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Asymmetric co-evolution in the lichen symbiosis caused by a limited capacity for adaptation in the photobiont.

Introduction

Lichens are one of the best known groups of symbiotic organisms. Law and Lewis (1983) first suggested, in looking at mutualistic symbioses in general, that the evolution of the algal symbiont in lichens was limited by the absence of sexual reproduction. They reviewed the differing mutualisms amongst symbiotic associations and in some symbiotic systems other than lichens, for example the genus Ficus and the wasps that pollinate the syconium (flower head), both wasps and species of Ficus are similarly species diverse (Berg & Wiebes, 1992; Proctor et al., 1996). The wasp is supported by the fig tree throughout its entire life-cycle. Both organisms pass though their sexual cycle together and are able to evolve and adapt in consort through mutual evolutionary co-development and adaptation (co-evolution leading to co-speciation). In temperate ectotrophic mycorrhizas, the species of the fungi and the trees are both similarly numerous with possibly up to, or more than, 10,000 spp of fungi being involved (Cairney, 2000) spanning a wide range of the Basidiomycotina. The fruiting body of the fungus is created by its utilisation of the carbohydrate resource of the tree, both partners completing the sexual cycle whilst in symbiotic association. There are far fewer vesicular--arbuscular mycorrhizal fungal species (about 150 species) than host species and the fungus (e.g. Glomus) does not have clear evidence sexual cycle (Kuhn et al., 2001). The vesicular mycorrhizas are amongst the oldest mycorrhizas known, most widely distributed in higher plants and have changed little in 400 my (Cairney, 2000).

In lichens there are perhaps 18,000 species of lichenised fungi (of which 13,500 are currently described; Sipman & Aproot, 2001) and they occur across not only a wide range of the Ascomycota but include some Basidiomycota and, though very polyphyletic, some groups may have evolutionary origins in the Cambrian. Lichenised fungi, termed mycobionts, show a striking array of adaptations, the most obvious are structural, to accommodate their photosynthetic partners (photobionts). The lichen photobionts, in contrast, represent only perhaps a hundredth of that number with possibly only 25-44 genera but no exact enumeration of species (Ahmadjian, 1993a). Ahmadjian (1993b) also pointed to a lack of evidence for adaptation in the photobiont. Kappen (1994) questions whether the fungus should be seen as a host rather than the photobiont; photobionts could be tolerant of fungal parasitism without any need for considering any reciprocal 'benefits' of mutualistic symbiosis. Most mycobionts associate with the chlorophyte genus Trebouxia. What is the reason for this? Is it merely that the photobionts are mainly unicellular in the lichen thallus and as such have little capability for diversity and adaptation? Although, one author bas rightly suggested that "we still have an insufficient understanding of factors that induce re-and de-lichenization events that promote phylogenetic change in lichen symbionts over evolutionary rime" (Rikkinen, 2003), it is reasonable to revisit possible answers to this question.

The following discussion aims to consider the evidence, including recent molecular genetic evidence unavailable to Law and Lewis or Ahmadjian. Seeking evidence of possible adaptation by the photobiont is essential research for our understanding of the symbiosis. (The terre photobiont is used whether it is lichenized or unlichenized.) What is the weight of evidence for photobionts having adaptations or being able to evolve adaptations to lichenization? Previous reviews including molecular evidence have concluded that there is a lack of co-speciation in photobionts (e.g. DePriest, 2004). In dealing with these issues, we need, for clarity, to establish what is meant here by the difference between speciation and adaptation.

Adaptation constitutes heritable changes in phenotypic characters that enables the photobiont to function with a greater level of fitness (or chance of success), here in the lichenized state compared with those characters the species may have had when unlichenized. Lack of adaptation in a species does not mean that it cannot evolve; indeed, there is considerable genetic diversity within some putative photobiont species.

In considering speciation, we assume that populations, here of photobiont cells in lichen thalli, are genetically discrete and isolated e.g. from unlichenized populations and populations in other lichen thalli. A species can be recognised as a genetically self-sustaining population which diverges sufficiently from others genetically (and usually phenotypically). The divergence can be an expression of differences which can be functional (usually adaptive) and non-functional (non-adaptive). Two similar populations can evolve divergently to become quite distinct (even different species) with scarcely any divergent adaptations just as two unrelated species can have very similar adaptations.

