Circadian clock-associated gene differentiation along elevation gradients in lichenized fungi

Circadian regulation is linked to local environmental adaptation. Accordingly, many species with broad geographic and climatic niches display variation in circadian clock genes. Here we hypothesize that lichen-forming fungi, which occupy different climate zones along elevation gradients, tune their metabolism to local environmental conditions with the help of their circadian systems. We study two species of the genus Umbilicaria, which occupy similar climatic niches along elevation in different continents. Using homology to known functional genes from Neurospora crassa, we identify gene sets associated with circadian rhythms (11 core, 39 peripheral genes) as well as temperature response (37 genes). Population genomics approaches indicate that nucleotide diversity of these genes is significantly correlated with mean annual temperature, minimum temperature of the coldest month, and mean temperature of the coldest quarter. Altitudinal clines in allele frequencies pertain to several non-synonymous substitutions in core clock components, e.g. white collar-like, frh-like and various ccg-like genes. A dN/dS approach revealed a small number of significant peripheral clock- and temperature-associated genes (e.g. ras-1-like, gna-1-like) that may play a role in fine-tuning the circadian clock and temperature-response machinery. These results highlight the likely relevance of the circadian clock in environmental adaptation, particularly frost tolerance, of lichenized fungi. Whether or not the fungal clock modulates the symbiotic interaction within the lichen consortium remains to be investigated. We corroborate the finding of significant genetic variation in clock components along altitude – not only latitude – as has been reported in a variety of species.