98/100175/99 ...- .:.:1o:.;::o/.:.:1o:.::o/.:.:1o:.::o:.:./1o:.::oC:...:H~apl'h~~70~t~%oi1l~~ei c:=====~~r;II:ee7;ubbii:aaTclattfnOJ~~ubia I Calobryales & Treubiales (leafy) L-:1i(;00nt/li'G00nt/1i'ii00O,/1i'iioo1o nana 99/100/661199 fy1onor;:lea gottschei

:::;~~/53 74/100/60197 Df!?7dg~~£~p~~siiJrans .....-=-"""":"'".--:-. R/ccla SI?. 83/·/-196 100/100199/10laro/.Jf}h~i~Yli-ggpl/,~ 98/100/59/96 Asterella wallichiana Wiesnerella denudata 99/100/-/100 58/100/-199 Conocephalum conicum (Complex thalloids) ~::::::::7~~M~all;c~h~a~nt;;iaJ,p~O~/y~m;;:o,,~p~h~a_ J Cyathodium tuberosum I ~~~~=~~N~eo.t3~BfaO;j~J!Jt;~~~iS 100/100/100/100 b s8~grhg/7~~~~~J~6~O~s

L..-.,."."."..".".".."."."..".".,-- caBi~~!:%tgz~sa .....------~/~~~fo~!foo71~~kaynii PetalophYJlum ralfsii 100/100/100/100 Aust~?d~~~,/J6fif!J'/~~~¥ralis Fossombroma 5£' 68/100/-/60 ..... 9_9/1_0_0/9_9/1~hYllotht,~~s~/JJg67£'ia oveolata 100/100/·/89 Hattorianthus erimonus 66/-/-/88 Moerckia sp. 100/100/100/100 Symp.~9gynOPSiS filicum Moerckla 15I III 69/100/-/88 87/100/-197 100/100/100/10 connivens 83/100/-/99 Jensenia spinosa 86/100/-/100 100/100/100/100 Iyelli Symphyogyna marginata 76/100/-/- L..- ..,..._ Hymenophyton flabellatum L..- ..:.l0::::0:.:./10::::0:.:./1::::00:.:./1;;::00~ 8a~cu'aria crispula

1001100/100/100 a ¥J~lf!h~acgJf%~7a ..... ~~ p"ttf;~i~p~g~ffaata Pelliidae (Simple thalloids) L..- .;.;10;.;;;0/.;.;10;.;;;0/.:.:10;,;;;0/.:.:100~%OJtJPo~faet!a~~r;J~Yu~'h~ L .....l1!.2!00l!l/1!.2!00~/1~00~/1!.9.00~===:..::S~c~h~istO§t//;~t~~Ii(,~'blumei + Schistochilaceae (Leafy) 98/100/1001100 Jubula bogotensis 100/100/100/100 Jubulajavanica ==::-::::'lLN/~~gg~~jJ~g~~~eg~Y£.~a 77/100/86172 [§gp~6~:%t~~~r!/~OJb~gmae Acrolejeunea p'usilla Bryopteris filicina 84/-/-/- r--"1'-----_P--'y'---cnolejeunea densistipula

96/100/55/99 81/100/56/- 100/100/100/100 sp. 50/-/63/- Pleurozia gigantean JJ15!?e°coleopsis sacculata oPtilidium pUIC~JgO?c~'JJa ulophylla 100/100/100/100 Porella vemicosa .. ~;;.;.;.;;.;.;.;;.;.;.~----- Goebellella cormgera 99/100/99/100 Lepidolaena clavigera

