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The study of insular populations was key in the development of evolutionary theory. The successful colonisation of an island depends on the geographic context, and specific characteristics of the organism and the island, but also on stochastic processes. As a result, apparently identical islands may harbour populations with contrasting histories. Here, we use whole genome sequences of 65 barn owls to investigate the patterns of inbreeding and genetic diversity of insular populations in the eastern Mediterranean Sea. We focus on Crete and Cyprus, islands with similar size, climate and distance to mainland, that provide natural replicates for a comparative analysis of the impacts of microevolutionary processes on isolated populations. We show that barn owl populations from each island have a separate origin, Crete being genetically more similar to other Greek islands and mainland Greece, and Cyprus more similar to the Levant. Further, our data show that their respective demographic histories following colonisation were also distinct. On the one hand, Crete harbours a small population and maintains very low levels of gene flow with neighbouring populations. This has resulted in low genetic diversity, strong genetic drift, increased relatedness in the population and remote inbreeding. Cyprus, on the other hand, appears to maintain enough gene flow with the mainland to avoid such an outcome. Our study provides a comparative population genomic analysis of the effects of neutral processes on a classical island-mainland model system. It provides empirical evidence for the role of stochastic processes in determining the fate of diverging isolated populations.

The climate fluctuations of the Quaternary shaped the movement of species in and out of glacial refugia. In Europe, the majority of species followed one of the described traditional postglacial recolonization routes from the southern peninsulas towards the north. Like most organisms, barn owls are assumed to have colonized the British Isles by crossing over Doggerland, a land bridge that connected Britain to northern Europe. However, while they are dark rufous in northern Europe, barn owls in the British Isles are conspicuously white, a contrast that could suggest selective forces are at play on the islands. However, analysis of known candidate genes involved in colouration found no signature of selection. Instead, using whole genome sequences and species distribution modelling, we found that owls colonised the British Isles soon after the last glaciation, directly from a white coloured refugium in the Iberian Peninsula, before colonising northern Europe. They would have followed a yet unknown post-glacial colonization route to the Isles over a westwards path of suitable habitat in now submerged land in the Bay of Biscay, thus not crossing Doggerland. As such, they inherited the white colour of their Iberian founders and maintained it through low gene flow with the mainland that prevents the import of rufous alleles. Thus, we contend that neutral processes likely explain this contrasting white colour compared to continental owls. With the barn owl being a top predator, we expect future research will show this unanticipated route was used by other species from its paleo community.

Melanins are widespread pigments in vertebrates, with important roles in visual signaling, UV protection, and homeostasis. Fossil evidence of melanin and melanin-bearing organelles – melanosomes – in ancient vertebrates may illuminate the evolution of melanin and its functions, but macroevolutionary trends are poorly resolved. Here, we integrate fossil data with current understanding of melanin function, biochemistry, and genetics. Mapping key genes onto phenotypic attributes of fossil vertebrates identifies potential genomic controls on melanin evolution. Taxonomic trends in the anatomical location, geometry, and chemistry of vertebrate melanosomes are linked to the evolution of endothermy. These shifts in melanin biology suggest fundamental links between melanization and vertebrate ecology. Tissue-specific and taxonomic trends in melanin chemistry support evidence for evolutionary tradeoffs between function and cytotoxicity.

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.

New genomic tools open doors to study ecology, evolution, and population genomics of wild animals. For the Barn owl species complex, a cosmopolitan nocturnal raptor, a very fragmented draft genome was assembled for the American species (Tyto furcata pratincola) (Jarvis et al. 2014). To improve the genome, we assembled de novo Illumina and Pacific Biosciences (PacBio) long reads sequences of its European counterpart (Tyto alba alba). This genome assembly of 1.219 Gbp comprises 21,509 scaffolds and results in a N50 of 4,615,526 bp. BUSCO (Universal Single‐Copy Orthologs) analysis revealed an assembly completeness of 94.8% with only 1.8% of the genes missing out of 4,915 avian orthologs searched, a proportion similar to that found in the genomes of the zebra finch (Taeniopygia guttata) or the collared flycatcher (Ficedula albicollis). By mapping the reads of the female American barn owl to the male European barn owl reads, we detected several structural variants and identified 70 Mbp of the Z chromosome. The barn owl scaffolds were further mapped to the chromosomes of the zebra finch. In addition, the completeness of the European barn owl genome is demonstrated with 94 of 128 proteins missing in the chicken genome retrieved in the European barn owl transcripts. This improved genome will help future barn owl population genomic investigations.

