Arctoa (2016) 25: 119-130 doi: 10.15298/arctoa.25.10 ON THE SYSTEMATIC POSITION OF HYMENOLOMA (BRYOPHYTA) О СИСТЕМАТИЧЕСКОМ ПОЛОЖЕНИИ РОДА HYMENOLOMA (BRYOPHYTA) VLADIMIR E. FEDOSOV1, ALINA V. F EDOROVA2, ALEXEY V. T ROITSKY2, VERA K. BOBROVA2 & MICHAEL S. IGNATOV1,3 ВЛАДИМИР Э. ФЕДОСОВ1, АЛИНА В. ФЕДОРОВА2, АЛЕКСЕЙ В. ТРОИЦКИЙ2, ВЕРА К. БОБРОВА2, МИХАИЛ С. ИГНАТОВ1,3 Abstract Molecular phylogenetic analyses based on nad5, rps4 and trnL-F sequences suggest the position of the genus Hymenoloma in the order Scouleriales. This order includes two monogeneric families: Scouleriaceae, with aquatic plants, and Drummondiaceae that includes mostly epiphytic mosses. Mainly epilithic Hymenoloma strongly differs from both of them, as well as they differ from each other, thus a new family Hymenolomataceae is suggested for this genus. Morphologically, Hymenoloma has no unique characters, although its outstanding plasticity provides some explanation of its relationships with Scouleria and Drummondia. Резюме Согласно данным молекулярно-филогенетического анализа, основанного на последова- тельностях генов nad5, rps4 и trnL-F, род Hymenoloma следует относить к порядку Scouleriales. Этот порядок включает два семейства, в каждом из которых по одному роду: Scouleriaceae, пред- ставители которого растут в воде, и Drummondiaceae, куда входят эпифитные виды. Виды рода Hymenoloma растут преимущественно на каменистых субстратах и резко отличаются от видов из обоих других семейств порядка, которые, в свою очередь, совершенно не похожи друг на друга. Поскольку род Hymenoloma не представляется возможным включить ни в одно из двух семейств порядка по морфологическим признакам, то описывается новое семейство Hymenolomataceae. Этот род не имеет каких-либо уникальных морфологических признаков; с другой стороны, его выдающаяся морфологическая пластичность позволяет объяснить родство со Scouleria и Drummondia. KEYWORDS: Dicranidae, mosses, nad5, rps4, trnL-F, Scouleriales, molecular phylogenetics INTRODUCTION the system of Brotherus (1924). Reimers argued his de- The genus Hymenoloma has been installed by Dusén cision by complex costa structure with guide cells and (1905) for one Patagonian species, H. nordenskjoeldii stereid bands, as well as non Seligerioid peristome, as Dusén. Brotherus (1924) accepted it in the Seligeriaceae the latter was described by Brotherus. and also added to this genus three other species from However, when the attention to structural botany re- Subantarctic islands and southern South America, de- vived in 1970s, it resulted, among others, in the discov- scribed originally in the genera Blindia Bruch et al., Di- ery of considerable distinction between Seligeria-type and cranoweisia Milde, and Verrucidens Cardot. Reimers Dicranum-type of peristome (Edwards, 1979, 1984). As (1936) synonymized Hymenoloma with Dicranoweisia a consequence, the position of Seligeriaceae was reeval- (fam. Dicranaceae), bringing the former genus to the long uated and a separate order was established for its accom- oblivion. This decision had been invariably followed by modation (Nyholm, 1987; Anderson et al., 1990). bryologists up to 1990s. Ochyra (1993, 1998) was the first who noticed a dis- The transfer from Seligeriaceae to Dicranaceae was agreement between the peristome structure of Hymeno- not considered conspicuous, as these two families were loma crispulum (Hedw.) Ochyra, that time called Dicra- placed one by one within the same order Dicranales in noweisia crispula (Hedw.) Milde, with its position in 1 – Lomonosov Moscow State University, Faculty of Biology, Geobotany Dept., Leninskie Gory Str. 1-12, Moscow 119991 Russia – Россия, 119991, Москва, Ленинские Горы, д. 1 стр. 12, Московский государственный университет, биологический факультет, кафедра геоботаники; email: [email protected] & [email protected] 2 – Lomonosov Moscow State University, Belozersky Institute of Physico-Chemical Biology, Leninskie Gory 1-40, Moscow 119991 Russia – Россия, 119991, Москва, Ленинские Горы, д. 1 стр. 40, Московский государственный университет, НИИ Физико- химической биологии им. А.