100/100/99/100 Gack:f,.b~ojf;~n;e~~rJg~~ri 100/100/100/100 Gackstroemia schwabei 100/100/100/100 Metacaly'pogeia cordifolia Metacalypowia a/ternifolia r~======::.~o~ca~/~YPe:0:!g~e~ia~qu(;~;t:J~~f~usericetorum Calypogeiaceae ... 1_00_/1_00_11_00_/1_00_-e~MitW~rJ~i~CJcffgt~:grcJeJ2 .....------~~ Mnioloma fuscum + Gongylanthus 57/100/-/- 100/100/100/100 ~c:!Yfp~~8jrc/g~ejj5u~ula 72/·/·/· I 46/100/-/61 r:;:.::=:....- Geocalyx graveolens L_~----,:""",,:~Jungermannia subulata Oo78:mciijl----- Leiocolea heterocolpos 100/100199/100 100/1001991100 Isotachis multiceps IL~~~~1-~~.Isotachis japonica 99/100/63199 Balanti°fog!1~01!~ci~~ohylla Tylimanthus laxus 90/100/971100 Marsup.idium latifolium 84/100/80/· Goebelobryum unguiculatum 9mOo78:mciQL-~~ ~__L_e_th_o_c_o_lea ~~~~~gg~j/~aruto-toganensis 100/100/100/100 Jungermannia sp. L..-__.....,,__~J...,u-n-g-ermc!;r'iffht~~i&~{r:rwoodiana '-----_~-- Gvmnomitrion concmnaPtim Marsupella emarginata -'-"'1J..----::----'- Anastrophyllum michauxii ,.------....- Barbilophozia hatcheri 79/-/-/- Lophozia ventricosa DiploQhyllum serrulatum 61/100/95/100'------r-- sCWeania !$tephanii 99/100/84/10099/100/99/1 00 8a.j1;~~i~~5/;;aoi~gurvifolia (Leafy) ~===~::::::==Cie~p~ha~/~oz~ie~~~7i~~~~ifolia L SChi~~C!l:/~:~1i~~aruensis zz§~~~J~7£1~dens 96/100/60/- ,..:.;;.;;.:.:;.;;.:.::.::.:.::.::c==--,B...a...... ==-- Acromastigum colensoanum ='J'~----:p~sil'561~§~i~/~~~~~1i~a 75/-/·/- ~Lef~~~~ijCWe1gftt:1~7a 100/100199/100 w---".__ 100/100199/100 T~Y!J~~~fgff~i(!t~s .....----..",~...,ric...,h-o-c-OlfJ7gPn~gf~~~major r!4~~?oc&~'Io~/~'/);droides

89/100/88/86 99/100195jjilODOO-0-0/1-00'-/9-9/-10-0-- P'aBh9/~hjb~t~e~e#~6~:~s 1

65/-/-/68 611-1971100 Triandrop.hYIIu/n°ftb~~~'J:J,/;eteroPhYlla ...._-- Herbenus aduncus .....----- Mastigophora diclados

L..----:1:':'::00""/1:':'::00""/1:'::00""/1:'::0;;"'0-c:=-..:.:M:.!.Y/~~ff§le~rrucosa 1""""---,.;...------: Verdoornia succulenta 911100/100/100 Aneura pi(lgui$ L~iQQIl~~==10=0=/100=/10=0=/10:0~=3~~~~Anewa pmgUls 79/100198/100 LObati~2~%:Jif~~g~}~ _l22!l22!l22!:!.22.-{52:/':/9:1I-~::::::::::::::~Riccardia L Ri[g~lJi~dj;u1f;Rg::ceavi/rea (Simple thalloids) 90/-196/99 Metzgeria lindbergii 100/100/100/100 Metzge1fa0f'[}r~~f1aeria pubescens 2/100fL8196',....------...,...... ,...-- Tetraphis geniculata I I [::..;;;;~~:c:::::::::~A~n~dll~e~a~e~a~ru~p~e~s~t~~/s~~'E:2~~:£!:.Sphagnum cuspidatum 0 t 100/100/100/100 Nitella translucens Takakia lepidozioides U 9rou pS Coleochaete Orbf6~t:J~/ulgaris 453 Masuzaki & al. • Systematic position ofMizutania TAXON 59 (2) • April 2010: 448-458

