern hemisphere taxa for which a Erysiphales; these studies again identified Cyttariales robust fossil record and well studied phylogeny exist as members of Leotiomycetes and acknowledged (Jordan and Hill 1999) and often is included in Helotiales to be an unnatural group. Hibbett et al. biogeographic studies (e.g. Cook and Crisp 2005, (2007), placed Cyttariales in Leotiomycetes in their Heads 2006, Knapp et al. 2005, Swenson et al. 2001). revised higher-level phylogenetic classification of the It comprises 35 extant species divided into four fungi based on molecular data. subgenera (Dettmann et al. 1990, Hill and Jordan Relationships within Cyttaria.—Relationships among 1993, Hill and Read 1991): subgenus Brassospora with species belonging to Cyttaria have been considered by 19 species in New Caledonia and New Guinea, from Kobayasi (1966), Korf (1983), Humphries et al. which no Cyttaria species have been recorded; (1986) and Crisci et al. (1988), the latter two using subgenus Fuscospora with five species in South cladistic analyses of morphological characters. In America and Australasia, from which no Cyttaria general these hypotheses infer a non-monophyletic species have been recorded; subgenus Lophozonia grade of South American Cyttaria species on subge- with six species in South America and Australasia, all nus Nothofagus basal to a non-monophyletic grade of which host Cyttaria species; and subgenus Nothofagus South American species on subgenus Lophozonia that with five species in South America, all which host is itself basal to a monophyletic clade of Australasian Cyttaria species. Seven Cyttaria species are endemic to species on subgenus Lophozonia. Korf’s (1983) southern South
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