Н. Белозерского; e-mail: [email protected] & [email protected] 3 – Tsitsin Main Botanical Garden, Russian Academy of Sciences, Botanicheskaya Str., 4, Moscow 127276 Russia – Россия 127276 Москва, Ботаническая 4, ГБС РАН 120 V.E. FEDOSOV, A.V. FEDOROVA, A.V. TROITSKY, V.K. BOBROVA & M.S. IGNATOV Dicranaceae, and placed Antarctic species, including D. deous-alternate (Bryum pseudotriquetrum (Hedw.) crispula, in the Seligeriaceae. Subsequent studies revealed P.Gaertn., B. Mey. & Scherb., Hedwigia ciliata (Hedw.) that the type of the genus Dicranoweisia, Mediterranean P. Beauv., Hookeria lucens (Hedw.) Sm.) peristomes were D. cirrata (Hedw.) Lindb., is so different from the cos- involved as outgroups. Totally 110 sequences from 37 mopolitan D. crispula, that another generic name is re- specimens representing 35 species were involved into the quired for the group of taxa around D. crispula. This analysis, including 25 sequences of 12 species obtained problem was solved later by Ochyra, as he resurrected de novo. Vouchers of newly sequenced specimens and the genus Hymenoloma, accepting it in the Seligeriaceae GenBank accession numbers of all used sequences are (Ochyra et al., 2003). compiled in Appendix 1. Laboratory protocol was essen- Since the beginning of molecular phylogenetic stud- tially the same as in previous moss studies, described in ies, the close position of Hymenoloma to the Scouleri- detail by, e.g., Fedosov et al. (2016). aceae and Drummondiaceae was revealed, while Dicra- Sequences were aligned manually in Bioedit (Hall, noweisia was found within Rhabdoweisiaceae (Hedder- 1999). Four dataset were built. The first three of them son et al., 2004; Tsubota et al., 2003, 2004). The most correspond to the individual gene alignments, nad5 (1130 comprehensive molecular phylogenetic studies of the bp), rps4 (568 bp) and trnL (624 bp); they were analyzed genus Hymenoloma by Werner et al. (2013) also sup- separately to check their congruence. The fourth dataset ported a remote position of this genus from Dicranowei- represented concatenated rps4 – nad5 – trnL sequences sia. Their analysis placed Hymenoloma within the strong- (2322 positions). Best-fit substitution models were iden- ly supported clade with Scouleria and Drummondia. tified for each gene separately using Partitionfinder V1.1.1 However, their set did not include any Seligeriaceae. An (Lanfear et al., 2012). Best-scoring Maximum Likelihood important point of this study was the inclusion of H. ant- (ML) trees were estimated using RaxML (Stamatakis, arcticum (Müll. Hal.) Ochyra, because H. nordenskjoel- 2006) from 1000 independent searches each starting from dii, the type of the genus Hymenoloma, was synonymized distinct random trees. Robustness of the nodes was as- with this species by Ochyra et al. (2008a). sessed using the thorough bootstrapping algorithm (Felsen- Subsequent wider analyses of haplolepideous mosses stein, 1985) with 1000 iterations. RaxML was performed constantly resolved Hymenoloma in a clade with Scoule- on the Cipres Science Gateway (http://www.phylo.org/por- riaceae or/and Drummondiaceae (Stech et al., 2012; In- tal2), using RAxML-HPC2 on XSEDE. oue & Tsubota, 2014; Fedosov et al., 2016). However, no Bayesian Analyses (BA) were performed running two taxonomic implications were made so far, thus Hymeno- parallel analyses in MrBayes (Huelsenbeck & Ronquist, loma has been treated either in the Seligeriaceae (Ochyra 2001). For single gene analyses each run consisted of six et al., 2008a, b), or in the Rhabdoweisiaceae (Goffinet et Markov chains and 5,000,000 generations with default al., 2009; Ignatov et al., 2006; Ros et al., 2013), or in number of swaps chains. For rps4 – nad5 – trnL dataset the Oncophoraceae (Frye & Stech, 2009). the analysis consisted of eight Markov chains and In the present paper we revisit the problem, invoking 50.000.000 generations with the number of swaps chains both molecular and morphological data on the genus set to five was performed. A sampling frequency was one Hymenoloma. tree each 10.000 generations, and the chain temperature MATERIAL AND METHODS was set at 0.02 in all analyses. Convergence of each anal- Molecular phylogenetic study The material used in ysis was evaluated using Tracer1.4.1 (Rambaut & Drum- the present study was sampled from MW and MHA and mond, 2007) to check that all ESS values exceeded 200. supplemented by sequences available in GenBank. As Consensus tree were calculated after omitting the first most species of Hymenoloma occur in Antarctic region, 25% trees as burn-in. The combined dataset was sepa- only two of them, H. crispulum and H. mulahaceni rated into eight unlinked partitions respectively: three (Höhn.) Ochyra (= H. intermedium (J.J. Amann) Ochyra) codon positions of rps4 gene, three codon positions for were involved in present study. For molecular study we coding portion of the nad5 gene, the intron in the nad5 used three markers, mitochondrial nad5, chloroplastic gene and trnL-F gene. Analyses were performed on the rps4 and trnL-F regions, commonly used for molecular- Cipres Science Gateway (http://www.phylo.org/portal2), phylogenetic studies at generic and familial levels. The using tool MrBayes 3.2.2 on XSEDE. dataset was compiled with special attention to former Morphological studies Three structures were in the Dicranaceae, Seligeriaceae, and several lineages of pro- main focus of the study: (1) cuticular papillae on the leaf,