Quantifying the climatic niche of symbiont partners in a lichen symbiosis indicates mutualist‐mediated niche expansions

Abstract

The large distributional areas and ecological niches of many lichenized fungi may in part be due to the plasticity in interactions between the fungus (mycobiont) and its algal or cyanobacterial partners (photobionts). On the one hand, broad-scale phylogenetic analyses show that partner compatibility in lichens is rather constrained and shaped by reciprocal selection pressures and codiversification independent of ecological drivers. On the other hand, sub-species-level associations among lichen symbionts appear to be environmentally structured rather than phylogenetically constrained. In particular, switching between photobiont ecotypes with distinct environmental preferences has been hypothesized as an adaptive strategy for lichen-forming fungi to broaden their ecological niche. The extent and direction of photobiont-mediated range expansions in lichens, however, have not been examined comprehensively at a broad geographic scale. Here we investigate the population genetic structure of Lasallia pustulata symbionts at sub-species-level resolution across the mycobiont's Europe-wide range, using fungal MCM7 and algal ITS rDNA sequence markers. We show that variance in occurrence probabilities in the geographic distribution of genetic diversity in mycobiontphotobiont interactions is closely related to changes in climatic niches. Quantification of niche extent and overlap based on species distribution modeling and construction of Hutchinsonian climatic hypervolumes revealed that combinations of fungal-algal interactions change at the sub-species level along latitudinal temperature gradients and in Mediterranean climate zones. Our study provides evidence for symbiontmediated niche expansion in lichens. We discuss our results in the light of symbiont polymorphism and partner switching as potential mechanisms of environmental adaptation and niche evolution in mutualisms.

The complexity of symbiotic interactions influences the ecological amplitude of the host: A case study inStereocaulon(lichenized Ascomycota)

“…A similar pattern was described by Rolshausen et al. () on the example of Lasallia pustulata . This generalist mycobiont associated with one Trebouxia species in the majority of its climatic niche, but on the periphery, it chooses more specialized phycobionts.…”

“…Several studies have investigated the effects of various climatic conditions (Fernández‐Mendoza et al., ; Grande et al., ; Leavitt et al., ; Marini, Nascimbene, & Nimis, ; Peksa & Škaloud, ; G. Singh et al., ). As of late, Rolshausen, Dal Grande, Sadowska‐Deś, Otte, and Schmitt () described mutualist‐mediated climatic niche expansion. Moreover, global climate change events have also been discussed in association with lichen phycobionts.…”

“…Singh et al, 2017). As of late, Rolshausen, Dal Grande, Sadowska-Deś, Otte, and Schmitt (2017) described mutualist-mediated climatic niche expansion. Moreover, global climate change events have also been discussed in association with lichen phycobionts.…”

A niche perspective on the range expansion of symbionts

“…The existence of environmental filters is well known in some mutualistic symbioses. Autotrophic symbionts of lichens often show distinct environmental preferences (Rolshausen et al, 2018). High temperatures break down the mutualistic association between dinoflagellates and corals (Herre et al, 1999).…”

“…Mutualistic symbionts may also enhance their own range expansion capacity through biotic facilitation on hosts (Traveset & Richardson, 2014). Mutualistic symbionts expand the abiotic niche of their hosts (Poisot et al, 2011;Peay, 2016), thus enabling colonisation of otherwise harsh abiotic environments for the host (Afkhami, McIntyre & Strauss, 2014;Rolshausen et al, 2018). For instance, mutualistic fungal endophytes associated with the grass Bromus laevipes ameliorate drought stress and expand the geographical range of this host species into drier habitats (Afkhami, McIntyre & Strauss, 2014).…”