Melanin-based plumage coloration and melanin content in organs in the barn owl.

Although the evolutionary ecology of melanin pigments and melanin-based coloration has been studied in great details, particularly in birds, little is known about the function of melanin stored inside the body. In the barn owl Tyto alba, in which individuals vary in the degree of reddish pheomelanin-based coloration and in the size of black eumelanic feather spots, we measured the concentration in melanin pigments in seven organs. The eyes had by far the most melanin then the skin, pectoral muscle, heart, liver, trachea, and uropygial gland. The concentration in eumelanin was not necessarily correlated with the concentration in pheomelanin suggesting that their production can be regulated independently from each other. Redder barn owls had more pheomelanin in the skin and uropygial gland than white owls, while owls displaying larger black feather spots had more eumelanin in the skin than small-spotted owls. More data are required to evaluate whether melanin-based traits can evolve as an indirect response to selection exerted on melanin deposition in organs.

Limited associations between MHC diversity and reproductive success in a bird species with biparental care.

The selective pressure from pathogens on individuals can have direct consequences on reproduction. Genes from the major histocompatibility complex (MHC) are central to the vertebrate adaptive immune system and pathogen resistance. In species with biparental care, each sex has distinct reproductive roles and levels of investment, and due to a trade-off with immunity, one can expect different selective regimes acting upon the MHC of each parent. Here, we addressed whether couples combine each other's variation at MHC loci to increase their breeding success. Specifically, we used a 23-year dataset from a barn owl population (Tyto alba) to understand how MHC class Iα and IIß functional divergence and supertypes of each parent were associated with clutch size and fledging success. We did not detect associations between MHC diversity and supertypes with the clutch size or with the fledging success. In addition, to understand the relative contribution from the MHC of the genetic parents and the social parents, we analyzed the fledging success using only a cross-fostered dataset. We found several associations of weak-to-moderate effect sizes between the father's MHC and fledging success: (i) lower MHC-Iα divergence in the genetic father increases fledging success, which might improve paternal care during incubation, and (ii) one and two MHC-IIß DAB2 supertypes in the social father decrease and increase, respectively, fledging success, which may affect the paternal care after hatching. Furthermore, fledging success increased when both parents did not carry MHC-IIß DAB1 supertype 2, which could suggest conditional effects of this supertype. Although our study relied on a substantial dataset, we showed that the associations between MHC diversity and reproductive success remain scarce and of complex interpretation in the barn owl. Moreover, our results highlighted the need to incorporate more than one proxy of reproductive success and several MHC classes to capture more complex associations.

The genomic architecture of continuous plumage colour variation in the European barn owl (Tyto alba).

The maintenance of colour variation in wild populations has long fascinated evolutionary biologists, although most studies have focused on discrete traits exhibiting rather simple inheritance patterns and genetic architectures. However, the study of continuous colour traits and their potentially oligo- or polygenic genetic bases remains rare in wild populations. We studied the genetics of the continuously varying white-to-rufous plumage coloration of the European barn owl (Tyto alba) using a genome-wide association approach on the whole-genome data of 75 individuals. We confirmed a mutation at the melanocortin-1-receptor gene (MC1R) is involved in the coloration and identified two new regions, located in super-scaffolds 9 and 42. The combination of the three regions explains most of the colour variation (80.37%, 95% credible interval 58.45-100%). One discovered region, located in the sex chromosome, differs between the most extreme colorations in owls sharing a specific MC1R genotype. This region may play a role in the colour sex dimorphism of this species, possibly in interaction with the autosomal MC1R. We thus provide insights into the genetic architecture of continuous colour variation, pointing to an oligogenic basis with potential epistatic effects among loci that should aid future studies understanding how continuous colour variation is maintained in nature.

Binocular field configuration in owls: the role of foraging ecology.

The binocular field of vision differs widely in birds depending on ecological traits such as foraging. Owls (Strigiformes) have been considered to have a unique binocular field, but whether it is related to foraging has remained unknown. While taking into account allometry and phylogeny, we hypothesized that both daily activity cycle and diet determine the size and shape of the binocular field in owls. Here, we compared the binocular field configuration of 23 species of owls. While we found no effect of allometry and phylogeny, ecological traits strongly influence the binocular field shape and size. Binocular field shape of owls significantly differed from that of diurnal raptors. Among owls, binocular field shape was relatively conserved, but binocular field size differed among species depending on ecological traits, with larger binocular fields in species living in dense habitat and foraging on invertebrates. Our results suggest that (i) binocular field shape is associated with the time of foraging in the daily cycle (owls versus diurnal raptors) and (ii) that binocular field size differs between closely related owl species even though the general shape is conserved, possibly because the field of view is partially restricted by feathers, in a trade-off with auditory localization.

