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Fungal-Algal Interactions in Ramalina Menziesii and Its Associated Epiphytic Lichen Community

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Fungal-Algal Interactions in Ramalina Menziesii and Its Associated Epiphytic Lichen Community The Lichenologist 44(4): 543–560 (2012) 6 British Lichen Society, 2012 doi:10.1017/S0024282912000138 Fungal-algal interactions in Ramalina menziesii and its associated epiphytic lichen community Silke WERTH Abstract: Lichens are a fascinating example of a symbiotic mutualism. It is still uncertain which processes guide fungal-photobiont interactions, and whether they are random or of a more complex nature. Here, the fungal-algal interactions in Ramalina menziesii and co-occurring taxa are analyzed by using DNA sequences of the algal Internal Transcribed Spacer region (ITS), to investigate fungal- algal associations in juvenile R. menziesii and allied species. Algal species were identified by a com- bination of BLAST searches, median-joining network analysis, and Bayesian phylogenetics. Fungal- algal networks were analyzed for nestedness, both at the species and haplotype level (fungal species vs. algal haplotypes), and the networks were inspected for evidence of compartmentalization. Bayesian phylogenetic trees indicated that the widespread green alga Trebouxia decolorans associated with R. menziesii, as well as six other fungal species. Four additional fungal species interacted with four different species of Trebouxia. Only in one out of ten samples were algal haplotypes shared with the nearest neighbours of juvenile R. menziesii. Fungal-algal species interactions were compartmen- talized, while at the level of algal haplotypes, nestedness was found. This pattern is similar to the compartmentalization found in other intimately interacting mutualists. Key words: compartmentalization, lichen-forming fungi, nestedness, photobiont, species interactions, specificity, symbiosis Accepted for publication 7 February 2012 Introduction one-to-one species, as well as haplotype in- teractions, have been analyzed in the lichen Species interactions are a major factor struc- symbiosis. turing biological communities, and symbiotic The symbiotic mutualistic associations of interactions can be an important force driv- lichen fungi and their photobionts can be ing evolution (Margulis & Fester 1991). In described by their degree of specificity and lichens, one of the ‘textbook examples’ of selectivity. These terms characterize the symbiosis, the local composition of sym- taxonomic range of the partners with which biotic partnerships between lichen-forming an organism associates (Smith & Douglas fungi and their photobionts is a fascinating 1987). Following the suggestion by Beck issue (Beck et al. 1998, 2002; Yahr et al. et al. (2002), I use the term specificity for 2004; Ohmura et al. 2006). Progress has the symbiotic association as a whole, that is, been made in recent years due to the devel- from the view of both photobionts and myco- opment of molecular techniques that allow bionts. A narrow taxonomic range (e.g., a a straightforward identification of photo- one-to one relationship) would be indicative biont and fungal genetic strains and species of the high specificity of the association. I (Scheidegger & Werth 2009; Werth 2010). refer to selectivity as the taxonomic range of In this way, photobiont guild structure and the interaction viewed from the perspective of only one biont (Beck et al. 2002). Accord- ingly, a mycobiont would be highly selective S. Werth: Department of Ecology and Evolutionary in its partner choice if it were found in asso- Biology, University of California Los Angeles, Box ciation with few, closely related photobiont 951606, Los Angeles, California 90095-1606, USA and species. Biodiversity and Conservation Biology, Swiss Federal Previous studies have shown that lichen Research Institute for Forest, Snow and Landscape Research WSL, Zu¨rcherstrasse 111, CH-8903 Birmens- fungi may exhibit a varying degree of selec- dorf, Switzerland. Email: [email protected] tivity towards their photobionts. Some fungi Downloaded from https:/www.cambridge.org/core. Library of Eawag, Empa, PSI & WSL, on 02 Feb 2017 at 11:59:57, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282912000138 544 THE LICHENOLOGIST Vol. 44 show high selectivity, and they associate species, but also at the level of haplotypes of with a particular photobiont phylogenetic each symbiosis partner. clade or species (Kroken & Taylor 2000; In the case of compartmentalized species Helms et al. 2001; Beck et al. 2002; Piercey- interactions (Bascompte et al. 2003; Jordano Normore 2004, 2006; Yahr et al. 2004; et al. 2003), certain fungal species would Stenroos et al. 2006; Myllys et al. 2007). interact with a defined subset of photobiont Other fungal species are far less