Mycol Progress (2010) 9:261–266 DOI 10.1007/s11557-009-0636-y

ORIGINAL ARTICLE

The systematic position of Lasallia caroliniana (Tuck.) Davydov, Peršoh & Rambold comb. nova and considerations on the generic concept of Lasallia (Umbilicariaceae, Ascomycota) Evgeny A. Davydov & Derek Peršoh & Gerhard Rambold

Received: 16 July 2009 / Revised: 29 October 2009 / Accepted: 5 November 2009 / Published online: 25 November 2009 # German Mycological Society and Springer 2009

Abstract Detailed morphological investigations and phylogenetic analyses of the ITS/5.8S nrDNA reveal Umbilicaria caroliniana to be a member of Lasallia. A new combination, Lasallia caroliniana (Tuck.) Davydov, Peršoh & Rambold comb. nov., is proposed. The circumscription of Lasallia is extended by the character state of eightspored asci. According to the new concept, Lasallia is distinguished from Umbilicaria by comprising species which combine large, multicellular, brown ascospores and a pustulate thallus. The functionally significant differences in ascospore morphology justify the current division of Umbilicariaceae into Lasallia and Umbilicaria, although Umbilicaria remains paraphyletic. Keywords ITS nrDNA . Phylogeny . Lasallia . Umbilicaria

Introduction Umbilicaria caroliniana Tuck. is a representative of the family Umbilicariaceae Chevall., with a North American– Asian, i.e. amphiberingean distribution. It combines traits of the two genera Umbilicaria and Lasallia as currently circumscribed. Detailed morphological analyses of U. caroliniana, however, indicated closer affinities of this species to the genus Lasallia. E. A. Davydov (*) Herbarium (ALTB), Altai State University, Lenin Ave. 61, Barnaul 656049, Russia e-mail: [email protected] D. Peršoh : G. Rambold Department of Mycology, University of Bayreuth, Universitätsstraße 30, 95540 Bayreuth, Germany

Umbilicaria caroliniana was described by E. Tuckerman (1877) and placed in Umbilicaria Hoffm. sect. Umbilicaria [= Lasallia Mérat] (Tuckerman 1882). While the presence of two-spored asci was tentatively implied in the original diagnosis, U. caroliniana was the only taxon listed by Tuckerman (1882: 89) where the diagnosis lacked ascospore data. Subsequently, Minks (1900) reported eight muriform ascospores for this species. Elenkin and Savicz (1910) confirmed these observations following their investigation of new material from Yakutia. Due to the distinctly gyrodisc apothecia, an almost complete lack of pustules, and eight muriform ascospores, the authors considered U. caroliniana to be intermediate between Lasallia and “Gyrophora (Ach.) Körber” [= Umbilicaria], and placed it in a monotypic genus of its own, Gyrophoropsis. The genus was later reduced to the rank of a section within “Gyrophora” [= Umbilicaria] by Zahlbruckner (1926) and subsequently synonymized with “Umbilicaria” [= Lasallia] (Zahlbruckner 1927) following Lindau’s (1899) acceptance of the variability of apothecial structures within Umbilicariaceae. While Frey (1931, 1933) treated Umbilicariaceae as a monogeneric family and used the name Umbilicaria caroliniana Tuck., Scholander (1934) proposed the combination Gyrophora caroliniana (Tuck.) Schol. Subsequently, Llano (1950) synonymized Gyrophora with Umbilicaria Hoffm. sens. str. and reinstated Lasallia Mérat, replacing the misapplied name “Umbilicaria”. Thereafter, Umbilicaria caroliniana Tuck. has been the accepted name for this taxon. The Llano (1950) concept, recognizing five genera of Umbilicariaceae, was not followed by Savicz (1950), Poelt (1962), Wei (1966) or Wei and Jiang (1993), who all preferred to recognize only two genera, Umbilicaria Hoffm. and Lasallia Mérat (for a detailed survey, see Davydov 2007). All these authors based their concept of Lasallia on the following combination of characters: 1–2 spored asci,

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pustulate thallus and plane apothecial discs, i.e. leiodisc (except for L. mayebarae (Satô) Asahina with gyrodiscs). The aim of the present study was to clarify the position of U. caroliniana and to re-evaluate using the number and septation of ascospores as diagnostic characters for a generic segregation within the Umbilicariaceae