Fig. S. The ML tree based on integristipula 0 the analysis ofthe rps4 gene Calypogeia muelleriana 0 Calypogeiaceae Mnioloma fuscum 0 sequences. Numbers above the 100/100/1001100 Mnioloma fuscum 0 branches are LBP/BP/PPB/AU; 100/100/100/100 Mizutania riccardioides • .....------...... - ... Mizutania riccardioides • in %. incubous: 0; saccubous: o 6; transverse: D; thalloid: •. o b. b. b. o o o o o b. b. 85/-1-1- b. b. b. b. b. b. b. 69/-1-1- b. b. D D A Jungermanniineae b. 99/-/100/96 b. b. b. b. b. b. b. b. b...... ------Jackiella curvata b. Diplophyllum albicans I Barbilophozia f1oe.rkei Cephaloziineae Anastrophyllum auntum ~----- Jamesoniella rubricaulis 100/100/100/100 ~eiomyli~. anomala I Jungermanniineae (Myliaceae) Mylla taylom 69/-1-1- Lepidozia cupressina Ch!astocaulon. dendroides ILophocoleineae Pedmophyllum mterruptum Clasmatocolea vermicularis ....._- Lophocolea concreta L-~~:!.Q2L1.2£.C===:- Pachyschistochila carnosa Perssoniellineae Schistochila lehmanniana I 1------Riccardia capensis .....------Marchantia polymorpha in the leafy liverworts by Tsubota & Deguchi (2004) might be Calypogeiaceae (Jungermanniales suborder Jungermanni­ ascribed to contamination by gemmae ofCalypogeia. The anal­ ineae) are a nearly cosmopolitan family comprising four genera: yses, however, were conducted on the basis ofthe three samples Calypogeia, Eocalypogeia, Metacalypogeia, and Mnioloma. from three different localities (Genting Highlands, Cameron Characteristic are the incubous leaves, ventral intercalary or Highlands, Fraser's Hill) in the Malay Peninsula and no trace of occasionally terminal female branches, and well-developed fragments ofplants including gemmae ofCalypogeiaceae were marsupium. Although the thalloid morphology of Mizutania detected in the samples. It is therefore highly improbable that is entirely different from the leafy morphology ofother Caly­ our results are derived from contamination. The present study, pogeiaceae, there are some close morphological similarities: also reveals that Pleurozia is not a sister to Metzgeriales but to (1) The rudimentary, intercalary sexual branches ofMizutania Radula (Fig. 4). Although there are gametophytic similarities are reminiscent ofthose ofCalypogeiaceae; they are short and between Pleurozia and Metzgeriales (Crandall-Stotler & aI., ofdeterminate length, and have reduced leaves and 2-3-lobed 2005), morphological differences have been observed in the which are irregularly or indistinctly triseriate. Interca­ : the capsule cell wall ofPleurozia is 9-10-stratose lary sexual branches seem to be a synapomorphy of Calypo­ and the valves lack an elaterophore (Schuster, 1984), while in geiaceae including Mizutania, but excluding Eocalypogeia. (2) Metzgeriales the capsule wall is bistratose and each valve has Oil bodies ofMizutania consist of minute granules similar to an elaterophore. It therefore seems doubtful that Pleuroziales those of many Calypogeiaceae. (3) The chromosome number and Metzgeriales are closely related. ofMizutania ofn = 9 (Inoue & Furuki, 1992) is consistent with

