Published by Maney Publishing (c) British Bryological Society O 10.1179/1743282012Y.0000000018 DOI ß ulg.ac.be of University Botany, of Lie Institute Vanderpoorten, Alain to: Correspondence polyphy- be to Geo- and shown letic, 2003). subsequently Gradstein, were Physothecoideae calycaeae & subfamily (Engel of in- new warrant (Geocalycaceae) suite the to Its to within thought was endemic clusion 2003). states species Gradstein, character and unique & genus (Engel liverwort Ecuador new a as autoica Physotheca Introduction Keywords: 1 Vanderpoorten Alain Mitt. with relationships actual its blurred Lophocoleaceae) (Marchantiophyta: Physotheca in evolution autapomorphic Striking obr Gradstein Robbert S nlsso w pN oi h eut niaeta h eu snse within nested is genus the that indicate results The loci. cpDNA two of analyses including Gradst., od etitdt nela ae n red-brown and Leptoscyphus base, of underleaf coloration rhi- to underleaves, restricted bifid zoids leaves, oriented strongly succubously undivided, of combination the While 2006a). n two includ- ing clade unsupported an within Lophocoleaceae, h aooi ttsadpyoeei oiino h ooyi iewr genus liverwort monotypic the of position phylogenetic and status taxonomic The Syste nraigbd feiec,ta xrm opooia rnfrain a bcr h phylogenetic the obscure can transformations data. morphological morphological extreme in that present signal evidence, of body increasing combination, e-iepratsta eakbyrsml the resemble remarkably that perianths blad- inflated, produces der-like abundantly and autoecious to gynoecium. opposed the of As bracteoles or bracts the below from h te ebr ftefml,temd fgrowth of mode the family, of Unlike the of features. members other unique the several by Lophocoleaceae nttt fBtn,Uiest fLie of University Botany, of Institute g,B2Sr imn -00Lie B-4000 Tilman, Sart B22 `ge, rts rooia oit 2012 Society Bryological British Physotheca ´ aiu vlto,Prs France Paris, Evolution, & matique Leptoscyphus atp Physotheca B- rbc , .autoicus L. Physotheca sb eetdinvtosoriginating innovations repeated by is ,Eudr iewrs oeua hlgn,Mrhlg,Pa Morphology, phylogeny, Molecular Liverworts, Ecuador, L, Physotheca Leptoscyphus ..ne rdt a described was Gradst. & J.J.Engel .autoica P. a eovda ebro the of member a as resolved was it pce (Hentschel species Mitt. g,Blim mi:a.vanderpoorten@ Email: Belgium. `ge, JJEgl&Gas. adr.&Gas. smd.Ti niae,aogwt an with along indicates, This made. is Gradst., & Vanderp. Gradst.) & (J.J.Engel r nedrmnsetof reminiscent indeed are ifr rmayother any from differs 2 ..ne Gradst. & J.J.Engel 1 Aure , species, ..ne rdt nei oEudr r nerdfo phylogenetic from inferred are Ecuador, to endemic Gradst. & J.J.Engel ` e Belgium, ge, ´ i De lie Physotheca ´ samore tal. et 2 uemNtoa ’itieNtrle De Naturelle, d’Histoire National Museum is , ´ 1 aooi infiac fisuiu morphological taxo- features. unique the its of of re-assess significance status taxonomic to and here position us nomic allows This 2009). Vanderpoorten, two & (Devos genera related within of closely at and species level discriminate appropriate amplified to the variation successfully displaying type loci the be chloroplast near could made collections locality two recently, Most Hentschel and (Vanderpoorten the failed collections previously in study additional used as extracts well DNA as material type (Engel 2003). spirals of Gradstein, uncoiling & the in collapse, of of resulting stages ultimately various elaters in frequently the are walls uncoil, their not persistent do a that Physotheca have spirals wall, and com- capsule wall, are the from Lophocoleaceae free other pletely of elaters Lophocoleaceae, the other while 30 of reach