Photobionts do not undergo sexual reproduction in the lichen thallus (Ahmadjian, 1993a; Friedl and Bfidel, 1996), although there has been a single report of zoosporogenesis being observed in Trebouxia (Slocum et al. 1980). Asexual habit by the photobiont may be a phenotypic response toits symbiotic state and photobionts may reproduce sexually whilst not lichenized. It is not known whether this situation affects their evolutionary potential as symbionts. Many recent studies about evolution in other asexual organisms are reviewed by reviewed by de Meeus et al. (2007) who pointed out "the (more or less) counterintuitive notion that more polymorphism can be maintained at individual loci in asexual populations than sexual populations". Birky et al. (2005) and Fontaneto et al. (2007) obtained evidence that asexual rotifers have undergone speciation and adaptation to different ecological niches much as sexual organisms have done although Barraclough et al. (2007) found evidence that asexual rotifers were unable to eliminate deleterious genes. In reviewing variation and adaptation in root nematodes, Castagnone-Sereno (2006) suggested that asexual nematodes were also able to rapidly adapt to new environmental constraints (e.g. host resistance). Hence, until there is direct evidence, it is best to assume that asexual photobionts may also be capable of evolution and adaptation by natural selection. Even if this is the case, in an asexually reproducing species, alleles conferring increased fitness arise extremely rarely. The chance of two occurring in the same individual are, by a multiple of probabilities, much rarer still: especially so, when compared with the chance of two alleles recombining in an offspring of two sexual individuals each carrying a beneficial allele. Recombination also eliminates more commonly arising deleterious genes from the population. Significant progressive adaptation usually requires the association in one individual of several beneficial alleles because organisms are complex and few adaptations involve single gene characters.

In lichens, with one symbiont reproducing sexually and the other asexually there is likely to be a considerable difference in their rates in evolving adaptive features. If one can evolve adaptive features faster than the other, after a period of time, the extent of adaptation displayed by each of the two symbionts is likely to be asymmetric. Indeed, if the mycobiont adapts much more rapidly than the photobiont, potential adaptations in the photobiont could be overridden, or made unnecessary, by faster adaptation in the mycobiont.

In looking at the evidence from molecular studies we have to consider what molecular evidence tells us about photobiont ecology (ecology being the context natural selection) and about photobiont occurrence in lichens based on DNA sequence diversity. Is there a pattern to the lineages of photobionts which associate with mycobionts from which we can make predictions? If there is no pattern, the photobiont lineage found in a lichen must be determined by other circumstances such as chance availability, the mycobiont acquiring its photobiont from particular types of unlichenized photobiont to which it bas become adapted.

The Photobiont Life Cycle

Most lichen species are spore reproducing with a much smaller number reproducing vegetatively by thallus generated propagules. For a new lichen thallus to develop, hyphae developing from a fungal spore have to find and associate mutualistically with cells of a photobiont. In most spore reproducing lichens, the photobiont is acquired by the mycobiont from a population of free-living cells. This process could be termed photobiont "acquisition" or "recruitment". "Acquisition" is the more frequent term in the existing recent symbiosis literature and so is used here. The term "selection" is avoided as it also implies a different process of Darwinian natural selection, which may, or may not, occur in photobiont acquisition. The success of the photobiont acquisition may occur later when the fitness of the resulting lichen is tested by its survival to reproduction (viable ascospores), in lichens reproducing asexually, it is possible that a photobiont is acquired relatively rarely and is retained during vegetative dispersal. The populations of photobiont cells in lichens are large compared with the unlichenized ones for which we have evidence.

When lichens die, docs the photobiont also die? Observation in the field suggest that it does. If so, any beneficial variants and characters in the photobiont cannot be acquired by another mycobiont. For Darwinian natural selection, there has to be not only variation of genetically determined phenotypic characters but also, and essentially, a continuity of the photobiont cells by selection from one lichen into symbiosis in another. This completes a Darwinian "evolutionary cycle" of genetic variation alternating with selection. Without whatever benefits sexual reproduction offers occurring in the photobiont, the lack of this "evolutionary cycle" puts the two symbionts on different footings as far as the process of evolving of adaptations is concerned.

