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The Phylogeny of Basal Peristomate : Evidence from cpDNA, and Implications for Peristome Evolution Author(s): Zacharia L. K. Magombo Source: Systematic , Vol. 28, No. 1 (Jan. - Mar., 2003), pp. 24-38 Published by: American Society of Taxonomists Stable URL: http://www.jstor.org/stable/3093935 Accessed: 17/11/2010 09:04

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http://www.jstor.org Systematic Botany (2003), 28(1): pp. 24-38 ? Copyright 2003 by the American Society of Plant Taxonomists

The Phylogeny of Basal Peristomate Mosses: Evidence from cpDNA, and Implications for Peristome Evolution

ZACHARIA L. K. MAGOMBO Missouri Botanical Garden, P.O.Box 299, St. Louis, Missouri 63166-0299 [[email protected]]

CommunicatingEditor: Alan T. Whittemore

ABSTRACT. Cladisticanalyses based on chloroplastprotein coding genes rbcLand rps4,and the chloroplastencoded trnL (UAA) intron were conducted(1) to investigatephylogenetic relationships among basal peristomatemosses, especiallythe nematodontousmosses (Tetraphidaceaeand ),and the arthrodontousmosses with pleatedendostomes (Bux- baumiaceaeand Diphysciaceae),and (2) to make inferenceson evolutionof the peristome.A combineddata matrix included 46 taxa and 2206 charactersof which 619 were parsimonyinformative. The resultsindicate that the basalperistomate mosses, particularlythe ,Polytrichaceae and Buxbaumiaceae,are paraphyletic.Sister group relationshipsbetween the following taxa are newly suggested:Tetraphidaceae and all peristomatemosses; Polytrichaceaeand the clade consistingof Buxbaumiaceae,Diphysciaceae, diplolepideous and haplolepideousmosses; Buxbaumiaceaeand the clade consistingof Di- physciaceae,diplolepideous and haplolepideousmosses. The following novel inferenceson peristome evolution are also suggested:the plesiomorphiccondition of the endostomeof the arthrodontousperistome was pleated;the pleatedendostome has been transformedinto a keeled endostomein the diplolepideous/haplolepideousclade; the similarityin cell divisions precedingdeposition of secondaryperistomial wall materialin peristomedevelopment is a synapomorphyin the peristomate mosses. The exostomehas been independentlylost or reducedin the Diphysciaceae,and the diplolepideous/haplolepideous clade.

The early diverging lineages of land include 1915; Dixon 1932; Philibert see Taylor 1962; Crosby a paraphyletic assemblage known as -liv- 1974, 1980; Buck 1980, 1991;Crum and Anderson 1981; erworts, and mosses (Mishler and Churchill Vitt 1984; Vitt et al. 1998) although gametophytic fea- 1984;Mishler et al. 1994;Kenrick and Crane 1997;Hed- tures were emphasized in a few classifications (Schim- derson et al. 1996, 1998; Garbary and Renzaglia 1998; per 1855; Mitten 1859; Brotherus 1909; Saito 1975; Nishiyama and Kato 1999; Goffinet 2000). While some Crundwell 1979; Buck and Crum 1990). In a recent studies suggest a sister group relationship between classification scheme (Buck and Goffinet 2000), mor- mosses and tracheophytes (Mishler and Churchill phological as well as molecular data (where available) 1984; Mishler et al. 1994; Kenrickand Crane 1997), oth- were used. er studies suggest a sister group relationship between Based on developmental patterns peristomes can be mosses and liverworts (Hedderson et al. 1996, 1998; classified as nematodontous or arthrodontous. Mature Garbary and Renzaglia 1998; Nishiyama and Kato nematodontous peristomes are formed from multiple 1999; Goffinet 2000). Among the bryophytes, mosses layers of whole cells whereas arthrodontous peri- are the most species rich, encompass great morpholog- stomes are typically formed from cell wall remnants ical diversity, and most of them possess a peristome. (Blomquist and Robertson 1941; Philibert, see Taylor A peristome is a uniquely derived structure that sur- 1962; Dixon 1932; Edwards 1984; Shaw and Robinson rounds the mouth of the capsule and appears to 1984; Shaw and Rohrer 1984; Vitt 1981, 1984; Shaw et influence release of spores from the capsule; its precise al. 1987, 1989b; Schwartz 1991, 1994). Nematodontous mode of action is poorly understood and may vary peristomes are found in two groups, Tetraphidaceae widely among mosses (Goebel 1895; Steinbrinck1897; and Polytrichaceaewhile arthrodontous peristomes oc- Lazarenko 1957; Ingold 1959; Pais 1964; Vitt 1981; Ko- cur in the majority of extant taxa. ponen 1982; Mueller 1973; Mueller and Neumann Almost all arthrodontous peristomes are formed 1988). Usually, peristomes are present as 2n teeth (i.e., from the three innermost concentric layers of cells of 4, 8, 16, 32, or 64), arranged in a single or double (rare- the amphithecium: (i) outer peristomial ly multiple) row(s) around the capsule mouth. layer (OPL), (ii) primary peristomial layer (PPL), and Since Philibert's (see Taylor 1962) late nineteenth (iii) inner peristomial layer (IPL) (Blomquist and Rob- century classic studies on moss peristomes, sporo- ertson 1941) (Fig. 1). Arthrodontous peristomes may phytic features (particularly peristomes) have been be diplolepideous or haplolepideous. In diplolepideous considered the most important indicators of phyloge- mosses those parts of the peristome formed from cell netic relationships among mosses. As a result, most wall remnants of OPL and PPL cells are called the ex- classification systems were based on peristome struc- ostome while those formed from cell wall remnants of ture (Braithwaite 1887; Brotherus 1924, 1925; Bridel- PPL and IPL cells are called the endostome. In haplo- Brideri 1826, 1827; Grout 1936; Fleischer 1904, 1906, lepideous mosses typically only the PPL and IPL cells

24 2003] MAGOMBO:PHYLOGENY OF BASAL PERISTOMATEMOSSES 25

A B

FIG. 1. Arthrodontous peristome at maturity showing peristomial layers of the amphithecium involved in its development (one eight of transverse sections of peristomial layers are represented). OPL = Outer peristomial layer. PPL = Primary peri- stomial layer. IPL = Inner peristomial layer. A. Haplolepideous peristome. The OPL:PPL:IPLcell ratio is 4:2:3. Fine lines cor- respond to cell walls that will be reabsorbed in latest stages of development. Shaded areas represent cell wall thickening. Note that on its inner surface each endostome segment is composed of one and a half cell. B. Typical diplolepideous peristome in which the exostome and endostome segments alternate. Note that due to additional cells divisions in the IPL, at one eight of the amphithecium, the OPL:PPL:IPLcell ratio is 4:2:6.Note also development of cilia in between the endostome segments. Fine lines correspond to cell walls that will be reabsorbedin latest stages of development. Shaded areas representcell wall thickening.

