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A re-interpretation of the Fabroniaceae, a phylogenetic perspective

Author(s): Paulo E. A. S. Câmara and William R. Buck Source: The Bryologist, 115(1):109-117. 2012. Published By: The American Bryological and Lichenological Society, Inc. DOI: http://dx.doi.org/10.1639/0007-2745-115.1.109 URL: http://www.bioone.org/doi/full/10.1639/0007-2745-115.1.109

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A re-interpretation of the Fabroniaceae, a phylogenetic perspective
ˆ mara1,3 and William R. Buck2 Paulo E. A. S. Ca
1

´lia, Depto de Bota ˆ nica, Campus Universita ´ rio Darcy Ribeiro, Universidade de Brası 2 ´ Brasılia, DF, Brasil; Institute of Systematic Botany, New York Botanical Garden, Bronx, NY 10458-5126, U.S.A.

ABSTRACT. The circumscription of the Fabroniaceae is revisited based on phylogenetic inferences from published rps4 (cpDNA) and nad5 (mtDNA) sequences. Only Ischyrodon forms a clade with Fabronia, a relationship defined by the wavy-walled exothecial cells as a possible synapomorphy. The genus Levierella is nested within the Entodontaceae, Dimerodontium among taxa traditionally associated with Leskeaceae and the position of Rhizofabronia is uncertain. KEYWORDS. Fabronia, Rhizofabronia, Dimerodontium, Levierella, Ischyrodon, Regmatodontaceae, Leskeaceae, rps4, nad5.

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The Fabroniaceae were established by Schimper (1855) to accommodate three genera: Fabronia Raddi, Anacamptodon Brid. and Anisodon Schimp. (5 Clasmatodon Hook. & Wilson). Only Fabronia is still considered a member of the family (Buck & Goffinet 2000; Goffinet & Buck 2004; Goffinet et al. 2009). The Fabroniaceae are well represented in the tropics with few species occurring in the North Temperate Zone. After the establishment of the Fabroniaceae, other genera were transferred into the family. Brotherus (1925) included over 15 genera in four subfamilies, Taoda (1977) reported six genera for Japan and Gao and Fu (2002) recognized 10 genera in China. Buck (1981) listed 25 genera included in or associated with the Fabroniaceae. Buck and Crum (1978) even suggested that the family should be ranked at the ordinal level. A series of studies (Buck 1977, 1980a, 1980b; Buck & Crum 1978; Catcheside Corresponding author’s e-mail: pcamara@unb.br DOI: 10.1639/0007-2745-115.1.109
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¨ s 2003) have placed most of & Stone 1980; Hedena the ‘‘Fabroniaceous’’ genera in other families and Fabroniaceae are currently circumscribed with only five genera: Fabronia, Dimerodontium Mitt., ¨ ll. Hal., Rhizofabronia (Broth.) M. Ischyrodon Mu ¨ ll. Hal. This concept was Fleisch. and Levierella Mu maintained in subsequent classifications (Goffinet & Buck 2004; Goffinet et al. 2009). Fabronia belongs in the Hypnales and is characterized by minute pleurocarpous plants, leaves with smooth, thin-walled laminal cells (rhombic above and quadrate at base) and a slender single costa, with a capsule with wavy-walled exothecial cells and a single peristome (exostomial). The Fabroniaceae were studied in detail in a series of re-interpretation papers (Buck 1980a, 1981; Buck & Crum 1978), but the boundaries of the family are still unclear as it lacks a unique diagnostic trait. According to Buck and Crum (1978: 348) the Fabroniaceae ‘‘cannot be defined, except as a miscellaneous assemblage of unusually slender pleurocarps with erect capsules’’ and the family is
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The Bryologist 115(1), pp. 109–117 Copyright E2012 by The American Bryological and Lichenological Society, Inc.

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‘‘no more than an assortment of left-over genera of uncertain relationships’’. As there has been little taxonomic agreement over the years, a robust phylogeny could help shed some light on the group. Unfortunately phylogenetic studies within the order Hypnales are few and a wellresolved phylogeny is still yet to be achieved. Shaw et al. (2003) suggested that the Hypnales underwent a rapid diversification over a short period of time, leading to some poorly defined lineages and very short deep internal branches and it will likely take large sets of nucleotide data to obtain robust resolution along the phylogenetic backbone of the order (Shaw & Renzaglia 2004). Therefore, it was not the purpose of this study to produce a wellsupported phylogeny for the Hypnales for this demands a much bigger effort. Cox et al. (2010) presented a wide phylogenetic analysis of extant mosses using loci from 3 different genomes including more than 600 genera of mosses and have retrieved the non-monophyletic nature of some families, including the Fabroniaceae. Considering this, many genera would have to be placed in other families and the phylogenetic data could be used as further evidence to better support morphological conclusions and new taxonomic placements. In this study we have reconstructed part of the Cox et al. (2010) phylogeny to address the following question: are the Fabroniaceae monophyletic?, if so, what would be a synapomorphy for the group and if not what would be the best new placement for the genera currently placed in Fabroniaceae?

