Cold winters have morph-specific effects on natal dispersal distance in a wild raptor

Dispersal is a key process with crucial implications in spatial distribution, density, and genetic structure of species' populations. Dispersal strategies can vary according to both individual and environmental features, but putative phenotype-by-environment interactions have rarely been accounted for. Melanin-based color polymorphism is a phenotypic trait associated with specific behavioral and physiological profiles and is, therefore, a good candidate trait to study dispersal tactics in different environments. Here, using a 40 years dataset of a population of color polymorphic tawny owls (Strix aluco), we investigated natal dispersal distance of recruiting gray and pheomelanic reddish-brown (hereafter brown) color morphs in relation to post-fledging winter temperature and individual characteristics. Because morphs are differently sensitive to cold winters, we predicted that morphs' natal dispersal distances vary according to winter conditions. Winter temperature did not affect the proportion of brown (or gray) among recruits. We found that dispersal distances correlate with winter temperature in an opposite manner in the two morphs. Although the gray morph undertakes larger movements in harsher conditions, likely because it copes better with winter severity, the brown morph disperses shorter distances when winters are harsher. We discuss this morph-specific natal dispersal pattern in the context of competition for territories between morphs and in terms of costs and benefits of these alternative strategies. Our results stress the importance of considering the interaction between phenotype and environment to fully disentangle dispersal movement patterns and provide further evidence that climate affects the behavior and local distribution of this species.In species displaying alternative colorations (morphs), climate may induce different responses according to the intensity of pigmentation. We show that brown, more pigmented, tawny owls tend to move away farthest from their place of birth in milder winters, whereas paler gray tawny owls move farthest in colder winters. The ongoing changes in winter severity will likely affect differently movement patterns of these two tawny owl color morphs, with important consequences on morph distribution and population dynamics