Evidence from Photohiont Molecular Analysis

Some examples of recent publications are very briefly reviewed below with the aim of finding any patterns in the mix of myco- and photobionts but a complete review of the literature is not attempted (see DePriest, 2004 and Nelsen & Gargas, 2008 for additional references). Here, there seems to be no logical story to tell so that this discussion starts with considering photobiont variation within an individual thallus, in populations, in species, in a genus and a family and then discussion of habitat and geographical distributions of photobionts and ends with lichens with more than one photobiont type.

Firstly therefore, if a photobiont has adapted to a particular lichen species, we might expect, at the very least, a lichen thallus would contain a uniform population of adapted photobionts. Indeed, Beck and Koop (2001) were unable to find distinguishable populations of photobiont cells within the different regions of the thallus in thalli of Pleurosticta acetabulum (photobiont Trebouxia arboricola) and Tremolecia atrata (photobiont Trebouxia sp.) so this might seem a reasonable assumption, but Piercey-Normore (2006) found more than one genotype in single thalli of Evernia mesomorpha. Within a population of a single lichen species, the photobiont genotype can vary even for a vegetatively reproducing species such as the common cosmopolitan isidiate lichen Parmotrema tinctorum. In this species, Ohmura et al. (2006) round that there were, in only 60 [km.sup.2], 28 combinations of four mycobionts and 21 photobiont genotypes, suggesting the possibility that either a) the area was colonised from several separate sources, on each occasion, the mycobiont bringing the photobiont strain with which it became symbiotic when it last reproduced from spores or b) lichens thalli change photobionts without reproducing by spores. Piercey-Normore (2006) similarly found a large number of Trebouxia genotypes in the sorediate Evernia mesomorpha collected from mixed deciduous--coniferous forest in Canada. When Guzow-Krzeminska (2006) and Blaha at al. (2006) examined the sexually reproducing species Protoparmeliopsis muralis and Lecanora rupicola respectively they also found a very diverse range of species and strains of Trebouxia. There appears to be no discernable pattern to the distribution of photobionts in lichens at the individual and species level.

At the generic level, there is no evident pattern that would suggest that the photobionts have become adapted to associating with related mycobionts. Tibell (2001) round in the lichen genus Chaenotheca which included 4 different genera of algal photobionts so that, although each species of Chaenotheca only contained one photobiont species, there is a far wider diversity of photobiont than of the mycobiont. Each of two subgeneric clades of Chaenotheca--Cvstophora and Allodium--contained Trebouxia (whose species occur free-living in a narrow range of habitats) and the unrelated Stichococcus (free-living in a wide range of habitats) respectively. Nelsen and Gargas (2008) have elegantly shown that in the genus Lepraria, a well-known genus with no evidence for producing sexual structures, the tree of ITS sequences of the mtSSU did hot have any correspondence with the ITS sequence tree (actin type 1 locus) of photobiont (Asterochloris). But Helms et al. (2001) found evidence of less diversity in the Physciaceae with species of Physcia being associated with one species of Trebouxia but species of Rinodina and Buellia being associated with several photobiont species. Baloch and Grube (2006) found in the Porinaceae that the lichen species contained a wide range of different Trentepohlia species many of which are known to occur unlichenized. For these albeit limited examples, there seems to be no consistent, or discernable, pattern of mycobiont versus photobiont diversity at the generic level.