454 TAXON 59 (2) • April 2010: 448-458 Masuzaki & al. • Systematic position ofMizutania

that of 9 or 18 in Calypogeiaceae (Tatuno, 1941). (4) Asexual stage, (2) primary stage with no underleaves, (3) juvenile stage reproduction by means of 1-3-celled ellipsoidal greenish ex­ characterized by constant phyllotaxis with one underleaf per ogenous gemmae on leaf margins or surface is common in each lateral leaf. Morphological variations are interpreted as the Calypogeiaceae and Mizutania (Calypogeiaceae: Schuster, the retention ofthese stages in the mature gametophyte (Grad­ 1969, fig. 119; Mizutania: fig. IH). (5) The massive cuticle on stein & aI., 2003). Recent molecular phylogenetic study re­ the thallus surface of Mizutania is reminiscent of the cuticle vealed that Cololejeunea metzgeriopsis is not phylogenetically found in several species ofMnioloma (Mizutania: fig. lC-F, H isolated from other Cololejeunea species (Gradstein & aI, 2006; and K; Mnioloma: Schuster, 2000, figs. 206, 209, 210, 21OA). Gradstein & Wilson, 2009). Protonemal neoteny is usually In the phylogenetic tree based on rbcL sequences (Fig. 4), interpreted as an adaption to the growth in short-lived habitats Calypogeia, Metacalypogeia, Eocalypogeia, Mizutania (Ca­ such as on living leaves where rapid maturation and completion lypogeiaceae), and Gongylanthus (Arnelliaceae) form a single ofthe life cycle are compulsory (Thiers, 1988; Gradstein, 1997; clade. However, in the phylogenetic analysis based on rps4, Gradstein & aI., 2006). It is not clear yet whether the morpho­ Calypogeiaceae is sister to the Antheliaceae, and Arnelliaceae logical features of Mizutania are also derived from neoteny. is closely related to Acrobolbaceae (Fig. 5). Heinrichs & aI. Study on the germination of Calypogeiaceae is needed (2007) resolved a sister relationship of Calypogeiaceae and to determine whether a free living stage of thalloid protone­ Arnelliaceae, while Roo & aI. (2007) found a less close relation­ mata occurs during development. Thus for, only filamentous ship between these two families. The presence ofmarsupium protonemata have been found in several species ofCalypogeia would be a synapomorphy ofthese two taxa. (Nehira, 1966). Evolution of the flattened form within leafy liverworts Several leafy liverworts growing on soil, such as Enig­ lineages. - In the leafy liverworts lineages, species with a mella (Acrobolbaceae), Pteropsiella (Lepidoziaceae), Schiff­ flattened form clearly lacking differentiated stem and leaves neria (Cephaloziaceae) and Zoopsis (Lepidoziaceae), also have occur sporadically in isolated genera. Schuster (1984) argued a thalloid appearance. Enigmella thallina G.A.M. Scott. & K.G. that modifications (adaptations) of the leafy gametophore to Beckm., having a multistratose thallus, has been described as the thalloid form occurred repeatedly in Jungermanniidae, and a member ofthe Acrobolbaceae by Beckmann & Scott (1992). suggested that the flattened gametophyte evolved via several They reported that Enigmella and Lethocolea were growing in steps in this group: the stem has changed intoa thallus-like mixed colonies on damp soil and the two genera have a long structure by flattening and broadening, and leaves became marsupium with numerous hairs on its whole surfaces. They reduced to the vestigial leaf primordia hardly recognizable mentioned that a thalloid habit might be a transient phenotypic as leaves. As a result, the body obtains a thalloid-like response to the environmental conditions as seen in Radula or unquestionably thalloid morphology, as seen in the case of yanoella which may remain in its juvenile phase due to environ­ Enigmella, Schiffneria and Zoopsis. The ultimate step, where mental pressure. ofEnigmella might have arisen from an the thallus becomes entirely unistratose with no indication ofa ancestral leafy form by the stem flattening and broadening; and recognizable axis, would be seen in such 'advanced' taxa like through reduction ofleaves as represented by the three species Cololejeunea and Radula. Mizutania grows in unstable places mentioned above. Leafy liverworts such as Zoopsis and Schiff­ in tropical regions as the species do mentioned above. Thalloid neria, with no distinctly differentiated stem and leaves, are both plants ofMizutania with leafy sexual branches are unistratose, also found in the places where Mizutania grows. These thalloid lacking differentiation ofleafand stem, and have an irregular Jungermanniidae have shared features in that the leaves are axis as a result of growth by apical and marginal meristems. extremely reduced, except on sexual branches. They also have These morphological modifications of Mizutania, indicate a similar habitat preferences: slightly dry habitats, where other more derivative character state than those ofPteropsiella and species do not grow, or unstable habitats which are disturbed Cololejeunea, where leaves are still recognizable as vestigials, by collapse ofthe substrate caused by squalls. These selection and could be considered a nearly final state ofreduction accord­ pressures may have caused morphological convergence in these ing to the modification theory proposed by Schuster (1984). leafy liverworts towards the flattened form. Several epiphytic species including Cololejeunea metzgeri­ Divergence time ofCalypogeiaceae based on the fossil re­ opsis (Schuster, 1966; Gradstein & aI., 2006), Radula aguirrei cord and molecular study was estimated about 50 Ma (Grolle & R.M. Schust. (Schuster, 1991) and Radula yanoella (Schuster, Meister, 2004; Heinrichs & aI., 2007). He-Nygren (2007) sug­ 1984, 1991) are similar to Mizutania in having leafy sexual gested that the long branches ofAntheliaceae, Calypogeiaceae branches on unistratose thalli, although the similarity might and Gyrothyraceae indicate isolation from common junger­ be a result of convergent evolution. The morphological fea­ mannioid ancestor. In our phylogenetic analysis, however, it tures found in Cololejeunea metzgeriopsis and several species appears that Mizutania is the most isolated taxon (Figs. 4-5). of Radula have been interpreted as neoteny (Schuster, 1984; Morphological diversity within the Jungermanniineae. Gradstein & aI., 2003), because Cololejeunea and Radula have - The Jungermanniineae are a morphologically highly diverse typical persistent thalloid protonemata injuvenile phase in their group as compared with other suborders of Jungermannia­ ontogeny. Morphological variations observed in Lejeuneaceae les (Hentschel & aI., 2006). Variability of characters such as seem to have originated by multiple heterochronic events, In leaf arrangement, sexual branches, underleaves and protec­ the early development ofgametophyte ofLejeuneaceae, three tive structures around archegonia and embryos, is generally developmental stages are recognizable: (1) thalloid protonemal considered to be oftaxonomic importance. He-Nygren (2007)

