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Multi-Gene Phylogeny Supports Single Origin of Jungermannioid Perigynium

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Multi-Gene Phylogeny Supports Single Origin of Jungermannioid Perigynium Ann. Bot. Fennici 44: 450–462 ISSN 0003-3847 (print) ISSN 1797-2442 (online) Helsinki 20 December 2007 © Finnish Zoological and Botanical Publishing Board 2007 Multi-gene phylogeny supports single origin of jungermannioid perigynium Xiaolan He-Nygrén Botanical Museum, Finnish Museum of Natural History, P.O. Box 7, FI-00014 University of Helsinki, Finland Received 23 Nov. 2006, revised version received 8 Feb. 2007, accepted 8 Feb. 2007 He-Nygrén, X. 2007: Multi-gene phylogeny supports single origin of jungermannioid perigynium. — Ann. Bot. Fennici 44: 450–462. Within the leafy liverworts, the evolution of the perigynium, the stem-derived struc- ture that protects the developing sporophytes, has been understood as merely a paral- lelism, and families that have this feature have been placed to various suborders. The present study suggests a single origin of the perigynium in the leafy liverworts and the presence of perigynium being a synapomorphy for the suborder Jungermanniineae. The phylogenetic analyses were conducted using thirty-four leafy liverworts including twelve genera bearing a perigynium, and sequence data for rbcL, rps4, trnL-F cpDNA and 26S nrDNA. Within the Jungermanniineae three monophyletic lineages are recog- nized: the Acrobolbaceae lineage, the Trichotemnomaceae–Balantiopsidaceae lineage, and the lineage consisting of Jungermanniaceae and its closest related Gymnomi- triaceae, Delavayellaceae, Geocalycaceae s. stricto, Antheliaceae, Calypogeiaceae and Gyrothyraceae. The long branches of the latter three families indicate that they are more isolated from a common jungermannioid ancestor. The family Jungermanniaceae is resolved as paraphyletic and its circumscription and relationships require further study. Key words: homology, Jungermanniineae, leafy liverworts, morphological innovation, perigynium, phylogeny, systematics Introduction rophyte. The substrata colonized by this group of species vary from soil and/or rock surface to The leafy liverworts, including 4000–6000 spe- tree trunks and even to living leaves; the species cies, are the most speciose and morphologically occur in greatest diversity and abundance in the diverse group of the liverworts. The immedi- humid subtropics and tropics. Because of their ate distinction of the leafy liverworts from rest remarkable variations in morphology and great of the liverworts is the development of a leaf, profusion of structure, comprehending evolu- two or three ranks of which are inserted on tion and taxonomy of the leafy liverworts has the stem; and a perianth, which is formed by been difficult and challenging. Schuster (1984) the fusion of two to three leaves surrounding listed abundant examples of presumable paral- the archegonia protecting the developing spo- lelism and homoplasy in this group and stated ANN. BOT. FENNICI Vol. 44 • Multi-gene phylogeny supports single origin of jungermannioid perigynium 451 that problems induced by parallelism and the been assigned to various suborders (see Schuster malleability of ontogenetic patterns hinder any 1972, 1984, Crandall-Stotler & Stotler 2000). attempt to construct a phylogenetically-sound However, it is noteworthy that the Jungermanni- classification. Nevertheless, leafy liverworts ineae comprise by all the leafy families that have have been classified in as many as 15 suborders a perigynium, the stem tissue-derived protective or orders based on morphological observations structure of the developing sporophyte. Only (Schljakov 1972, Schuster 1972, 1984, 2000, two families, Antheliaceae and Delavayellaceae 2002) representing independent evolutionary of the Jungermanniineae lack this feature. The lines, but the evolutionary relationships between study of Hentschel et al. (2006) based on single these groups have largely remained obscure. gene also suggests the union of families Junger- There are no morphological characters providing manniaceae, Geocalycaceae, Calypogeiaceae, clear-cut distinction between them. The above- Balantiopsidaceae, Trichotemnomaceae and Acro- mentioned assumption on leafy liverwort evolu- bolbaceae. These results have brought up ques- tion by Schuster and other authors has long been tions as whether the character perigynium in accepted and followed by hepaticologists until the Jungermanniineae represents a single origin. the recent outcome of the phylogenetic studies Previously, the occurrence of perigynium in dif- on leafy liverworts using multiple gene sequence ferent families had been understood as merely a data (Davis 2004, He-Nygrén et al. 2004, Forrest parallelism. In the present study, the monophyly et al. 2006) and using combined multiple gene of the perigynium and the circumscription of the sequences and morphology (He-Nygrén et al. Jungermanniineae will be addressed. 