A coincidence of photobiont species or strain and the habitat or geographical region is, on the other hand, apparent. In Peltigera, O'Brien et al. (2005) have found that the Nostoc cyanobiont strains are more like those in other symbioses and local free living populations of Nostoc than to each other indicating that the mycobiont acquires whatever Nostoc is available in its environment. With two unrelated spore reproducing species (Fulgensia fulgida and Toninia sediJolia) growing in the same community appeared to share the saine photobiont pool when colonising that habitat (Beck et al., 2002). Black fruited Caloplaca species (sect. Pyrenodesmia) in Italy shared similar lineages of Trebouxia (also shared with Lecanora rupicola) possibly associated with their spore reproduction and endolithic habit but a sorediate species (C. erodes) in this group had a different strain of Trebouxia (Muggia et al., 2008). These studies suggest that the mycobionts associated with whatever suitable photobionts were locally available. But this was not the conclusion of Yahr et al. (2004) who looked at the strains of fungi and photobionts in eight species of Cladonia in six disjoint Florida scrub sites. They did hot find evidence of distinct photobiont pools at the separate sites but for specificity by the eight mycobionts for one or two distinguishable Trebouxia genotypes and they concluded that differential photobiont availability did not explain the patterning of lichen associations in the field at this spatial scale but rather it was more closely associated with the different lichen species. Although not discussed by the authors, these species appear to be either branching-podetiate or large-squamulose thalli which probably reproduce by thallus fragmentation and can travel by, for example, wind or animal vectors. The distribution of these species was mainly within USA and some quite local to Florida and possibly a different circumstance to that of the widespread species Parmotrema tinctorum and other species above. In contrast to this study, a study of ITS in ribosomal DNA in Cladonia mycobionts and associated photobionts indicated that Trebouxia strains clustered together according to geographical location and more closely corresponded to environmental features (e.g. soil type) than fungal lineages (Beiggi & Piercey-Nonnore, 2007). With the recently evolved basidiolichen Omphalina, Zoller and Lutzoni (2003) concluded that the Coccomyra strain was genetically much more uniform than the mycobiont and distinct over a wide geographical range from cultures isolated from free-living populations and the strains found in lichens belonging to the Peltigeraceae. However in their study these authors did not indicate in their paper that they isolated free-living Coccomyxa from the same habitats in Greenland, Iceland and Canada from which they collected their Omphalina samples. Interestingly, a global scale geographical location may be significant as Cordeiro et al. (2005) has suggested by finding evidence of a tropical Trebouxia lineage of species and strains in Ramalina and Cladonia from coastal habitats of Brazil, on the basis of light microscopic and molecular analysis. Aproot and van Herk (2007) found that, in Western Europe, lichens most rapidly increasing in forests, although taxonomically unrelated, all contain Trentepohlia as phycobiont in addition to having a more southerly distribution, perhaps suggesting that the mycobionts are adapted to using this photobiont and they follow the photobiont which is migrating in response to global warming.

Summerfield et al. (2002) examined the cyanobionts (Nostoc) of Pseudocyphellaria crocata and P. neglecta and concluded that the two species differed only in the photobiont, rather than the mycobiont which appeared to be identical in both "species". Similarly, Sanders (2001) showed that in a species of Sticta in Brazil, identical lichen thalli were formed with cyanobiont and an algal photobiont. The thalli were made up of different lobes, some with phycobiont and some with cyanobiont, possibly suggesting that developing lobes on a mature lichen can acquire a new photobiont. The extreme polymorphism is only found in lichens which have evolved cephalodia (tripartite symbiosis; Hyvarinen et al., 2002). Cephalodia are apparently adaptations by the mycobiont to provide structures that enable the cyanobiont to fix nitrogen at enhanced rates. Lohtander et al. (2003) looked at the diversity of Nostoc in Nephroma species and found that those also having green algal photobionts were less specific in the acquisition of Nostoc cyanobiont but those with Nostoc as the only photobiont acquired a narrower range of strains.

Molecular studies of mycobionts have confirmed that some lichen genera contain lichen-forming and non-lichen forming species (Hawksworth and Hill, 1984; Wedin at al., 2005) indicating that the lichen-forming adaptations in mycobionts may evolve relatively quickly.

In conclusion, there appears to be no discemable pattern of photobiont variation based on molecular evidence associated with mycobiont diversity, confirming a very similar conclusion based on less molecular evidence by Ahmadjian (1993b).