contribute to the peristome and these are simply called astome (Edwards 1984). Homology between para- peristome teeth. stome associated with peristome in Buxbaumiaceae The endostome of a diplolepideous moss typically and the nematodontous peristome of Polytrichaceae consists of a basal membrane upon which are 16 seg- was suggested based on similarity in position, and ments that are usually alternating in position with the structure (Philibert see Taylor 1962; Edwards 1984). exostome teeth. These segments are usually keeled and However, the suggested homology was dismissed by perforated. Alternating on the basal membrane with Shaw et al. (1987) who argued that in terms of posi- the segments are cilia in groups of one to four. The tion, the parastome of Buxbaumiawas comparable to cilia are lacking in some diplolepideous mosses such preperistomes that occur external to the exostome the and Orthotrichacales(Buck and Goffinet teeth in many diplolepideous mosses. Furthermore 2000). they considered that the thick walled structure of the In haplolepideous mosses the peristome may have parastome cells might be related to the apparent func- individual free teeth, sometimes divided into filaments tion of the parastome to separate the operculum from or fused into a tube with or without free filaments at the urn (Shaw et al. 1987). On the other hand, Vitt its apex (Buck and Goffinet 2000). Arthrodontous peri- (1984) argued that although the peristomes in the Bux- stomes exhibit many varied features but they are all baumiaceae were highly complex they could be inter- made of cell wall remnants either on the OPL,PPL and preted as diplolepideous. IPL (diplolepideous) or the PPL and IPL (haplolepi- The Diphysciaceae also have pleated endostomes deous). Peristome teeth of haplolepideous mosses and but the parastome is absent, and exostomes are absent endostomes of diplolepideous mosses are homologous or rudimentary (Shaw et al. 1987). Monophyly and a on the basis of relative position, i.e., both are formed close relationship of the Buxbaumiaceae and the Di- from cell wall remnants from the PPL and IPL cells. physciaceae have usually been assumed on the basis Peristomes in the Buxbaumiaceae(Crosby 1980; Ed- of pleated endostomes, and they were therefore placed wards 1984; Vitt 1984) and the Diphysciaceae (Shaw et in the same taxonomic groups-order Buxbaumiales al. 1987) are arthrodontous as they are formed princi- (Brotherus 1925), suborder Buxbaumiineae (Vitt 1984), pally from cell wall remnants. However, the peristome or subclass Buxbaumiidae (Crosby 1980; Crum and structure in the Buxbaumiaceaeand the Diphysciaceae Anderson 1981; Norris 1994). Developmental studies of is unique in that the endostome forms a cone-like the peristome in Diphysciumfoliosumindicated no sim- pleated membrane not divided into teeth, segments or ilarity to nematodontous mosses but exhibited features cilia. In the Buxbaumiaceae there are one or more lay- that are typically haplolepideous (Shaw et al. 1987). ers of exostome teeth usually adhering to the endo- Views on relationships of moss groups and evolu- stome (Edwards 1984). External to the exostome in the tionary trends of moss peristomes are currently un- Buxbaumiaceaeis a layer of thick-walled cells forming dergoing massive revision with use of phylogenetic a pseudoannulus (Grout 1903) also known as a par- methods and molecular data, thereby increasing our 26 SYSTEMATIC BOTANY [Volume 28 understanding of evolution of the peristome (Vitt et al. to the clade consisting of diplolepideous and haplole- 1998; Beckert et al. 1999; Goffinet et al. 1998, 1999; pideous mosses. As a result the plesiomorphic condi- Newton et al. 2000; Cox et al. 2000; Goffinet and Cox tion of the arthrodontous peristome is ambiguous. 2000; La Farge et al. 2000; Goffinet et al. 2001). For This study assesses phylogenetic relationships example, recent studies based on molecular data (Vitt among basal peristomate moss groups, with emphasis et al. 1998; Beckert et al. 1999; Newton et al. 2000; Gof- on the nematodontous mosses and arthrodontous finet et al. 2001) have supported a hypothesis sug- mosses with pleated endostomes. The following ques- gested by Crosby (1980) that the haplolepideous moss- tions are specifically addressed: (1) what are the phy- es were derived from diplolepideous ancestors. logenetic relationships among the basal peristomate However, sister group relationships among the ne- moss groups i.e., nematodontous mosses (Tetraphida- matodontous mosses (Tetraphidaceaeand Polytricha- ceae and Polytrichaceae),and the arthrodontous moss- ceae), and the arthrodontous mosses with pleated en- es with pleated endostomes (Buxbaumiaceae and Di- dostomes (Buxbaumiaceae and Diphysciaceae) remain physciaceae)? (2) what inferences can be made on the controversial due to: (i) ambiguous or incongruent re- evolution of the peristome structure? sults from phylogenetic analyses; and (ii) a lack of on- togenetic data for some critical taxa making inferences MATERIALSAND METHODS about homologous features difficult. For example, the Taxonand Character and In Buxbaumiaceae and the Diphysciaceae have been Sampling, Fieldwork. this study classificationof mosses follows Buckand Goffinet(2000) who di- placed among nematodontous mosses because of close vided the peristomatemosses into two classes,Polytrichopsida for relationships suggested by 18S gene data (Vitt et al. nematodontousmosses and Bryopsidafor arthrodontousmosses. 1998). On the other hand, a sister group relationship The Polytrichopsidainclude two orders: (i) Tetraphidaleswith three families-the Tetraphidaceae,Oedipodiaceae, and Buxbau- between the Diphysciaceae and the clade consisting of miaceae;and (ii) Polytrichaleswith one family the Polytrichaceae. the diplolepideous and haplolepideous mosses has The class Bryopsidais divided into four subclasses:Diphysciidae, been suggested based on mitochondrial (Beckertet al. ,, and .The Diphysciaceaeare the in the subclass other arthrodontous nuclear and DNA only family Diphysciidae; 1999), chloroplast sequences (New- mosses were placed among the remainingthree subclasses.This ton et al. 2000). In recent analyses of rps4 sequence classificationguided choice of taxa for this study. Representative data (Goffinet et al. 2001) the Diphysciaceae are either taxa were chosen fromboth ordersof nematodontousmosses (i.e., and nested within the mosses or are sister Tetraphidalesand Polytrichales), from all four subclasses of haplolepideous the arthrodontousmosses (i.e., Diphysciaciidae,Funariidae, Di- to a clade of diplolepideous and haplolepideous moss- cranidaeand Bryidae)(Table 1). The sampled species included: es. A sister group relationship between the Buxbau- one of Oedipodiaceae,three of Tetraphidaceae,six of Polytricha- three of Buxbaumiaceae,12 of nine of miaceae and nematodontous mosses has been sug- ceae, Diphysciaceae, hap- lolepideous mosses and 14 of diplolepideousmosses (Table1). gested, with the Buxbaumiaceae sister either to the Te- Two species of Sphagnaceaeand threeof Andreaeaceaewere sam- traphidaceae (Hyvonen et al. 1998; Newton et al. 2000) pled and used as outgroups (Table1) following Beckertet al. or the Polytrichaceae (Goffinet et al. 2001). Further- (1999)and Newton et al. (2000). DNA sequences were assembled from the chloroplastprotein more Goffinet et al. (2001) concluded that the nema- coding genes rbcLand rps4,and from the chloroplastencoded trnL todontous mosses and Buxbaumiaceae formed a (UAA) intron. Specimenswere sampled from the herbariumat monophyletic lineage. MissouriBotanical Garden (MO) or collectedduring fieldworkin South America Boliviaand the Ca- studies thus the inferences that (Chile,Argentina, Suriname); Previous support ribbean Region (Puerto Rico); North America (United States of (1) the non-peristomate moss groups Sphagnaceae, America,Canada); and Asia (Sri Lanka,Viet Nam, ,Singa- and Oedipodiaceae are basal to all per- pore, and Indonesia).A few sequencesfor some of the taxa were all taxa are the has thus from GenBank(Table 1). Vouchersof depositedin the istomate mosses; peristome originated herbariumof the MissouriBotanical Garden (MO). once; (2) nematodontous mosses (Tetraphidaceaeand DNA Extraction,PCR (PolymeraseChain Reaction) and Se- Polytrichaceae) are basal in the peristomate clade; (3) quencingProtocols. Herbariumspecimens for DNA extraction were selected on abundanceof in the and the haplolepideous and diplolepideous mosses form a depending plants packet the condition of the sample, with a preferencefor recently col- clade and (4) haplolepideous mosses were derived lected samples.For collectionsconsisting exclusively or primarily from diplolepideous ancestors. Previous studies do not of ,two to five stem tips were sampled;for fruiting resolve the position of the mosses with pleated endo- specimensone to two capsuleswere used for DNA extraction. DNA extractionprotocols used were those of Doyle and Doyle stomes (Buxbaumiaceae and Diphysciaceae). Sister (1987, 1990) or the DNeasy Plant Kit (Qiagen,Chatsworth, CA). group relationships between the nematodontous moss- Amplification(PCR) of rbcL,trnL (UAA) intron,and rps4regions es and the arthrodontous mosses with pleated endo- and sequencingreactions were performedusing primersequences in 2. The rbcL was the M007F and remain given Table gene amplifiedusing stomes (Buxbaumiaceae Diphysciaceae) and M1390Rprimers and was sequencedusing Z1F,427F, 997F, unclear. The Buxbaumiaceae, Tetraphidaceae and Po- M665F,295R, M745R, 678R, 1081R and M1390R.The rps5 and trns lytrichaceae may form a monophyletic group or the (rps4),and trnC and tmD (trnL)primers were used for both am- and of the and the trnLintron Buxbaumiaceae are either sister to the Tetraphidaceae plification sequencing rps4 gene respectively.The PCRreactions were performedin 50plI reaction or the Polytrichaceae.The Diphysciaceae may be nest- volumes containing10X thermostable PCR buffer, 2.5 mM MgCl2, ed within the haplolepideous mosses or may be sister 0.2 mM dNTPs in equimolarratio, 1 unit 7TaqPolymerase (Pro- 2003] MAGOMBO:PHYLOGENY OF BASAL PERISTOMATEMOSSES 27

