Similar patterns of local barn owl adaptation in the Middle East and Europe with respect to melanic coloration

The maintenance of phenotypic variation is a central question in evolutionary biology. A commonly suggested mechanism is that of local adaptation, whereby different phenotypes are adapted to alternative environmental conditions. A recent study in the European barn owl (Tyto alba) has shown that natural selection maintains a strong clinal variation in reddish pheomelanin-based coloration. Studies in the region where phenotypic variation in this owl is the highest in Europe have further demonstrated that dark-reddish and pale-reddish owls exploit open and wooded habitats, predate voles and wood mice, and are long-tailed and short-tailed, respectively. However, it remains unclear as to whether these traits evolved as a consequence of allopatric evolution of dark colour in northern Europe and white colour in southern Europe, during which owls could have also evolved different morphologies and foraging behaviour. This scenario implies that covariation between coloration and foraging behaviour could be a specificity of the European continent, which is not found in other worldwide-distributed populations. To investigate this issue we studied a barn owl population in the Middle East. Our results show that, as in Central Europe, dark-reddish female owls breed more often in the open landscape than their pale-reddish female conspecifics, their offspring are fed with more voles than Muridae, and they are longer-winged and longer-tailed. These findings indicate that in the barn owl the association in females between pheomelanin-based coloration and foraging behaviour and morphology is not restricted to the European continent but may well evolve in sympatry in many barn owl populations worldwide.

Selection on a eumelanic ornament is stronger in the tropics than in temperate zones in the worldwide-distributed barn owl.

Spatial variation in the pattern of natural selection can promote local adaptation and genetic differentiation between populations. Because heritable melanin-based ornaments can signal resistance to environmentally mediated elevation in glucocorticoids, to oxidative stress and parasites, populations may vary in the mean degree of melanic coloration if selection on these phenotypic aspects varies geographically. Within a population of Swiss barn owls (Tyto alba), the size of eumelanic spots is positively associated with survival, immunity and resistance to stress, but it is yet unknown whether Tyto species that face stressful environments evolved towards a darker eumelanic plumage. Because selection regimes vary along environmental gradients, we examined whether melanin-based traits vary clinally and are expressed to a larger extent in the tropics where parasites are more abundant than in temperate zones. To this end, we considered 39 barn owl species distributed worldwide. Barn owl species living in the tropics displayed larger eumelanic spots than those found in temperate zones. This was, however, verified in the northern hemisphere only. Parasites being particularly abundant in the tropics, they may promote the evolution of darker eumelanic ornaments.

A record of communal nesting in the barn owl (Tyto alba)

We report a unique case of two female Barn Owls laying eggs and incubating together in a single nest cup in a communal nest. A trio of two females and one male bred in an abandoned water tower in 2013 in Israel. Both females incubated/brooded together in the communal nest, and all three individuals brought food to the communal family. The two females laid 20 eggs, of which 19 hatched and 16 fledged.

Partitioning of genetic (Rapd) variability among sexes and populations of the Barn Owl (Tyto alba) in Europe

The white Barn Owl subspecies (Tyto alba alba) is found in southern Europe and the reddish-brown subspecies (T a. guttata) in northern and eastern Europe. In central Europe, the two subspecies interbreed producing a large range of phenotypic variants. Because of the different ratios of the subspecies in different geographic regions, we predict that genetic variation should be greater in Switzerland than in Hungary. We tested this hypothesis by measuring genetic variation with the RAPD method. As predicted, the genetic differentiation within a Swiss population of Barn Owls was significantly greater than the variation within a Hungarian population. This suggests that gene flow is greater in central Europe than at the eastern limit of the Barn Owl distribution in Hungary. In both countries genetic variation was more pronounced in females than in males. As in other birds, this is probably because female Barn Owls are less philopatric than males. The number of migrants between Hungary and Switzerland is ca. 1 individual per generation; if calculated separately for the sexes, then 0.525 for males and ca. I for females (Nm values). The difference in the number of migrants between genders again is likely a consequence of higher male philopatry. The sexual differentiation is greater in the Swiss population than in the Hungarian and the genetic substructuring of the populations of the species is substantial. The reason for the considerable population substructuring could be the nonmigratory behavior and socially monogamous pairing of the species, as well as the geographical barriers (Alps) between the populations examined.