Influence of prey availability on habitat selection during the non-breeding period in a resident bird of prey.

BACKGROUND: For resident birds of prey in the temperate zone, the cold non-breeding period can have strong impacts on survival and reproduction with implications for population dynamics. Therefore, the non-breeding period should receive the same attention as other parts of the annual life cycle. Birds of prey in intensively managed agricultural areas are repeatedly confronted with unpredictable, rapid changes in their habitat due to agricultural practices such as mowing, harvesting, and ploughing. Such a dynamic landscape likely affects prey distribution and availability and may even result in changes in habitat selection of the predator throughout the annual cycle. METHODS: In the present study, we (1) quantified barn owl prey availability in different habitats across the annual cycle, (2) quantified the size and location of barn owl breeding and non-breeding home ranges using GPS-data, (3) assessed habitat selection in relation to prey availability during the non-breeding period, and (4) discussed differences in habitat selection during the non-breeding period to habitat selection during the breeding period. RESULTS: The patchier prey distribution during the non-breeding period compared to the breeding period led to habitat selection towards grassland during the non-breeding period. The size of barn owl home ranges during breeding and non-breeding were similar, but there was a small shift in home range location which was more pronounced in females than males. The changes in prey availability led to a mainly grassland-oriented habitat selection during the non-breeding period. Further, our results showed the importance of biodiversity promotion areas and undisturbed field margins within the intensively managed agricultural landscape. CONCLUSIONS: We showed that different prey availability in habitat categories can lead to changes in habitat preference between the breeding and the non-breeding period. Given these results we show how important it is to maintain and enhance structural diversity in intensive agricultural landscapes, to effectively protect birds of prey specialised on small mammals.

Prospecting movements link phenotypic traits to female annual potential fitness in a nocturnal predator.

Recent biologging technology reveals hidden life and breeding strategies of nocturnal animals. Combining animal movement patterns with individual characteristics and landscape features can uncover meaningful behaviours that directly influence fitness. Consequently, defining the proximate mechanisms and adaptive value of the identified behaviours is of paramount importance. Breeding female barn owls (Tyto alba), a colour-polymorphic species, recurrently visit other nest boxes at night. We described and quantified this behaviour for the first time, linking it with possible drivers, and individual fitness. We GPS-equipped 178 female barn owls and 122 male partners from 2016 to 2020 in western Switzerland during the chick rearing phase. We observed that 111 (65%) of the tracked breeding females were (re)visiting nest boxes while still carrying out their first brood. We modelled their prospecting parameters as a function of brood-, individual- and partner-related variables and found that female feather eumelanism predicted the emergence of prospecting behaviour (less melanic females are usually prospecting). More importantly we found that increasing male parental investment (e.g., feeding rate) increased female prospecting efforts. Ultimately, females would (re)visit a nest more often if they had used it in the past and were more likely to lay a second clutch afterwards, consequently having higher annual fecundity than non-prospecting females. Despite these apparent immediate benefits, they did not fledge more chicks. Through biologging and long-term field monitoring, we highlight how phenotypic traits (melanism and parental investment) can be related to movement patterns and the annual potential reproductive output (fecundity) of female barn owls.

Movement predictability of individual barn owls facilitates estimation of home range size and survival.

BACKGROUND: There is growing attention to individuality in movement, its causes and consequences. Similarly to other well-established personality traits (e.g., boldness or sociability), conspecifics also differ repeatedly in their spatial behaviors, forming behavioral types ("spatial-BTs"). These spatial-BTs are typically described as the difference in the mean-level among individuals, and the intra-individual variation (IIV, i.e., predictability) is only rarely considered. Furthermore, the factors determining predictability or its ecological consequences for broader space-use patterns are largely unknown, in part because predictability was mostly tested in captivity (e.g., with repeated boldness assays). Here we test if (i) individuals differ in their movement and specifically in their predictability. We then investigate (ii) the consequences of this variation for home-range size and survival estimates, and (iii) the factors that affect individual predictability. METHODS: We tracked 92 barn owls (Tyto alba) with an ATLAS system and monitored their survival. From these high-resolution (every few seconds) and extensive trajectories (115.2 ± 112.1 nights; X̅ ± SD) we calculated movement and space-use indices (e.g., max-displacement and home-range size, respectively). We then used double-hierarchical and generalized linear mix-models to assess spatial-BTs, individual predictability in nightly max-displacement, and its consistency across time. Finally, we explored if predictability levels were associated with home-range size and survival, as well as the seasonal, geographical, and demographic factors affecting it (e.g., age, sex, and owls' density). RESULTS: Our dataset (with 74 individuals after filtering) revealed clear patterns of individualism in owls' movement. Individuals differed consistently both in their mean movement (e.g., max-displacement) and their IIV around it (i.e., predictability). More predictable individuals had smaller home-ranges and lower survival rates, on top and beyond the expected effects of their spatial-BT (max-displacement), sex, age and ecological environments. Juveniles were less predictable than adults, but the sexes did not differ in their predictability. CONCLUSION: These results demonstrate that individual predictability may act as an overlooked axis of spatial-BT with potential implications for relevant ecological processes at the population level and individual fitness. Considering how individuals differ in their IIV of movement beyond the mean-effect can facilitate understanding the intraspecific diversity, predicting their responses to changing ecological conditions and their population management.