TABLE 1. List of taxa for which sequencedata was assembled.Taxon, voucher reference and GenBank(GB) accession numbers aw given. The accessionnumbers in bold were from the GenBank.Classification follows Buck & Goffinet(2000). Citation of authorsfor scientificnames follows Brummitt& Powell (1992).

Sphagnopsida. Sphagnales. Sphagnaceae. Sphagnumcuspidatum C. Mull. (Magombo 6015; rbcLAF478201, rps4 AF478246, trnL AF478292). Sphagnumpalustre L. (GB; rbcLAF231887, rps4 AF231892, trnL AF231902). Andreaeopsida. Andreaeales. Andreaeaceae. Andreaeanitida J. D. Hook.f. & Wilson (Churchill 19834, rbcLAF478198, rps4 AF478247, trnL AF478293).Andreaea rothii F Weber & D.Mohr (Magombo 6045, rbcLAF478200, rps4 AF478249, trnL AF478295).Andreaea rupestris Hedw. (Magombo 5644; rbcLAF478199, rps4 AF478248, trnL AF478294). Polytrichopsida. Tetraphidales.Tetraphidaceae. Tetraphis geniculata Girg. ex Milde (Magombo 6031; rbcLAF478204, rps4 AF478250, trnL AF478296). Tetraphispellucida Hedw. (Magombo 6057; rbcLAF478203, rps4 AF478251, trnL AF478297). Tetro dontiumbrownianum (Dicks.) Schwagr. (Magombo 6056; rbcLAF478205, rps4 AF478252, trnL AF478298). Buxbaumiaceae. aphylla Hedw. (GB/Magombo 6025; rbcLAF478212, rps4 AF231897, trnL AF478299). Buxbaunlz piperiBest (Magombo 6065; rbcLAF478211, rps4 AF478254, trnL AF478301). Buxbaumiaviridis (DC. in Lamarck & A. I' de Candolle) Moug. & Nestl. (Steve s.n.; rbcLAF478210, rps4 AF478253, trnL AF478300). Oedipodiaceae. Oedipodiumgriffithianum (Dicks.) Schwagr. (GB/Schofield & Talbot 98670; rbcLAF478202, rps4 AF306968, trnL AF478314). Polytrichales.Polytrichaceae. altecristatum (Renauld & Cardot) Ireland (Magombo 5633; rbcLAF478209, rps4 AF478256, trnL AF478315). Dawsoniapapuana Mull. Hal. ex SchliephackeGeheeb (GB; rbcLAF208410, rps4 AF208419, trnL AF246704).Notoligotrichum trichodon (J. D. Hook.f. & Wilson in Wilson) G. L. Sm. (Ramirez 11767; rbcLAF478208, rps4 AF478260, trnL AF478319). perichaetiale (Mont.) A. Jaeger (Magombo 5897; rbcLAF478206, rps4 AF478258, trnLAF478318). Polytrichadelphus aristatus (Hampe) Mitt. (Magombo 5692; rbcLAF478207, rps4 AF478257, trnL AF478316). Polytrichumcommune Hedw. (GB/Allen 21784; rbcLU87087, rps4 AF478259, trnL AF478317). . Diphysciales (Subclass Diphysciidae). Diphysciaceae. Diphysciumchiapense D.H. Norris (Holz CR-00-0692;rbcl AF478216, rps4 AF478265, trnL AF478304). Diphysciumfasciculatum Mitt. (Magombo 6330; rbcLAF478219, rps4 AF478270, trnL AF478308). Diphysciumfoliosum (Hedw.) D. Mohr (Magombo 5854; rbcLAF478220, rps4 AF478264, trnL AF478303). Diphysciumfulvifolium Mitt. (Deguchi 34983; rbcLAF478222, rps4 AF478266, trnL AF478310). Diphysciumlongifolium Griff (Magombo 5787; rbcLAF478217, rps4 AF478271, trnL AF478305). mucronifolium Mitt. (Reese 18545; rbcL AF478221, rps4 AF478267, trnL AF478302).Diphyscium perminutum Takaki (Ohya 35783; rbcLAF478215, rps4 AF478263, trnLAF478306). Diphysciumsatoi Tuzibe (Nishimura 10779; rbcLAF478223, rps4 AF478269, trnL AF478307). Diphyscium suzukii Z. Iwats. (Suzuki 35782; rbcLAF478218, rps4 AF478268, trnL AF478309).Muscoflorschuetzia pilmaiquen (Crosby) Cros by (Magombo 5982; rbcLAF478224, rps4 AF478272, trnLAF478311). Theriotiakashmirensis H. Rob. (Deguchi 35778; rbcL AF478214, rps4 AF478261, trnLAF478313). Theriotialorifolia Cardot (Itouga 3455; rbcLAF478213, rps4 AF478262, trnL AF478312). (Subclass Bryidae). Bartramiaceae.Leiomella bartramioides (Hook.) Paris (Magombo 5880; rbcLAF478238, rps4 AF478284, trnL AF478328). andina (Mitt.) Jaeger (Magombo 5729; rbcLAF478240, rps4 AF478276, trnL AF478337). Bryaceae.Bryum caespiticium Hedw. (Smith 3411; rbcLAF478245, rps4 AF478281, trnLAF478322). Rosulabryumbillarderii (Schwagr.)J. R. Spence (Lanares & Munoz 19423; rbcLAF478233, rps4 AF478288, trnL AF478335). Rhodobryumontar- iense (Kindb.) Paris in Kindberg (Allen 21531; rbcLAF478243). Mniaceae. Rhizomniumpunctatum (Hedw.) T. J. Kop. (Magombo 5627; rbcLAF478237, rps4 AF478290, trnL AF478321). Splachnales (Subclass Bryidae). Splachnaceae.Brachymitrion moritzianum (C. Miill.) A. K. Kop. (Dauphin 1959; rbcL AF478235, trnL AF478323). (Subclass Bryidae). . Hedwigiaciliata (Hedw.) P. Beauv. (Allen 20947; rbcLAF478234, rps4 AF478289, trnL AF478336). Funariales (Subclass Funariidae). .Neosharpiella aztecorum H. Rob. & Delgad. (Allen 12961; rbcLAF478244). Timmiales (Subclass Funariidae). Timmiaceae. Timmiamegapolitana Hedw. (Allen 10511; rbcLAF478242, rps4 AF478287, trnL AF478320). Timmiasibirica Lindb. & Arnell (GB; rbcLAJ275166, rps4 AF023775, trnL AF023715). (Subclass Funariidae). . intermedia Jur. (Shevock 17052; rbcLAF478241, rps4 AF478291, trnL AF478326). Encalyptaprocera Bruch (GB/Magombo 5649; rbcLAF005548, rps4 AF478286, trnL AF478324). Encalypta streptocarpaHedw. (Stebel M-29; rbcLAF478239, rps4 AF478282, trnL AF478325). (Subclass Dicranidae). . laevigata (Brid.) Brid. (Darigo 2589; rbcLAF478230, rps4 AF478283, trnL AF478334). Seligeriales (Subclass Dicranidae). .Blindia magellanica Schimp. in C. Muller (Ramirez 9798; rbcLAF478232, rps4 AF478278, trnL AF478329). (Subclass Dicranidae). . scoparium Hedw. (GB/Casado & Allen 303a; rbcLAF478226, rps4 AF478280, trnL AF234159). Dicnemonaceae. Dicnemonsemicryptum C. Mull. (Frahm 28-1; rbcLAF478228, rps4 AF478274, trnL AF478331). Dicnemon seriatum(Broth. & Paris) B.H. Allen (Werf& McPherson 15982; rbcLAF478229, rps4 AF478277, trnL AF478332). .Dicranowesia cirrata (Hedw.) Lindb. in Milde (Darigo 3164; rbcLAF478227, rps4 AF478279, trnL AF478333). (Subclas Dicranidae). . Barbulaconvoluta Hedw. (Si He s.n.; rbcLAF478225, rps4 AF478273, trnL AF478327). Streptopogoncalymperes C. Mull. ex Geheeb (Magombo 5695; rbcLAF478231, rps4 AF478285, trnL AF478330) Timmiellacrassinervis (Hampe) L.F.Koch (Janeway5514; rbcLAF478236, rps4 AF478275, trnLAF478338). 00