MATERIALS AND METHODS Taxon and locus sampling. In order to address the familial position of the genera among the Hypnales, at least two taxa from each family within the order were chosen among the exemplars sampled by Cox et al. (2010), for a total of 60 species. The Ptychomniales were chosen as outgroup the based on Buck et al. (2005). For these, the sequences of the gene encoding the ribosomal protein 4 (rps4) in the chloroplast and the NADH-dehydrogenase subunit 5 intron (nad5) in the mitochondrial genome were retrieved from GenBank (Supplementary on-line Table S1). Sequence alignment and analyses. All sequences were initially aligned using Clustal X (Higgins &

Sharp 1988), and alignment then manually adjusted. The alignments were checked again with the coding regions translated to the amino acid level when possible, using MacClade 4.08 (Maddison & Maddison 2000), and exported as Nexus files. Phylogenetic analyses were carried out using maximum parsimony (MP), maximum likelihood (ML), and Bayesian inference (BI) using PAUP* v. 4.0b10 for Macintosh (Swofford 2002), GARLI v. 0951 for Macintosh (Zwickl 2006) and Mr Bayes v. 3.1.2 (Ronquist & Huelsenbeck 2003), respectively. The rps4 and nad5 partions were first analyzed separately to assess congruence and then combined. Heuristic MP searches were done with 100 random addition replicates, and tree-bisection-reconnection (TBR) branch swapping, saving a maximum of 10,000 trees; all characters were unordered and equally weighted, and gaps were treated as missing data. For ML and BI analyses the best-fit model of evolution for each locus and combined matrix was obtained using Modeltest 3.06 (Posada & Crandall 1998) (Table 1). Branch or nodal support was estimated using the non-parametric bootstrap with 1000 replicates for MP and a 100 replicates for ML. BI support was evaluated using posterior probabilities, estimated using Markov Chain Monte Carlo simulations with four chains, each for 53106 generations, sampled every 1000th generations, starting with a random tree. For each run the first 1000 trees were discarded as ‘‘burnin.’’ Shimodaira-Hasegawa test. Even though Cox et al. (2010) retrieved the polyphyletic nature of Fabroniaceae, a Shimodaira-Hasegawa (SH) test (Goldman et al. 2000; Shimodaira & Hasegawa 1999) was performed to statistically compare the alternative hypotheses of monophyly of Fabroniaceae (sensu Goffinet et al. 2009). Constraint trees were constructed in MacClade, then loaded in PAUP* and a maximum likelihood search was done to find the optimal tree given the constraint. The new values were compared with the score of the original best tree using the SH test as implemented in PAUP* using 1000 replicates and under resampling estimated log likelihood (RELL).

RESULTS Our results are congruent with previous phylogenetic reconstructions within Hypnales, with

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Table 1. Tree statistics. CI5 Consistency index; RI5 Retention index. rps4 Taxa included Matrix length Variable sites Parsimony informative sites No. of MP trees Tree length CI RI Model Log. Likelihood of ML tree 60 638 250 143 10000 623 0.522 0.539 TVM+I+G 24234.985294 nad5 60 1150 219 98 10000 311 0.733 0.691 TIM+I+G 23579.279547 Combined 60 1788 463 231 10000 913 0.589 0.532 TVM+I+G 27854.776508

most of the nodes not supportted (below 50% bootstrap). However, as reconstructing a wellsupported phylogeny for Hypnales was not the goal of this paper, the obtained results (Fig. 1) were enough to be used as further evidence for the conclusions presented in this paper. Tree statistics are presented in Table 1. The Shimodaira-Hasegawa test statistically rejected the monophyly of the Fabroniaceae (as circumscribed today), corroborating the Cox et al. (2010) data (Table 2). Only Fabronia and Ischyrodon form a monophyletic unit with good support (above 80% bootstrap). Dimerodontium is not related to Fabronia and is nested, with moderate support (above 70% bootstrap), in a clade with Leskeadelphus, Lindbergia, Pseudoleskeopsis, Pseudoleskeela and Regmatodon, all of which are traditionally placed in the Leskeaceae. Levierella is not related to Fabronia and is nested within the Entodontaceae with good support (above 90% bootstrap). Finally Rhizofabronia is not closely related to Fabronia but its position is still uncertain.