Material and methods Investigations were based on material from the herbaria FH, LE, and VLA and the lichen collection at the Pacific Institute of Geography, Russian Academy of Science (PIG RAS), Vladivostok. Anatomical and morphological characters were examined by standard light microscopy. Ascospore measurements (20 per specimen) were performed using sections in water. Selected specimens examined USA: Carolina Septentrionalis: Mitchel County, 29 viii 1971, W. L. Culberson 15651, T. L. Esslinger (LE-L5346) [Vězda, Lich. Sel. Exs. 1071]; Tennessee: Roan Mountain, Carter County, 5 iv 1971, M. E. Hale [Hale, Lich. Amer. Exs. 149] (LE-L5348); Alaska: along the north ridge of the Colville River, at Umiat, 22 vii 1958, J. W. Thomson & S. Shushan [Thomson, Lich. Arct. 27] (LE-L5349). Russia: Kamchatka: 5 km SW to Esso, 19 viii 2003, D. E. Himelbrant & E. S. Kuznetsova (LE-L6456); Khabarovsky krai: Ulchsky region, 12 ix 2001, I. F. Skirina (PIG RAS 13502): EU909475; Yakutia: Stanovoi Range, vii 1903, I. M. Shchogolev (LE-L5332); Chitinskaya oblast’: Sokhondinsky strict reserve, 13 viii 2001, I. A. Galanina (VLA L86): EU909464; Buryatia: Yuzhno-Muisky Range, 30 vii 1965, V. M. Burkova (LE-L5335). To determine the phylogenetic position of the taxon, the ITS region of the nrDNA (ITS1, 5.8S, and ITS2 nrDNA) was sequenced from 12 Lasallia specimens, representing 7 species and 2 specimens of U. caroliniana. Because 2 specimens of L. rossica did not fully correspond to the type material, they are labeled as L. aff. rossica. DNA isolation, PCR, cleanup of the products, and dideoxynucleotide sequencing were conducted following the procedure as described in Peršoh and Rambold (2002). The doublestranded sequences obtained were aligned with all Umbilicariaceae ITS sequences deposited in GenBank (www. ncbi.nlm.nih.gov). The resulting alignment contained 50 sequences of Umbilicariaceae and 1 outgroup sequence. By manual inspection, positions 6–493 (according to EU909467, Lasallia pustulata) were selected for the phylogenetic reconstruction, with ambiguously alignable regions being excluded (positions 14–20, 29, 54, 84–87, 143, 175–178, 340, 374, 414, 415, 449, 450, and 488). The most likely tree and 500 bootstrap replicates were calculat-

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ed using RAxML (Stamatakis 2006), applying the GTRCAT model of substitution. Bootstrap support values were drawn onto the best scoring tree.

Results and discussion The phylogenetic analysis of Umbilicariaceae resulted in the recognition of a monophyletic grouping of members of Lasallia (group of ‘Lasallia-clades’), including U. caroliniana (Fig. 1), which is well supported (98%). The clade is nested within a paraphyletic group of ‘Umbilicariaclades’, in accordance with earlier findings (Ivanova et al. 1999; Miadlikowska et al. 2006). The paraphyletic group of ‘Umbilicaria-clades’ comprised the majority of species with regular, unicellular ascospores together with a few species with occasional oligocellular, but generally unicellular spores. Species with regularly developed multicellular-muriform spores cluster exclusively within the monophyletic group of ‘Lasalliaclades’ and all have 1(–2)-spored asci except for U. caroliniana. The seven specimens of U. caroliniana from different regions of the world which were investigated clearly have multicellular ascospores, from (25.0–)28.5– 33.1–37.7(–42.5) × (15.0–)17.3–19.7–22.1 (–25.0) μm in size when mature and with (50–)100 or more cells. Even when the spores are immature, i.e. with unpigmented walls, multi-septation was apparent (Fig. 2). The size of mature ascospores in U. caroliniana falls in between that of the genus Umbilicaria (15−19.1−25 × 8−12.4−18 μm) and of Lasallia (36−112 × 20−60 μm). Within the Umbilicariaceae, two ascospore characters, i.e. the number of spores per ascus and the type of spore septation, were used for separating Umbilicaria and Lasallia. As a consequence, special emphasis was laid in this study on this character complex. Species of Umbilicaria usually have non-muriform ascospores, but oligocellular-muriform, i.e. submuriform, spores do occur in a few species with unambiguous affiliation to Umbilicaria (e.g., U. cinereorufescens (Schaer.) Frey, U. crustulosa (Ach.) Frey, U. ruebeliana (Du Rietz et Frey) Frey, and U. spodochroa Ehrh. ex Hoffm.). However, this spore type is quite uncommon and usually restricted to the distally positioned spores within the ascus. With number of ascospore cells usually between 3 and 15, these species clearly differ from those with unambiguous affiliation to Lasallia which have (30−)50−100 cells per spore. Accordingly, spores with muriform ascospores may be classified into two subtypes: (1) the occasionally developed oligocellular-muriform spore subtype (with relatively few longitudinal and transversal septa and usually 12(–25) cells (‘submuriform’), and (2) the regularly developed multicellular-muriform spore subtype with (25–)30 or more septa and exceeding 50−100 cells (‘eumuriform’).

