Molecular basis of food intake, starvation response and energy homeostasis suggest adaptations to harsh winter environments
The most obvious target for the genetic regulation of coloration in melanin-based pigmentation is the coding sequence of the geneM1CR . Contrary to general expectations, comparisons between coding sequences of grey and brown tawny owl revealed MC1R to be 100% conserved between morphs. These observations are however not exceptional, as other avian species exhibiting equally remarkable colour polymorphisms also show conservation of MC1R coding region (Avilés et al., 2019; Hoffman et al., 2014; MacDougall-Shackleton et al., 2003). Among the investigated genes that are to some extent involved in the melanin-production pathway, only the melanin concentration hormone receptor (MCHR ) exhibits non-synonymous substitutions between colour morphs. However, a direct and functional relationship between MCHR polymorphism and melanin pigmentation has been found exclusively in teleost fishes, specifically trout and salmonids (Diniz & Bittencourt, 2019). Among mammal and avian taxa alike, the functionality of this neuromodulator is rather associated with fasting control and energy balance, physiological traits plausible to be under selection in food limitation conditions (Cui et al., 2017). The genome-wide association study expanded to 370 individuals and respective pedigrees – correcting for both relationships and population substructure – provided additional lines of evidence for colour-morph specific, resource-related physiological responses. Associations with colour phenotypes revealed two candidate loci, FAM135A andFTCD, whose biological functions were shown to be linked to lipid metabolism pathway, fat storage mechanisms, and maintenance of homeostasis under starvation in both pigs and chickens in captivity (Poleti et al., 2018; Zhang et al., 2021). In our tawny owl population, putative biological functionality of candidate loci is perhaps better contextualized in the harsh winter conditions in Southern Finland. At 60° N latitude, Finnish tawny owls experience snowfall periods that usually start in December and generally peaking in January and February with snow-coverage usually lasting until the months prior to the onset of the tawny owl’s breeding season (Karell et al., 2011). Previous work on the study population used here have shown that these extreme conditions do impose a strong selective pressure against brown tawny owls while resulting in a higher survival rate of grey tawny owls following snow-heavy winters (Karell et al., 2011). The high effect size of candidate loci in predicting grey coloration (up to 100% in some genotype combinations) strongly suggests our results have identified the majority of the genetic regulation of the grey colour morph in this population as well as some of the loci underlying adaptation to their local environment. The relevance of an adapted lipid metabolism (whether it would be degradation, accumulation, or deposition) to biological survival in cold environments has been reported multiple times across taxa (Blem, 1976; Lucassen, Koschnick, Eckerle, & Portner, 2006). To the best of our knowledge, this study is unique in demonstrating a genetic link between lipid metabolism and melanin-pigmentation in a natural population, effectively rendering the tawny owl system the first where the molecular basis of a melanin-phenotype has been unveiled. A brief exploration of signatures of selection – via HWE tests and temporal shifts of candidate loci’s genotype frequencies – showed that, when they did occur, deviations from HWE were associated with an excess of homozygotes for the most common allele in either locus implying that selection appears to be against grey-coated individuals.