Lesser kestrel males display inter-individual variation in melanin-based plumage traits, like ventral plumage colouration and breast/underwing spottiness. We explored whether such plumage variability was associated with single-nucleotide genetic polymorphisms of melanocortin-1-receptor (MC1R) and tyrosinase-related protein 1 (TYRP1), two genes involved in the melanogenesis pathway. No statistically significant associations between single-nucleotide mutations and male plumage traits emerged, though in some cases very rare (

The mean phenotypic effects of a discovered variant help to predict major aspects of the evolution and inheritance of a phenotype. However, differences in the phenotypic variance associated to distinct genotypes are often overlooked despite being suggestive of processes that largely influence phenotypic evolution, such as interactions between the genotypes with the environment or the genetic background. We present empirical evidence for a mutation at the melanocortin-1-receptor gene, a major vertebrate coloration gene, affecting phenotypic variance in the barn owl, Tyto alba. The white MC1R allele, which associates with whiter plumage coloration, also associates with a pronounced phenotypic and additive genetic variance for distinct color traits. Contrarily, the rufous allele, associated with a rufous coloration, relates to a lower phenotypic and additive genetic variance, suggesting that this allele may be epistatic over other color loci. Variance differences between genotypes entailed differences in the strength of phenotypic and genetic associations between color traits, suggesting that differences in variance also alter the level of integration between traits. This study highlights that addressing variance differences of genotypes in wild populations provides interesting new insights into the evolutionary mechanisms and the genetic architecture underlying the phenotype.

Knowledge of how and why secondary sexual characters are associated with sex hormones is important to understand their signalling function. Such a link can occur if i) testosterone participates in the elaboration of sex-traits, ii) the display of an ornament triggers behavioural response in conspecifics that induce a rise in testosterone, or iii) genes implicated in the elaboration of a sex-trait pleiotropically regulate testosterone physiology. To evaluate the origin of the co-variation between melanism and testosterone, we measured this hormone and the expression of enzymes involved in its metabolism in feathers of barn owl (Tyto alba) nestlings at the time of melanogenesis and in adults outside the period of melanogenesis. Male nestlings displaying smaller black feather spots had higher levels of circulating testosterone, potentially suggesting that testosterone could block the production of eumelanin pigments, or that genes involved in the production of small spots pleiotropically regulate testosterone production. In contrast, the enzyme 5α-reductase, that metabolizes testosterone to DHT, was more expressed in feathers of reddish-brown than light-reddish nestlings. This is consistent with the hypothesis that testosterone might be involved in the expression of reddish-brown pheomelanic pigments. In breeding adults, male barn owls displaying smaller black spots had higher levels of circulating testosterone, whereas in females the opposite result was detected during the rearing period, but not during incubation. The observed sex- and age-specific co-variations between black spottiness and testosterone in nestling and adult barn owls may not result from testosterone-dependent melanogenesis, but from melanogenic genes pleiotropically regulating testosterone, or from colour-specific life history strategies that influence testosterone levels.

[EN]: Melanin-based colorations in birds constitute a paradigm for the study of the molecular basis of phenotypic variation. Variation in the melanocortin-1 receptor (MCR1) gene, a key regulator of melanin synthesis in feather melanocytes, can lead to changes in the production of melanin and hence in feather colour. Here we investigate the proximate mechanisms behind colour plumage polymorphism in the Eurasian Scops-owl Otus scops, a species showing pronounced variation in the degree of redness. Although eumelanin pigment was three times more abundant than pheomelanin pigments, the degree of plumage redness was more strongly associated with the amount of pheomelanin than eumelanin pigments. We detected only one synonymous substitution and one non-synonymous substitution in MC1R which were, however, not associated with variation in plumage coloration. Redness variation in Eurasian Scops-Owls is primarily due to variation in pheomelanin, and to genes or regulatory elements other than MCR1. [ES]: Las coloraciones basadas en melanina en las aves constituyen un paradigma para el estudio de las bases moleculares de la variación fenotípica. La variación en el gen del receptor de melanocortina-1 (MCR1), un regulador clave de la síntesis de melanina en los melanocitos de las plumas, puede provocar cambios en la producción de melanina y, por lo tanto, en el color de las plumas. Aquí investigamos los mecanismos próximos detrás del polimorfismo del plumaje de color en los autillos europeos Otus scops, una especie que muestra una marcada variación en el grado de rojismo. Aunque la cantidad de eumelanina era tres veces más abundante que la de feomelanina, el grado de rojismo del plumaje se asoció más fuertemente con la cantidad de feomelanina que con la eumelanina. Sólo detectamos una sustitución sinónima y una sustitución no sinónima en el MC1R que, sin embargo, no se asociaron con la variación en la coloración del plumaje. La variación de rojismo en el autillo europeo se debe principalmente a la variación en el contenido de feomelanina, y a genes o elementos reguladores de estos distintos del MCR1. This work was funded by the Spanish Ministry of Economy and Competitiveness, projects CgL2008-00718, CgL2011-27561, CgL2014-56769-p and CgL2017-83503-p to JMA and Dp. Dp was supported by the regional government of Extremadura (TA13002) and AC by a phD grant from the Spanish Ministry of Science (BES-2015-074948) during the redaction of this manuscript.