those they wherein than diameter) in of spores Further- the Lophocoleaceae. more, most in than thicker genus is wall unrelated completely the Pleurozia of perianths sterile ejmnLaenen Benjamin , rm,Sxa systems, Sexual ´ramo, eea tepsa sequencing at attempts Several Dumort. Leptoscyphus r rqetyvrosyucie and uncoiled variously frequently are ora fBryology of Journal Physotheca trn Physotheca L m ttevr ot Finally, most. very the at m Leptoscyphus 1 , Physotheca s78srts capsule stratose 7–8 ’s r agr(31–39 larger are Physotheca 2012 ´ Physotheca partement tal. et tal. et Leptoscyphus n h new the and VOL ..ne & J.J.Engel .34 2010a). , n the and (2006a) from NO m m .4 251 Published by Maney Publishing (c) British Bryological Society adrore tal. et Vanderpoorten 252 ora fBryology of Journal uot) eioica ( Lepidoziaceae Dumort.), al oce nomto n eBn ceso ubr o h w cesosof accessions two the for numbers accession GenBank and information Voucher 1 Table ( pidozia ( bertaceae of members included and ( taxa Plagiochilaceae Outgroup the latter. the in and ner, Pachyglossa including Hentschel thus by genera circumscribed other including as for Lophocoleaceae, GenBank from of available those compared to amplification, subsequently were Long sequences extraction, & These Vanderpoorten (2006). in DNA described sequencing of and protocols of accessions the two the for First, produced genus. the and of status position the phylogenetic were test its strategies determine to sampling employed taxonomic Two 1). and (Table Ecuador molecular southern in locality of same the collections two The Methods and Material .autoica P. h eei oiinof position generic accessionthe Lophoco- the GenBank to (Heinrichs related and leaceae closely are details which further numbers), for 2006, .autoica P. the The - (2006). Long & Vanderpoorten in of accessions rbc eersoe noasprt arx neswere Indels indels matrix. homologous and separate indels presence–absence, a for and scored into homology, rescored positional were preserve to ment out- & as Vanderpoorten (2006). of used Long analyses the were upon R.M.Schust. based groups Nees) and & Lindenb. Solari genus. that (C.Massal.) of species the with affinities closer 1–5 potential investigate by to represented specimens, being species each (2009), poorten Trichocolea rbc aswr netdweencsayi h align- the in necessary where inserted were Gaps negncsae a eune o h two the for sequenced was spacer intergenic L Leptoscyphus eune eete oprdt hs of those to compared then were sequences L Pedinophyllopsis Leptoscyphus Dmr. uot)adTrichocoleaceae and Dumort.) (Dumort.) 1 2 hlgntcpsto of position Phylogenetic Herbertus MB6984 Haro-Carrion X. & Burghardt M. MB6973 Haro-Carrion X. & Burghardt M. ezg&Grolle), & Herzog uot)(e adrore Long, & Vanderpoorten (see Dumort.) .autoica P. Lophocolea oce Locality Voucher pce nlddb eo Vander- & Devos by included species 2012 tal. et L,PC) (LG, L,PC) (LG, Plagiochila ry,Lpclaee( Lepicoleaceae Gray), sn n ceso e species per accession one using , ..cut nu) Her- Inoue), & R.M.Schust. Physotheca 05,i re odetermine to order in 2005), , sn h rtcl described protocols the using .autoica P. VOL Bazzania .australis L. Dmr. uot and Dumort. (Dumort.) etsyhsantarcticus Leptoscyphus .34 cao,Zmr-hnhp,Pru ainlPodocarpus, Estacio Nacional Parque Zamora-Chinchipe, Ecuador, cao,Zmr-hnhp,Pru ainlPodocarpus, Estacio Nacional Parque Zamora-Chinchipe, Ecuador, hub subpa shrubby hub subpa shrubby Physotheca Heteroscyphus tal. et Chiloscyphus Dmr. Dumort. (Dumort.) trn eod the Second, . NO nCientı ´n nCientı ´n eune were sequences L .4 .autoica P. rgntdfrom originated ryand Gray 20b 2007), (2006b, trn rm,eiht