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Testing Morphological Concepts of Orders of Pleurocarpous Mosses (Bryophyta) Using Phylogenetic Reconstructions Based on TRNL-TRNF and RPS4 Sequences William R

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Testing Morphological Concepts of Orders of Pleurocarpous Mosses (Bryophyta) Using Phylogenetic Reconstructions Based on TRNL-TRNF and RPS4 Sequences William R Molecular Phylogenetics and Evolution Vol. 16, No. 2, August, pp. 180–198, 2000 doi:10.1006/mpev.2000.0805, available online at http://www.idealibrary.com on Testing Morphological Concepts of Orders of Pleurocarpous Mosses (Bryophyta) Using Phylogenetic Reconstructions Based on TRNL-TRNF and RPS4 Sequences William R. Buck,* Bernard Goffinet,†,‡ and A. Jonathan Shaw† *Institute of Systematic Botany, New York Botanical Garden, Bronx, New York 10458-5126; †Department of Botany, Duke University, Box 90339, Durham, North Carolina 27708-0338; and ‡Department of Ecology and Evolutionary Biology, Box U-43, University of Connecticut, Storrs, Connecticut 06269-3043 Received May 6, 1999; revised January 19, 2000 INTRODUCTION The ordinal classification of pleurocarpous mosses rests on characters such as branching mode and architecture of Familial definition and generic inclusions in mosses, the peristome teeth that line the mouth of the capsule. The the Bryophyta sensu Vitt et al. (1998), are undergoing Leucodontales comprise mainly epiphytic taxa, character- frequent reevaluation based on morphological (e.g., ized by sympodial branching and reduced peristomes, Buck, 1988, 1994; Hedena¨s, 1994, 1995, 1996a,b) and whereas the Hypnales are primarily terricolous and molecular (e.g., Goffinet and Vitt, 1998; Goffinet et al., monopodially branching. The third order, the Hookeriales, 1998; Cox and Hedderson, 1999) data. Until recently, is defined by a unique architecture of the endostome. We several generations of bryologists have utilized the sampled 78 exemplar taxa representing most families of classification of mosses proposed by Brotherus (1924– these orders and sequenced two chloroplast loci, the trnL- 1925), and for the most part showed little interest in trnF region and the rps4 gene, to test the monophyly and higher level classification (see Vitt et al., 1998). As relationships of these orders of pleurocarpous mosses. Es- classifications have come to be accepted as reflections timates of levels of saturation suggest that the trnL-trnF of phylogeny, older classifications subsequently have spacer and the third codon position of the rps4 gene have come to be viewed as phylogenetically informative reached saturation, in at least the transitions. Analyses of when there is little evidence that the originators even the combined data set were performed under three opti- thought about evolutionary history. These older classi- mality criteria with different sets of assumptions, such as fications have thus become infused with meaning never excluding hypervariable positions, downweighting the intended by their original proponents. Such is the case most likely transformations, and indirect weighting of with pleurocarpous mosses. rps4 codon positions by including amino acid translations. The pleurocarps, those mosses characterized by ex- Multiple parallelism in nonsynonymous mutations led to tensive branching and lateral sporophyte placement, little or no improvement in various indices upon inclusion compose one of the major groups of mosses. Typical of amino acid sequences. Trees obtained under likelihood pleurocarps are immediately recognizable on the basis were significantly better under likelihood than the trees of the elaborate branching pattern alone. The term derived from the same matrix under parsimony. Our phy- “pleurocarpy” refers to the lateral female gametangia logenetic analyses suggest that (1) the pleurocarpous (i.e., the perichaetia) versus the terminal perichaetia mosses, with the exception of the Cyrtopodaceae, form a in acrocarpous mosses (Bridel, 1826–1827). The rela- monophyletic group which is here given formal recogni- tionship of pleurocarpy to cladocarpy, a situation in tion as the Hypnidae; (2) the Leucodontales are at least which the perichaetia are produced terminally on lat- paraphyletic; and (3) the Hypnales form, with most mem- eral branches rather than being sessile, has recently bers of the Leucodontalean grade, a monophyletic group been examined by LaFarge-England (1996). Her study sister to a Hookerialean lineage. The Hypopterygiaceae, was prompted by the presence within typical acrocar- Hookeriales, and a clade composed of Neorutenbergia, pous lineages of isolated occurrences of taxa with fe- Pseudocryphaea, and Trachyloma likely represent a basal male gametangia that are produced laterally and are clade or grade within the Hypnidae. These results suggest sessile or nearly so (e.g., Molendoa, Pottiales). She that mode of branching and reduced peristomes are homo- distinguished pleurocarpy from analogous forms of re- plastic at the