This investigation demonstrates that the Fulgensia fulgida-population is highly selective in its photobiont choice, being associated with only one photobiont species, namely T. asymmetrica. As this photobiont is associated with other lichen mycobionts as well (e.g. Toninia sedifolia), the fungal–algal association is not a specific one at morpho-species level. T. asymmetrica is also known from very distantly related lichens as Diploschistes Norman (Graphidales, Thelotremataceae; Friedl & Gärtner, 1988). However it might be possible that different strains within a morpho-species are confined to certain lichen groups. The genetic investigations showed that two different strains of T. asymmetrica, which were almost identical in their ITS-sequence, are acceptable algal partners for F. fulgida at this stand. Only one of these strains has been shown to form lichens with other mycobionts, namely Toninia sedifolia. If the other strain should not be found in other lichens, this association would be a specific one.
Contrary to the photobionts, the mycobionts have been found to be genetically homogenous. The fact that genetic differences exist between mycobionts of Fulgensia fulgida from different localities, for example France and Italy (Kasalicky et al., 2000), gives significance to the observed homogeneity within the population. Mycobiontal genetic variation within lichen populations has been observed already, for example by Zoller et al. (1999), who showed that the ITS-region – and specifically the ITS1-region – revealed genetic variation within and among different populations of Lobaria pulmonaria (L.) Hoffm. mycobionts. The fact that only one ITS-sequence has been found in apothecia of one and the same thallus could be explained by homothallism, which means a fertilisation of trichogynes with pycnospores (which are bacilliform and could serve as spermatia) from the same thallus or cytogamy. Pycnospores have already been interpreted as spermatia, for example by Poelt (1986), amongst others referring to observations made by Honegger (1984) on fusions of pycnospores and trichogynes in Cladonia furcata (Hudson) Schrader. Pycnidia and apothecia were observed on one and the same thallus.
The finding of the uniformity of ITS-sequences within the apothecia of the mycobionts and heterogeneity of the photobionts suggests that the lichen thalli of this stand derive from propagation by ascospore dispersal (which had identical ITS-sequences) and multiple independent relichenization events rather than by thallus fragmentation. Alternatively, independent relichenization events may have occurred already before the establishment of this population and lichenized propagules have played the major role as secondary dispersal units, despite the presence of apothecia. However, nothing is indicative of such a scenario, as F. fulgida appears to be a purely sexual species, showing sterile thalli only at the juvenile stage and never forming asexual, lichenized propagules. In other Fulgensia species, a special type of vegetative diaspore has been recognized and described by Poelt (1965). These flake-like structures have been called schizidia. They are parallel aligned to the thallus and develop from the upper thalline layers, consisting of the upper cortex and parts of the photobiontal and medullar layers, lacking a lower cortex. These fragile structures can easily split off the thallus and are therefore assumed to serve as lichenized dispersal units. Within the genus Fulgensia, they are known from F. bracteata ssp. deformis (Erichsen) Poelt, F. fulgens, F. delphinensis Poelt, F. desertorum (Tomin) Poelt, F. poeltii Llimona and F. subbracteata (Nyl.) Poelt (Poelt, 1965; Gilbert, 1978; Westberg & Kärnefelt, 1998), and are assumed to be of taxonomic relevance, for example by Poelt (1973). F. fulgida has no schizidia and the strictly monophyllous and placodioid thalli also lack other structures, which might facilitate thallus fragmentation. Its compact thallus is firmly fixed to the substrate. For these reasons, dispersal by ascospores seems the most likely distribution mechanism of this species.
The examination of this lichen community from southern France also suggests that Toninia sedifolia and Fulgensia fulgida share the same photobiont pool, a finding that might support the observations of Ott et al. (1995) on Fulgensia bracteata, which is supposed to take over the photobionts of Toninia sedifolia (= T. caeruleonigricans). However it has not yet been shown that Toninia sedifolia is really a potential photobiont source for germinating or aposymbiotic hyphae of Fulgensia. Toninia sedifolia at least seems to be a suitable substrate providing improved conditions for the thallus establishment of Fulgensia, and the results from this study demonstrate that the two lichens have photobionts with identical ITS-sequences. Co-existence of the two lichens in the same habitat and with a narrow ecological amplitude of the photobiont may have favoured photobiont-sharing between Toninia and Fulgensia. It can be estimated that additional lichen species participate in this pool, without being involved in close interactions. Cyanolichens, as Collema cristatum in the investigated stand, often occur together with F. fulgida and may serve as a substrate during the initial growth of the phycolichen by representing a suitable environment with improved water and nitrogen supply.