= TABLE 2. Oligonucleotideprimers used to amplify and sequencethe rbcL,rps4 and trnL (UAA) intron genes. Primersequences, direction and authorreferences are given. (Mishler Prof.B. D. Mishler,Department of IntegrativeBiology, University of California,Berkeley).

Primer Sequence Direction Reference rbcL Z1 5'-ATG TCA CCA CAA ACA GAA ACT AAA GCA AGT-3' Forward Wolf et al. 1994 M007F 5'-CCA CAA ACG GAG ACT AAA GC-3' Forward Mishler, personal communication 427F 5'-GCT TAT TCA AAA TTC CAA GGC CCG CC-3' Forward Goffinet et al. 1998

997F 5'-GGT AAA CTT GAA GGA GAA CG-3' Forward Goffinet et al. 1998 u) M665F 5'-GGA GAG ATC GTT TCG TAT TTG TAG C-3' Forward Mishler, personal communication 'Si mHI 295R 5'-CTA ATG GGT AAG CAA CAT AAG C-3' Reverse Goffinet et al. 1998 M745R 5'-CTT CAC AWGTAC CTG CRG TAG C-3' Reverse Lewis et al. 1997 I TTG TGC TTT ATA Reverse Goffinet et al. 1998 678R 5'-GAT TTC GCC TGT TTC GGC AA-3' 0 H rbcL H 1081R 5'-CCC AGT CTT GAG TGA AGTAAA TAC C-3' Reverse Goffinet et al. 1998. M1390R 5'-CTT TCC AAA TTT CAC AAG CAG CAG-3' Reverse Lewis et al. 1997 rps4 rps5 5'-ATG TCC CGT TAT CGA GGA CCT-3' Forward Souza-Chies et al. 1997 trns 5'-TAC CGA GGGTTC GAA TC-3' Reverse Souza-Chies et al. 1997 trnL trnC 5'-CGA AAT CGG TAG ACG CTA CG-3' Forward Taberlet et al. 1991 trnD 5'-GGG GAT AGA GGGACT TGA AC-3' Reverse Taberlet et al. 1991

S-;I CDC EQ 2003] MAGOMBO:PHYLOGENY OF BASAL PERISTOMATEMOSSES 29

TABLE 3. Tree and characterstatistics from the phylogeneticanalyses of differentdata partitions.The following abbreviationsrefer to the columns:Total Char. = total number of characters;Inform. = number of parsimonyinformative characters; CI = consistency index;RI = retentionindex; HI = homoplasyindex; gl = gl statistics;TL = tree length;MPTs = numberof most parsimonioustrees; ILD = P value of incongruencelength differencetest. Only parsimonyinformative characters were used in the analyses.

Data partition Total Char. Inform. CI RI HI TL MPTs gl ILD rbcL+ rps4 + trnL 2206 619 0.3995 0.6677 0.6005 2213 6 -0.4828 rbcL+ rps4 1959 545 0.3985 0.6651 0.6015 1950 2 -0.4859 0.058 rbcL+ trnL 1626 410 0.4032 0.6891 0.5968 1416 18 -0.4935 0.0498 rps4 + trnL 827 283 0.4371 0.6765 0.5629 934 36 -0.5361 0.061 rbcL 1379 336 0.392 0.6869 0.608 1171 24 -0.4917 rps4 580 209 0.4555 0.676 0.5445 764 2348 -0.5172 trnL 247 74 0.4735 0.7601 0.5265 226 6604 -0.5259