ntisadbace,26/04/2008 branches, and twigs on epiphyte ´ramo, rm,eiht ntisadbace,26/04/2008 branches, and twigs on epiphyte ´ramo, fc rnic,Cmn Antenas, Camino Fransisco, ´fica fc rnic,Cmn Antenas, Camino Fransisco, ´fica and L (Gottsche, Lepicolea Schiff- Corda atp using atp Le- B- B Leptoscyphus to The non-parametric Results a replicates. after 100 with assessed analysis bootstrap was branches Support implemented for (http://code.google.com/garli/). as 2.0 analysis, Garli by partitioned a in employed 6.20) sncsayt accommodate to within necessary is 2003), Gradst. 764. & Vanderp. ( Gradst.) & combination, Engel new and synonym the Leptoscyphoideae), a (subfam. as Lophocoleaceae abandoned of be must Physothecoideae within nested of position evidence phylogenetic previous (Hentschel confirm results The Discussion rle,adtelarge the and ( Grolle), E.W.Jones of of up made accessions amphibolius clade the two between resolved the 2, Figure ( tree ML whose lyses, niae httesieo nqefaue displayed features unique of suite the that indicates combined the In 1). (Figure of accessions two the included support bootstrap and 69% low fairly a with monophyletic ( tree mn tts h w oesdsrbn DNA describing models simultaneously were variation two indel and was rate The substitutions transition single evolution states. a with among Indel model a by using 2008). described implemented (Posada, as the using jModeltest Criterion substitution Information DNA of Akaike model selection best-fit after the analysis of (ML) Likelihood Maximum analyses. char- the multistate from excluded as were scored Gaps were acters. lengths different of hsteaautoica Physotheca h nlso of inclusion The h w aamtie eesbitdt a to submitted were matrices data two The .porphyrius L. trn 2 Leptoscyphus. ln nlsscnegdtwrsasnl ML single a towards converged analyses L L tal. et 5 Physotheca ca ca Ne)Gol and Grolle (Nees) ). 3422.15). 5 Leptoscyphus 60m, 2650 60m, 2650 Leptoscyphus 06)cnenn h phylogenetic the concerning 2006a) , Ne)Gol ld ( clade Grolle (Nees) .autoica P. ..ne rdt,Txn52: Taxon Gradst., & J.J.Engel 2 Leptoscyphus .gradsteinii L. n niaeta h eu is genus the that indicate and ln etsyhsautoicus Leptoscyphus hsteaautoica Physotheca L sacneune the consequence, a As . 5 733)i rsne in presented is 3773.35) Q456JQ446574 JQ446576 Q457JQ446575 JQ446577 trn subg. within .infuscatus L. trn L hsteaautoica Physotheca z L .autoica P. a eovdas resolved was atp number accession GenBank Vanderp. Leptoscyphus Physoscyphus Leptoscyphus B- atp ob nov. comb. 5 rbc .autoica P. B- L. ana- L rbc (Mitt.) tal. et subg. were L (J.J. Published by Maney Publishing (c) British Bryological Society iue1Ms ieyte fteaayi of analysis the of tree likely Most 1 Figure ubr eo h rnhsaennprmti otta values. bootstrap non-parametric are branches the below Numbers trn eune in sequences L hsteaautoica Physotheca n te ebr fteLophocoleaceae. the of members other and adrore tal. et Vanderpoorten ora fBryology of Journal hlgntcpsto of position Phylogenetic 2012 VOL .34 NO Physotheca .4 253 Published by Maney Publishing (c) British Bryological Society adrore tal. et Vanderpoorten 254 ora fBryology of Journal iue2Ms ieyte fteaayi of analysis the of tree likely Most 2 Figure eo h rnhsaennprmti otta values. bootstrap non-parametric are branches the below hlgntcpsto of position Phylogenetic 2012 VOL .34 Physotheca NO .4 trn and L atp B- rbc eune in sequences L hsteaautoica Physotheca and Leptoscyphus Numbers . Published by Maney Publishing (c) British Bryological Society n ayoeaee(Gradstein Calypogeiaceae and respectively [genus families, liverwort Lejeuneaceae leafy proved of which members be Asia, to Southeast from both