ordinal level in pleurocarpous mosses. © 2000 duced cladocarpy based on features of the juvenile Academic Press leaves at the base of the gametangia and of the short axis supporting the gametangia that lacks sub- 180 1055-7903/00 $35.00 Copyright © 2000 by Academic Press All rights of reproduction in any form reserved. MOLECULAR PHYLOGENY OF PLEUROCARPOUS MOSSES 181 perichaetial innovations. Other characters used for de- of the pleurocarpous lineage and the three orders com- fining a clade of pleurocarpous mosses include the posing it. Based on phylogenetic inferences from anal- mode of branching, the presence of pseudoparaphyllia yses of two chloroplast loci, the trnL-trnF region and that surround lateral primordia, and the anatomical the rps4 gene, the following issues are addressed: (1) homogeneity of the costa. Modes of branch develop- Do pleurocarpous mosses form a monophyletic group ment per se (i.e., sympodial or monopodial) are not as defined by Buck and Vitt (1986)? (2) Are the three informative for defining a clade of pleurocarpous orders (Hypnales, Hookeriales, and Leucodontales) as mosses, as both types occur in pleurocarpous (e.g., Leu- defined by Buck and Vitt (1986) and amended by Buck codontales) and acrocarpous (e.g., Orthotrichaceae) (1994), monophyletic? taxa (LaFarge-England, 1996). Buck and Vitt (1986) suggested the presence of pseudoparaphyllia around branch primordia as another synapomorphy for defin- MATERIAL AND METHODS ing the pleurocarpous lineage. Hedena¨s (1994) defined Taxon sampling. Exemplars of most pleurocarp- the monophyly of the pleurocarps based on the homo- ous families (sensu Vitt, 1984 and Buck, 1998) have geneous anatomy of the costa of the leaves. Neither been sampled. For speciose genera one or more rep- definition appears satisfactory since pseudoparaphyl- resentatives were included (Table 1). A special effort lia are lacking is some pleurocarps (ϭpseudopleuro- was made to include taxa of tropical latitudes in carps sensu Buck and Vitt, 1986), and costae are ab- order not to introduce a geographical bias into the sent in many other taxa. sampling. Potential outgroup taxa were selected Pleurocarpous mosses, which as a group lack formal based on the phylogenetic hypothesis proposed by nomenclatural recognition, have long been accommo- Cox and Hedderson (1999) for arthrodontous mosses dated in three orders, the Isobryales (ϭLeucodontales), and on ongoing phylogenetic analyses for all mosses Hookeriales, and Hypnobryales (ϭHypnales). Buck (B. Goffinet et al., unpublished). Vouchers for all and Vitt (1986) defined these orders by characters per- taxa are deposited in the herbarium of the New York taining to the mode of branching and associated leaf Botanical Garden (NY). differentiation between primary and secondary mod- ule, the differentiation of alar cells, the number of DNA extraction, PCR amplification, and sequencing. costae in the leaf, and the architecture of the inner row Apical portions of stems or branches or occasionally oper- of teeth that line the mouth of the sporophyte. The culate capsules were removed from dried herbarium col- Hookeriales are best defined by their endostome with lections or from samples placed in silica in the field. The the baffle-like crosswalls (Buck, 1998). This architec- dry weight of the material used for extraction likely never ture is unique among mosses and likely identifies a exceeded 5 mg. DNA was extracted from plant tissues monophyletic group. Whether this group is restricted following a modification of Doyle and Doyle’s (1987) pro- to the Hookeriales as defined by Buck (1998) remains, tocol. Plant material was ground using a small teflon however, uncertain. pestle in 700 ␮Lof2ϫ hexadecyltrimethylamonium bro- The Leucodontales typically lack well-developed mide (CTAB)–0.2% beta-mercaptoethanol, heated to peristome teeth, branch sympodially and in many 60°C, and incubated at this temperature for at least 30 cases also monopodially, and are epiphytic. Sympodial min. An equal volume of chloroform–isoamyl (24:1) was branching is likely a primitive state in mosses, being added. The emulsified solution was centrifuged for 1 min the dominant mode of branching in all other mosses, at 6500 rpm, and the aqueous phase was transferred to a i.e., the acrocarps. The apparent correlated occurrence new tube to which an equal volume of ice-cold isopropanol of epiphytism and sympodial branching for all Leuc- was added. DNA was precipitated at 0°C for 30–60 min. odontales led Buck (1991) to revise relationships pro- Tubes were centrifuged first for 10 min at 13,000 rpm. posed earlier (Buck and Vitt, 1986) and to suggest that The pellet was washed with 70% ethanol, and the tubes this order likely represents an evolutionary grade were then centrifuged for 3 min at 13,000 rpm. The pellet reached via convergent evolution from various terri- was dried in a vacuum centrifuge and suspended in 30 ␮L colous and monopodially branching taxa of the Hyp- Tris–EDTA
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