Plagiochilaceae (Inoue, 1966)

Patzak, Simon D. F., Renner, Matt A. M., Schäfer-Verwimp, Alfons, Feldberg, Kathrin, Heslewood, Margaret M., Peralta, Denilson F., de Souza, Aline Matos, Schneider, Harald & Heinrichs, Jochen, 2016, A phylogeny of Lophocoleaceae-Plagiochilaceae-Brevianthaceae and a revised classification of Plagiochilaceae, Organisms Diversity & Evolution (New York, N. Y.) 16 (3), pp. 481-495 : 488-489

Plagiochilaceae

The extended sampling in the present study identifies conflicts between the current classification of the Plagiochilaceae and the presented phylogenetic hypothesis. Two genera belonging to the lineage sister to Plagiochila were not monophyletic; Acrochila was resolved polyphyletic and Plagiochilion paraphyletic with Chiastocaulon . The paraphyly of Plagiochilion is particularly surprising given that the genus was erected for species possessing the apparently unique feature of leaves in opposing pairs. The tree topology suggests a reversal to the ancestral leaf arrangement or two independent origins of opposing leaf-pairs; these alternatives have yet to be tested. Either way, the result highlights again the homoplastic nature of many morphological characters employed to circumscribe sections, subgenera and genera within liverworts, which is becoming a common theme in liverwort taxonomy ( Devos et al. 2011; Dong et al. 2012; Bechteler et al. 2015).

Plagiochila represents the largest genus of the liverworts ( Inoue 1984). In its current circumscription, the genus is characterized by dioicy, alternating, rarely subopposite foliation, nearly exclusively lateral branching and a laterally compressed perianth with a dorsal keel which is usually slightly longer than the ventral one (Heinrichs 2002). The presented sectional classification ( Figs. 3 and 4 ) is consistent with results of earlier studies (e.g. Heinrichs 2002; Heinrichs et al. 2004a, 2005b, 2006; Groth et al. 2004; Groth 2006; Söderström et al. 2015) and is thus not discussed here; however, for the time being, we use the taxon Plagiochila sect. Fuscae rather than P. sect. Tayloriae Carl ( Söderström et al. 2015) for a clade depicted in Fig. 3 . Plagiochila sect. Fuscae was placed in the synonymy of P. sect. Tayloriae by Söderström et al. (2015) based on Groth (2006). However, the treatment of Groth (2006) of P. sect. Tayloriae relied on Inoue and Schuster (1971) who considered the sectional type species Plagiochila taylorii Steph. a synonym of Plagiochila stephensoniana Mitt. Both P. fusca Sande Lac. and P. stephensoniana nest in the same clade ( Groth 2006; this study); however, Engel and Merrill (2009) rejected the above synonymy and proposed that P. stephensoniana and Plagiochila fuscella (Hook. f. & Taylor) Gottsche, Lindenb. & Nees were conspecific. The latter species has not yet been included in molecular phylogenies, and its systematic position should thus be regarded as unknown.

Earlier authors included several species in Plagiochila that are now placed in a couple of satellite genera based on morphological and molecular evidence. Dinckleria was separated from Plagiochila (as Proskauera Heinrichs & J.J. Engel , nom. illeg.) based on its position in molecular phylogenies and its spherical leaf papillae ( Heinrichs et al. 2006). Pedinophyllum includes the four autoicous members of the Plagiochilaceae ( Inoue 1966) ; its generic status was confirmed in several molecular phylogenetic studies including the generitype P. interruptum (e.g. Groth and Heinrichs 2003; Heinrichs et al. 2006; Feldberg et al. 2010c). The monospecific genus Pedinophyllopsis R.M. Schust. & Inoue was originally placed in Geocalycaceae ( Schuster and Engel 1981) but transferred to Plagiochilaceae by He-Nygrén and Piippo (2003) based on molecular phylogenetic evidence. It forms a well-supported sister relationship with Pedinophyllum ( Fig. 3 ). Pedinophyllopsis abdita (Sull.) R.M. Schust. & Inoue differs from other members of Plagiochilaceae by androecia on ventral-intercalary branches, ventral intercalary gynoecial innovations and the presence of one to two very large oil bodies that nearly fill the complete cell lumen ( Grolle 1962; Schuster and Engel 1981; Hässel de Menéndez 1990). Two accessions of P. radiculosa are sister to the Pedinophyllopsis- Pedinophyllum clade ( Fig. 3 ), confirming the phylogeny of Groth (2006). Based on its position outside of Plagiochila , P. radiculosa is transferred to a new genus, Cryptoplagiochila S.D.F. Patzak, M.A.M. Renner & Heinrichs. Based on morphology alone, Cryptoplagiochila would hardly be excluded from Plagiochila , although Inoue and Schuster (1971) suggested its isolated position based on the “ Jamesoniella -like” habit of the species. Oil bodies of P. radiculosa are granular, ellipsoidal or with tapering ends, and light brownish pigments, four to seven per leaf medial cell. It can be separated from other Plagiochilaceae by its specific character state combination but not by apomorphies. Finally, the synonymy of Plagiochila sect. Radiculosae Inoue & R.M. Schust. and P. sect. Tayloriae suggested by Söderström et al. (2015) is best considered as ambiguous and should not be employed until further studies confirm the status.