taniaceae), showed however, sequences, unusual that its DNA and anatomy. insertion, hyaline narrow stem very broad, a a and with including border features leaves morphological complicate-bilobed unique its of of series because Perssoniellaceae a family own its to assigned cincta genus monospecific liverwort the example, For data. morphological in present signal trans- phylogenetic the morphological obscure Gradstein can extreme formations that (see review), evidence for 2011, of body increasing of suite substantial observed. and a transformations sudden morphological the explain to may which (Crawford 2009), correlated transformations typically morphological are systems the times of multiple branches (Devos recent phylogeny occurred most the monoecy along independently to dioecy from h eprt otenhmshrcgenera glossa southern-hemispheric temperate the al. et and ceae) thalloid genera the are cases remarkable Other 2010). Glenny, Schistochila bryophytes. in rapid fairly be Within can systems shifts sexual that in indicates however, evidence, Phylogenetic condi- autoecious of the tion particular, of In accessions Mitt.). different (Hook.) the leading to length leading branch short fairly to the (see typical phology an the from displaying rapidly comparatively ancestor evolved taxon the by etdwithin data nested genus monospecific molecular the docu- Hattorioceros where recently hornworts, on was in case mented similar based A 2002). (Heinrichs, Dumort. (Dumort.) (Hentschel ( ( to belong Corda to shown were which Schust., and Schust., yuuulaeulrpoutv eie,and of members be devices, to proved reproductive leaves, saccate asexual monospecific Szweykowskia the unusual Plagiochilaceae, by In genera neotropical 2010). He, Amphilophocolea loehr hs aaidct,aogwt an with along indicate, data these Altogether, .autoica P. 00.Eape rmLpooeca include Lophocoleaceae from Examples 2010). , Perssoniella ezgedmct e aeoi,wslong was Caledonia, New to endemic Herzog ezg&Grolle, & Herzog Metzgeriopsis Radula .autoica P. Pachyglossa tal. et Mizutania uot,fml citciaee(e& (He Schistochilaceae family Dumort., Cyanolophocolea JHsg)JHsg a hw obe to shown was J.Haseg. (J.Haseg.) nFgr scmae oteones the to compared as 2 Figure in rdt .enr ihbizarre with E.Reiner, & Gradst. Phaeoceros uot o ntne h transition the instance, for Dumort. Perssoniella 07 Engel 2007; , , a etdwti h ag genus large the within nested was tal. et Steereochila )and suiu within unique is Cyanolophocolea Cololejeunea ..Gee (Metzgeriopsida- Goebel K.I. 01.Teesit nsexual in shifts These 2011). , uui&Iask (Mizu- Iwatsuki & Furuki rs. hra unique whereas Prosk., Heteroscyphus ezg with Herzog, Amphilophocolea tal. et tal. et RMShs. R.M. (R.M.Schust.) nu,characterized Inoue, Leptoscyphus Src)Schiffn.] (Spruce) 06 Masuzaki 2006; , 00 ne & Engel 2010; , respectively ) Leptoscyphus .cuneifolius L. Chiloscyphus Plagiochila .vitreo- P. Schiffn., tal. et Pachy- tal. et R.M. mor- , , . ne,JJ rdti,SR 2003. S.R. Gradstein, & J.J. Engel, ne,JJ e .2010. X. He, & J.J. Engel, eto hrce vlto n biogeographic and evolution group. the character assess- in accurate patterns more of a allow of ment and liverworts context of tion classifica- revised a the propose to framework appropriate in (http://www.bio- the offer project certainly genera Life’ will logy.duke.edu/bryology.LiTol/) of Tree those ‘Liverwort the of Masuzaki assessment 2010; Glenny, Fuselier & He ancestral Engel (e.g. 2010; be derived recently be to to contrast, appear in but, not do of morphologies suites their unique since testing be phylogenetic to to shown vulnerable been recently have that genera stenotypic (see Vanderpoorten features are