455 Masuzaki & al. • Systematic position ofMizutania TAXON 59 (2) • April 2010: 448-458

considered the presence ofperigynium to be a synapomorphy By its morphological features, Mizutania may be regarded as for Jungermanniineae, although several taxa lack this charac­ the most derived taxon in the Jungermanniineae. Molecular­ ter. In leafy liverworts, the perigynium is considered the most phylogenetic analyses show, that Mizutania is nested within recently evolved device protecting the developing sporophyte Calypogeiaceae. We therefore propose that Mizutaniaceae be (Hentschel & al., 2006; He-Nygren, 2007). Acquisition ofnew reduced to the synonymy ofCalypogeiaceae. protective structures might open up possibilities for adaptation to new habitats and thus may lead to divergent evolution in Calypogeiaceae Arnell this group. Specifically, in the acquisition of a marsupium (a Mizutaniaceae Furuki & Z. Iwats. in J. Hattori Bot. Lab. highly specialized perigynium penetrating the substrate), the 67: 291. 1989, syn. novo - Type: Mizutania Furuki & Calypogeiaceae and other related families might have gained Z.Iwats. an advantage through facilitation ofprostrate growth. Presence ofa marsupium would be a character supporting placement of Mizutania in the Calypogeiaceae; however, no such structure • ACKNOWLEDGEMENTS has yet been discovered. We would predict its occurance in Mizutania. We would like to acknowledge Prof. R.D. Seppelt and Mr. K.T. In the Jungermanniineae, all four fundamental leafinser­ Yong for reading the manuscript and their helpful comments, and the tion patterns ofliverworts are observed: incubous, succubous, editor-in-chief of Taxon for correction of the manuscript. We also transverse and thalloid with no differentiation ofleafand stem. gratefully acknowledge the help ofS. Tazawa and H. Matsuda in col­ The leafarrangement variation is reflected in the phylogenetic lecting materials and providing technical supports. This work was tree (Fig. 5). Taxa with incubous leaves, indicated by open supported by research grants from the Ministry ofEducation, Science, circles, correspond to Calypogeiaceae and Balantiopsidaceae; Sports and Culture (MESSC) 19570088 to H. Deguchi. those with succubous leaves (open triangles) to Acrobolbaceae, Arnelliaceae, Delavayellaceae, Geocalycaceae, Gyrothyra­ ceae, Jackiellaceae, Jungermanniaceae, Mesoptychiaceae and • LITERATURE CITED Trichotemnomaceae; those with transversely inserted leaves Adachi, J. & Hasegawa, M. 1996. MOLPHY version 2.3: Programs (open squares) to Gymnomitriaceae; and those with a thalloid for molecular phylogenetics based on maximum likelihood. structure (solid square) to Mizutania. Mapping ofleafinsertion Comput. Sci. Monogr. 28: 1-150. types on the phylogenetic tree indicates that the thalloid struc­ Akaike, H. 1974. A new look at the statistical model identification. ture of Mizutania might have evolved through modification IEEE Trans. Automat. Contr. 19: 716-723. of a gametophore with incubous leaf insertion. In the Junger­ Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, manniineae, the incubous leafinsertion and the thalloid form Z., Miller, W. & Lipman, D.J. 1997. Gapped BLAST and PSI­ BLAST: A new generation of protein database search programs. derived from it might be associated with increasing desiccation Nucleic Acids Res. 25: 3389-3402. tolerance. The incubous leaf insertion is considered to be a Beckmann, K.G. & Scott, G.A.M. 1992. A new thallose of more adaptive form for prostrate growth in a dry environment leafy liverworts from Australia. J Bryol. 17: 297-305. compared with a succubous and transverse leafinsertion pat­ Crandall-Stotler, B.J., Forrest, L.L. & Stotler, RE. 2005. Evolution­ tern (Schuster, 1984; Renzaglia & al., 2000). This is because ary trends in the simple thalloid liverworts (, subclass Metzgeriidae). Taxon 54: 299-316. the shoot apex is always protected from exposure to the air by Crandall-Stotler, B.J., Furuki, T. & Iwatsuki, Z. 1994. The develop­ the large lateral leaves. Massive verrucae on the surface ofthe mental anatomy of Mizutania riccardiodes Furuki and Iwatsuki, thallus ofMizutania including the apical cell, seem to enhance an exotic liverwort from Southeast Asia. J Hattori Bot. Lab. 75: desiccation tolerance. We suggest that the occurrence ofmas­ 243-255. sive verrucae in several other species ofCalypogeiaceae might Crandall-Stotler, B.J. & Stotler, RE. 2000. Morphology and classifi­ be a pre-adaptation for evolution to the simple gametophore of cation ofthe Marchantiophyta. Pp. 21-70 in: Shaw, A.J. & Goffinet B. (eds.), biology. Cambridge: Cambridge Univ. Press. Mizutania. Crandall-Stotler, B.J., Stotler, R.E. & Long, D.G. 2008. Morphol­ ogy and classification ofthe Marchantiophyta. Pp. 1-54 in: Shaw, A.I. & Goffinet, B. (eds.), Bryophyte biology, 2nd ed. Cambridge: • TAXONOMIC CONCLUSIONS Cambridge Univ. Press. Crandall-Stotler, B.J., Stotler, RE. & Long, D.G. 2009. Phylogeny There are several morphological similarities between and classification ofthe Marchantiophyta. Edinburgh J Bot. 66: 155-198. Calypogeiaceae and Mizutania, including (1) short sexual Efron, B. 1979. Bootstrap methods: Another look at the jackknife. Ann. branches of determinate length with 2-3-lobed, irregularly Statist. 7: 1-26. or indistinctly triseriate, reduced leaves (bracts); (2) oil bod­ Felsenstein, J. 1981. Evolutionary trees from DNA sequences: A maxi­ ies consisting ofminute granules; (3) chromosome number n mum likelihood approach. J Molec. Evol. 17: 368-376. = 9; (4) asexual reproduction by means of 1-3-celled ellip­ Felsenstein, J. 1985. Confidence limits on phylogenies: An ap­ proach using the bootstrap. Evolution 39: 783-791. soidal greenish exogenous gemmae on leaf margins or leaf Fitch, W.M. 1971. Toward defining the course ofevolution: Minimum surface; and (5) a massive cuticle (also in Mnioloma). Inter­ change for a specific tree topology. Syst. Zool. 20: 406-416. calary sexual branches seem to be synapomorphous charac­ Forrest, L.L. & Crandall-Stotler, B.J. 2004. A phylogeny of the ters ofCalypogeiaceae (except Eocalypogeia) and Mizutania. simple thalloid liverworts (Jungermanniopsida, Metzgeriidae) as