mega), 0.5mMeach primerand 1-2 (1(approximately 2-30 ng) of ferencetest (ILD)(Farris et al. 1994),implemented as the partition templateDNA. 1,Il of 5%freshly made DMSO(Dimethyl Sulfox- homogeneitytest in PAUP4.0b2 (Swofford1999), was performed, ide) and 1l1 of BSA (Bovine Serum Albumin Acetylated)were using 500 replicates,equally weighted characters,gaps treatedas added to PCR tubes. The PCR reactionswere performedusing missing, 5 additionrandom replicates, and TBRbranch swapping. PiltierThermal Cycler (PTC-200) under the following conditions: Finally,a non-parametricWilcoxon sign ranks test (Siegel 1956) 35 cycles of 94(C for 1 minute,55(C for 2 minutes,and 72(Cfor 3 was used as proposed by Templeton(1983). Only parsimonyin- minutes. After 35 cycles a final extension at 72(C for 10 minutes formativecharacters were used in all analysestesting congruence was performed,and reactionswere held at 4(C until furtherpro- between data partitions(Cunningham 1997). cessing. PCRreactions were precededby a hot start at 97(C for 4 minutes and Taqpolymerase was added at the end of the 4thmi- nute. RESULTS PCRproducts were cleaned and concentratedaccording to the manufacturersprotocol (PerkinElmer). Approximately 10-60 ng Incongruence length difference tests. ILD and non- of cleaned PCR served as in product template either Dye Termi- tests indicated that all data set nator or Big Dye Terminatorcycle sequencingreactions (Perkin parametric (Templeton) Elmer),performed according to the manufacturer'sprotocol but partitions were not significantly different at the p<0.04 modified to half size reactions.Excess terminators were removed level, suggesting no conflict of phylogenetic signal (Ta- from cycle sequencingproducts by ethanolprecipitation. Labeled ble 3). All data were therefore combined in the final fragmentswere separatedon polyacrylamidegels using an ABI Prism377 automatedDNA sequencer(Perkin Elmer). analysis. Distribution of tree lengths of 50000 random- Alignmentand PhylogeneticAnalyses. Sequenceswere initial- ly generated trees was significantly left skewed for all ly aligned using CLUSTAL(Thompson et al. 1994) and edited data set partitions, suggesting phylogenetic signal in Editor manuallyusing SequenceAlignment (Rambaut1996). The the data first and the last 30 base pairs of aligned rbcLsequences at the (Table3). 5(and 3(exonwere excludedfrom analysisdue to missing data for Character variation and combined molecular data some taxa. The alignmentof the trnL(UAA) intron sequences re- (rbcL + rps4 + trnL). All three genes combined (rbcL inclusionof all of which were excludedfrom quired many gaps, + rps4 + trnL) for 46 taxa resulted in a data matrix analysis to avoid difficulties in assessing positional correspon- dence. Sequences obtained in this study were submitted to of 2206 characters of which 1379 were from rbcL, 580 GenBank(Table 1). from rps4, and 247 from trnL. A total of 619 (28%)of Parsimonyanalyses (Fitch 1971) were conducted using PAUP the 2206 characters were parsimony informative. The 4.0b2a(Swofford 1999). To investigatecongruence of datasets each of the threegenes was analysedseparately; one analysiswas done informative characters consisted of 54% rbcL (336 for each data partition,rbcL + rps4,rbcL + trnL,rps4 + trnL,and sites), 34% rps4 (209 sites), and 12% trnL (74 sites). rbcL + rps4 + trnL. For all analyses characterswere equally Parsimony analyses excluding uninformative charac- included were treatedas and multi- weighted, gaps missing data, ters resulted in six most trees state characterswere treated as uncertaintiesrather than poly- parsimonious (MPTs) morphisms. Heuristic searches used 1000 random addition se- with tree length (TL) = 2213; consistency index (CI) = quences, TBRbranch-swapping, MULTREES option on, steepest 0.40; homoplasy index (HI) = 0.60; and retention index descent off, and branches when maximum collapsed length was (RI) = 0.67. A phylogram of one of the six MPTs show- zero.When multiple most parsimonioustrees were found,one tree from each analysis was selected for reconstructionof branch ing branch lengths and relationships of the major length optimized accordingto the ACCTRAN(accelerated trans- groups of peristomate mosses is shown in Fig. 2. The formation)algorithm. Bootstrap analyses (Felsenstein1985) used strict consensus tree is shown in Fig. 3. Rooting trees 1000 replicateswith 10 randomaddition sequencesper replicate, and all otheroptions as above.Branch support was also estimated with Sphagnaceae as outgroups resulted in topologies by Bremer support analysis (Bremer1996) using the program similar to those obtained with Andreaeaceae as out- AutoDecay(Erickson 1998) with randomsearches, each of 100rep- group. The results and discussion below are based on licates. the of all three + + For all data partitionsthe gl statistic(Huelsenbeck 1991) was analysis genes (rbcL rps4 trnL) calculatedbased on 50,000 randomlygenerated trees to test for for the 46 taxa with Andreaeaceae as outgroup (Fig. phylogeneticsignal. Before combined analyses were performed, 3). data were tested for partitions congruence.Initially, tree-based Basal clades (Class The best esti- comparisonwas performedby inspectionof pair-wisetopologies Polytrichopsida). and assessmentof bootstrapsupport of clades within trees (Ma- mate of the phylogeny indicates that the class Polytri- son-Gamerand Kellogg 1996).Next, the incongruencelength dif- chopsida (consisting of Buxbaumiaceae,Polytrichaceae, 30 SYSTEMATICBOTANY [Volume 28

a nitida - Andreaea rothii --- Outgrou . Andreaea rupestris

Oedipodiumgriffithianum . Oedipodiaceae 0 - Tetraphispellucida LTetraphisE geniculata - Tetraphidaceae f Tetrodontiumbrownianum Tetra hdaceae rA ---Pogonatun perichaetiale Atrichum altecristatum =0 commune Polytrichacea C) r- Notoligotrichumtrichodon ^ 0'S4 PO-

-Diphysciaceae

CZ ._

0M Haplolepideous CQo

I = = = FIG.2. Phylogram of one of the six MPTs based on rbcL, rps4 and trnL sequence data (Length 2213; CI 0.3995; HI 0.6005; RI = 0.6677) showing branch lengths. Bars marked by numbers refer to capsule and peristome characters:1 = differ- entiation of endothecium into outer sporogenous tissue and central columella; 2 = nematodontous peristome; 3 = additional anticlinal cell divisions in amphithecium at the point in peristome development when there are 12 cells (4 endothecium and 8 amphithecium), which upon differentiation of IPL results in double the number of cells in the IPL layer (16 cells instead of typical 8 cells); 4 = arthrodontous peristome with exostome and pleated endostome; 5 = transformationof a pleated endostome into a keeled endostome; 6 = reduction or loss of exostome.

Tetraphidaceae,and the monotypic Oedipodiaceae) is DI = 2). Within the Tetraphidaceae,Tetraphis is mono- paraphyletic and basal to the class Bryopsida. The phyletic (BP = 100, DI = 40). eperistomate Oedipodiumgriffithianum is sister to all Polytrichaceae (Clades 2 and 3) plus Dawsoniapap- peristomate mosses (BP = 92, DI = 6). Tetraphidaceae uana are basal to the Buxbaumiaceae,and are sister to = formed a strongly supported monophyletic group (BP the Buxbaumiaceae/Bryopsida clade (BP = 63, DI = 98, DI = 11). A weakly supported sister group re- 3). Polytrichaceaeformed a strongly supported mono- = lationship (as also indicated by the short branch in Fig. phyletic group (BP = 100, DI 30). Within the Poly- 2) between the Tetraphidaceaeand the clade consisting trichaceae, Dawsoniapapuana is basal to all other spe- of all other peristomate mosses is suggested (BP = 54, cies (Clades 2 and 3). The clade consisting of Pogonatum 2003] MAGOMBO:PHYLOGENY OF BASAL PERISTOMATEMOSSES 31