the morphological activity, extreme of (60 tectonic by opening characterized period continuous the and long since Atlantic the isolation South to of years) owing million Tertiary the diverged have to during assumed are part, most the for which, (e.g. apomorphic Cephalantholejeunea highly Haesselia and is each) genera Zoopsidella stenotypic liverwort species are genera in endemic (1–3 the rate of most endemism observed, highest where example, the for phylogenetic Neotropics the the In as increases. effort taxonomy liverwort in expected 2011). eo,N adrore,A 2009. A. Vanderpoorten, & N. Devos, rrdaemr,wudsgetohrie(Li otherwise suggest a would of absence mark, spores and triradiate surface small canaliculated-striate including a with hornworts, among features eo,N,Rne,M,Gasen .. hw ..& A.J. Shaw, S.R., Gradstein, M., Renner, N., Devos, rwod . esn ..&GrokJns ..2009. P.J. Garnock-Jones, & L.K. Jesson, M., Crawford, References nov. comb. Changes: autoicus and Additions Taxonomic for acknowledged. Funds is 2.4557.11) from PhD (grant Belgian support FNRS and Financial the (FNRS). associate Research of research Scientific are respectively, BL students, and AD AV, Acknowledgements usata aooi hne uthnebe hence must changes taxonomic Substantial un iewr rmNwZaadadAsrla ae on based Australia, and Zealand New from liverwort guing ufm hsteoda ..ne Gradst. & Geocalycaeeae subfamily, J.J.Engel 763–73. new Physothecoideae a to subfam. belonging Ecuador, from Physotheca ytmtciett of identity systematic in n opooia rnfrainrtsi h liverwort the in rates genus transformation morphological and tion, taeisadhbttslcini h iewr genus liverwort the Phytologist in New selection habitat and strategies 2011. A. Vanderpoorten, orltdeouino eulsse n iehsoytraits life-history and system mosses. sexual in of evolution Correlated Leptoscyphus tal. et JJEgl&Gas. adr.&Gradst. & Vanderp. Gradst.) & (J.J.Engel rle&Gradst., & Grolle ( Evolution hsteaautoica Physotheca ..ne rdt,anwgnso Hepaticae of genus new a Gradst., & J.J.Engel 01.Amr opeetxnmcre- taxonomic complete more A 2011). , R.M.Schust., adrore tal. et Vanderpoorten ora fBryology of Journal 9() 225–36. 192(1): , tal. et . 35:1129–42. 63(5): , Evolution ..cut,ec) hs genera, These etc.). R.M.Schust., Cyanolophocolea 00) ti rcsl those precisely is It 2010b). , tde nLpooeca.XX The XIX. Lophocoleaceae. on Studies vlto fsxa ytm,dispersal systems, sexual of Evolution 33:779–92. 63(3): , tde nGoayaeeXIV. Geocalycaceae on Studies Schusterolejeunea Pteropsiella ag ijntos specia- disjunctions, Range ..ne Gradst.) & J.J.Engel hlgntcpsto of position Phylogenetic 2012 ..cut,a intri- an R.M.Schust., Leptoscyphus tal. et VOL Taxon .34 Spruce, 2010; , Grolle, Radula tal. et 2(4): , tal. et NO Physotheca .4 , , . 255 Published by Maney Publishing (c) British Bryological Society adrore tal. et Vanderpoorten 256 ora fBryology of Journal etce,J,Flbr,K,Zu K., Feldberg, J., Hentschel, enih,J,Gasen .. isn .&Shedr .2005. H. Schneider, & R. Wilson, S.R., Gradstein, J., Heinrichs, enih,J 2002. J. Heinrichs, 2010. D. Glenny, & X.L. He, J. Heinrichs, & A.-L. Ilkiu-Borges, R., Wilson, S.R., Gradstein, rdti,SR,IkuBre,AL adrore,A 2011. A. Vanderpoorten, & A.L. Ilkiu-Borges, S.R., Gradstein, ueir .. hw . ne,JJ,vnKna,M,Csa D.P., Costa, M., Konrat, von J.J., Engel, 2010. B., Shaw, D. L.C., Fuselier, Glenny, & X.L. He, J.J., Engel, cnie,H enih,J 2007. J. Heinrichs, of & H. Schneider, 131–50. etoiswt rlmnr udvso fNeotropical of subdivision lineages. nine preliminary into a Plagiochilaceae with Neotropics ae nteclrpatgene chloroplast the on based classification natural a Towards 1–184. 