selective species, while other fungal species would towards their photobiont partners (Wirtz interact with a non-overlapping subset of et al. 2003; Piercey-Normore 2004; Yahr photobiont species; interaction matrices et al. 2004; Myllys et al. 2007); some may would thus exhibit independent subwebs. occasionally or always associate with two Compartmentalization and participation of photobiont species (Piercey-Normore 2006; comparatively few species has recently been Casano et al. 2011). Some fungal species are documented from networks of mutualistic, able to partner up with photobionts belong- symbiotic ant and plant species with a high ing to different kingdoms, and which photo- degree of interaction intimacy, while networks biont partner gets involved in the symbiosis with low interaction intimacy were generally may depend on environmental conditions species-rich and nested (Guimara˜es et al. (Goffinet & Bayer 1997; Tønsberg & Goward 2007). Results from previous studies indi- 2001; Summerfield et al. 2002). cate that mycobiont-photobiont interactions Many open questions remain in the field are not random, and they seem to be inde- of fungal-algal associations in lichens: for pendent of the green algal species present in instance, are fungal-photobiont relationships free-living populations at a site (Beck et al. entirely random or are they structured in a 1998; Rambold et al. 1998). complex way, that is, nested or compartmen- Many lichen fungi disperse clonally with talized? In the case of random associations, symbiotic propagules which contain photo- no apparent pattern of association would biont cells, which leads to vertical transmis- be found in species interaction matrices sion of the photobiont (Nash 1996; Werth (Bascompte et al. 2003; Jordano et al. 2003). et al. 2006a,b) unless the photobiont is In nested species interactions, specialists tend exchanged during establishment (Ohmura to interact with subsets of the species that et al. 2006; Wornik & Grube 2010; Werth & interact with generalist species (Bascompte Scheidegger 2012). Also, lichen-forming et al. 2003). In terms of the lichen symbiosis, ascomycetes reproduce sexually with asco- this would mean that the specialized fungal spores, which are dispersed independently of species are interacting almost exclusively their photobiont cells (i.e., horizontal trans- with the photobiont species that the general- mission), though a few exceptions exist where istic fungi are interacting with. This nested both partners are co-dispersed (Honegger type of species interaction leads to a pattern 2008). Germinating ascospores have to asso- in species interaction matrices that resembles ciate with new photobionts (relichenization) an asymptotic curve (Bascompte et al. 2003; in order to form a thallus. This phenomenon Jordano et al. 2003). Translated to the world is probably common, but has been reported of lichen fungi and their photobionts, that from only a few species (Beck et al. 2002; would mean that few generalist mycobiont Romeike et al. 2002; Sanders & Lu¨cking species interact with many photobiont species, 2002; Werth & Sork 2008). It has also been and few generalist photobiont species interact suggested that germinating spores could with many mycobiont species. Additionally, gain photobionts either from vegetative specialized mycobiont species would interact propagules produced by other lichen species, with a subset of the photobiont species used or from adult thalli of other species (Ott by the generalists, and vice versa, specialized 1987a; Ott et al. 2000; Rikkinen 2003). photobionts would interact with a subset of Alternatively, they may retrieve cells from the mycobiont species. Nestedness can not free-living Trebouxia populations (Beck et al. only be studied at the level of fungal and algal 1998). Downloaded from https:/www.cambridge.org/core. Library of Eawag, Empa, PSI & WSL, on 02 Feb 2017 at 11:59:57, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282912000138 2012 Fungal-algal interactions in Ramalina menziesii—Werth 545 Ramalina menziesii (Ramalinaceae)isacom- Data sampling mon epiphytic lichen in coastal oak savannas To study the potential for interaction with other lichen of southern California. It is associated with species, juvenile thalli (a5cmlong)ofRamalina menziesii the photobiont genus Trebouxia (Brodo et al. Tayl. (Ramalinaceae) were observed in the field, and it 2001), which contains some frequent and was recorded whether they were growing by themselves widely distributed photobiont species. Re- or within 2 mm from another lichen species, or from an cently, the local genetic structure was investi- adult conspecific. A cut-off level of 2 mm was chosen because preliminary observations of distance, between gated for this lichen fungus across four sites, thalli indicated that within this
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