Andreaea nitida Andreaea rothii Outgroup Andreaea rupestris Oedipodiumgriffithianum Tetraphispellucida 1 Tetraphisgeniculata Clade 1 ITetraphidales TetrodontiumbrownianumJ Pogonatumperichaetiale Atrichumaltecristatum Clade 2 Polytrichumcommune J Notoligotrichumtrichodon l 3 Polytrichadelphusaristatus ade Dawsoniapapuana Buxbaumiapiperi 1 Buxbaumiaviridis Clade 4 Tetraphidales Buxbaumiaaphylla] Theriotialorifolia -" Theriotiakashmirensis Diphysciumperminutum |-

Diphysciumsatoi Diphysciidae 57 Diphysciumchiapense 1 I Diphysciumfulvifolium 88 Diphysciumlongifolium 50 1 Diphysciumsuzukii I Diphysciumfasciculatum Diphysciummucronifolium 100, Barbula convoluta ji4918[ if IStreptopogon 6 Dicranoweisiacirrata Dicranumscoparium 99 1001 Haplolepideous li3101--- Dicnemon semicryptum Dicnemon seriatum - 86 Grimmialaevigata 5 Lii Blindia magellanica 100 Timmiasibirica 20 L Timmiamegapolitana 72 r ciliata {76 TEZ Rosulabryumbillarderii 83 Rhizomniumpunctatum 8 96 Encalyptastreptocarpa Diplolepideous .98 Encalyptaprocera 20 I Encalyptaintermedia 88 - Leiomela bartramioides 11 IL.. Philonotis andina FIG.3. Strict consensus of six MPTs based on rbcL, rps4 and trnL sequence data (Length = 2213; CI = 0.3995;HI = 0.6005; RI = 0.6677). Characterswere unordered and equally weighted. Bootstrap percentages shown above branches, decay indices below branches.

