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Phylogenetic Analysis Indicates Transitions from Vegetative to Sexual Reproduction in the Lobaria Retigera Group (Lecanoromycetidae, Ascomycota)

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Phylogenetic Analysis Indicates Transitions from Vegetative to Sexual Reproduction in the Lobaria Retigera Group (Lecanoromycetidae, Ascomycota) The Lichenologist 41(3): 275–284 (2009) © 2009 British Lichen Society doi:10.1017/S0024282909006240 Printed in the United Kingdom Phylogenetic analysis indicates transitions from vegetative to sexual reproduction in the Lobaria retigera group (Lecanoromycetidae, Ascomycota) Carolina CORNEJO, Svetlana CHABANENKO and Christoph SCHEIDEGGER Abstract: Phylogenetic relationships among the hypothetical species pairs Lobaria kurokawae / L. retigera and L. pseudopulmonaria / L. isidiosa were investigated based on TLC techniques and the phylogenetic analysis of the internal transcribed spacers (ITS) nrDNA. Results of TLC demonstrate that L. retigera and L. kurokawae can be chemically distinguished from L. isidiosa and L. pseudopulmo- naria by the absence of retigeranic acid. Parsimony analysis of 18 specimens shows two monophyletic clades – a L. retigera lineage and a L. isidiosa lineage—both including their apotheciate counterparts. Unlike the original hypothesis of species pairs, our study reveals transitions from isidiate morphs that have the potential to rarely form apothecia, towards apotheciate morphs that produce no vegetative propagules. Key words: evolutionary significant units, lichen-forming ascomycetes, Lobaria, species pairs Introduction (2003) demonstrated that Pseudocyphellaria The lichen genus Lobaria (Schreb.) Hoffm. is paraphyletic and Lobaria formed a mono- includes a number of closely related taxa that phyletic group, Thomas et al. (2002), are morphologically very similar, except for Stenroos et al. (2003) and Mia˛dlikowska & the production of sexual fruiting bodies or Lutzoni (2004) using nuclear rDNA showed vegetative propagules, and are considered that both Lobaria and Pseudocyphellaria are typical examples of species pairs sensu Poelt polyphyletic. However, these divergent re- (1970, 1972). Yoshimura (1971) mentioned sults seem to reflect incongruence between five species pairs in this genus; two of them in nuclear and mitochondrial DNA that can the Lobaria retigera group: L. kurokawae only be resolved by a multi-gene approach Yoshim./L. retigera (Bory) Trev. and L. combined with an extensive dataset of pseudopulmonaria Gyeln./L. isidiosa (Müll. Lobaria s. lat. Yoshimura (1971) distin- Arg.) Vain. The first species of each pair guished different sections of Lobaria based reproduces sexually with apothecia, while on ascospore characteristics and the species its counterpart propagates mainly asexually on further morphological and chemical with isidia. attributes, but rejected the photobiont as a The current understanding of the genus character of taxonomic value above the Lobaria is still controversial. While phylo- species level. Within the Lobaria retigera com- genetic research based on nuclear and plex he defined species according to chemical mitochondrial rDNA by Wiklund & Wedin characteristics, distinguishing L. kurokawae from the morphologically very similar L. pseudopulmonaria by the absence of the stictic C. Cornejo, S. Chabanenko and C. Scheidegger: Swiss acid complex. Furthermore, he referred to Federal Institute for Forest, Snow and Landscape Re- terpenoids for both taxa but did not identify search WSL, Zuercherstrasse 111, 8903 Birmensdorf, Switzerland. Email: [email protected] them. Rao et al. (1965, 1966) first described S. Chabanenko: 2 Sakhalin Botanical Garden, Gorky- the terpenoids, retigeradiol and retigeranic street 25, 693023 Yuzhno-Sakhalinsk, Russia. acid, from samples of the Lobaria retigera Downloaded from https:/www.cambridge.org/core. Library of Eawag, Empa, PSI & WSL, on 02 Feb 2017 at 08:55:54, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282909006240 276 THE LICHENOLOGIST Vol. 41 group but with uncertain taxonomic specifi- until interaction with a more favourable pho- cations. Thin layer chromatography (TLC) tobiont triggers a switch to the sexual repro- analysis of Takahashi et al. (1972) confirmed ductive mode. Consequently, some currently the diagnostic system of Yoshimura (1971) sterile species might gain fertility in a later distinguishing L. kurokawae and L. retigera generation. from L. pseudopulmonaria and L. isidiosa by In recent years, molecular studies have the absence of stictic acid and the occurrence contributed to our understanding of the of retigeric acids A and B. In addition, the phylogenetic relationships between sexual authors described a new compound as and asexual taxa of lichen forming fungi. characteristic for L. pseudopulmonaria and The internal transcribed spacers (ITS) of L. isidiosa that was identified