The significance of competition for lichen ecology and evolution

When characterizing photobionts as hosts and mycobionts as parasites, the question remains what causes Trebouxia to adapt to the symbiotic life style. It is suggested here that it is the strong competitive stress it experiences in the aposymbiotic state. Free-living Trebouxia cells are exposed to competition with a variety of subaerial algae and probably also suffer from consumers. A model of interactions between lichen bionts that depicts such interactions is shown inFIG. 5.7. This model incorporates two distinct life stages of the photobiont as well as its exposure to competitive stress in its free-living phase. This concept assumes an antagonistic relationship between lichen bionts while supporting the evolutionary stability of the symbiosis.

Interestingly, it agrees with the very earliest concepts of the lichen symbioses as described by Schwendener (1873) and DeBary (1879) who both considered lichens to be parasites. An antagonistic concept, which includes free-living stages of the photobiont, stresses the importance of the environmental requirements of the photobiont for lichen existence. Maybe it is the fitness of the free-living photobiont populations available for lichenization that determines occurrence and abundance of lichens, especially for the asorediate species as already suggested by Wirth (1983).

Symbiosis in Associations of Physciaceae and Trebouxia

Assuming low densities of free-living photobiont populations as well as a dependency of asorediate lichens on these free-living photobionts, the availability of compatible photobionts for relichenization might be a limiting resource for lichen populations. This assumption receives support when comparing the ecological success of sorediate with their asorediate sister species (Bowler & Rundel 1975). Hence, competition for accessible and compatible photobionts might be suspected in asorediate lichens. Therefore, evolutionary forces might be in effect that minimize competition. Several options can be postulated. Development of dual propagules, change or restriction of the mycobiont’s ecological niche within the ecological range of the compatible photobiont, switch to another photobiont of the same environment, or a switch to another photobiont in another environment. All these strategies have apparently been realized in lichens and contribute to their diversity. Competition for a common set of photobionts might therefore promote an increase of selectivity as a strategy to minimize resource overlap (analoguous to the principle of resource partitioning, Futuyma & Slatkin 1983 and citations therein, Roughgarden 1983, Buckling & Rainey 2002). In case sympatric mycobionts are selective for the same photobiont, competition might have just the opposite effect on the degree of selectivity. In such situations an alga switch might be promoted (van Baalen et al.

2001). Therefore, competition for photobionts is suspected to be a major cause for the apparently contradictory findings of ecological dependence (i.e. selectivity) and evolutionary independence.

When considering competition for photobionts as an evolutionary force that promotes diversification in lichens, an interesting correlation emerges. The lower the density of free-living compatible photobionts, the more diverse are the mycobionts that depend on it. To illustrate this correlation the diversity of lichen taxa that are associated with the three most common photobionts Trebouxia, Trentepohlia, and Nostoc might be compared to the abundance of these photobionts in the aposymbiotic state. Trentepohlia as well as Nostoc are frequently observed in the free-living state but Trebouxia is not. Accordingly, the diversity of lichens that depend on Trebouxia is greatest. Further, the order of fungi that includes the highest percentage of lichens depending on Trebouxia, the Lecanorales, is also the most diverse order. Therefore, the general finding that most lichens adopt Trebouxia as their photobiont, might be explained by an accelerated rate of diversification caused by an especial strong competition in those fungi that become dependent on Trebouxia.

Also the fact that sorediate lichens often do not continue to speciate might be interpreted under the aspect of a "diversifying competition" for compatible photobionts. Sorediate lichens escape this competition and so

"lose" their motor of diversification.

Symbiosis in Associations of Physciaceae and Trebouxia

Fig. 6.1: Flow diagram of hypothetical interactions between lichen bionts and subaerial algae

It is assumed that photobionts (PB) occur in two distinct stages: lichenized (PBl) and non-lichenized (PBnl). The lichenized stage is symbolized by the area enclosed by the mycobiont (MB); the aposymbiotic stage is symbolized by the area outside the mycobiont. The close proximity of the two distinct photobiont areas depicts the genetic connection between the two stages but not necessarily any spatial or temporal proximity. Lichenized photobionts are supposed to interact only with the mycobiont while photobionts in the aposymbiotic stage are supposed to interact with a variety of organisms, such as subaerial algae (SA). Thin arrows are of purely hypothetical nature and may have variable intensities in different taxa. Further, interactions symbolized with these thin arrows might even not be realized in many cases (e.g.

PBnl1-PBnl2 / PBnl2-PBnl1 or PBnl-SA). Thick arrows indicate intensive interactions which are observed in all lichens and are either beneficial or detrimental (indicated by “+” and “-“ signs). PBl1-MB1 / PBl2-MB2: Beneficial and intensive effect of the photobiont on the mycobiont. The transfer of carbohydrates from the photobiont to the mycobiont is a long established fact (Richardson et al. 1967). MB1-PBl1 / MB2-PBl2: A direct beneficial effect of the mycobiont on the photobiont has not been proven. The loss of carbohydrates is the only effect that has been ascertained. Therefore, this effect is suspected to be negative although not lethal. MB1-SA / MB2-SA: Lichens overgrow subaerial algae and are therefore superior when competing for space. Intensity and nature of effects of SA on MB is not known but might be suspected to be weak or even absent in many cases. SA-PBnl1 / SA-PBnl2: The fact that most Trebouxia strains seem readily cultivable, i.e. grow well although slowly in the absence of competition suggests that the rarity of Trebouxia in the free-living state is due to competition with faster growing subaerial algae. Therefore, subaerial algae are suspected to have an intense and negative effect on growth rates of free-living photobionts. In the case of Trebouxia, free-living photobionts might possibly have no effect on other subaerial algae.

Introns of the Physciaceae nrSSU