perichaetiale, Atrichum altecristatum, and Polytrichum Diphysciaceae the diplolepideous/haplolepideous commune (Clade 2) is well supported (BP = 84, DI = mosses clade (BP = 100, DI = 10). The Diphysciaceae 5). Clade 3 is weakly supported (BP = 60, DI = 2) and formed a strongly supported monophyletic group (BP consists of Notoligotrichum trichodon and Polytrichadel- = 100, DI = 28). Within the Diphysciaceae, Diphyscium phus aristatus. is paraphyletic, with Muscoflorschuetzia and Theriotia Buxbaumiaceae formed a strongly supported nested within Diphyscium. Theriotia formed a strongly monophyletic group (Clade 4; BP = 100, DI = 38), sis- supported monophyletic group (BP = 100, DI = 8). ter to the class Bryopsida (BP = 99, DI = 15). Within The results suggested two sister clades within the Di- Buxbaumiaceae, and B. piperi formed physciaceae; the first clade (Clade 5) (BP = 76, DI = a monophyletic group (BP = 98, DI = 13), while B. 3) consisting of the two species of Theriotia (T lorifolia aphylla is sister to the B. viridis/B. piperi clade. and T. kashmirensis), the monotypic Muscoflorschuetzia Diphysciaceae. The class Bryopsida formed a and some members of Diphyscium (D. foliosum, D. satoi, strongly supported monophyletic group (BP = 99, DI and D. perminutum); the second clade (Clade 6) (BP = = 15), with a sister group relationship between the 88, DI = 5) consisted of D. chiapense, D. fulvifolium, D. 32 SYSTEMATICBOTANY [Volume 28 longifolium,D. suzukii, D. fasciculatum,and D. mucroni- (Lawton 1971). The sister group relationship between folium. Tetraphidaceaeand the Polytrichaceae/arthrodontous Diplolepideous and haplolepideous mosses. The mosses clade was previously suggested based on phy- clade consisting of diplolepideous and haplolepideous logenetic analyses of morphological data (Mishler and mosses was strongly supported (BP = 100, DI = 10). Churchill 1984). In another analysis of nuclear-encoded The subclasses Funariidae and Bryidae of the diplole- rRNA gene sequences (Hedderson et al. 1996) a weakly pideous mosses are paraphyletic and basal to the hap- supported sister group relationship between Tetraphis lolepideous mosses. Within the diplolepideous/hap- and members of the Polytrichaceae (Atrichumand Po- lolepideous clade, the haplolepideous mosses formed a lytrichum)was suggested. Furthermore the clade con- strongly supported monophyletic group (BP = 99, DI sisting of Tetraphisand members of the Polytrichaceae = 9). was sister to the Andreaeaceae (Andreaea)and the Tak- akiaceae ()rather than the arthrodontous moss- DISCUSSION es. In this study a sister group relationship between the and other mosses is Comparison of phylogenetic relationships resolved Tetraphidales peristomate sug- but = 54, DI = here with other studies. Results from the present study gestive, weakly supported (BP 2). The are dis- conflict with previous studies that suggested a sister Polytrichaceae. Polytrichaceae typically from other mosses the mor- group relationship between Buxbaumiaceae and ne- tinguished by following features: the of adaxial lamel- matodontous mosses (Hyv6nen et al. 1998; Vitt et al. phological presence differentiated into a distinct blade and a 1998; Newton et al. 2000; Goffinet et al. 2001). This lae, and a columella that forms an study suggests that the class Polytrichopsida as pro- sheathing base, expand- ed or a membrane over the mouth posed by Buck and Goffinet (2000) is paraphyletic, as epiphragm capsule van Zanten et is the order Tetraphidales. (see Smith 1971, 1974; 1973; Hyvonen al. Molecular evidence that taxa within Oedipodiaceae. The family Oedipodiaceae consists 1998). suggests the exhibit in some of their of a single and species, Oedipodiumgriffithianum. Polytrichaceae homoplasy characters et al. Mono- Traditionally 0. griffithianumhas been placed either in morphological (Hyvonen 1998). of as resolved here is its own family, Oedipodiaceae, and assumed closely phyly the Polytrichaceae congru- al. related to the family Splachnaceae (Brotherus 1925; ent with previous studies (Hyvonen et 1998). Vitt 1984), or placed within the family Splachnaceae Phylogenetic relationships among the Tetraphida- In (Lawton 1971; Nyholm 1989). However, recent molec- ceae, Polytrichaceae and Buxbaumiaceae. previous ular evidence (Newton et al. 2000; Goffinet et al. 2001) studies (Hyvonen et al. 1998; Newton et al. 2000) a sister between suggests that 0. griffithianummay occupy a critical po- group relationship Tetraphispellucida sition in the transformation between the non-peristo- (Tetraphidaceae) and Buxbaumiaaphylla (Buxbaumi- has been FurthermoreGoffinet et al. mate and peristomate mosses. Most recently 0. griffi- aceae) suggested. thianumwas placed in its own family Oedipodiaceae (2001) concluded that the Tetraphidaceae,Polytricha- but classified among the nematodontous mosses, Class ceae, and Buxbaumiaceaeform a monophyletic lineage. Polytrichopsida (Buck and Goffinet 2000). This species Nevertheless, the Tetraphidaceae and the Buxbaumi- has an operculate capsule but lacks a peristome. Its aceae are not known to share any unique morpholog- capsule has a rounded ovate urn (spore bearing por- ical characters,and differ in a number of features. The tion of the capsule), and long, narrow neck. The family Tetraphidaceaehave small conic calyptrae, erect and shares with the peristomate group an endothecium symmetric capsules, lack air spaces between the spore that is differentiated into an outer cylinder of sporog- sac and capsule wall, and structurally have nemato- enous tissue and a central columella (character1; Fig. dontous peristomes that consist of four massive teeth 2). The basal position of Oedipodiaceae to all peristo- (Lawton 1971; Crosby 1980; Crum and Anderson mate mosses indicated by this study is consistent with 1981). In contrast the Buxbaumiaceaehave cucullate or previous results by Newton et al. (2000), and Goffinet mitrate calyptra, asymmetric and horizontally placed et al. (2001). capsules, air spaces between the spore sac and capsule Tetraphidaceae.The Tetraphidaceae are best char- wall, and arthrodontous peristomes consisting of 32 or acterized by their nematodontous peristome that con- more exostome teeth in one or more layers and an en- sists of four massive teeth. There are two genera in the dostome of 32 pleats (Crosby 1980; Crum and Ander- family, Tetraphis(two species) and (three son 1981; Edwards 1984; Schofield 1985). species, see Crosby et al. 2000). Tetraphisis distin- Separation of Tetraphidaceae, Polytrichaceae and guished from Tetrodontiumon the basis of its long Buxbaumiaceaeinto distinct lineages suggested by this stems, weak costa, and short calyptra i.e., reaching to study is consistent with the differences in their mor- mid-capsule (Lawton 1971). In contrast, plants of Te- phological features. The placement of Tetraphispellucida trodontiumare almost stemless, the costa is weak or (Tetraphidaceae) and Buxbaumiaaphylla (Buxbaumi- absent, and the calyptra covers most of the capsule aceae) in the same clade, as indicated in other molec- 2003] MAGOMBO:PHYLOGENY OF BASAL PERISTOMATEMOSSES 33 ular studies (Hyvonen et al. 1998;Vitt et al. 1998;New- Diphysciaceae. Three features characterize the Di- ton et al. 2000), may be due to inadequate taxon sam- physciaceae: short setae (to 0.3 mm long), an unusual pling, character sampling, or both (Felsenstein 1978; arthrodontous peristome (lacking exostomes or exo- Wendel and Doyle 1998). The resolution of the Tetra- stomes rudimentary, and pleated endostomes), and phidaceae, Polytrichaceaeand the Buxbaumiaceaeas a collared axillary hairs. None of these features are monophyletic lineage by Goffinet et al. (2001) may be unique to the Diphysciaceae; arthrodontous peri- due to both insufficient character sampling (for taxa stomes with pleated endostomes are found in the Bux- representing those particular groups) and insufficient baumiaceae, and short setae are found scattered data as only one gene, rps4 (which performs poorly among many moss groups. Collared axillary hairs are alone) was used. Constraint analyses in the present uniseriate hairs found in the leaf axils of some mosses study forcing the three families (Tetraphidaceae,Po- with remnants of primary cell walls covering the end lytrichaceae and Buxbaumiaceae) into a monophyletic of each cell. They have been considered one of the most group resulted in an increase in length of the shortest important diagnostic features for the Diphysciaceae tree by 8 steps from 2213 to 2221. However, a non- (Deguchi 1975; Iwatsuki 1976; Crosby 1977; Norris parametric (Templeton)test comparing topology of the 1981). However, collared axillary hairs have also been shortest tree obtained in this study to the constrained reported in several unrelated moss groups, e.g., Poly- topology was not significantly different (p = 0.2760). trichum(Wanstall 1950) and (Saito The results of the non-parametric test indicate that 1975) although they are most abundant in the Diphys- while the phylogenetic relationships of the basal per- ciaceae. The developmental patterns of collared axil- istomate mosses as suggested by this study are novel, lary hairs have been studied in Diphysciaceae (Degu- the previous hypotheses of a monophyletic assemblage chi 1975) and Polytrichaceae (Wanstall 1950). When of the Tetraphidaceae,Buxbaumiaceae and the Polytri- these studies are compared it is evident that this fea- chaceae (Goffinet et al. 2001), or sister group relation- ture is quite similar in both groups, suggesting ho- ships between the Tetraphidaceaeand Buxbaumiaceae mology. (Newton et al. 2000; Hyvonen et al. 1998) may not be All analyses in this study resolved Diphysciaceae rejected completely. as monophyletic, confirming recent analysis of the rps4 Phylogenetic relationships between the Buxbaumi- gene (Goffinet et al. 2001). Furthermore,in the present aceae and Diphysciaceae. This study suggests a sister study all analyses resolved and strongly supported Di- group relationship between the Buxbaumiaceae and physciaceae as sister to the haplolepideous and diplo- class Bryopsida. Peristomes of the Buxbaumiaceae lepideous mosses (BP = 100, DI = 10). These results have pleated endostomes similar to those of the Di- reaffirm the previously suggested sister group rela- physciaceae, and therefore the two