as retigeranic the nuclear rRNA gene cluster have been acids A and B by Kaneda et al. (1972) and successfully used in infra-familiar and infra- Sugawara et al. (1991). generic reviews (Arup & Grube 2000; Yoshimura (1971) also considered the Lohtander et al. 2000; Ihlen & Ekman 2002; production of soredia, isidia or lobules as Thomas et al. 2002), for delimiting species characteristics for delimiting species; thus, (Tehler & Källersjö 2001; Mia˛dlikowska the asexual taxa were treated as different et al. 2002), in diverse analyses of species species from their fertile counterparts. Poelt pairs (Lohtander et al. 1998a, b; Kroken & (1970, 1972) and Tehler (1982) understood Taylor 2001; Myllys et al. 1999, 2001), asexual species as genetically isolated clones or in studies of the infraspecific genetic varia- because they were considered unable to re- bility (Martı´n et al. 2000; Crespo et al. combine with sexual relatives. Tehler (1982) 2002). also recognized intermediate forms bearing The aim of the present study is to examine isidia and apothecia that, over time, would the phylogenetic relationship between apoth- lose sexual reproduction completely. How- eciate and isidiate taxa of the Lobaria retigera ever, Mattsson & Lumbsch (1989) argued group. Lobaria kurokawae and L. pseudo- that sterile species were genetically variable pulmonaria consistently form apothecia but and that it is probably wrong to regard sterile never soredia or isidia, whereas L. retigera lichens as evolutionary dead ends. The and L. isidiosa produce abundant vegetative authors further suggested that sterile taxa propagules and rarely form apothecia in might have the chance of generating new addition to the vegetative propagules ones. In fact, all phylogenetic studies on (Yoshimura 1971). We investigated if the species pairs to date have shown that sterile species L. kurokawae, L. retigera, L. pseudo- species are genetically diverse (Lohtander pulmonaria and L. isidiosa form monophyletic et al. 1998a, b, 2000; Kroken & Taylor 2001; groups. Furthermore, we assessed the taxo- Myllys et al. 1999, 2001; Buschbom & nomic significance of the chemical com- Mueller 2006). In addition, these analyses pounds by determining whether their demonstrated that neither the sexual nor the differentiation of the two species pairs could vegetative reproducing species were mono- be confirmed by the molecular data. phyletic. Tehler (1982) suggested that the asexual form of species pairs may have devel- oped on multiple occasions from the fertile ones and should only be treated as indepen- Material and Methods dent taxa if they have irreversibly lost the The specimens studied were collected in Bhutan, ability to produce fruiting bodies. A recent Canada, China, Madagascar and Russia. To test the study on evolutionary processes in the phylogenetic status of the ingroup, we included two species pair Porpidia flavocoerulescens and species of Lobaria from different infrageneric units, L. P. melinodes may contribute to this debate. amplissima (Scop.) Forss. and L. oregana (Tuck.) Müll. Arg. Sticta fuliginosa (Hoffm.) Ach. and S. canariensis Buschbom & Mueller (2006) proposed that (Bory) Bory ex Delise were used as outgroup taxa. the mycobiont might reproduce predomi- Information on the taxa, herbarium number and nantly with vegetative, symbiotic propagules GenBank accession numbers are given in Table 1. Downloaded from https:/www.cambridge.org/core. Library of Eawag, Empa, PSI & WSL, on 02 Feb 2017 at 08:55:54, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282909006240 2009 Transitions of reproductive systems in Lobaria—Cornejo et al. 277 T 1. Taxa used in this study and the GenBank accession numbers of the ITS nrDNA sequenced for the present study or obtained from GenBank Taxon and code Voucher specimen* GenBank Acces- sion no. Lobaria kurokawae 1 Bhutan, Flor Province; GZU 00-411-17/01 DQ419932 2 China, Yunnan Province; 525SAKH, SCH-CY01 DQ419924 3 China, Yunnan Province; 548SAKH, SCH-CY14 DQ419942 4 China, Yunnan Province; 518SAKH, SCH-CY15 DQ419937 5 Russia, Sakhalin; 498SAKH, SCH-CY18 DQ419938 L. retigera 1 Bhutan, Flor Province; GZU 00-159-10(1)/01 DQ419940 2 Bhutan, Flor Province; GZU 00-237-10/02 DQ419941 3 Bhutan, Flor Province; GZU 00-166-34/01 DQ419936 4 China, Yunnan Province; 544SAKH, SCH-CY52 DQ419930 5 Canada, British Columbia; SCH-CY09 DQ419934 6 Canada, British Columbia; SCH-CB05 DQ419929 7 Russia, Sakhalin; 490SAKH, SCH-CY26 DQ419926 8 Madagascar; SCH-MP DQ419928 9 Madagascar; SCH-X23 EU626996 10 Madagascar; SCH-X25 EU626997 11 Madagascar; SCH-X26 EU626998 12 Madagascar; SCH-X28 EU626999 L. pseudopulmonaria 1 Bhutan, Flor Province; GZU 00-37803/01 DQ419935 2 Bhutan, Flor Province; GZU 00-183-18/01 DQ419933 3 Bhutan, Flor Province; GZU 00-339-02/03 DQ419939 4 China, Yunnan Province; 533SAKH, SCH-CY02 DQ419931 5 China, Yunnan Province; 530SAKH, SCH-CY53
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