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.