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Fig. 1 Phylogenetic relationships among selected Umbilicariaceae. Best scoring tree found by the RAxML analysis. Bootstrap support values are noted above or close to the respective branches. The species names corresponding to the sequences are preceded by the GenBank accession number. Long branches were bisected (//)

EU909473, Lasallia hispanica EU909474, L. pustulata EU909467, L. pustulata 100 EU909470, L. asiae-orientalis 83 EU909471, L. daliensis var. caeongshanensis 99 EU909465, L. aff. rossica EU909468, L. aff. rossica 100 EU909463, L. rossica 46 EU909469, L. rossica 100 AF096203, L. pertusa 48 EU909466, L. pertusa 100 EU909464, Umbilicaria (Lasallia) caroliniana 98 EU909465, Umbilicaria (Lasallia) caroliniana 98 EU909462, AF096202, AF097674, L. pennsylvanica 100 EU909472, L. pennsylvanica 36 AF297675, L. pennsylvanica 96 AF096205, Umbilicaria nylanderiana 67 AY603133, U. nylanderiana 16 AF096216, U. hyperborea 86 AY603121, U. umbilicarioides 100 AJ431606, U. umbilicarioides 98 AF096210, U. umbilicarioides 56 AF096209, U. cylindrica AF096199, U. cylindrica 7 AY603127, U. antarctica AY603131, U. kappenii 100 AJ431599, U. kappenii AF096213, U. antarctica 12 81 AY603134, U. krascheninnikovii 81 AJ431600, U. decussata 32 AY603122, U. decussata 7 AF096214, U. decussata 99 AF096211, U. leiocarpa 35 AF096212, U. rigida 43 AF096200, U. subglabra 98 AF096217, U. lyngei AF297669, U. lyngei 99 AF096204, U. muehlenbergii 95 AF297667, U. muehlenbergii AF297666, U. muehlenbergii 32 100 AF096206, U. deusta 3 AF297670, U. deusta 65 AF096215, U. crustulosa 61 AF297671, U. loboperipherica 13 AF096208, U. vellea 15 AF096207, U. spodochroa 100 AF284447, U. esculenta 21 AF284448, U. mammulata AF096218, U. americana AF096219, U. ruebeliana AY530886, Boreoplaca ultrafrigida 82

100

74

// 0.10

The results of the phylogenetic analysis indicate that the regularly developed multicellular and the oligocellular muriform ascospore types evolved independently within the Umbilicariaceae. The ascospores of U. caroliniana are clearly of the multicellular-muriform type, which has been recognized as