Genomic basis of insularity and ecological divergence in barn owls (Tyto alba) of the Canary Islands.

Islands, and the particular organisms that populate them, have long fascinated biologists. Due to their isolation, islands offer unique opportunities to study the effect of neutral and adaptive mechanisms in determining genomic and phenotypical divergence. In the Canary Islands, an archipelago rich in endemics, the barn owl (Tyto alba), present in all the islands, is thought to have diverged into a subspecies (T. a. gracilirostris) on the eastern ones, Fuerteventura and Lanzarote. Taking advantage of 40 whole-genomes and modern population genomics tools, we provide the first look at the origin and genetic makeup of barn owls of this archipelago. We show that the Canaries hold diverse, long-standing and monophyletic populations with a neat distinction of gene pools from the different islands. Using a new method, less sensitive to structure than classical FST, to detect regions involved in local adaptation to insular environments, we identified a haplotype-like region likely under selection in all Canaries individuals and genes in this region suggest morphological adaptations to insularity. In the eastern islands, where the subspecies is present, genomic traces of selection pinpoint signs of adapted body proportions and blood pressure, consistent with the smaller size of this population living in a hot arid climate. In turn, genomic regions under selection in the western barn owls from Tenerife showed an enrichment in genes linked to hypoxia, a potential response to inhabiting a small island with a marked altitudinal gradient. Our results illustrate the interplay of neutral and adaptive forces in shaping divergence and early onset speciation.

The role of wingbeat frequency and amplitude in flight power.

Body-mounted accelerometers provide a new prospect for estimating power use in flying birds, as the signal varies with the two major kinematic determinants of aerodynamic power: wingbeat frequency and amplitude. Yet wingbeat frequency is sometimes used as a proxy for power output in isolation. There is, therefore, a need to understand which kinematic parameter birds vary and whether this is predicted by flight mode (e.g. accelerating, ascending/descending flight), speed or morphology. We investigate this using high-frequency acceleration data from (i) 14 species flying in the wild, (ii) two species flying in controlled conditions in a wind tunnel and (iii) a review of experimental and field studies. While wingbeat frequency and amplitude were positively correlated, R2 values were generally low, supporting the idea that parameters can vary independently. Indeed, birds were more likely to modulate wingbeat amplitude for more energy-demanding flight modes, including climbing and take-off. Nonetheless, the striking variability, even within species and flight types, highlights the complexity of describing the kinematic relationships, which appear sensitive to both the biological and physical context. Notwithstanding this, acceleration metrics that incorporate both kinematic parameters should be more robust proxies for power than wingbeat frequency alone.

Density-dependent selection and the maintenance of colour polymorphism in barn owls.

The capacity of natural selection to generate adaptive changes is (according to the fundamental theorem of natural selection) proportional to the additive genetic variance in fitness. In spite of its importance for development of new adaptations to a changing environment, processes affecting the magnitude of the genetic variance in fitness-related traits are poorly understood. Here, we show that the red-white colour polymorphism in female barn owls is subject to density-dependent selection at the phenotypic and genotypic level. The diallelic melanocortin-1 receptor gene explained a large amount of the phenotypic variance in reddish coloration in the females ([Formula: see text]). Red individuals (RR genotype) were selected for at low densities, while white individuals (WW genotype) were favoured at high densities and were less sensitive to changes in density. We show that this density-dependent selection favours white individuals and predicts fixation of the white allele in this population at longer time scales without immigration or other selective forces. Still, fluctuating population density will cause selection to fluctuate and periodically favour red individuals. These results suggest how balancing selection caused by fluctuations in population density can be a general mechanism affecting the level of additive genetic variance in natural populations.

Home range size and habitat quality affect breeding success but not parental investment in barn owl males.

