Unravelling the Secret of Phantom Phenotypes in Macrolichens: Insights From Cladonia bellidiflora Complex

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Lichens are unique among symbiotic organisms because their distinctive features develop only through interactions between the partners and differ from the appearance of each partner when grown separately in culture. Traditionally, lichen phenotype has been assumed to be determined by the mycobiont; however, exceptions exist that challenge the universal validity of this rule. One example is the phenomenon of 'phantom phenotypes', where lichens with genetically indistinguishable mycobionts exhibit distinct morphologies, sometimes better explained by differences among other symbiotic partners. In previous work, we documented such a case in the Cladonia bellidiflora complex, a group of red-fruited macrolichens with striking morphological and ecological variation, in which photobiont identity corresponded more closely to phenotype than the mycobiont when studied using five molecular markers. Here, we investigate this phenomenon using restriction-site associated DNA sequencing (RADseq) of both fungal and algal symbionts, combined with Sanger sequencing of ITS rDNA and the actin locus of the photobiont. Our results indicate that recent fungal divergence, together with correlated photobiont differentiation, is associated with the observed phenotypic differentiation, highlighting the importance of sensitive methods in similar cases. Specifically, RADseq analyses revealed a clear split between C. bellidiflora and all sorediate taxa, including C. polydactyla and C. umbricola, which showed no genomic differentiation, supporting their recognition as a single species. Additionally, substrate preference, symbiont associations and dispersal strategy appear to have acted in parallel to shape diversification in this complex. Photobiont data revealed unexpected patterns: esorediate C. bellidiflora associated with narrow photobiont sets, whereas sorediate lineages harboured a broader photobiont pool.

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