The occurrence of reptiles in Barn Owl diet in Europe

Capsule We present a review of the propensity to eat reptiles in the Barn Owl Tyto alba in Europe. Based on the analysis of 591 published studies reporting 3.07 million prey items identified in pellets, only 2402 reptiles (0.08%) were found. Reptiles were most often captured in southern parts of the European continent and on islands. A large proportion of the 1304 identified reptiles to the species level were nocturnal Gekkonidae (77.1%).

Covariation between plumage colour polymorphism and diet in the Barn Owl Tyto alba

Several hypotheses might explain the evolution and maintenance of colour morphs within animal populations. The 'alternative foraging strategy' hypothesis states that alternative colour morphs exploit different ecological niches. This hypothesis predicts that morphs differ in diet, either because foraging success on alternative prey species is morph-dependent or because differently coloured individuals exploit alternative habitats. I examined this prediction in the Barn Owl Tyto alba, a bird that varies in plumage coloration continuously from dark reddish-brown to white. On the European continent, Owls are light-coloured (subspecies T. a. alba) in the south and reddish-brown (T. a. guttata) in the north; in central Europe the two subspecies interbreed, generating many colour variants. If plumage coloration indicates alternative foraging strategies, in sympatry dark- and light-coloured owls should consume prey species that are typical of the diets of T. a. guttata and T. a. alba in allopatry, respectively. In line with this prediction, both in allopatry and in sympatry in Switzerland T. a. guttata fed primarily upon Common Voles Microtus arvalis and T. a. alba upon Wood Mice Apodemus spp. Statistical analyses suggest that morph-dependent diet did not arise from a non-random habitat distribution of owls with respect to plumage coloration. This suggests that foraging success upon alternative prey is morph-dependent.