DISCUSSION The phylogeny of the Hypnales is, despite repeated attempts (Cox et al. 2010; De Luna et al. 2000; Merget & Wolf 2010; Tsubota et al. 1999) poorly resolved. The phylogenetic ambiguity may result from a rapid diversification (Shaw et al. 2003), that shortly predated or paralleled the rapid rise of angiosperm-dominated forests (Newton et al. 2007; Wang et al. 2009). The consequence of such rapid diversification is a paucity of fixed mutations within individual genetic regions, and thus insufficient

characters to robustly support deep cladogenic events within the Hypnales. Clearly, extensive sampling of genetic loci is imperative to resolve the relationships among the Hypnales. The Fabroniaceae as circumscribed by Goffinet et al. (2009) are unambiguously polyphyletic. This reflects the broad morphological heterogeneity of the family (Buck and Crum 1978, 1990). The newly defined Fabroniaceae as well as the alternative relationships for several of the genera, as revealed and supported here, are, however, congruent with patterns in variation of morphological characters. Circumscription of the Fabroniaceae. Among the genera currently included in the Fabroniaceae only Ischyrodon is resolved as closely related to Fabronia. These two genera have indeed many similarities (e.g., both have a single costa and paired peristome teeth) and most important, both share wavy-walled exothecial cells (Fig. 2), a characteristic absent in all other genera in the Fabroniaceae in the sensu Goffinet et al. (2009). Fabronia has a worldwide distribution but Ischyrodon is only known from South Africa, Australia and New Zealand. Placement of Levierella. This genus with only two species was known only from Africa and Asia (O’Shea & Matcham 2005), until Delgadillo and ¨ ller Buck (1988) reported it from Mexico. When Mu (1897) erected Levierella within the Fabroniaceae, he recognized that this genus may belong to the Entodontaceae, a hypothesis subsequently endorsed by Brotherus (1909) who transferred Levierella to the Entodontaceae. Chen et al. (1978) retained the genus in the Fabroniaceae based on the presence of a single costa, a feature considered by them as typical of the

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Figure 1. Cladogram of the maximum likely tree inferred from nad5 and rps4. Numbers above branches are bootstrap values and Bayesian posterior probabilities, respectively. Only bootstrap from likelihood is shown and only values above 60 for bootstrap and 0.95 for posterior probabilities are shown. Bold names indicate taxa in the Fabroniaceae according to Goffinet et al. (2009).

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Table 2. Results from SH test for testing the monophyly of Fabroniaceae. Tree Constrained topology Unconstrained topology 2ln L 7956.50960 7855.21957 Diff 2ln L 101.29003 (best) P 0.006*

Fabroniaceae but virtually non-existent in the Entodontaceae. Buck (1980b) followed their concept and ‘‘reluctantly’’ transferred the genus back to the Fabroniaceae. Levierella resembles Fabronia in the ovate to lanceolate leaf shape, plane and serrulate leaf margins and usually single costa, but differs by the much larger plants. The genus also shares some characters with the Entodontaceae, e.g., differentiated alar cells, the upright capsules and the peristome with 16 teeth in 8 pairs. This conflict in putative phylogenetic signal in the morphological characters may explain the difficulty of assigning Levierella to any one family (O’Shea & Matcham 2005). The most problematic character for the placement of Levierella in the Entodontaceae is the presence of a usually single costa. However, the presence of double costae is not atypical of Levierella (O’Shea & Matcham 2005), and the same individual may present both single and double costae. Levierella is here resolved as sister to a clade containing Entodon and Erythrodontium (Fig. 1). Based on the morphology discussed above and as Levierella belongs to a well supported clade that includes the type genus Entodon and no other family, we transfer Levierella back to the Entodontaceae.

Figure 2. Wavy-walled exothecial cells in Fabronia, a putative synapomorphy for a monophyletic Fabroniaceae.