Fig. 2 Lasallia caroliniana: a Ascus containing 8 multicellularmuriform ascospores. b Immature ascospore

being diagnostic for species of the ‘Lasallia-clades’ (Fig. 2) and as being absent in species of the ‘Umbilicaria-clades’. Within Umbilicariaceae, multicellular-muriform ascospores therefore represent a synapomorphy of Lasallia. A second ascospore character considered to be diagnostic for members of the species of the Lasallia-clades is the 1–2-spored asci. It appears to be another apomorphic trait, but with a paraphyletic topology given the fact that U. caroliniana with 8-spored asci, is nested within the Lasallia-clades. Assuming that the hypothetical ancestor of Lasallia had 1–2-spored asci, the presence of 8-spored asci in U. caroliniana may be interpreted as reversion to the initial state of this character and would accordingly represent an autapomorphy within the Lasallia-clades. If the development of 8-spored asci within the Lasallia-clades is considered a plesiomorphic trait, reduction of the number of ascospores would have occurred in that clade independently at least twice. Oligospory in the Ascomycetes is often accompanied by enlargement of the ascospore and an increase in septation, e.g., in Rhizocarpon (Rambold et al. 1998). Thus, the number of spores per ascus and septation are considered

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Table 1 Diagnostic characters of L. caroliniana and the genera Umbilicaria and Lasallia Characters\taxon

Umbilicaria

L. caroliniana

Lasallia

Ascospore number per ascus Ascospore cell number and septation type Apothecium type Thallus pustules Rhizinomorphs or rhizines Thalloconidia Lasallic acid Umbilicaric acid

8 Unicellular, bicellular, oligocellular-muriform Gyrodisc, omphalodisc, actinodisc, leiodisc – ± ± – ±

8 Multicellular-muriform Gyrodisc ± + – – –

1(–2) Multicellular-muriform Leiodisc, gyrodisc + – – ± –

interdependent morphological traits, i.e. reduction of the number of ascospores is coupled with increasing spore septation, or vice versa. Consequently for the Lasalliaclades, both character states may be regarded as synapomorphic traits. Given that 1–2-spored asci commonly result on maturation of eight nuclei due to abortion of immature spores (Read and Becket 1996), the assumption that octospory in U. caroliniana is the result of a reversion seems more plausible. A reversion to octospory would only require that nucleic abortion is inhibited. U. caroliniana exhibits a unique combination of morphological traits (Table 1). In contrast to most other species of the Lasallia-clades, U. caroliniana has gyrodisc apothecia, a trait it shares with L. mayebarae. Like all other species of Lasallia, U. caroliniana has a pustulate thallus and lacks thalloconidia. While pustule-like formations are very rare in species of Umbilicaria, thalloconidia are only known from this genus. Furthermore, U. caroliniana is characterized by its specific, cushion-like growth habit and its crowded, strongly undulated convex lobes (Fig. 3). As U. caroliniana lacks both umbilicaric and lasallic acid, secondary metabolites specific for Umbilicaria and Lasallia, respectively (Narui et al. 1996), chemical data cannot be used to support the phylogenetic position of this species. The presence of gyrodisc apothecia 8-spored asci and rhizinoid structures at the lower surface in U. caroliniana are typical of species of the Umbilicaria clades and in accordance with U. caroliniana being positioned on a divergent branch, close to the root of the Lasallia-clades (Fig. 1). As a consequence of our molecular and morphological analyses, a new combination is proposed: Lasallia caroliniana (Tuck.) Davydov, Peršoh & Rambold comb. nov. Umbilicaria caroliniana Tuck. Proc Am Acad Arts & Sci 12: 167 (1877); type: Rocks, Grandfather Mountain, North Carolina, 1845, M. A. Curtis 88 (FH—holotypus, photograph of upper and lower surface!).—Gyrophoropsis caroliniana (Tuck.) Elenkin & Savicz, Trav Mus Bot Acad St.-Petersbourg 8: 34 (1910).—Gyrophora caroliniana

(Tuck.) Schol. Nyt Mag Naturvid 75: 28 (1934).— Umbilicaria mammulata Tuck. Proc Am Acad Arts & Sci 1: 261 (1848) [non Ach.]; type: North Carolina, 1858. S. B. Buckley (5) (FH—holotypus, photograph of upper and lower surface!). ITS nrDNA data indicated that Lasallia caroliniana was most closely related to L. pennsylvanica (Hoffm.) Llano and L. pertusa (Rass.) Llano (Fig. 1). Representatives of L. pennsylvanica occasionally have reduced rhizines on a rough papillate, black lower surface and a sterile hyphal column in the hymenial layer. These morphological features and the presence of similar lobulae supported the close relationship between these species. Moreover, both species have an Asian–North American distribution. Nevertheless, L. pennsylvanica is distributed more widely both in North America, where it occurs throughout the temperate zone, and in Eurasia, where it is found from the Far East to the Caucasus Mountains and Turkey. In North America, L. caroliniana is restricted to the Appalachian Mountains, North Yukon, and Brooks Range (Llano 1950; Brodo et al. 2001), and occurs in East Asia from Kamchatka and Japan to eastern Siberia. While the close relationship between L. pennsylvanica and L. caroliniana is therefore well supported by their morphology data and their geographical distribution, L. pertusa differs morphologically from both,