Questions about Photobionts

Whether or not we assume there to be no photobiont adaption to lichenization, we need to ask questions about the sexual cycle, recombination and natural selection of photobionts both when lichenized and unlichenized. What appears to happen is that the mycobiont acquires a photobiont phenotype from the existing unlichenized population and, later, when the lichen thallus senesces, these cells eventually die without allowing the genotypes to enter into combination with another mycobiont. With the Darwinian "evolutionary cycle" incomplete, mutations are not apparently recombined nor selected through the phenotype in a lasting or directional way. In testing this argument, we need experimental evidence about the possible vital missing links in the "evolutionary cycle". Is there is evidence for the existence of any endothalline evolutionary processes? For example, what happens to photobiont cells after they have been acquired and integrated into the lichen thallus? Do they survive, and their daughter cells become available, for continued lichenization in another lichen? Some photobiont cells apparently can survive after being browsed by invertebrates (Froberg et al., 2001; Meier et al., 2002) but this probably represents only a very minor proportion of lichen thalli. Where do the "free-living" photobiont cells come from that occur on surfaces being colonised for the first time by a lichen? Although Beck and Koop (2001) showed uniform photobiont populations in single lichen thalli, we do not know how uniform photobiont populations are vertically in time either when lichenized or when unlichenized. Hill (1994a) found that, in Parmelia sulcata, the number of cell divisions required for the photobiont to populate a young lobe of 2 [mm.sup.2] from a soredium was about nine but the additional number then needed to form mature lobe 25 [mm.sup.2] was less than one indicating that the very early stages of thallus development are the most likely stage in determining the characteristics of the photobiont population in the mature thallus. Piercey-Normore and DePreist (2001; see also DePreist, 2004) discussed the molecular evidence, especially in the Cladoniaceae, that co-speciation of the fungal and algal symbionts does not appear occur and as a result have suggested the concept of "algal switching" to explain the unpredictable distribution of recognisable photobiont strains amongst different unrelated lichen species. They did not indicate any possible mechanism and the distribution of strains could equally have originated from similar unlichenized sources. In Lepraria, whose species have apparently no opportunity for photobiont acquisition when colonising a substrate from a spore, Nelsen and Gargas (2008) found similar results and support DePriest's concept of "algal-switching'. As mentioned, the most likely time for "switching" photobionts would seem to be early on during the development from soredium or srnall fragment when a faster growing photobiont might possibly usurp or oust the original one. It is conceivable that 'algal-switching' is a result of adaptation by mycobionts to providing a habitat or niche which different photobionts can inhabit and which photobiont genotype strain, or species is not important to the mycobiont. One strain might replace another, without any change in fitness, when a small propagule develops into a new thallus in a new location.

Piercey-Normore and DePriest (2001) describe the algal genotypes as "'highly selected" without specifying what features they might be selected for. The suggestion that a "superior genotype", as a result of a random mutation, would sweep through lichen populations assumes that a superior phenotype is possible. More evidence of the differences between lichenized and unlichenized photobionts would be very valuable in suggesting what adaptations there could be.

If photobiont adaptation to the lichenized state were to occur, what results might we see? One possibility is the joint dispersal of mycobiont spores and photobiont cells. This is because the chance of a spore, and a specific strain of photobiont, being present together close enough in space and time on a suitable substrate in a suitable habitat, an essential requirement for most lichen reproduction, would seem to be small. Such joint dispersal does apparently happen in some genera in the Verrucariaceae. Stichococcus, a genus subaerial unicellular algae, is the photobiont in Staurothele and Endocarpon and forms small rectangular cells within the ascocarp amongst the asci. These photobiont cells are a smaller size than those in the thallus and are dispersed with the ascospores and are present when the spores germinate and can immediately form a continuation of the symbiosis (Ahmadjian, 1993a). If we assume this is an adaptation to being lichenized, it has neither spread to other lichens nor are the species of these genera particularly common or found as early colonisers of new habitats. One wonders whether this potentially advantageous "adaptation" of an apparently "superior" photobiont confers any great advantage to the lichen.

Single species of lichen can form thalli with very different structures depending on whether the photobiont is green alga or cyanobacterium (e.g. Peltigera, Lobaria and Sticta symbiodemes). Perhaps these structures simulate niches suitable for the photobiont concerned. For example, Nostoc photobiont in homoiomerous gels such as Collema seem to mimic gel-like free-living Nostoc colonies. We ask whether, in numerous other lichens with a "heteromerous" thallus, photobiont layer mimics the bark-tissues of the endophloeodal habitat or the rock pores of the endolithic habitat. (In filamentous structures in which the fungal hyphae appear to grow along algal filaments (Coenogonium, Dictyonema) the thallus structure seems to be determined by the growth pattern of the photobiont.)