Placement of Dimerodontium. This genus comprises only three species that are restricted to southern South America and South Africa. Dimerodontium was first described by Mitten (1869) and even though it had been placed in the Fabroniaceae for more than a century (Vitt 1984), ˆ mara & Magill (2009) argued that a close affinity Ca to Fabronia is ambiguous based on morphological characters. The genus is characterized by densely foliate plants with entire leaf margins, thick-walled leaf cells, and exothecial cells not wavy-walled. Dimerodontium resembles some taxa currently placed in the Leskeaceae in plant size, leaf shape, lack of differentiated stem and branches leaves, alar cell arrangement, and strong costae. These similarities led Fleischer (1915) to consider a close association of Dimerodontium with Leskea Hedw. The former lacks, however, both paraphyllia and leaf cell papillae. Dimerodontium is here resolved within a clade comprising Leskeadelphus Herzog, Regmatodon Brid., Lindbergia Kindb. and Rhytidium (Sull.) Kindb. All these are taxa traditionally placed in the Leskeaceae (except Rhytidium) despite the fact that they often lack paraphyllia. Dimerodontium fits, however, poorly in the Leskeaceae for it also has smooth laminal cells (and no paraphyllia), but instead resembles ‘‘corticolous Leskeaceae’’ sensu Buck and Crum (1990), which have no paraphyllia, smooth laminal cells, irregular branching plants and erect capsules with the reduced peristomes inserted below the mouth. Gardiner et al. (2005) resolved the Leskeaceae as polyphyletic, comprising at least four different clades. The phylogenetic segregation of the genera matches patterns in variation of morphological characters of the gametophyte, but not of the sporophyte. In order to accommodate some clades, Gardiner et al. (2005) resurrected the family Pseudoleskeaceae Schimp. Ignatov and Ignatova (2004) described the family Pseudoleskeellaceae as another segregate from the Leskeaceae, to accommodate two genera that lack

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paraphyllia: Pseudoleskeella and Iwatsukiella W.R. Buck & H.A. Crum. Lacking paraphyllia, Dimerodontium also fits in the brief Latin diagnosis of the Pseudoleskellaceae (‘‘A Leskeaceae paraphyllis nullis differt’’) provided by Ignatov and Ignatova (2004). Dimerodontium and Pseudoleskeella are in the same clade, and the relationship has moderate support. However, Dimerodontium could just as easily be a member of Regmatodontaceae, as a member of the clade with Regmatodon that has moderate support. Furthermore this family has priority over the Pseudoleskeellaceae. Dimerodontium belongs to a clade of Leskeaceae sensu lato but its placement may be revised pending a resolution of the circumscription of the Leskeaceae and its segregates. Placement of Rhizofabronia. Rhizofabronia includes three species and one variety from tropical Africa, the Comoros and China. It was described as a section of Fabronia and later raised to the generic level by Fleischer (1923). It is charcaterized by highly reduced gametophytes and sporophytes (e.g., no peristome). Rhizofabronia resembles Fabronia in leaf shape, the presence of thin-walled cells and a single costa. However, the present phylogenetic inference does not support a recent common ancestry of these genera, and the affinities of Rhizofabronia presented here are ambiguous. The genus is resolved sister to a clade comprising Henicodium, Vesicularia and Ectropothecium, but the monophyly of this lineage is not supported. ¨ s (2001, 2002) considered Pedersen and Hedena Rhizofabronia as a member of the Plagiotheciaceae. Morphological and cpDNA characters supported the monophyly of the genus, which together with Isopterygiopsis is sister to the OrthotheciumPlagiothecium clade. According to Pedersen and ¨ s (2002), the only synapomorphy for Hedena Isopterygiopsis and Rhizofabronia (as sister taxa) are elongate median lamina cells in the stem leaves, short setae, short exothecial cells, and at most two cilia between two endostome processes. Cox et al. (2010) resolved Rhizofabronia within a well supported clade containing the Rutenbergiaceae plus Trachyloma. However, as the morphology of this genus is still poorly known and its placement still dubious we suggest its retention in the Plagiotheciaceae, at least until more data are gathered.

The relative importance and use of gametophytic morphological characters. Most of the earlier worldwide classifications of mosses were influenced by pre-existing European classifications. As more plants were collected in tropical areas, they were placed into these previously described families (mostly from Europe). This procedure has consequently stretched familial concepts and often generated polyphyletic groups. Later classifications in mosses were influenced by the idea that sporophyte characters are less subject to natural selection than the gametophytic ones (Crosby 1974), and therefore are of more significance in phylogenetic reconstruction. This has often led to overlooking the importance of the gametophyte characters (Buck 2007). Phylogenetic reconstruction, using molecular markers, has brought new insights and re-evaluations of this question, revealing that molecular data often show a better correspondence with gametophyte characters ˆ mara 2006; Gardiner than with sporophyte ones (Ca et al. 2005; Huttunen et al. 2004). That is certainly the case of Fabroniaceae: a family that has been traditionally defined by sporophyte features.