The genera Acrochila , Chiastocaulon and Plagiochilion were erected for plagiochiloid species which frequently or exclusively produce ventral-intercalary vegetative branches. Chiastocaulon was established for species with alternating leaves and lateral-terminal, lateral-intercalary as well as ventral-intercalary branches ( Carl 1931). Plagiochilion includes species with opposite leaves and predominantly or exclusively ventral-intercalary branching ( Inoue 1964) while Acrochila has alternating leaves and only ventral-intercalary branches ( Schuster 1963; Inoue and Schuster 1971). The generic status of Chiastocaulon and Plagiochilion was confirmed in several molecular phylogenies (e.g. Groth and Heinrichs 2003; Groth 2006; Heinrichs et al. 2006; Feldberg et al. 2014). Groth (2006) identified Acrochila as a member of Plagiochilaceae based on an rps 4 sequence; however, he treat- ed it as a member of Jamesonielloideae based on an rbc L dataset. According to our phylogeny, the latter must be rejected; the incomplete rbc L sequence used in Groth (2006) [GenBank accession DQ194104] is derived from a member of the Adelanthaceae sensu Feldberg et al. (2010b) rather than from Acrochila . Extension of the molecular taxon sampling in the current study indicates that Chiastocaulon and Acrochila nest in Plagiochilion and that Acrochila is polyphyletic ( Fig. 3 ). Although the backbone of the Acrochila-Chiastocaulon-Plagiochilion clade is not fully resolved, we consider current evidence sufficient to treat Acrochila and Plagiochilion as synonyms of Chiastocaulon . We transfer only currently accepted Acrochila and Plagiochilion binomials to Chiastocaulon . The internal structure of Chiastocaulon oppositum (Reinw., Blume & Nees) S.D.F. Patzak, M.A.M. Renner, Schäf. -Verw. & Heinrichs and C. dendroides provides some evidence for further entities; however, a detailed taxonomical revision of Chiastocaulon is beyond the scope of this study. South American taxa that were assigned to Plagiochilion by some authors ( Plagiochila bryhnii Steph., Inoue 1964 ; Plagiochila heteromalla (Lehm. & Lindenb.) Lindenb., Hässel de Menéndez 1983 ) lack the typical ventral branching systems of Plagiochilion and may belong to Plagiochila (Heinrichs 2002; Söderström et al. 2016). Their definite taxonomical treatment should await their inclusion in molecular phylogenetic analyses; however, material suitable for DNA extraction has not yet become available. Both Plagiochila and Chiastocaulon s.l. express broad morphological variation in leaf shape, dentition and arrangement. Alternating foliation is typical for Plagiochila (e.g. Inoue 1984); however, a few species have (sub-)opposite leaves, e.g. Plagiochila macrostachya Lindenb. (Heinrichs 2002) . Similarly to the situation in Chiastocaulon , Plagiochila includes species with different branching systems. Several independent lineages share lateral-intercalary plus lateral-terminal branching [e.g. P. sect. Glaucescentes ( Heinrichs et al. 2000), P. sect. Vagae ( Heinrichs et al. 2002)] whereas others produce only lateral-intercalary branches [e.g. P. sect. Plagiochila ( So and Grolle 2000) , P. sect. Fuscoluteae (Heinrichs 2002)]. The variation of leaf orientation from wide spreading to laterally appressed in Chiastocaulon s.l. is also seen in Plagiochila . In summary, Chiastocaulon s.l. represents a morphologically variable lineage that can be separated from other Plagiochilaceae by the frequent occurrence of ventral branches. It may include some 20 species ( Söderström et al. 2016). According to our phylogeny, Plagiochilaceae consists of Chiastocaulon , Dinckleria , Pedinophyllopsis , Pedinophyllum , Plagiochila , Pseudolophocolea and Cryptoplagiochila . Two further putative members, Plagiochilidium Herzog and Xenochila R.M. Schust. ( Söderström et al. 2015, 2016) have alternatively been related to Jamesoniella (Spruce) Carrington [= Syzygiella Spruce ( Feldberg et al. 2010a) ] of the Adelanthaceae ( Inoue 1963) . Their undifferentiated stems and their rhizoids restricted to ventral leaf bases ( Herzog 1931; Singh et al. 2015) are indeed untypical for Plagiochilaceae ; however, neither genus has not yet been included in a molecular phylogeny. The Patagonian Arctoscyphus ronsmithii Hässel , which Schuster (2001) attributed to the Jungermanniaceae may, like Bragginsella R.M. Schust. , belong to the Plagiochilaceae-LophocoleaceaeBrevianthaceae familial complex given its lateral compressed perianths with a low basal stem-perigynium and succubously inserted leaves ( Schuster 2001); again this species has not been included in molecular studies.

Species diversity is unequally distributed among the genera of Plagiochilaceae . The Dinckleria lineage contains two described species, and the Chiastocaulon lineage (including Pedinophyllum , Pedinophyllopsis and Cryptoplagiochila ) around 30. The Plagiochila lineage in contrast contains around 1000 species ( Söderström et al. 2016). As yet there are no explanations for this asymmetrical distribution of species diversity among lineages of Plagiochilaceae . A similar pattern has been recognized in the leafy liverwort family Lejeuneaceae ( Porellales ) and its sister family Jubulaceae . Lejeuneaceae includes some 1500 species ( He and Zhu 2011) whereas Jubulaceae consists of less than 10 species ( Larraín et al. 2015).

Figures

Fig. 3 Maximum likelihood phylogeny of Plagiochilaceae-Lophocoleaceae- Brevianthaceae; includes the early diverging lineages of Plagiochilaceae. Chiastocaulon is extended to include Acrochila and Plagiochilion.

Fig. 4 Maximum likelihood phylogeny of Plagiochilaceae-Lophocoleaceae-Brevianthaceae; shows one main clade of Plagiochila