families have been tionship between Diphysciumfoliosum and the diplole- assumed to be closely related (Brotherus 1925; Crosby pideous/haplolepideous mosses (Beckert et al. 1999; 1980; Crum and Anderson 1981; Vitt 1984; Norris Newton et al. 2000). The sister group relationship be- 1994). The two families, however, have disparate ga- tween the Diphysciaceae and diplolepideous and hap- metophytic and sporophytic charactersthat contradict lolepideous mosses was also suggested by Goffinet et this view. For example, Buxbaumiaceae have greatly al. (2001) although in some of their analyses the Di- reduced gametophytes, persistent protonemata, undif- physciaceae were nested within the haplolepideous ferentiated perichaetial leaves, and long setae, up to 27 mosses. mm long (see Brotherus 1925; Crum and Anderson Diplolepideous and haplolepideous mosses. The re- 1981; Norris 1984; Schofield 1985). In contrast plants in sults of this study suggest that the diplolepideous sub- the Diphysciaceae have well-developed gametophytes, classes Bryidae and Funariidae as proposed by Buck ephemeral protonemata, strongly differentiated peri- and Goffinet (2000) are paraphyletic. These results are chaetial leaves, and short setae, up to 0.30 mm long consistent with Goffinet and Cox (2000) who conclud- (see Brotherus 1925; Schofield 1985; Crosby 1977, 1978; ed that the suborder Funariineae and family Funari- Deguchi 1975; Deguchi et al. 1997; Magombo 2002c). aceae as circumscribed by Vitt (1984) are paraphyletic. Constraining Buxbaumiaceae and Diphysciaceae into The monophyly of haplolepideous mosses (Subclass a monophyletic group increased the length of the Dicranidae) as suggested by this study also reaffirm shortest tree by 18 steps from 2213 to 2231. Non-para- previous works (Beckertet al. 1999; Newton et al. 2000; metric tests (Templeton 1983) showed that the increase La Farge et al. 2000; Goffinet et al. 2001). Although the in length was significant (p < 0.0004). Thus monophy- trees presented here differ in some respects from pre- ly of the two families was rejected. Paraphyly of the vious studies, this may be due to relatively limited tax- Buxbaumiaceae and Diphysciaceae as presented here on sampling within the diplolepideous/haplolepi- is congruent with recent analyses of other molecular deous group. data (Hyv6nen et al. 1998; Newton et al. 2000; Goffinet Nematodontous peristomes. Peristomes in Tetra- et al. 2001). phidaceae and Polytrichaceae are similar and strictly 34 SYSTEMATIC BOTANY [Volume 28 nematodontous because they are formed of whole cells to as keeled. The phylogeny presented in this study with thickened walls ratherthan remnants of cell walls suggests that the pleated endostome is plesiomorphic as in the arthrodontous mosses. On this basis, Tetra- and was transformed into a keeled endostome in the phidaceae have been considered more closely related clade consisting of diplolepideous and haplolepideous to Polytrichaceae than to arthrodontous mosses (Phi- mosses (character 5; Fig. 2). Furthermore, the keeled libert in Taylor 1962; Campbell 1905; Cavers 1911; Dix- endostomes in the diplolepideous/haplolepideous on 1924; Grout 1936; Crosby 1980; Schofield 1985). But mosses clade are similar to the pleated endostomes in peristomes in the Tetraphidaceaeconsist of four mas- the Buxbaumiaceae and Diphysciaceae because the en- sive teeth, while typical Polytrichaceaeperistomes con- dostomes in the Buxbaumiaceae (Edwards 1984), as sist of 32 or 64 teeth (rarely 16 teeth). This study sug- well as Diphysciaceae (Shaw et al. 1987) and the di- gests that the nematodontous peristome in the Tetra- plolepideous mosses (Edwards 1984), are keeled. A phidaceae and the Polytrichaceaeis plesiomorphic and fundamental difference between the pleated endo- nematodonty is a synapomorphy for the peristomate stome in Buxbaumiaceae and Diphysciaceae and the mosses. keeled endostome in a diplolepideous peristome is that Contrary to the suggested close relationship of Te- in the Buxbaumiaceae and Diphysciaceae the endo- traphidaceae to Polytrichaceae based on peristome stome is keeled on both the outside and inside while structure (i.e., both have nematodontous peristomes), in the diplolepideous mosses the endostome is keeled se- patterns of peristome development, particularly only on the outside. In terms of position the outside of cell divisions of sec- quence preceding deposition keel in a pleated endostome and the outside keel in a wall material in ondary peristomial Tetraphidaceae, keeled endostome are homologous. are more similar to those of arthrodontous mosses Endostomes of Buxbaumiaceae and Diphysciaceae than and Anderson 1988). Pre- Polytrichaceae (Shaw have been compared to endostomes of haplolepideous (Crum and Anderson 1981; Edwards 1984) ar- viously mosses, particularly those of the Encalyptaceae (Ed- that on the basis of gued gametophytic morphology wards 1984; Vitt 1984). Peristomes of some species of the similarity in peristomes in Tetraphidaceaeand Po- the Encalyptaceae consist of two rows, the outer row lytrichaceae might not suggest a close phylogenetic re- of exostome teeth positioned opposite endostome seg- between the two families. The phylogeny lationship ments of the inner row (see Horton 1982; Edwards presented in this study suggests that Tetraphidaceae 1984). The endostome segments arise from a well-de- are sister to Polytrichaceae plus all arthrodontous veloped pleated basal membrane (Horton 1982). On mosses. Polytrichaceae appear to be sister to the ar- the outer surface of the basal membrane, the joint be- throdontous mosses. Based on the phylogeny present- tween each segment consists of two fused, revolute ed in this study, therefore, the similarity in sequence flanges (Horton 1982; Vitt 1984) also called interme- of cell divisions preceding deposition of secondary diate exostome teeth (Edwards 1984). The intermediate peristomial wall material in Tetraphidaceae and ar- exostome teeth or revolute flanges in Encalyptaceae throdontous mosses is a synapomorphy for the peris- are similar to the thickened the keels of tomate mosses. ridges along the outer endostomial surface in Buxbaumiaceae and In the Polytrichaceae the sequence of cell divisions and since they both consist after the 12-cell stage (four cells of the endothecium Diphysciaceae by position, of endostomial and exostomial cell wall remnants they and eight cells of the amphithecium), differ from all were assumed to be 1982, 1983; other mosses in that the next step in peristome devel- homologous (Horton Vitt 1984; Edwards 1984). As a result, a type opment is an anticlinal division in the eight cells of the separate of arthrodontous amphithecium. As a result, when the IPL layer is dif- peristomes, diplolepideous-flanged of the Di- ferentiated, there is twice the number of cells (16 cells) or Encalyptaceous peristomes (consisting and was instead of the typical eight cells in the IPL as is found physciaceae, Buxbaumiaceae Encalyptaceae), The of the in Tetraphidaceaeand arthrodontous mosses (van der proposed (Vitt 1984). suggested homology in the Wijk 1929; Wenderoth 1931; Blomquist and Robertson intermediate teeth Buxbaumiaceae, Diphysci- 1941; Saito and Shimoze 1954; Chopra and Sharma aceae and Encalyptaceae, however, has been contro- 1958; Chopra and Bhandari 1959; Shaw et al. 1987, versial (Shaw et al. 1987) due to lack of a phylogenetic 1989a; Shaw and Anderson 1988; Goffinet et al. 1999). framework and insufficient comparative data on de- This study suggests that the peristome development velopment of peristomes in the Buxbaumiaceae and pattern in the Polytrichaceae (character 3; Fig. 2) is Encalyptaceae. While developmental data of peri- uniquely derived. stomes in the Buxbaumiaceae and Encalyptaceae are Transformationof pleated endostome to keeled en- necessary before conclusions on homologous features dostome. The endostomes in the Buxbaumiaceae and of the endostome can be made, the phylogeny pre- Diphysciaceae are normally referred to as pleated sented here suggests that the similarities among peri- while those in the Diplolepideous mosses are referred stomes in the three families (i.e., Buxbaumiaceae,Di- 2003] MAGOMBO:PHYLOGENY OF BASAL PERISTOMATEMOSSES 35 physciaceae and Encalyptaceae) are actually plesiom- ly supported (character6; Fig. 2). Finally, the similarity orphic. in cell divisions preceding deposition of secondary Peristomes of the Encalyptaceae, however, are ex- peristomial wall material is a synapomorphy of the tremely variable and may be superficially similar to peristomate mosses. peristomes of the nematodontous, haplolepideous and diplolepideous mosses (Philibert, see Taylor 1962; Vitt ACKNOWLEDGEMENTS.This study was made possible with fi- and Hamilton 1974; Horton 1982,1983; Edwards 1984). nancialsupport from the NationalScience Foundation PEET grant no. DEB-9522034,International Center for TropicalEcology (ICTE) Fleischer (1904) the taxon to proposed Heterolepideae of the Universityof MissouriSt. Louis (UMSL),Des Lee Labora- accommodate Encalyptawith its variable peristome tory of MolecularSystematics (UMSL), and two grantsto D. Hard- structure within the arthrodontous mosses. er (NSF grant no. DEB-9870231and NationalGeographic Society Reduction or loss of exostome. Exostome teeth in grant no. 6733-00).I am especiallygrateful to B. Allen, R. E. Ma- and E. for their and the Buxbaumiaceae (homologous with exostome teeth gill, Kellogg support encouragementduring the I thankJohn Shaw, Alan Whittemoreand an anonymous are al- study. in diplolepideous peristomes) conspicuous reviewerfor detailed commentsthat greatlyimproved the manu- though not as well developed as in typical diplolepi- script. Help with fieldworkand collectionof specimenswas pro- deous mosses. Exostome teeth in the Diphysciaceae are vided by H. Deguchi,T. Yamaguchiand their students(HIRO), N. sporadically present in the circumference of the cap- Nishimura,Z. Iwatsuki,T. Suzuki, J. Snider,B. Tan,I. Holz, Nguy- D. Tran N. D. T. sule et al. and when are ru- en Hiep, Harder, Ninh, Gunatilleke, Wijesundara, (Shaw 1987) present they Triono,and F Indah. dimentary (Edwards 1984; Shaw et al. 1987). Similarly exostome teeth are lacking in haplolepideous mosses LITERATURECITED or are rudimentary. 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