Sibling rivalry and vocal negotiation in the barn owl Tyto alba

Chez les animaux, les jeunes dépendant des parents durant leur développement sont en compétition pour obtenir la nourriture, qu'ils quémandent par des cris et postures ostentatoires et se disputent physiquement. Les frères et soeurs n'ont pas la même compétitivité, en particulier s'ils diffèrent en âge, et leur niveau de faim fluctue dans le temps. Comme dans tout type de compétition, chacun doit ajuster son investissement aux rivaux, c'est à dire aux besoins et comportements de ses frères et soeurs. Dans le contexte de la famille, selon la théorie de sélection de parentèle, les jeunes bénéficient de leur survie mutuelle et donc de la propagation de la part de gènes qu'ils ont en commun. L'hypothèse de la « négociation frères-soeurs » prédit que, sous certaines conditions, les jeunes négocient entre eux la nourriture, ce qui réduit les coûts de compétition et permet de favoriser les frères et soeurs les plus affamés. La littérature actuelle se focalise sur les signaux de quémande entre enfants et parents et les interactions compétitives frères-soeurs sont étudiées principalement au sein de paires, alors que les nichées ou portées en comprennent souvent de nombreux. Cette thèse vise à mieux comprendre comment et jusqu'à quel point plusieurs jeunes ajustent mutuellement leurs signaux de besoin. C'est une question importante, étant donné que cela influence la répartition de nourriture entre eux, donc la résolution du conflit qui les oppose et à terme leur valeur évolutive. Le modèle d'étude est la chouette effraie (Tyto alba), chez laquelle jusqu'à neufs poussins émettent des milliers de cris chacun par nuit. Ils négocieraient entre eux la prochaine proie indivisible rapportée au nid avant que les parents ne reviennent : un poussin affamé crie plus qu'un autre moins affamé, ce qui dissuade ce dernier de crier en retour et par la suite de quémander la nourriture aux parents. L'investissement optimal correspondrait donc à écarter son frère en permanence vu que l'arrivée des parents est imprévisible, mais à moindre coût. Dans un premier axe, nous avons exploré au sein de dyades les mécanismes acoustiques permettant aux poussins de doser leur effort vocal durant les heures de compétition où ils sont laissés seuls au nid. Nous avons trouvé que les poussins évitent de crier simultanément, ce qui optimiserait la discrimination du nombre et de la durée de leurs cris, lesquels reflètent de façon honnête leur niveau de faim et donc leur motivation. L'alternance des cris paraît particulièrement adaptée au fait que les poussins se fient à des variations temporelles subtiles dans le rythme et la durée de leurs vocalisations pour prendre la parole. En particulier, allonger ses cris tout en criant moins dissuade efficacement le rival de répondre, ce qui permet de monopoliser la parole dans de longs « monologues ». Ces règles seraient universelles puisqu'elles ne dépendent pas de la séniorité, de la faim, ni de la parenté et les poussins répondent à un playback de façon similaire à un vrai frère. Tous ces résultats apportent la première preuve expérimentale que les juvéniles communiquent de façon honnête sur leurs besoins, ajustent activement le rythme de leurs cris et utilisent des composantes multiples de leurs vocalisations d'une façon qui réduit le coût de la compétition. De plus, il s'agit de la première démonstration que des règles de conversation régissent de longs échanges vocaux chez les animaux de façon comparable aux règles basiques observées chez l'Homme. Dans un second axe, nous avons exploré les stratégies comportementales que les poussins adoptent pour rivaliser avec plusieurs frères et soeurs, par le biais d'expériences de playback. Nous avons trouvé que les poussins mémorisent des asymétries de compétitivité entre deux individus qui dialoguent et répondent plus agressivement au moins compétitif une fois qu'ils sont confrontés à chacun isolément. Dans la même ligne, quand ils entendent un nombre variable d'individus criant à un taux variable, les poussins investissent le plus contre des rivaux moins nombreux et moins motivés. En accord avec les prédictions des modèles théoriques, les poussins de chouette effraie escaladent donc les conflits pour lesquels leur chance de gagner contrebalance le plus l'énergie dépensée. Nous révélons ainsi que 1) les jeunes frères et soeurs 'espionnent' les interactions de leurs rivaux pour évaluer leur compétitivité relative, ce qui est sans doute moins coûteux qu'une confrontation directe avec chacun, et 2) dosent leur investissement vocal en fonction du nombre de rivaux actuellement en compétition et de leur motivation de façon concomitante. Ces résultats montrent que les interactions entre frères et soeurs au nid reposent sur des mécanismes similaires à ceux observés, mais encore de façon anecdotique, chez les adultes non apparentés qui se disputent les territoires et partenaires sexuels. Cette thèse souligne donc combien il est crucial de considérer dorénavant la famille comme un réseau de communication à part entière