Examination of genetic polymorphisms in outbred wild-living species provides insights into the evolution of complex systems. In higher vertebrates, the proopiomelanocortin (POMC) precursor gives rise to α-, β-, and γ-melanocyte-stimulating hormones (MSH), which are involved in numerous physiological aspects. Genetic defects in POMC are linked to metabolic disorders in humans and animals. In the present study, we undertook an evolutionary genetic approach complemented with biochemistry to investigate the functional consequences of genetic polymorphisms in the POMC system of free-living outbred barn owl species (family Tytonidae) at the molecular level. Our phylogenetic studies revealed a striking correlation between a loss-of-function H9P mutation in the β-MSH receptor-binding motif and an extension of a poly-serine stretch in γ3-MSH to ≥7 residues that arose in the barn owl group 6-8 MYA ago. We found that extension of the poly-serine stretches in the γ-MSH locus affects POMC precursor processing, increasing γ3-MSH production at the expense of γ2-MSH and resulting in an overall reduction of γ-MSH signaling, which may be part of a negative feedback mechanism. Extension of the γ3-MSH poly-serine stretches ≥7 further markedly increases peptide hormone stability in plasma, which is conserved in humans, and is likely relevant to its endocrine function. In sum, our phylogenetic analysis of POMC in wild living owls uncovered a H9P β-MSH mutation subsequent to serine extension in γ3-MSH to 7 residues, which was then followed by further serine extension. The linked MSH mutations highlight the genetic plasticity enabled by the modular design of the POMC gene.

Life history traits differ between organisms living in the tropics, Northern and Southern Hemispheres, and sexual selection is thought to be stronger close to the equator than in temperate regions. Although birds are often supposed to be more brightly coloured in the tropics, the current evidence of geographic variation in the intensity of sexual selection and sex-specific natural selection is equivocal. Whether sex-specific traits signal aspects of individual quality better in the tropics than in the temperate regions of the Northern and Southern Hemispheres therefore remains an open question. We examined predictions of this hypothesis in the Tytonidae family (barn owls and their relatives) because females, on average, display larger black spots on the tip of their ventral body feathers than males, and this trait is associated with aspects of individual quality. We measured the size of melanic spots and the wing length of 7893 Tytonidae skins collected worldwide and preserved in natural history museums. The covariation between spot size and wing length was stronger in females than in males, in large- than small-spotted Tyto taxa and close to the equator than in temperate regions. This suggests that selection for spot size, which can be used by owls as an additional cue to assess individual body size and other aspects of phenotypic quality, is stronger in females than in males, particularly near the equator.

Aim: Geological barriers within a species range play a key role in shaping patterns of genetic variation by restricting gene flow. Mountain ranges are particularly imposing barriers responsible for creating genetic differentiation across multiple taxa, from small amphibians to large mammals and birds. Here, we examined the population structure of North American barn owls (Tyto alba) and investigated whether the Rocky Mountains influence gene flow and dispersal at the continental scale. Location: Continental North America. Methods: We collected 292 museum samples covering the species range, genotyped them at 20 microsatellite markers and sequenced 410 bp of the mitochondrial gene ND6. Population and landscape genetics tools were used to study range-wide patterns of structure and identify gene flow barriers. Ring recapture data were also analysed to investigate individual movement patterns and frequency of exchanges between both sides of the Rocky Mountains. Results: We found faint overall genetic structure, which is consistent with barn owl's high mobility across its continuous range. Nonetheless, we identified two distinct genetic groups on the western and eastern regions of the Rocky Mountains with a likely contact point through the narrow southern pass between them and the Sierra Madre Occidental in Mexico. Accordingly, most recaptured barn owls remain on the same side of the mountains. The Rockies appear to significantly isolate the populations in the west, which, as a consequence, display lower genetic diversity than their counterparts to the east. Main conclusions: The Rocky Mountains appear to constrain barn owl dispersal and gene flow. Our study supports the hypothesis that regional landscape barriers can shape gene flow and population structure even in highly mobile organisms.

The owl family Tytonidae comprises two genera: Phodilus, limited to the forests of central Africa and South-East Asia, and the ubiquitous Tyto. The genus Tyto is majorly represented by the cosmopolitan Common Barn Owl group, with more than 30 subspecies worldwide. Discrete differences in body size and plumage colouration have led to the classification of this family into many species and subspecies, but the taxonomic status and phylo-genetic relationships between taxa remain unclear, and in some groups controversial. Although several previous studies attempted to resolve this problem, they have been limited in their taxonomic and geographical coverage, or have relied on restricted molecular evidence and low sample sizes. Based on the most comprehensive sampling to date (16 out of 17 Tyto species, and one out of three Phodilus species), a multi-locus approach using seven mitochondrial and two nuclear markers, and taking advantage of field data and museum collections available worldwide, our main questions in this study were: (1) what are the phylogenetic relationships and classification status of the whole family; (2) when and where did the most important speciation events occur? We confirm that the Common Barn Owl, Tyto alba is divided into three main evolutionary units: the American Barn Owl, T. furcata; the Western Barn Owl, T. alba; and the Eastern Barn Owl, T. javanica, and suggest a Late Miocene (ca. 6 mya) Australasian and African origin of the group. Our results are supported by fossil age information, given that the most recent common ancestor between the Tytonidae genera Phodilus and Tyto was probably from the Oligocene (ca. 28 mya) of Australasia. We finally reveal six major Pleistocene radiations of Tyto, all resulting in wide-range distributions.