Life-history theory predicts that parents should balance their limited resources to maximize lifetime fitness, limiting their investment in current reproduction when the fitness value of current progeny is lower than that gained by producing offspring in the future. Here, we examined whether male barn owls (Tyto alba) breeding in low-quality habitats increased their parental effort to successfully complete offspring rearing or limited their investment by paying a fitness cost while saving energy for the future. We equipped 128 males with GPS devices between 2016 and 2020 to collect information on home range size, habitat composition, food provisioning rate to the brood and nightly distances covered. We also recorded nestlings' growth and survival, as well as males' body mass variation and future reproductive success. Males living in lower-quality habitats exploited bigger home ranges compared to individuals whose nests were settled in prey-rich habitats. They fed their brood less frequently, while covering longer nightly distance, resulting in a slower growth of late-hatched nestlings and ultimately in a lower fledging success. As males did not differ in body mass variation or future reproductive success our findings suggest that males hunting in home ranges with less prey-rich structures do not jeopardize future reproduction by investing disproportionately larger resources to compensate for their current low home range quality.

Unexpected post-glacial colonisation route explains the white colour of barn owls (Tyto alba) from the British Isles.

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. Yet, our analysis of known candidate genes involved in coloration 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 hitherto 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 probably 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.

Landscape and Climatic Variations Shaped Secondary Contacts amid Barn Owls of the Western Palearctic.

The combined actions of climatic variations and landscape barriers shape the history of natural populations. When organisms follow their shifting niches, obstacles in the landscape can lead to the splitting of populations, on which evolution will then act independently. When two such populations are reunited, secondary contact occurs in a broad range of admixture patterns, from narrow hybrid zones to the complete dissolution of lineages. A previous study suggested that barn owls colonized the Western Palearctic after the last glaciation in a ring-like fashion around the Mediterranean Sea, and conjectured an admixture zone in the Balkans. Here, we take advantage of whole-genome sequences of 94 individuals across the Western Palearctic to reveal the complex history of the species in the region using observational and modeling approaches. Even though our results confirm that two distinct lineages colonized the region, one in Europe and one in the Levant, they suggest that it predates the last glaciation and identify a secondary contact zone between the two in Anatolia. We also show that barn owls recolonized Europe after the glaciation from two distinct glacial refugia: a previously identified western one in Iberia and a new eastern one in Italy. Both glacial lineages now communicate via eastern Europe, in a wide and permeable contact zone. This complex history of populations enlightens the taxonomy of Tyto alba in the region, highlights the key role played by mountain ranges and large water bodies as barriers and illustrates the power of population genomics in uncovering intricate demographic patterns.

Genomic consequences of colonisation, migration and genetic drift in barn owl insular populations of the eastern Mediterranean.

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.

Exogenous corticosterone and melanin-based coloration explain variation in juvenile dispersal behaviour in the barn owl (Tyto alba).

Natal dispersal affects many processes such as population dynamics. So far, most studies have examined the intrinsic and extrinsic factors that determine the distance between the place of birth and of first breeding. In contrast, few researchers followed the first steps of dispersal soon after fledging. To study this gap, we radio-tracked 95 barn owl nestlings (Tyto alba) to locate their diurnal roost sites from the fledging stage until December. This was used to test whether the age of nest departure, post-fledging movements and dispersal distance were related to melanin-based coloration, which is correlated to fitness-related traits, as well as to corticosterone, a hormone that mediates a number of life history trade-offs and the physiological and behavioural responses to stressful situations. We found that the artificial administration of corticosterone delayed the age when juveniles left their parental home-range in females but not in males. During the first few months after fledging, longer dispersal distances were reached by females compared to males, by individuals marked with larger black feather spots compared to individuals with smaller spots, by larger individuals and by those experimentally treated with corticosterone. We conclude that the onset and magnitude of dispersal is sensitive to the stress hormone corticosterone, melanin-based coloration and body size.

Behaviour-specific habitat selection patterns of breeding barn owls.