pour mieux comprendre comment les jeunes résolvent les conflits autour du partage des ressources parentales. Plus généralement, elle révèle l'importance de la dynamique temporelle des vocalisations dans les conflits et la communication des animaux. A la lumière de nos résultats, la chouette effraie apparaît comme un modèle clé pour de futures recherches sur la résolution des conflits et la communication acoustique. - In species with parental care, offspring contest priority access to food by begging through conspicuous postures and vocalisations and by physically jockeying. Siblings differ in their competitiveness, especially in the case of age and size hierarchies, and their hunger level fluctuates in time. As in competition in general, each individual should adjust its investment to opponents that is to say to its siblings' needs and behaviours. In the particular context of family, according to kin selection theory, siblings derive extra fitness benefits from their mutual survival and hence the spreading of the genes they share. The "sibling negotiation" predicts that, under certain conditions, young would negotiate among them priority access to food, which reduces competition costs and enables promoting the most hungry siblings. To date, the literature focuses on signals of need between parents and offspring and competitive interactions (in particular among siblings) are mostly studied within pairwise interactions, yet they commonly involve more numerous rivals. This PhD aims at better understanding how and the extent to which several young siblings compete through signalling. This is important since this influences how food is allocated among them, thus the outcome of sibling rivalry and ultimately their fitness. I use the barn owl (Tyto alba) as a model, in which the one to nine nestlings emit a simple noisy call thousands of times per night. Thereby, they would negotiate among them priority access to the indivisible food next delivered prior to parents' feeding visits. A hungry nestling emits more calls than a less hungry sibling, which deters it to call in return and ultimately beg food at parents. The optimal investment thus corresponds to constantly deterring the rival to compete, given that parents' arrival is unpredictable, but at the lowest costs. In the first axis of my thesis, we explored within dyads the acoustic mechanisms by which owlets dose vocal effort when competing during the hours they are left alone. We found that owlets avoid overlapping each other's calls. This would enhance the discrimination of both call number and duration, which honestly reflect individuals' hunger level and hence motivation to compete. Such antiphony seems best adapted to the fact that siblings actually use subtle temporal variations in the rhythm and duration of their calls to take or give their turn. Owlets alternate monologs, in which lengthening calls efficiently deters the rival to respond while reducing call number. Such rules depend neither on seniority, hunger level nor kinship since nestlings responded similarly to a live sibling and an unrelated playback individual. Taken together, these findings provide the first experimental proof that dependent young honestly communicate about their need, actively adjust the timing of their calls and use multicomponent signals in a way that reduces vocal costs. Moreover, this is the first demonstration of conversational rules underlying animal long-lasting vocal exchanges comparable to the basic turn-taking signals observed in humans. In the second axis, we focused on the behavioural strategies owlets adopt to compete with more than one sibling, using playback experiments. We found that singleton bystanders memorised competitive asymmetries between two playback individuals dialoguing and responded more aggressively to the submissive one once they later faced each of both alone. Moreover, when hearing a varying number of nestlings calling at varying rates, owlets vocally invested the most towards fewer and less motivated rivals. In line with predictions from models on conflict settlement, barn owls thus escalate contests in which their chance of winning best counterbalances the energy spent. These results reveal that young socially eavesdrop on their siblings' interactions to assess their relative competitiveness at likely lower costs than direct confrontation, and dose vocal effort relative to both their number and motivation. This shows that young siblings' interactions imply mechanisms similar to those observed, yet still anecdotally, in unrelated adults that contest mates and territories. This PhD therefore highlights how crucial it is to further consider family as a communication network to better understand how siblings resolve conflicts over the share of parental resources. More generally, it provides important insights into the role of the temporal dynamics of signalling during animal contests and communication. In the light of our findings, the barn owl emerges as a key model for future research on conflict resolution and acoustic communication in animals.