456 TAXON 59 (2) • April 2010: 448-458 Masuzaki & al. • Systematic position ofMizutania

inferred from five chloroplast genes. Monogr. Syst. Bot. Missouri Mizutania riccardioides (Mizutaniaceae). Acta Phytotax. Geo­ Bot. Gard. 98: ll9-140. bot. 59: 239-247. Forrest, L.L. & Crandall-Stotler, B.J. 2005. Progress towards a robust Inoue, S. & Furuki, T. 1992. Chromosome study ofMizutania riccar­ phylogeny for the liverworts, with particular focus on the simple dioides (Hepaticae). J Hattori Bot. Lab. 71: 263-266. thalloids. J Hattori Bot. Lab. 97: 127-159. Lanave, c., Preparata, G., Saccone, C. & Serio, G. 1984. A new Forrest, L.L., Davis, KC., Long, D.G., Crandall-Stotler, B.J., method for calculating evolutionary substitution rates. J Molec. Clark, A. & Hollingsworth, L.M. 2006. Unraveling the evolu­ Evol. 20: 86-93. tionary history ofthe liverworts (Marchantiophyta). Bryologist Nehira, K. 1966. Sporelings in the Jungermanniales. J Sci. Hiroshima 109: 303-334. Univ., Ser. B, Div. 2, Bot. ll: 1-49. Furuki, T. 1991. A taxonomical revision ofthe Aneuraceae (Hepaticae) Nixon, K.C. 1999. The parsimony ratchet, a new method for rapid ofJapan. J Hattori Bot. Lab. 70: 293-397. parsimony analysis. Cladistics 15: 407-414. Furuki, T. & Iwatsuki, Z. 1989. Mizutania riccardioides, gen. et sp. Nylander, J.A.A. 2004. MrModeltest, version 2.1. Evolutionary Biology novo (Mizutaniaceae, fam. nov.): A unique liverwort from tropical Centre, Uppsala University: Program distributed by the author. Asia. J Hattori Bot. Lab. 67: 291-296. Ohyama, K., Fukuzawa, H., Kohchi, T., Shirai, H., Sano, T., Sano, Goebel, K. 1905. Organography ofplants, especially ofthe Archego­ S., Umenoso, K., Shiki, Y., Takeuchi, M., Chang, Z., Aota, S., niatae and Spermophyta, part 2, Special organography, English Inokuchi, H. & Ozeki, H. 1986. Chloroplast gene organization ed. Oxford: Clarendon Press. deduced from complete sequence of liverwort Marchantia poly­ Gradstein, S.R. 1997. The taxonomic diversity of epiphyllous bryo­ morpha chloroplast DNA. Nature 322: 572-575. phytes. Abstr. Bot. (Budapest) 21: 15-19. Qiu, Y.L., Li, L., Wang, B., Chen, Z., Knoop, V., Groth-Malonek, Gradstein, S.R., Reiner-Drehwald, K & Schneider, H. 2003. A M., Dombrovska, 0., Lee, J., Kent, L., Rest, J., Estabrook, phylogenetic analysis ofthe genera ofLejeuneaceae (Hepaticae). G.F., Hendry, T.A., Taylor, n.w., Testa, C.M., Ambros, M., Bot. J Linn. Soc. 143: 391-410. Crandall-Stotler, B.J., Duff, RJ., Stech, M., Frey, W., Quandt, Gradstein, S.R. & Wilson, R. 2009. Protonemal neoteny in Bryo­ D. & Davis, C.c. 2006. The deepest divergences in land plants in­ phytes. Pp. 1-11 in: Mohamed, H., Bakar, B.B., Nasrulhaq­ ferred from phylogenomic evidence. Proc. Nat!' Acad. Sci. US.A. Boyce, A. & Lee, P.KY. (eds.), Bryology in the new millennium: 103: 155ll-15516. Proceedings ofthe World Bryology Conference 2007 Kuala Lum­ Ozeki, M., Isagi, Y., Tsubota, H., Jacklyn, P. & Bowman, S.J.M.D. pur Malaysia. Kuala Lumpur: Univ. ofMalaya. 2007. Phylogeography ofan Australian termite, Amitermes lau­ Gradstein, S.R., Wilson, R., Ilkiu-Borges, A.L. & Heinrichs, J. 2006. rensis (Isoptera, Termitidae), with special reference to the variety Phylogenetic relationships and neotenic evolution ofMetzgeriopsis ofmound shapes. Molec. Phylog. Evo!. 42: 236-247. (Lejeuneaceae) based on chloroplast DNA sequences and morphol­ Renzaglia, K.S. 1982. A comparative developmental investigation of ogy. Bot. J Linn Soc. 151: 293-308. the gametophyte generation in the Metzgeriales (Hepatophyta). Grolle, R. & Meister, K. 2004. The liverworts in Baltic andBitterfeId Bryophyt. Biblioth. 