2006). In these studies, novel, and well resolved phylogenetic relationships of major groups of leafy liverworts were provided; they do not sup- Material and methods port previous assumptions on leafy liverwort evolution. Their results imply that our current Taxon sampling understanding of many morphological characters should be re-examined. Thirty-four taxa of leafy liverworts were chosen In He-Nygrén et al. (2004), leafy liverworts as exemplars. All the 14 species that consti- were suggested to be the most derived lineage tute the Jungermanniineae in He-Nygrén et al. among the liverworts. Except Pleurozia, a very (2006) were included in the present study, and isolated leafy lineage, two major clades were rec- are marked with asterisks in Fig. 1. Eleven addi- ognized. Based on the result derived from more tional ingroup species from five families were extensive data, He-Nygrén et al. (2006) classi- added. They are Jungermannia crenuliformis, fied the leafy liverworts into three orders, Pleu- J. exsertifolia, and Nardia scalaris (Jungerman- roziales, Porellales, and Jungermanniales. The niaceae); Gymnomitrion sp. (Gymnomitriaceae); Jungermanniales are classified to four suborders, Balantiopsis diplophylla, Isotachis lyallii, I. mul­ Perssoniellineae, Cephaloziineae, Jungermannii- ticeps, and Neesioscyphus bicuspidatus (Balanti- neae and Lophocoleineae. Their result on the opsidaceae); Lethocolea glossophylla (Acrobol- Jungermanniineae is striking, since it suggests a baceae); and Harpanthus scutatus (Geocalyc- close affinity between various families that were eceae). Harpanthus was included in the present previously thought unrelated. The families of the study because it bears a perigynium. Other fami- Jungermanniineae in the analysis (He-Nygrén lies which possess also perigynia, Arnelliaceae et al. 2006) are Jungermanniaceae, Delavayel- (Arnellia and Southbya) and Jackiellaceae (Jack­ laceae, Gyrothyraceae, Acrobolbaceae, Gym- iella) were unfortunately not able to be included nomitriaceae, Antheliaceae, Calypogeiaceae, in the analysis. Mylia taylorii, representing Trichotemnomataceae, and Balantiopsidaceae. Mylioideae of Jungermanniaceae (Grolle 1963) Among them, Jungermanniaceae, Delavayel- or Myliaceae in the suborder Myliineae (Engel laceae and Gymnomitriaceae are the only families & Braggins 2005), was included in the present that belong to the traditionally recognized Junger- analysis in order to test further its systematic manniineae (Schuster 1984). Other families have position. Mylia is a genus that lacks perigynium 452 He-Nygrén • ANN. BOT. FENNICI Vol. 44 but is resolved as sister to a group of species RNA. The amount of missing data was possessing a perigynium in Hentschel et al. 6%. There is no sequence length variation (2006) based on rbcL sequences. Nine species of in the rps4 sequences. leafy liverworts were selected as outgroup taxa trnL–trnF The data set consisted of two exons according to He-Nygrén et al. (2006), two of and the intron of partial sequence of the which are from Schistochilales, and seven from leucine transfer RNA(UAA) and a partial Cephaloziineae. Details on voucher specimens sequence of phenylalanine tRNA(GAA). are given in Table 1. The gene areas of P6 and P8 of intron and intergenic spacer were excluded in the analysis because certain elements in Morphological character these regions are not homologous but have independent origins (see Stech et al. Character perigynium is scored as present or 2003, Quandt et al. 2004). Recognition of absent in the analysis. It was examined by the P6 and P8 regions was based on presenta- author based on specimens available at H, and tions of secondary structures by Stech et also according to previous studies (Schuster al. (2003) and Quandt et al. (2004). The 1966, 1969, 1974, 1984, 1996, Gradstein & Pin- amount of missing data was about 17%. heiro da Costa 2003). 26S In the data set of nuclear large subunit ribosomal DNA sequences the amount of missing data was approximately 28%. DNA markers and sequences The sequence lengths vary from 1037– 1045 bp. Sequence data for rbcL, rps4 and trnL-F cpDNA and 26S nrDNA were utilized in the present study. Novel sequences were generated for rbcL Phylogenetic analyses and trnL-F cpDNA of Neesioscyphus bicuspida­ tus; the rest were obtained respectively from pre- Two optimality criteria, parsimony and Bayesian vious studies of He-Nygrén et al. (2004, 2006), inference of phylogenetic analysis were used in and from the GenBank. The protocols for DNA the present study. The sequences from each gene extraction, PCR, and sequencing followed the were aligned using DIALIGN2 (Morgenstern methods used by the author in He-Nygrén et al. 1999). 2941 equally weighted nucleotide char- (2004). All 34 taxa represent data
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