Age-specific fitness components and their temporal variation in the barn owl.

Theory predicts that temporal variability plays an important role in the evolution of life histories, but empirical studies evaluating this prediction are rare. In constant environments, fitness can be measured by the population growth rate lambda, and the sensitivity of lambda to changes in fitness components estimates selection on these traits. In variable environments, fitness is measured by the stochastic growth rate lambda(S), and stochastic sensitivities estimate selection pressure. Here we examine age-specific schedules for reproduction and survival in a barn owl population (Tyto alba). We estimated how temporal variability affected fitness and selection, accounting for sampling variance. Despite large sample sizes of old individuals, we found no strong evidence for senescence. The most variable fitness components were associated with reproduction. Survival was less variable. Stochastic simulations showed that the observed variation decreased fitness by about 30%, but the sensitivities of lambda and lambda(S) to changes in all fitness components were almost equal, suggesting that temporal variation had negligible effects on selection. We obtained these results despite high observed variability in the fitness components and relatively short generation time of the study organism, a situation in which temporal variability should be particularly important for natural selection and early senescence is expected.

Demographic effects of extreme winter weather in the barn owl.

Extreme weather events can lead to immediate catastrophic mortality. Due to their rare occurrence, however, the long-term impacts of such events for ecological processes are unclear. We examined the effect of extreme winters on barn owl (Tyto alba) survival and reproduction in Switzerland over a 68-year period (approximately 20 generations). This long-term data set allowed us to compare events that occurred only once in several decades to more frequent events. Winter harshness explained 17 and 49% of the variance in juvenile and adult survival, respectively, and the two harshest winters were associated with major population crashes caused by simultaneous low juvenile and adult survival. These two winters increased the correlation between juvenile and adult survival from 0.63 to 0.69. Overall, survival decreased non-linearly with increasing winter harshness in adults, and linearly in juveniles. In contrast, brood size was not related to the harshness of the preceding winter. Our results thus reveal complex interactions between climate and demography. The relationship between weather and survival observed during regular years is likely to underestimate the importance of climate variation for population dynamics.

Individual vocal signatures in barn owl nestlings: does individual recognition have an adaptive role in sibling vocal competition?

To compete over limited parental resources, young animals communicate with their parents and siblings by producing honest vocal signals of need. Components of begging calls that are sensitive to food deprivation may honestly signal need, whereas other components may be associated with individual-specific attributes that do not change with time such as identity, sex, absolute age and hierarchy. In a sib-sib communication system where barn owl (Tyto alba) nestlings vocally negotiate priority access to food resources, we show that calls have individual signatures that are used by nestlings to recognize which siblings are motivated to compete, even if most vocalization features vary with hunger level. Nestlings were more identifiable when food-deprived than food-satiated, suggesting that vocal identity is emphasized when the benefit of winning a vocal contest is higher. In broods where siblings interact iteratively, we speculate that individual-specific signature permits siblings to verify that the most vocal individual in the absence of parents is the one that indeed perceived the food brought by parents. Individual recognition may also allow nestlings to associate identity with individual-specific characteristics such as position in the within-brood dominance hierarchy. Calls indeed revealed age hierarchy and to a lower extent sex and absolute age. Using a cross-fostering experimental design, we show that most acoustic features were related to the nest of origin (but not the nest of rearing), suggesting a genetic or an early developmental effect on the ontogeny of vocal signatures. To conclude, our study suggests that sibling competition has promoted the evolution of vocal behaviours that signal not only hunger level but also intrinsic individual characteristics such as identity, family, sex and age.

Pheomelanin-based colouration is correlated with indices of flying strategies in the barn owl

Resource polymorphism refers to individuals from the same population foraging in alternative habitats or on alternative food. Food specialization can be associated with adaptations such as colour polymorphism, with pale and dark colours conferring differential camouflage in different habitats. Pale and dark-reddish pheomelanic Barn Owls (Tyto alba) forage on different prey species in closed and open habitats, respectively. We show here that darker-reddish owls have heavier stomach content when found dead, and their 5th secondary wing feather is more deeply anchored inside the integument. These correlations suggest that their feathers bend less when flying, and that darker-reddish Barn Owls are able sustain more intense flying than their paler conspecifics.

Melanin-based colouration predicts natal dispersal in the barn owl, Tyto alba

Searching for a suitable breeding site is an important decision in the life of most animals. The decisions where to settle and how far to travel before doing so depend on many factors. Individual differences in dispersal distance could result from different strategies (e.g. specialists versus generalists), which might result in similar reproductive success in different habitats, or different competitive abilities to acquire a territory close to the natal site. The barn owl is polymorphic in melanic coloration, which is associated with many physiological and behavioural traits such as habitat choice, stress response and docility, raising the possibility that the coloration is also related to dispersal. We studied natal dispersal (from rearing site to site of first breeding attempt) and breeding dispersal (from one breeding site to the next) in barn owls using a long-term data set. Darker reddish individuals moved further than paler individuals during natal dispersal, but not during breeding dispersal. A cross-fostering experiment showed that the colour of the biological and foster parents had no influence on dispersal distance. The distance dispersed by parents and same-sex offspring was correlated, whereas natal and breeding dispersal were not repeatable within individuals, indicating that they are two different processes. Given that the distance travelled in natal dispersal appears to be heritable, the underlying genes might be coupled to those related to coloration. We discuss hypotheses to explain the potential adaptive function of the link between coloration and natal dispersal.