58: Hylacoetes Society morphology. and sequences Metzgeriopsis 2006. citciaee e lsiiainbsdo molecular on based classification new phylogenies. a Schistochilaceae: unusual of of evolution Ecuador. case from the the – triggers morphologies specialization Habitat ohclaeeXI.Tesseai oiinof position systematic of R.M.Schust. The status XXII. Amphilophocolea Lophocoleaceae Bryologist genus liverwort 2011. the A.J. of Shaw, & N. Devos, 149–63. opooia n oeua evidence. molecular and morphological Pachyglossa hlgntcrltosisadnoei vlto of evolution neotenic and relationships Phylogenetic 5() 293–308. 151(3): , hlgntcpsto of position Phylogenetic 1() 92–101. 114(1): , sect. , utainSseai Botany Systematic Australian Phytotaxa Tetracymbaliella Ljueca)bsdo hools DNA chloroplast on based (Lejeuneaceae) Bryologist ..cut oehrwt omnso the on comments with together R.M.Schust. aooi eiinof revision taxonomic A Adiantoideae and 2012 Apometzgeria :41–52. 9: , Clasmatocolea 1() 9–22. 114(1): , VOL rbc oaia ora fteLinnean the of Journal Botanical ooeenastotleriana Cololejeunea Perssoniella ¨ndorf,H.-J.,Hellwig,F.H., h ttsadphylogeography and status The flvrot (Marchantiophyta) liverworts of .34 L. n sect. and Physotheca rleand Grolle rpoai Bryologie Cryptogamie rohtrmBibliotheca Bryophytorum ua.(Metzgeriaceae). Kuwah. h ytmtcposition systematic The NO (Jungermanniopsida: .4 34:229–38. 23(4): , n h eeaof genera the and Fuscoluteae Bryologist Plagiochila Lamellocolea tde on Studies 113(1): , p nov. sp. 26(2): , nthe in sect. , etce,J,Zu J., Hentschel, etce,J,Wlo,R,Brhrt . Zu M., Burghardt, R., Wilson, J., Hentschel, adrore,A og ..2006. D.G. Long, & A. Vanderpoorten, adrore,A,Scha A., Vanderpoorten, adrore,A,Gasen .. aieMA&Dvs .2010b. N. Devos, & M.A Carine S.R., Gradstein, A., Vanderpoorten, oaa .2008. D. Posada, 2011. L. Zhou, & L. Zhang, J., Li, auai H. Masuzaki, enih,J 2006b. J. Heinrichs, & od Jnemnils ohclaee ae nnrITS on based Lophocoleaceae) (Jungermanniales: Corda xlrn h motneo eaeivlce o the for involucres female Jungermanniales. of Evolution of importance systematics the exploring ohclaee nerdfo rN T eune and sequences ITS nrDNA morphology. from inferred Lophocoleaceae) Jnemnipia ae nclrpatgene chloroplast on 2006a. based J. (Jungermanniopsida) Heinrichs, & H. etoia rgno h zra nei liverwort, endemic Azorean the 73–83. 40(1): of azoricus Leptoscyphus origin Neotropical h hsso odaaadLuai nmdr liverwort modern in Laurasia and Gondwana distributions. of ghosts The 86. Leptoscyphus 2010a. D.G. Long, 6(–) 125–37. 262(1–2): morphology. and sequences oeua ilg n Evolution and Biology Molecular ana- phylogenetic molecular lyses. from inferred Marchantiophyta) h ngai liverwort enigmatic 2010. H. Deguchi, the & H.M.A. Majid, T., 6. genus Taxon Hattorioceros 5(–) 211–26. 258(3–4): , , hmmr,M,Frk,T,Tuoa . Yamaguchi, H., Tsubota, T., Furuki, M., Shimamura, nof .J,Hlwg .. Scha F.H., Hellwig, H.-J., ¨ndorf, 92:448–58. 59(2): , Taxon ilgclReviews Biological Lpooeca)revisited. (Lophocoleaceae) Mdlet hlgntcmdlaveraging. model phylogenetic jModelTest: frVrip . enih,J,Dvs .& N. Devos, J., Heinrichs, A., ¨fer-Verwimp, h aooyo h ef iewr genus liverwort leafy the of taxonomy The 64:1136–42. 56(4): , (Anthocerotophyta). . oeua hlgntc n Evolution and Phylogenetics Molecular aooi tde in studies Taxonomic enttmn fLophocoleaceae of Reinstatement ln ytmtc n Evolution and Systematics Plant 53:471–87. 85(3): , 57:1253–6. 25(7): , Mizutania hlgntcpsto fthe of position Phylogenetic ln ytmtc and Systematics Plant udn pcainand speciation Budding nof .J,Schneider, H.-J., ¨ndorf, ytmtcpsto of position Systematic Taxon Taxon frVrip A. ¨fer-Verwimp, (Mizutaniaceae, 06:1633– 60(6): , 91:176– 59(1): , Chiloscyphus rbc data: L , ,