24: 1-253. amber. Jena: Weissdorn. Renzaglia, K.S., Duff, RJ., Nickrent, D.L. & Garbary, D.J. 2000. Guindon, S.R. & Gascuel, O. 2003. A simple, fast, and accurate al­ Vegetative and reproductive innovations of early land plants: gorithm to estimate large phylogenies by maximum likelihood. Implications for a unified phylogeny. Phi/os. Trans., Ser. B 355: Syst. Bio!. 52: 696-704. 769-793. Hasegawa, M., Kishino, H. & Yano, T. 1985. Dating ofthe human-ape Rodriguez, F., Oliver, J.F., Marin, A. & Medina, J.R. 1990. The splitting by a molecular clock of mitochondrial DNA. J Molec. general stochastic model of nucleotide substitutions. J Theor. Evo!. 22: 160-174. Bioi. 142: 485-501. He-Nygren, X. 2007. Multi-gene phylogeny supports single origin Ronquist, F. & Huelsenbeck, J.P. 2003. MrBayes 3: Bayesian phyloge­ ofjungermannioid perigynium. Ann. Bot. Fenn. 44: 450-462. netic inference under mixed models. Bioinformatics 19: 1572-1574. He-Nygren, X., Juslen, A., Ahonen, I., Glenny, D. & Piippo, S. 2006. Roo, RT., Hedderson, T.A. & Soderstrom, L. 2007. Molecular in­ Illuminating the evolutionary history of liverworts (Marchan­ sights into the phylogeny ofthe leafy liverwort family Lophozia­ tiophyta)-towards a natural classification. Cladistics 22: 1-31. ceae Cavers. Taxon 56: 301-314. Heinrichs, J., Gradstein, S.R, Wilson, R & Schneider, H. 2005. Saito, N. & Nei, M. 1987. The neighbor-joining method: A new method Towards a natural classification ofliverworts (Marchiantiophyta) for reconstructing phylogenetic trees. Molec. Bio!. Evo!. 4: 406­ based on the chloroplast gene rbcL. Cryptog. Bryo!. 26: 131-150. 425. Heinrichs, J., Hentschel, J., Wilson, R., Feldberg, K. & Schnei­ Schuster, R.M. 1966. The Hepaticae and Anthocerotae ofNorth der, H. 2007. Evolution of leafy liverworts (Jungermanniidae, America, vol. 1. New York: Columbia Univ. Press. Marchantiophyta): Estimating divergence times from chloroplast Schuster, RM. 1969. The Hepaticae andAnthocerotae ofNorth Amer­ DNA sequences using penalized likelihood with integrated fossil ica, vol. 2. New York: Columbia Univ. Press. evidence. Taxon 56: 31-44. Schuster, RM. 1984. Evolution, phylogeny and classification of the Hendry, T.A., Wang, B., Yang, Y., Davis, B.C., Braggins, J.E., Schus­ Hepaticae. Pp. 892-1070 in: Schuster, R.M. (ed.), New Manual of ter, R.M. & Qiu, Y.L. 2007. Evaluating phylogenetic positions of Bryology, vol. 2. Nichinan: Hattori Botanical Laboratory. four liverworts from New Zealand, Neogrollea notabilis, Jacki­ Schuster, RM. 1991. On neotenic species of Radula. J Hattori Bot. ella curvata, Goebelobryum unguiculatum and Herzogianfhus Lab. 70: 51-62. vaginafus, using three chloroplast genes. Bryologist 110: 738-751. Schuster, RM. 1992. The Hepaticae andAnthocerotae ofNorth Amer­ Hentschel, J., Wilson, R., Burghardt, M., Ziindorf, H.J., Schnei­ ica, east ofthe hundredth meridian, vol. 5. Chicago: Field Museum der, H. & Heinrichs, J. 2006. Reinstatement ofLophocoleaceae ofNatural History. (Jungermanniopsida) based on chloroplast gene rbcL data: Ex­ Schuster, R.M. 2000. Austral Hepaticae, part 1. Nova Hedwigia Beih. ploring the importance offemale involucres for the systematics ll8: 1-524. ofJungermanniales. P!. Syst. Evol. 258: 211-226. Shimodaira, H. 2002. An approximately unbiased test of phyloge­ Hewson, J.H. 1970. The family Aneuraceae in Australia and New netic tree selection. Syst. Bio!. 51: 492-508. Guinea: 11, The genus Riccardia. Proc. Linn. Soc. New South Shimodaira, H. & Hasegawa, M. 2001. CONSEL: For assessing the Wales 95: 60-121. confidence of phylogenetic tree selection. Bioinformafics 17: Inoue, A., Furuki, T. & Imaichi, R. 2008. Developmental mor­ 1246-1247. phology of irregularly-shaped gametophytes of the liverwort Sikes, D.S. & Lewis, P.O. 2001. PAUPRat: PAUP* implementation

