Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera

Abstract

Ecological interactions range from purely specialized to extremely generalized in nature. Recent research has showed very high levels of specialization in the cyanolichens involving Peltigera (mycobionts) and their Nostoc photosynthetic partners (cyanobionts). Yet, little is known about the mechanisms contributing to the establishment and maintenance of such high specialization levels. Here, we characterized interactions between Peltigera and Nostoc partners at a global scale, using more than one thousand thalli. We used tools from network theory, community phylogenetics and biogeographical history reconstruction to evaluate how these symbiotic interactions may have evolved. After splitting the interaction matrix into modules of preferentially interacting partners, we evaluated how module membership might have evolved along the mycobionts’ phylogeny. We also teased apart the contributions of geographical overlap vs phylogeny in driving interaction establishment between Peltigera and Nostoc taxa. Module affiliation rarely evolves through the splitting of large ancestral modules. Instead, new modules appear to emerge independently, which is often associated with a fungal speciation event. We also found strong phylogenetic signal in these interactions, which suggests that partner switching is constrained by conserved traits. Therefore, it seems that a high rate of fungal diversification following a switch to a new cyanobiont can lead to the formation of large modules, with cyanobionts associating with multiple closely retated Peltigera species. Finally, when restricting our analyses to Peltigera sister species, the latter differed more through partner acquisition/loss than replacement (i.e., switching). This pattern vanishes as we look at sister species that have diverged longer ago. This suggests that fungal speciation may be accompanied by a stepwise process of (a) novel partner acquisition and (b) loss of the ancestral partner. This could explain the maintenance of high specialization levels in this symbiotic system where the transmission of the cyanobiont to the next generation is assumed to be predominantly horizontal. Synthesis. Overall, our study suggests that oscillation between generalization and ancestral partner loss may maintain high specialization within the lichen genus Peltigera, and that partner selection is not only driven by partners’ geographical overlap, but also by their phylogenetically conserved traits.

Evolutionary conservation of within-family biodiversity patterns

“…Both features are generally associated with life in harsh/windy environments 27,41 , and may thus favour the settlement of species bearing these characteristics in highlands. We also found a deep phylogenetic constraint in the incidence of interactions with plants in animals and type of photobiont in lichens, in line with results obtained with a finer categorisation of these interactions by other studies [42][43][44][45] . These interactions appear to be associated with the complexity of diversity-elevation relationships, which increases with the incidence of green algal photobionts in lichens, and of plant resource/host in animals (Fig.…”

History sets the stage: Macroevolutionary influence on biotic interactions

“…Another two focus on above‐ground herbivory (Coley et al ; Foisy et al ). One contribution dissects the lichen as a particularly interesting, co‐evolved symbiosis (Chagnon et al, ), and another presents a framework to understand the evolution of key nutritional trade‐offs in plants, with applicability to a wide range of biotic interactions (Goud et al, ).…”

“…The papers address three main questions that dominate the contem- (Chagnon et al, 2019), and another presents a framework to understand the evolution of key nutritional trade-offs in plants, with applicability to a wide range of biotic interactions (Goud et al, 2019).…”

Peltigera hydrophila (Lecanoromycetes, Ascomycota), a new semi-aquatic cyanolichen species from Chile

“…Peltigera sp. 14 is one of the rare cases in the genus Peltigera where both symbionts are specialists and associate almost exclusively with each other (Magain et al 2017a(Magain et al , b, 2018Miadlikowska et al 2018;Pardo-De la Hoz et al 2018;Chagnon et al 2019). The mycobiont forms thalli with Nostoc phylogroup XXIII, which was also found in a single specimen of its closest relative, P. aubertii, a species also found in Chile that otherwise associates with phylogroup XXII (Magain et al 2018).…”