Pre-hatching maternal effects inhibit nestling humoral immune response in the tawny owl Strix aluco

Although evidence is accumulating that mothers can transfer antibodies to their offspring, little is known about the consequences of such a transfer to the offspring immune system. Because maternal antibodies are effective only during a short period of time after their transfer to offspring, one hypothesis is that maternal antibodies provides a transitory antigen-specific protection to offspring, thus lessening the need for offspring to mount their own humoral immune response towards these specific antigens. In birds, this scenario predicts that offspring immune response towards a specific antigen is inhibited to a larger extent in hatchlings than in older nestlings. We tested this hypothesis in tawny owls Strix aluco by cross-fostering clutches between nests and then challenging siblings with a vaccine either two times (at 4- and 11-d-old) or only one time at 11-d-old to compare the strength of the humoral response between nestlings born from mothers with naturally high and low levels of antibodies against this vaccine. Because maternal antibodies are expected to be effective only during a short period of time after hatching, we predict that maternal antibodies should inhibit the immune response of nestlings vaccinated from the fourth day after hatching more than in nestlings vaccinated only at a later age. As expected, the inhibitory effect of maternal antibodies was stronger in nestlings vaccinated soon after hatching than in siblings injected at a later age. Therefore, in wild avian populations pre-hatching maternal effects may confer offspring with a transitory immune protection in the first days following hatching.

Isolation and characterization of 21 microsatellite markers in the barn owl (Tyto alba).

We report 21 new polymorphic microsatellite markers in the European barn owl (Tyto alba). The polymorphism of the reported markers was evaluated in a population situated in western Switzerland and in another from Tenerife, Canary Islands. The number of alleles per locus varies between two and 31, and expected heterozygosity per population ranges from 0.16 to 0.95. All loci are in Hardy-Weinberg equilibrium and no linkage disequilibrium was detected. Two loci exhibit a null allele in the Tenerife population.

Effects of hatching asynchrony on sibling negotiation, begging, jostling for position and within-brood food allocation in the barn owl Tyto alba

When siblings differ markedly in their need for food, they may benefit from signalling to each other their willingness to contest the next indivisible food item delivered by the parents. This sib-sib communication system, referred to as 'sibling negotiation', may allow them to adjust optimally to investment in begging. Using barn owl (Two alba) broods. I assessed the role of within-brood age hierarchy on sibling negotiation, and in turn on jostling for position where parents predictably deliver food (i.e. nest-box entrance), begging and within-brood food allocation. More specifically, I examined three predictions derived from a game-theoretical model of sibling negotiation where a senior and a junior sibling compete for food resources (Roulin, 2002a, Johnstone and Roulin, 2003): (1) begging effort invested by the senior sibling should be less sensitive to the junior sibling's negotiation than vice versa; (2) the junior should invest less effort in sibling negotiation than its senior sibling but a similar amount of effort in begging; and (3) within-brood food allocation should be directly related to begging but only indirectly to sibling negotiation. Two-chick broods were created and vocalization in the absence (negotiation signals directed to siblings) and presence (begging signals directed to parents) of parents was recorded. In support of the first prediction, juniors begged at a low cadence after their senior sibling negotiated intensely, probably because negotiation reflects prospective investment in begging and hence willingness to compete. In contrast, the begging of senior siblings was not sensitive to their junior sibling's negotiation. In contrast to the second prediction, juniors negotiated and begged more intensely than their senior sibling apparently because they were hungrier rather than younger. In line with the third prediction, juniors monopolized food delivered by their parents when their senior sibling begged at a low level. The begging cadence of both the junior and senior sibling, the junior's negotiation cadence, the difference in age between the two nest-mates and jostling for position were not associated with the likelihood of monopolizing food. In conclusion, sibling negotiation appears to influence begging behaviour, which, in turn, affects within-brood food allocation. Juniors may negotiate to challenge their senior siblings, and thereby determine whether seniors are less hungry before deciding to beg for food. In contrast, seniors may negotiate to deter juniors from begging.