The absence of adaptation of photobionts to lichenization would also mean that there is no difference between unlichenized ("free-living") and lichenized photobionts and for example lichenized Trebouxia would not be genetically different from free-living Trebouxia strains notwithstanding the old, but now hopefully resolved, debate about whether or not Trebouxia occurs in a "free-living" state (Ahmadjian, 1993a). In cases where there are no suitable unlichenized populations available, lichen fungi would have to adapt to either reproducing vegetatively or to usurping other mycobionts by starting as lichenicolous fungi and taking over an existing lichenized photobiont population (e.g. as in Diploschistes muscorum). In Parmeliaceae (heteromous thallus), Parmelia (sensu lato) species from personal observation are usually vegetatively reproducing on the trunks of trees and most of the spore reproducing species occurring on twigs. Ellis and Coppins (2007) have shown that the mix of crustose lichen species occurring on aspen bark are more likely to be spore reproducing on young twig bark but there is a vegetatively reproducing mix on older branch bark with a clear trend from one to the other as the bark ages. The hyphae from germinating lichen spores presumably find endophloeodal Trebouxia cells on, or, possibly more likely, in the dead epidermal cells which might be an enclosed habitat similar to that within a lichen thallus. Beck at al. (1998) found molecular evidence that Xanthoria parietina acquires free-living Trebouxia arboricola rather than the Trebouxia strains found in vegetatively reproducing members of the Physciaceae that colonise the same twigs. Old bark on a branch or trunk is of a different structure and is already colonised by lichens, various algae and non-lichenized fungi, mosses and other organisms which might out-compete early algal colonisers of young bark. Hedenas et al. (2007) provide some supportive evidence for this in finding that the frequency of free-living Trebouxia on bark of the trunks of Populus tremula decreased with age of the trees. Lichen hyphae from germinating spores, are less likely to locate suitable algal cells on tree trunks. Spore producing lichens (such as Pertusaria spp.) appear to take longer to colonise old rough bark of tree trunks than they do thin twig bark. Ecological studies of the colonisation process could add to our understanding of how spore reproducing lichens colonise surfaces already covered by cryptogamic swards. Hill (1994b) recorded lichen colonisation on dated gravestones and found late colonisers such as Lecanora sulphurea and Toninia aromatica which seem to colonise on other species and may be, like Diploschistes muscorum, lichenicolous before acquiring a photobiont from its host. This could be a more widespread phenomenon of later colonisers in succession than is currently supposed.