Perspectives of studies on myco-photobiont relationships in lichenized systems
For characterising symbiotic interactions Galun & Bubrik (1984) distinguished between the terms ‘selectivity’, meaning ‘preferential interaction between organisms’, and ‘specificity’, meaning ‘cell–cell interactions with absolute exclusivity’. Smith & Douglas (1987) referred to specificity as the degree of taxonomic difference between partners with which an organism associates. Other authors treat the two terms as synonyms. The terminology describing preferential partner selection in symbiotic systems is therefore in need of clarification. In lichenological literature, ‘selectivity’ has hitherto been attributed only to the mycobiont of a lichenized system but has never been applied to the photobiontal partner. However, in a classification that has to cover the whole range of possible kinds of reciprocal interactions, it seems appropriate that this term should be addressed to each biont of a symbiotic system. We suggest using the term ‘selectivity’ for the characterisation of interactions between organisms viewed from the perspective of one biont only. Thus it characterises the range of possible partners that can be selected by this biont – its degree of selectivity. ‘Specificity’ should be used for the symbiotic association as a whole, therefore depending on the degree of selectivity of the partaking bionts. A suitable classification of selectivity and specificity may be best elaborated by considering the whole range of theoretically possible constellations. Five levels of selectivity can be distinguished, covering the whole range from very high – association with members of the same strain only – to very low – association with members of different orders or even classes (Table 4, Fig. 2). It is evident from this definition that the correct systematic placement of the bionts is a prerequisite for determining the degree of selectivity.
Table 4. Levels of selectivity in symbioses (with minor alterations from Smith & Douglas, 1987)
|Levels of selectivity||Ranges of acceptable partners|
|Very high||Within the same strain|
|High||Within the same species|
|Moderate||Within the same genus|
|Low||Within the same order|
|Very low||Within groupings of higher taxonomic levels|
If a mycobiont forms a lichen with photobionts of different families, it exhibits a low degree of selectivity. An example of this kind of interaction is Chaenotheca chrysocephala (Turner ex Ach.) Th.Fr., which can form lichen thalli with either Trebouxia (ord.: Trebouxiales, class: Trebouxiophyceae) or Stichococcus (ord.: inc. sed., class: Trebouxiophyceae) (Tibell, 1980). As other mycobionts can form lichens with the same photobionts, the association is not exclusive. A mycobiont that is found lichenized with only one photobiont species is considered to exhibit a high selectivity. Phlyctis argena (Sprengel) Flotow is an example of this type of association, where the mycobiont was found to be always associated with Dictyochloropsis splendida Geitler (Tschermak-Woess, 1995). The corresponding photobiont establishes associations also with other mycobionts, for instance Chaenotheca brunneola (Ach.) Müll.Arg. (Tschermak-Woess, 1978), so the interaction as a whole is therefore an unspecific one.
If both (or all) partaking organisms exhibit a high degree of selectivity, the association is specific (Table 5). Actually it is impossible to give an example of a truly specific association, because the identity of the photobiont at the species level is only known for about 3% of all described lichens (Honegger, 1996). For this reason it is premature to assign an exclusive selectivity to a photobiont. However, judging by the available data, most photobiont species seem to have a relatively low degree of selectivity, for instance Trebouxia jamesii, which is associated with several Lecanoralean fungi (Beck, 1999).
Table 5. Definition of the different degrees of specificity in binary symbiotic associations
Tripartite associations, as present in cephalodiate lichens, have to be resolved in three binary ones and the pairs have to be estimated individually.
The study of the kind of selectivity in lichen associations will be an important task for the near future to clarify whether a high degree of mycobiontal and/or photobiontal selectivity can be found in certain lichen groups, which would be indicative that coevolutionary processes may have taken place there. These studies are also necessary to test whether the photobionts are potential indicators of phylogenetic relationships of the mycobionts (Rambold et al., 1998).