BACKGROUND: The intensification of agricultural practices over the twentieth century led to a cascade of detrimental effects on ecosystems. In Europe, agri-environment schemes (AES) have since been adopted to counter the decrease in farmland biodiversity, with the promotion of extensive habitats such as wildflower strips and extensive meadows. Despite having beneficial effects documented for multiple taxa, their profitability for top farmland predators, like raptors, is still debated. Such species with high movement capabilities have large home ranges with fluctuation in habitat use depending on specific needs. METHODS: Using GPS devices, we recorded positions for 134 barn owls (Tyto alba) breeding in Swiss farmland and distinguished three main behavioural modes with the Expectation-Maximization binary Clustering (EMbC) method: perching, hunting and commuting. We described barn owl habitat use at different levels during the breeding season by combining step and path selection functions. In particular, we examined the association between behavioural modes and habitat type, with special consideration for AES habitat structures. RESULTS: Despite a preference for the most common habitats at the home range level, behaviour-specific analyses revealed more specific habitat use depending on the behavioural mode. During the day, owls roosted almost exclusively in buildings, while pastures, meadows and forest edges were preferred as nocturnal perching sites. For hunting, barn owls preferentially used AES habitat structures though without neglecting more intensively exploited areas. For commuting, open habitats were preferred over wooded areas. CONCLUSIONS: The behaviour-specific approach used here provides a comprehensive breakdown of barn owl habitat selection during the reproductive season and highlights its importance to understand complex animal habitat preferences. Our results highlight the importance of AES in restoring and maintaining functional trophic chains in farmland.

Non-Vocal Behaviors Are More Frequent During the Decisive Negotiation Phases in Barn Owl Siblings.

Animals produce vibrations or noises by means of body movements, which can play a role in communication. These behaviors enhance signal transmission or receiver attention and could be specifically used during turn-taking phases of a reciprocal exchange of signals. In the barn owl Tyto alba, nestlings vocalize one after the other to negotiate which individual will have priority access to the impending prey item to be delivered by the parents. Owlets adjust their vocalization to their own hunger level and to their siblings' vocalization, withdrawing from the contest in front of highly vocal, and hence hungry, motivated nestmates. As sibling negotiation is a multicomponent display, we examined whether body movements could also be part of the negotiation process. To this end, we analyzed whether the vocalizations of one nestling affected its nestmate's movements in three separate experiments: in natural nests, in the lab, and using a playback procedure. Nestling barn owls move in a variety of ways, such as repeated tapping of the floor with a foot, scratching the floor with claws, or flapping wings. Body movements were more frequent during the turn-taking phases of vocal interactions, when siblings emitted longer calls and at a greater rate. Once an individual monopolized vocal activity, siblings became less vocal and less active. Moreover, owlets produced more noisy body movements during the phases of vocal interactions which are crucial to prevail in negotiation. Non-vocal physical activities might reinforce vocal signals during sibling to sibling (sib-sib) interactions, or reflect owlets' arousal, in the critical period during which they vocally settle which individual will dominate the competition.

Glucocorticoid levels are linked to lifetime reproductive success and survival of adult barn owls.

Glucocorticoid hormones, such as corticosterone, are crucial in regulating daily life metabolism and energy expenditure, as well as promoting short-term physiological and behavioural responses to unpredictable environmental challenges. Therefore, glucocorticoids are considered to mediate trade-offs between survival and reproduction. Relatively little is known about how selection has shaped glucocorticoid levels. We used 15 years of capture-recapture and dead recovery data combined with 13 years of corticosterone and breeding success data taken on breeding barn owls (Tyto alba) to investigate such trade-offs. We found that survival was positively correlated with stress-induced corticosterone levels in both sexes, whereas annual and lifetime reproductive success (i.e. the sum of young successfully fledged during the entire reproductive career) was positively correlated with both baseline and stress-induced corticosterone levels in females only. Our results suggest that, in the barn owl, the stress-induced corticosterone response is a good proxy for adult survival and lifetime reproductive success. However, selection pressure appears to act differently on corticosterone levels of males and females.

C-terminal tails mimicking bioactive intermediates cause different plasma degradation patterns and kinetics in neuropeptides γ-MSH, α-MSH, and neurotensin.

Peptides are attractive drugs because of their specificity and minimal off-target effects. Short half-lives are within their major drawbacks, limiting actual use in clinics. The golden standard in therapeutic peptide development implies identification of a minimal core sequence, then modified to increase stability through several strategies, including the introduction of nonnatural amino acids, cyclization, and lipidation. Here, we investigated plasma degradations of hormone sequences all composed of a minimal active core peptide and a C-terminal extension. We first investigated pro-opimelanocortin (POMC) γ2/γ3-MSH hormone behavior and extended our analysis to POMC-derived α-melanocyte stimulating hormone/adrenocorticotropic hormone signaling neuropeptides and neurotensin. We demonstrated that in all the three cases analyzed in this study, few additional residues mimicking the natural sequence alter both peptide stability and the mechanism(s) of degradation of the minimal conserved functional pattern. Our results suggest that the impact of extensions on the bioactivity of a peptide drug has to be carefully evaluated throughout the optimization process.