ACKNOWLEDGMENTS
The authors thank Bruce Allen, Elizabeth Kellogg, Peter Stevens and Daniel Vital. We are deeply grateful to Angela Newton for her comments that much improved this manuscript. This manuscript was also greatly improved by comments from Bernard Goffinet and two annonymous reviewers. Paulo ˆ mara is thankful to CAPES, the Brazilian government. Ca

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ms received Oct. 10, 2010; accepted Jan. 8, 2012.

Appendix 1. List of GenBank accession numbers for the rps4 and nad5 locus for taxa included in the phylogenetic analysis.
Abietinella abietina: AY907953/AY908386; Acroporium pungens: AY908207/AY908539; Amblystegium fluviatile/AF469808/–––; Anacamptodon splachnoides/AF143031/AY908419; Anomodon rugelii/AF143023/–––; Brachythecium

novae-angliae: AY908308/AY908523; Brotherella recurvans: AY908227/AY908470; Claopodium whippleanum: AY908294/AY908746; Clasmatodon parvulus: AY663329/AY908519; Cryphaea patens: AY908184/AY908695; Cyptodon muelleri: AY908586/ AY908686: Cyrto-hypnum schistocalyx: AY908336/ AY908396: Dimerodontium balansae: AY907952/ AY908409; Ectropothecium leptochaeton: AY908558/ AY908405; Entodon hampeanus: DQ467882/ AY908767; Entodontopsis leucostega: AY908295/ AY908501; Erythrodontium longisetum: AY908256/ AY908527; Fabronia pusilla: AY908199/AY908754; Felipponea montevidensis: AY908576/AY908714; Floribundaria aurea: AY306910/AY908724; Garovaglia elegans: AY631145.1/DQ200893.1; Haplocladium virginianum: AF143040/AY908401; Helicodontium capillare: AF143043/AY908516; Henicodium geniculatum: AF14301/AY908691; Herpetineuron toccoae: AY908566/AY908638; Hildebrandtiella endotrichelloides: AY306925/ AY908702; Homalothecium sericeum: DQ294319/ AY908521; Hookeria lucens: AJ269689/AY908489; Hylocomiopsis cylindricarpa: AY908342/AY908394; Hypnum cupressiforme: AJ269690/AY908444; Ischyrodon lepturus: AY908591/AY908755; Lembophyllum divulsum: AY306936/AY908656; Lescuraea radicosa: AY908326/AY908737; Leskea gracilescens: AY908343/–––; Leskea polycarpa: –––/ DQ098682; Leskeella nervosa: AY908325/AY908414; Leskeadelphus bolivianus: AY907948/AY908411; Leucodon sciuroides: AY908186/AY908716; Levierella fabroniacea: AY907961/AY908528; Lindbergia brachyptera: AY907949/AY908412; Meteorium illecebrum: AY908187/AY908733; Neckeropsis disticha: AF143010/AY908675; Neckera pennata: AY908265/AY908652; Orthostichella pentasticha: AY907962/AY908655; Papillaria nigrescens: AY306968/–––; Plagiothecium cavifolium: AY908321/ AY908763; Pseudoleskeella tectorum: AY907950/ AY908416; Pseudoleskeopsis imbricata: AY908582/ AY908410; Pseudotaxiphyllum elegans: AY908578/ AY908753; Pseudoleskea andina: AY908257/ AY908410; Pterobryon densum: AF143013/AY908693; Ptychodium plicatum: AY908327/AY908735; Ptychomnion aciculare: AY306983.1/DQ200900.1; Pylaisia speciosa: AY908555/AY908475; Pylaisiadelpha tenuirostris: AF143053/AY908547;

ˆ mara & Buck: Phylogenetic circumscription of Fabroniaceae Ca

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Regmatodon declinatus: AY908191.1/AY908413.1; Rhizofabronia persoonii: AY908607/AY908765; Rhizofabronia sphaerocarpa: AF469838/–––; Rigodiadelphus robustus: AY908569/AY908736; Schoenobryum concavifolium: AY908580/AY908697; Schwetschkea grateloupii: AY908305/AY908509; Schwetschkeopsis fabronia: AF143041/AY908743;

Sematophyllum demissum: AF143055/AY908479; Stereophyllum radiculosum: AF469846/AY908750; Taxithelium planum: AF143054/AY908549; Thelia lescurii: AF143024/AY908745; Thuidium delicatulum: AF143039/AY908398; Trichosteleum papillosum: AF143056/AY908541; Vesicularia vesicularis: AY908559/AY908406