Fig. 3 Lasallia caroliniana: Thallus with apothecia

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as it is characterized by a thallus with abundant fenestrate pustules, soredia, and few isidia. Furthermore, it lacks rhizinomorphs and apothecia and is distributed in Asia and Africa (Wei and Jiang 1993). The inclusion of a species with 8-spored asci extends the generic circumscription of Lasallia and an amended version follows. Lasallia Mérat emend. Davydov, Peršoh & Rambold Mérat, Nouv. Fl. Paris ed. 2. 1: 202 (1821); Llano, Monograph of the Lichen. family Umbilicariaceae in the Western Hemisphere: 27 (1950); J. C. Wei, Acta Phytotax Sin 6 (1): 4 (1966).—Umbilicaria sect. Lasallia Endlich., Gen Pl: 13 (1836); A. Zahlbr., Cat Lich IV: 745 (1927).— Umbilicaria subgen. Lasallia Frey, Hedwigia 71: 106 (1931); Frey, Rabenh Krypt Fl IX. 4 (1): 208 (1933).— Gyrophoropsis Elenkin & Savicz, Trav Mus Bot Acad St.Petersbourg 8: 34 (1910). Typus generis: Lasallia pustulata (L.) Mérat, Nouv Fl Paris ed. 2. 1: 202 (1821).—Lichen pustulatus L. Sp Pl: 1150 (1753). The assignment of U. caroliniana to Lasallia implies accepting Umbilicaria as a paraphyletic genus. The question of whether paraphyly may or must be accepted under certain conditions has been controversially and extensively discussed (Brummitt 2003, 2006; Dias et al. 2005; Nordal and Stedje 2005; versus: Potter and Freudenstein 2005; Williams et al. 2005). The discussion culminated in papers by Ebach et al. (2006) pleading for the application of monophyly to taxonomic units, whereas that of Zander (2007) indicated that the acceptance of paraphyletic taxa is unavoidable. We propose to accept Umbilicaria as a paraphyletic genus for the following reasons: (1) The most prominent autapomorphic trait of the species of the Lasallia-clades is the increase in ascospore septation (multicellular-muriform) together with an enlargement of the spores and the reduction of spore number (except for L. caroliniana), which appears functionally significant and associated with spore ejection. Thus, Lasallia represents a taxon within the Umbilicariaceae characterized by a derived and functionally significant morphological trait. (2) The group of paraphyletic Umbilicaria-clades is morphologically welldefined by 8-spored asci with non-multicellular (but unicellular to oligocellular-muriform) spores and predominantly non-pustulate thalli lacking isidia and lobuli, but frequently possessing rhizinomorphs and thalloconidia, despite considerable variation within the clades (i.e. in apothecial morphology, the presence and type of thalloconidia, secondary metabolites and reproductive strategy). However, morphological support for further subdivision of the clades into genera is currently not apparent. Therefore, we recommend accepting Umbilicaria as a paraphyletic genus and maintaining the current bipartite classification of the Umbilicariaceae and the genera Lasallia and Umbilicaria.

265 Acknowledgements We thank the curators of FH, LE, VLA, and PIG RAS for the loan of material, and the colleagues, who kindly provided additional specimens. John A. Elix (Canberra) is thanked for correcting the English and Christina Leistner (Bayreuth) for assistance with the laboratory work. The first author was supported by DAAD (German Academic Exchange Service) no. A/03/01054, by the Grants of President of Russian Federation no. MK 5671.2006.4, and of Russian Foundation of Basic Research no. 07-04-90800 and no. 09-04-90703.

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