Uncovering the genetic basis of phenotypic variation and the population history under which it established is key to understand the trajectories along which local adaptation evolves. Here, we investigated the genetic basis and evolutionary history of a clinal plumage color polymorphism in European barn owls (Tyto alba). Our results suggest that barn owls colonized the Western Palearctic in a ring-like manner around the Mediterranean and meet in secondary contact in Greece. Rufous coloration appears to be linked to a recently evolved nonsynonymous-derived variant of the melanocortin 1 receptor (MC1R) gene, which according to quantitative genetic analyses evolved under local adaptation during or following the colonization of Central Europe. Admixture patterns and linkage disequilibrium between the neutral genetic background and color found exclusively within the secondary contact zone suggest limited introgression at secondary contact. These results from a system reminiscent of ring species provide a striking example of how local adaptation can evolve from derived genetic variation.

Knowledge of the role of origin-related, environmental, sex, and age factors on host defence mechanisms is important to understand variation in parasite intensity. Because alternative components of parasite defence may be differently sensitive to various factors, they may not necessarily covary. Many components should therefore be considered to tackle the evolution of host-parasite interactions. In a population of barn owls (Tyto alba), we investigated the role of origin-related, environmental (i.e. year, season, nest of rearing, and body condition), sex, and age factors on 12 traits linked to immune responses [humoral immune responses towards sheep red blood cells (SRBC), human serum albumin (HSA) and toxoid toxin TT, T-cell mediated immune response towards the mitogen phytohemagglutinin (PHA)], susceptibility to ectoparasites (number and fecundity of Carnus haemapterus, number of Ixodes ricinus), and disease symptoms (size of the bursa of Fabricius and spleen, proportion of proteins that are immunoglobulins, haematocrit and blood concentration in leucocytes). Cross-fostering experiments allowed us to detect a heritable component of variation in only four out of nine immune and parasitic parameters (i.e. SRBC- and HSA-responses, haematocrit, and number of C. haemapterus). However, because nestlings were not always cross-fostered just after hatching, the finding that 44% of the immune and parasitic parameters were heritable is probably an overestimation. These experiments also showed that five out of these nine parameters were sensitive to the nest environment (i.e. SRBC- and PHA-responses, number of C. haemapterus, haematocrit and blood concentration in leucocytes). Female nestlings were more infested by the blood-sucking fly C. haemapterus than their male nestmates, and their blood was less concentrated in leucocytes. The effect of year, season, age (i.e. reflecting the degree of maturation of the immune system), brood size, position in the within-brood age hierarchy, and body mass strongly differed between the 12 parameters. Different components of host defence mechanisms are therefore not equally heritable and sensitive to environmental, sex, and age factors, potentially explaining why most of these components did not covary. (c) 2007 The Linnean Society of London.

Secondary sexual characters are thought to indicate individual quality. Expression of sex-limited traits in an extravagant state may require both the underlying genes and the available nutrient resources. The assessment of the relative contribution of genes, environment, and body condition is relevant for understanding to that extent the extravagant trait may signal genotypic or phenotypic quality of the individual. In birds, usually only the males are ornamented. In the barn owl, Tyto alba, both females and males display sex-limited plumage traits. Males are commonly lighter colored and females spottier. In an experiment with combined cross-fostering and brood size manipulation we determined the relative contribution of genes, environment, and body condition to the variation in plumage coloration and plumage spottiness. The partial cross-fostering experiment tested the relative importance of shared genes and a shared environment for the resemblance of related birds. Siblings raised in different nests converged toward similar trait values, offspring resembled the true but not the foster parents, and plumage traits of unrelated nestlings sharing the same nest were not correlated. Results were not inflated by maternal effects detectable in the mother's phenotype, because middaughter to mother resemblance was not higher than midson to father resemblance. This suggests that plumage coloration and spottiness are largely genetically inherited traits, and that the rearing environment does not have a strong impact on the expression of these traits. To further investigate whether the two sex-limited traits are condition dependent, brood sizes were manipulated. Enlargement or reduction of broods by two nestlings resulted in lower and higher body mass of nestlings, respectively. However, nestlings raised in enlarged or reduced broods did not show either a significantly darker or lighter or a more or less spotted plumage. We did not detect any genotype- by-environment interaction. In conclusion, simultaneous cross-fostering and brood size manipulation demonstrate that additive genetic variance for plumage coloration and spottiness is maintained and that both the rearing environment and body condition do not account for a large proportion of the phenotypic variance in female and male ornamentations.