Investigations of the selectivity of single mycobiont species from different localities and their algal counterparts can focus on various aspects: focusing on individual lichen thalli; on whole lichen populations; and on the phylogenetic relationships (of the mycobionts). The investigation of a single mycobiont species may be of interest and may be carried out at a local or global scale. On a local scale, it may reveal polymorphism in the mycobiontal populations. However, to test for the degree of selectivity of a mycobiont, the associated photobionts have to be investigated at a global scale, preferentially from the most diverse habitats. Based on morphology, studies of this kind have first been performed by Tschermak-Woess on Phlyctis argena by Tschermak-Woess (1995). Currently various working groups focus on such questions by applying molecular techniques. Recently Kroken & Taylor (2000) demonstrated selectivity of photobiont choice in the genus Letharia, always being associated with algae from the Trebouxia jamesii species complex. Analysing both, the myco- and photobionts of each thallus by molecular techniques they conclude, that cospeciation is not a common rule, but that there is evidence for selectivity of a given fungal species for an algal species. More such investigations will certainly provide better insights on the degree of photobiont-referring selectivity of lichen mycobionts.
Information on the environmental influence of selectivity is provided by studies of whole lichen communities. Different lichen species may share the photobionts when growing side by side, an observation that can only be addressed when all thalli of a lichen community are analysed (Beck, 1999). Studies of this kind are very important in order to make estimations on the relichenization events taking place in saturated communities, where established lichen thalli may act as a photobiont source for arriving mycobiontal spore material.
Population studies like the present one, combined with mycobiontal spore germination capability tests, will allow the investigation of the modes of relichenization in more detail. Furthermore, experiments on lichen resynthesis with the bionts of the original association and lichen resynthesis with one mycobiontal strain and with different algal strains and vice versa will provide further knowledge on the potential range of compatible partners.
The only way of proving specificity of the partner selection is to investigate different lichen species and to determine whether the partners are exclusively associated with each other (even when occurring in different lichen communities). This means there is a huge number of lichens to be investigated, which means that only a very limited number of thalli per species can be investigated. Possible results of such investigations include the verification of perfect coevolution – leading to cospeciation. Should such cospeciation have taken place, it could be visualized by congruent underlying myco- and photobiontal phylogenies (Fig. 3).
Figure 3. Scheme for supposed coevolution between myco-(MB) and photobionts (PB) in a lichen associations leading to cospeciation.
Download figure to PowerPoint
Up until now not enough data are available to estimate whether such scenarios exist for taxa associated in lichenized systems at all. In the case of trebouxiophyte photobiont Coccomyxa (Friedl, 1998) being found in families of various relationships, as in the Icmadophilaceae, Peltigeraceae, Clavariaceae (Multiclavula) and Tricholomataceae (Omphalina), it is evident that cospeciation did not occur as these unrelated mycobionts are associated with members of the same photobiont genus.
Existing patterns of selectivity in lichens may also be due to environmental factors. It seems possible that certain ancestral, as well as recent, myco-photobiontal-constellations were due to the similar ecological preferences of both bionts (Fig. 4a). In this case, the underlying phylogeny of the myco- and photobionts would not need to be congruent (Fig. 4b). It is an important task for upcoming studies to investigate such preferences in detail.
Figure 4. (a) Partner selection in lichen symbioses could be due to similar ecological preferences of the corresponding bionts. Thus the phylogenies of the underlying myco- and photobionts do not need to be congruent (b).
Download figure to PowerPoint
As phylogenetically related species might share similar environmental demands, the resulting pattern of photobiont distribution would look similar to one caused by perfect coevolution (but lack congruence of the underlying phylogenies).
As many lichen photobionts are found mainly within lichen thalli (e.g. Trebouxia, the most common lichen photobiont), mycobiontal factors are an important part of their environment. Therefore even distantly related taxa may share the same photobiont taxon through providing a suitable environment for these algae (Fig. 5). Perfect cospeciation between the partaking bionts would not be a precondition for such patterns, only a general ability to associate by lichenization. Recent results from investigations of the Acarosporetum sinopicae Hil. 1924 seem to support this hypothesis (Beck, 1999).
Figure 5. Partner selection in lichen symbioses might be due to similar environmental factors for the photobiont provided by the mycobionts because of convergent mycobiontal evolution.
Download figure to PowerPoint