Understanding the Main Basis of the Symbiosis

The main selective advantage fungi have in becoming symbiotic in lichens is the supply of carbohydrate, as its source of energy, produced by photosynthesis in the photobiont. This feature requires the photobiont to release the carbohydrate without fatal detriment to itself. The release of carbohydrate by the photobiont was once thought of as an evolutionary adaptation to being lichenized in a "trade-off" for other survival "benefits" such as the mycobiont providing a microhabitat for the photobiont, safe from browsing herbivores. But is this interpretation now useful? There has been little new information on carbohydrate movement from the alga to the fungus since the 1970s (readers can compare reviews such as Hill, 1976; Palmqvist, 2000; Smith, 1980). It seems extremely unlikely that the same mechanism of carbohydrate release would have evolved in the very wide range of unrelated organisms that occur as lichen photobionts. The type of carbohydrate, a polyol or glucose, and the structure of the molecule are all very similar amongst unrelated photobionts and mycobionts (Hill, 1976). It is proposed here that carbohydrate movement may not be the result of any adaptation on behalf of the photobiont but that a photobiont is acquired by a fungus because of the carbohydrate that it can locate and absorb. Although photobionts belong to very diverse groups of organisms, the only major groups of algae represented those that include multicellular species i.e. not only the green algae (Chlorophycae) but now also the red algae (Phaeospora lemaneae and a species of red alga probably Lemanea sp., Rhodophycae; Hawksworth, 1987, 1988; Hill, 1992a) and the brown algae (Petroderma maculliforme, Phaeophycae: Sanders et al., 2005). All these groups capable of multicellular organisation have physiological features in common (e.g. cell wall elongation (Van Sandt et al., 2007)) and it can be expected that all have mechanisms for the transfer of carbohydrate between the cells of their tissues. Most of the cyanobionts appear to be heterocystous which is as close to a multicellular organisation as is possible in these bacteria in which hexose, produced by photosynthesis, moves from the vegetative cells to the heterocyst (Meeks & Elhai, 2002). In cyanobiont lichens, the fungus absorbs glucose from the cyanobacterial cells. In non-heterocystous cyanobacteria, which do occur in lichens (e.g. Heppia spp (Rikkinen, 2002)), how the mechanism of nitrogen fixation is fuelled is not yet clearly understood although it is clear that cells cannot be photosynthetic and nitrogen fixing at the same time. All these multicellular, differentiated organisms require the movement of substances from one cell to another. It is suggested here that the mycobionts have taken advantage of interceding in this movement, thereby absorbing the carbohydrate, and nitrogen from heterocysts in cyanobacteria, to the mycobiont. As Trebouxia, in common with several other green algal photobionts, is apparently unicellular and autospore forming, carbohydrate release by the cells in the unlichenized state would not necessarily be expected but such a feature may never have been investigated in these green terrestrial algae. Another aspect of the symbiosis that might include the possibility of adaptation is the regulation of co-development of the myco- and photobiont especially regulation of the photobiont cell cycle (Hill, 1992b; Honegger, 1993).

Conclusions

1. From the evidence of molecular studies, there are no readily predicable patterns of photobiont genotype or species acquired by mycobionts in the formation of licbens thalli.

2. The populations of photobiont cells within lichens are far larger than those outwith lichens but the unlichenized populations are the source of photobionts for most new mycobiont-photobiont combinations.

3. Until there is further evidence to the contrary, it is likely that the photobiont cells in most lichens die with the lichen thallus and are not acquired by another mycobiont and are not subject to further selection.

4. As a result of 3, mycobiont selection during photobiont acquisition has little effect on the available genotypes and hence lichen photobionts have little opportunity to adapt to lichenization. Adaptation may be further restricted by the apparent lack of photobiont sexual reproduction and resultant gene recombination when lichenized.

5. The concept of photobiont acquisition, or recmitment, is more appropriate than photobiont selection although in the process the mycobiont may acquire strains (species, varieties, forms or genotypes) that are more suitable than others but this is unlikely have any evolutionary consequence.

6. Mycobionts associate with any available alga or cyanobacterium that will allow it to survive and may adapt to acquiring any photosynthetic organism so that it can incorporate it mutualistically into its thallus. Mycobiont adaptations are extensive and may occur relatively rapidly.

7. The terms "free-living" and "unlichenized" describe physiological and other phenotypic differences caused by being lichenized rather than genetic differences. There is no genetic difference between populations of "free-living" and "lichenized" photobionts.

8. Lichen photobionts are acquired from those groups of photosynthetic organisms that are capable of developing multicellular structures in one-, two- or three-dimensions (such as Chlorophyta, Phaeophyta, Rhodophyta and Cyanobacteria). Groups that are exclusively unicellular (such as Bacillariophyta, Cryptophyta and Dinophyta).

9. Future research on the lichen symbiosis would benefit from not presuming that lichen photobionts have any specifically adaptive genes to being lichenized or that a photobiont is restricted to specifically associating with any particular mycobiont.

Peter Crittenden and Richard Law very kindly provided valuable advice on earlier drafts of the manuscript. I am also grateful for the comments and suggestions of Ted Ahti, Andre Aproot, Allan Green, Ludger Kappen, Jim Lawrey, Robert Lucking, Gary Perlmutter and Pat Wolseley.

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David J. Hill (1,2)

(1) School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK

(2) Author for Correspondence; e-mail: d.j.hill(a bris.ac.uk

Published online: 9 May 2009

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