457 Masuzaki & al. • Systematic position ofMizutania TAXON 59 (2)· April 2010: 448-458

of the parsimony ratchet, beta software, version 1. Department penalties and weight matrix choice. Nucleic Acids Res. 22: ofEcology and Evolutionary Biology, University of Connecticut, 4673-4680. Storrs. Tsubota, H. & Deguchi, H. 2004. Molecular phylogenetic relationships Swofford, D.L. 2002. PAUP*. Phylogenetic analysis using parsimony ofJungermanniidae based on rbcL sequences, with special refer­ (*and other methods), version 4. Sunderland, Massachusetts: ence to Mizutania riccardioides. P. 7 in: Gradstein, S.R., Heinrichs, Sinauer. 1. & Wilson, R. (orgs.), Bryophylogeny 2004, SecondInternational Tamura, K. & Nei, M. 1993. Estimation of the number of nucleotide Symposium on Molecular Systematics ofBryophytes. Albrecht von substitutions in the control region of mitochondrial DNA in hu­ HaIler Institute ofPlant Science, Gottingen, Germany. [Abstract.] mans and chimpanzees. Molec. Bio!. Evo!. 10: 512-526. Tsubota, H., Nakao, N., Arikawa, T., Yamaguchi, T., Higuchi, M., Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA 4: Mo­ Deguchi, H. & Seki, T. 1999. A preliminary phylogeny ofHyp­ lecular evolutionary genetic analysis (MEGA) software version nales (Musci) as inferred from chloroplast rbcL sequence data. 4.0. Molec. BioI. Evo!. 24: 1596-1599. Bryo!. Res. 7: 233-248. Tatuno, S. 1941. Zytologische untersuchungen ilber die Lebermoose Tsubota, H, De Luna, E., Gonzalez, D., Ignatov, M.S. & Deguchi, H. von Japan. 1. Sei. Hiroshima Univ., Ser. B. Div. 2, Bot. 4: 73-187. 2004. Molecular phylogenetic and ordinal relationships based on Tavare, S. 1986. Some probabilistic and statistical problems in the analyses ofa large-scale data set of600 rbcL sequences ofmosses. analysis ofDNA sequences. Lecf. Math. Life Sei. 17: 57-86. Hikobia 14: 149-169. Thiers, B. 1988. Morphological adaptations of the Jungermanniales Tsubota, H., Takahashi, K., Nakahara, M., Mohamed, H. & Degu­ (Hepaticae) to the tropical rainforest habitat. 1. Hattori Bot. Lab. chi, H. 2005. A simple procedure for DNA isolation using small 64: 5-14. quantities oflichen thallus. Lichenology 4: 25-28. Thompson, J.D., Higgins, D.G. & Gibson, T.J. 1994. CLUSTAL Yang, Z. 1997. PAML: A program package for phylogenetic analysis by W: Improving the sensitivity of progressive multiple sequence maximum likelihood. Comput. Appl. Biosci.13: 555-556. alignment through sequence weighting, positions-specific gap

458