Adaptive differentiation coincides with local bioclimatic conditions along an elevational cline in populations of a lichen-forming fungus

Abstract

BackgroundMany fungal species occur across a variety of habitats. Particularly lichens, fungi forming symbioses with photosynthetic partners, have evolved remarkable tolerances for environmental extremes. Despite their ecological importance and ubiquity, little is known about the genetic basis of adaption in lichen populations. Here we studied patterns of genome-wide differentiation in the lichen-forming fungus Lasallia pustulata along an altitudinal gradient in the Mediterranean region. We resequenced six populations as pools and identified highly differentiated genomic regions. We then detected gene-environment correlations while controlling for shared population history and pooled sequencing bias, and performed ecophysiological experiments to assess fitness differences of individuals from different environments.ResultsWe detected two strongly differentiated genetic clusters linked to Mediterranean and temperate-oceanic climate, and an admixture zone, which coincided with the transition between the two bioclimates. High altitude individuals showed ecophysiological adaptations to wetter and more shaded conditions. Highly differentiated genome regions contained a number of genes associated with stress response, local environmental adaptation, and sexual reproduction.ConclusionsTaken together our results provide evidence for a complex interplay between demographic history and spatially varying selection acting on a number of key biological processes, suggesting a scenario of ecological speciation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-0929-8) contains supplementary material, which is available to authorized users.

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

“…S5), additional genome-wide analyses -as opposed to our rather conservative set of genetic markers (ITS rDNA for algae and MCM7 for fungi) -would be valuable. For instance, a recent study found genome-wide differentiation among L. pustulata mycobionts from the Mediterranean (Sardinia, Italy) that is likely driven by adaptive divergence along an elevational cline (Dal Grande et al 2017b). Taken together, our results provide evidence for mutualist-mediated niche (and range) expansion in lichens -a strategy also observed in other mutualisms (Afkhami et al 2014, Bongaerts et al 2015, Maher et al 2017) -thereby corroborating theoretical predictions for symbiosis as an adaptive process (Moran 2007, Poisot et al 2011, Friesen and Jones 2012.…”

“…Accordingly, regarding the interaction hotspots of symbiont partners (depicted as the product of their respective occurrence probabilities), the generalist mycobiont (OTU fungus 1) will also likely encounter these Trebouxia strains at the outer margins of its distribution (Fig. For instance, a recent study found genome-wide differentiation among L. pustulata mycobionts from the Mediterranean (Sardinia, Italy) that is likely driven by adaptive divergence along an elevational cline (Dal Grande et al 2017b). Notably, the remaining genetically differentiated mycobionts (OTU fungus 2-4) primarily clustered in the Mediterranean (Supplementary material Appendix 1 Fig.…”

Environment and host identity structure communities of green algal symbionts in lichens

“…This might result in the formation of geographically structured host–symbiont combinations experiencing different selection pressure as a result of differences in regional biotic and abiotic factors (geographic mosaic of coevolution; Thompson, ). In support of this hypothesis, we showed in a recent study that the fungal partners in a metapopulation of L. pustulata along an altitudinal gradient consisted of locally adapted ecotypes (Dal Grande et al ., ). Interestingly, the ecotone between warm and cool temperate biomes corresponds to the upper limit of the distribution for both the warm‐adapted Lasallia ecotype and Trebouxia OTU3.…”

What is in a lichen? A metagenomic approach to reconstruct the holo-genome of Umbilicaria pustulata

“…For the reconstruction of the metatranscriptome, we assembled the RNAseq data provided in (Dal Grande, et al 2017) with Trinity release 2013-11-10 (Haas, et al 2013), using thejaccard-clip -normalize_reads parameters.…”

“…Details on the biology and distribution of U. pustulata have been published elsewhere (e,g. (Hestmark 1992;Dal Grande, et al 2017). We inferred the genome sequences of the lichenized fungus Umbilicaria pustulata, its green algal symbiont Trebouxia sp., and its bacterial microbiome.…”