Bioclimatic factors at an intrabiome scale are more limiting than cyanobiont availability for the lichen‐forming genus Peltigera

Abstract

For these cyanolichens, factors driving patterns of symbiotic associations are scale dependent. Contrary to global-scale findings, generalist Peltigera species were not more widespread within the boreal biome than specialists. Nostoc availability was not the only driver of Peltigera species' geographic ranges; environmental factors also contributed to their intrabiome distributions. Climatic conditions (especially precipitation) limited the range of some Peltigera species more than the range of their cyanobacterial partners at an intrabiome (boreal) scale.

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

“…This not only provides a potential explanation for the maintenance of specialization by the mycobiont, but also the asymmetry of specificity in lichens, which is resulting from a gradual increase in generalism by broadly distributed Nostoc partners that are hosting an increasingly large number of Peltigera species sharing a most recent common ancestor. This is in agreement with the results from Lu et al (), where Peltigera species have narrower latitudinal ranges than their broadly distributed generalist Nostoc partners.…”

“…If Peltigera species are not distributed randomly within our geographic regions, in a way that is linked to phylogeny, habitat partitioning may still be the underlying cause for part of the phylogenetically conserved partner selection observed in our system (Jüriado, Kaasalainen, Jylhä, & Rikkinen, ). For example, Lu et al () observed that along a latitudinal gradient crossing the entire boreal belt, some Peltigera species were restricted to specific portions of the gradient, well correlated to climatic variables such as total precipitation and mean temperature during the warmest quarter of the year. This study demonstrated that appropriate Nostoc phylogroup availability was not limiting for the Peltigera species sampled along this intra‐biome latitudinal gradient.…”

“…This is in contrast to a complete switch, that is, complete replacement of ancestral symbionts by new symbionts. Based on our previous observations of interaction patterns in section Polydactylon of the genus Peltigera, where we found high specialization levels by Peltigera species on Nostoc phylogroups that were more generalists than their Peltigera partners (Chagnon et al, 2018;Lu et al, 2018), we hypothesized that during fungal speciation, we would find either no change in Nostoc partner or Nostoc symbiont switching, rather than acquisitions or losses. We further hypothesized that shifts in Nostoc partners may be a stepwise process, whereby a fungus first acquires a new cyanobiont, to then lose their ancestral Nostoc partner.…”

“…We assembled a dataset of Peltigera-Nostoc interaction pairs summing up all information from the literature for which we could confidently assess the identity of the Peltigera species and Nostoc phylogroups or haplotypes (Chagnon et al, 2018;Lu et al, 2018;Magain, Miadlikowska, Goffinet, et al, 2017a;Magain, Miadlikowska, Mueller, et al, 2017b;Magain et al, 2018;Miadlikowska et al, 2014Miadlikowska et al, , 2018O'Brien, Miadlikowska, & Lutzoni, 2005;O'Brien, Miadlikowska, & Lutzoni, 2013;Pardo De la Hoz et al, 2018). The total dataset consisted of 1,026 thalli, or interaction pairs, representing 155 Peltigera species and 95 Nostoc phylogroups or haplotypes (Tables S1 and S2).…”

“…These lichenforming fungi (also referred to as mycobionts) are typically highly specialized on one or very few cyanobacterial phylogroup partners (also referred to as cyanobionts) that commonly associate with multiple Peltigera species (asymmetric specificity). The evolution of specialization has fuelled a large body of literature in ecology and evolution (Fisher, 1930;Levins, 1968;MacArthur, 1955;May, 1974) and one question that might be asked when looking at current patterns of specialization is whether selection towards such patterns was directional or stabilizing: in other words, is there a directional evolution towards specialization (Jaenike, 1990) or generalization (Waser, Chittka, Price, Williams, & Ollerton, 1996) or a combination of both, that is, specialization of Peltigera and generalization of Nostoc, which could be advantageous especially when symbionts are transmitted mostly horizontally (Chagnon et al, 2018;Lu et al, 2018;Lutzoni & Miadlikowska, 2009;Magain, Miadlikowska, Goffinet, Sérusiaux, & Lutzoni, 2017a)? Alternatively, has the specialization level of a guild been stable for a long time due to selection against higher, or lower, levels of specialization (i.e., stabilizing selection)?…”