The role of ecology in the evolution of coloration in owls

Las aves muestran una extraordinaria variabilidad en sus patrones de color modelados por la selección natural y sexual para cumplir diferentes funciones como la comunicación, el camuflaje y/o de protección. Los factores ambientales que promueven dicha variación pueden ser muy diversos y actuar de forma diferente sobre distintos rasgos y niveles de organización. Por esta razón, para comprender de manera integral como la ecología influye en la evolución de tan excepcional diversidad de formas coloreadas, es necesario considerar aproximaciones holísticas que combinen múltiples niveles de estudio, incluyendo diferentes rasgos y diferentes especies que ocupen un amplio rango de condiciones ecológicas. En esta tesis doctoral, he utilizado una aproximación multidisciplinar en la que se combinan i) análisis eco-geográficos a escala mundial, ii) análisis comparativos para controlar por el posible efecto de un ancestro común, y iii) datos de campo de dos especies recogidos en una población, para evaluar la importancia relativa de una serie de factores ecológicos y evolutivos a la hora de determinar la variación de rasgos coloreados en los estrígidos. Más concretamente, he estudiado i) la variación geográfica a gran escala de la coloración con base melánica en relación a gradientes ambientales en el marco de reglas eco-geográficas clásicas, ii) la variabilidad interespecífica en el polimorfismo de color en relación a factores ecológicos clave, iii) la evolución de la variación interespecífica de la coloración del iris en relación al ritmo de actividad y iv) he analizado el potencial de la coloración del iris como indicador de la calidad en diferentes contextos de comunicación en dos especies de búhos. Los análisis eco-geográficos a escala global mostraron que los búhos presentan fenotipos más oscuros cerca del ecuador. En particular, las especies de búhos que viven en regiones con temperatura más altas y vegetación más densa son más oscuras, lo cual excluye un posible papel de la termorregulación a la hora promover la variación del plumaje a una escala global. Por otro lado, se observó que las especies de búhos que habitan en áreas con una cobertura arbórea mayor eran más eumelánicas, lo cual está de acuerdo con un potencial papel de la coloración basada en eumelanina en el camuflaje. Finalmente, la importancia de la coloración basada en feomelanina era mayor en especies que viven en zonas más cálidas y húmedas, sugiriendo en conjunto que distintas fuerzas selectivas podrían haber simultáneamente contribuido a modelar la variación global en el color del plumaje en este clado. En segundo lugar, se examinó en un contexto comparativo la importancia relativa de diferentes factores ecológicos a la hora de promover la evolución del polimorfismo de color en los búhos en el marco de tres escenarios evolutivos mutuamente no exclusivos: la hipótesis de la selección apostática, la hipótesis de la divergencia de nicho y la hipótesis de no selección. De acuerdo con la hipótesis de la divergencia de nicho, se encontró que las especies que viven bajo condiciones lumínicas variables, i.e. especies con hábitos crepusculares y diurnos, y aquellas que ocupan una mezcla de hábitats abiertos y cerrados, eran con más probabilidad polimórficas. Los análisis de coevolución mostraron que un cambio en el nicho lumínico podría ser un prerrequisito fundamental para la evolución del polimorfismo de color en los búhos. Además, el polimorfismo resultó más frecuente entre las especies que ocupan los niveles tróficos más bajos, lo cual podría venir explicado por una selección más fuerte para la cripsis en las especies depredadoras de pequeño tamaño. Los resultados, por tanto, proporcionan apoyo a la idea de que el polimorfismo de color en los búhos es un rasgo con valor adaptativo probablemente mantenido por una ventaja selectiva de los morfos bajo diferentes condiciones ambientales a través de mecanismos de selección disruptiva. A continuación, se utilizaron modelos filogenéticos comparativos para testar la hipótesis del camuflaje para el color del iris, un rasgo coloreado cuya base funcional no está aun suficientemente clara. Se encontró que la proporción de especies con ojos oscuros es más alta entre las especies estrictamente nocturnas que en las diurnas. La reconstrucción ancestral mostró que el ancestro de la familia Strigidae tenía con más probabilidad ojos claros, mientras que el ancestro de la familia Tytonidae tendría probablemente ojos oscuros. Estos resultados proporcionan evidencia en favor de una coevolución de la coloración del iris y la nocturnalidad en los búhos, y sugieren que el cambio a un nicho nocturno sería un prerrequisito que ha llevado a la evolución de los ojos oscuros en los búhos. Sin embargo, la ruta evolutiva mediante la cual la coloración del iris y el ritmo de actividad han evolucionado en concierto necesitaría ser más investigada, dado que se encontró solo un apoyo parcial a la idea que los ojos oscuros podrían haber evolucionado por una ventaja selectiva de ocultación frente a receptores visuales no deseados. Finalmente, puesto que el color del iris es un rasgo muy llamativo en el diseño generalmente críptico de los búhos, sugiriendo que podría jugar un posible papel señalizador, evalué la variación y el potencial para señalizar calidad del color amarillo del iris en la comunicación paterno-filial y entre conspecíficos en el mochuelo Athene noctua y en el autillo Otus scops. La coloración del iris no varió entre sexos; sin embargo, los adultos de ambas especies presentaron iris más intensamente coloreados que sus pollos. La mayor parte de la variación en la coloración del iris de los pollos se dio entre los nidos, y no dentro de ellos, y pareció estar relacionada con la calidad de los padres sólo en los mochuelos, mientras en los pollos de autillos no se encontró ninguna relación con la condición. En los adultos, se encontró que la intensidad del color amarillo de las hembras se asociaba positivamente con el éxito del nido (un índice del fitness) en el mochuelo, pero no en el autillo. Este estudio sugiere que es muy improbable que la variación de color del iris esté involucrada en la comunicación paternofilial en estas dos especies, pero que, en las hembras de mochuelo, el color del iris podría potencialmente desempeñar un papel en la señalización en contextos sociales. En conclusión, los resultados de esta tesis muestran que la variación ambiental podría actuar de manera diferentes promoviendo la evolución de la variación de color en los búhos a diferentes escalas espaciales y, más específicamente, que el color del plumaje y de los ojos podría potencialmente servir para diferentes funciones adaptativas previamente poco consideradas en este clado

Cold winters have morph-specific effects on natal dispersal distance in a wild raptor

Dispersal is a key process with crucial implications in spatial distribution, density, and genetic structure of species' populations. Dispersal strategies can vary according to both individual and environmental features, but putative phenotype-by-environment interactions have rarely been accounted for. Melanin-based color polymorphism is a phenotypic trait associated with specific behavioral and physiological profiles and is, therefore, a good candidate trait to study dispersal tactics in different environments. Here, using a 40 years dataset of a population of color polymorphic tawny owls (Strix aluco), we investigated natal dispersal distance of recruiting gray and pheomelanic reddish-brown (hereafter brown) color morphs in relation to post-fledging winter temperature and individual characteristics. Because morphs are differently sensitive to cold winters, we predicted that morphs' natal dispersal distances vary according to winter conditions. Winter temperature did not affect the proportion of brown (or gray) among recruits. We found that dispersal distances correlate with winter temperature in an opposite manner in the two morphs. Although the gray morph undertakes larger movements in harsher conditions, likely because it copes better with winter severity, the brown morph disperses shorter distances when winters are harsher. We discuss this morph-specific natal dispersal pattern in the context of competition for territories between morphs and in terms of costs and benefits of these alternative strategies. Our results stress the importance of considering the interaction between phenotype and environment to fully disentangle dispersal movement patterns and provide further evidence that climate affects the behavior and local distribution of this species

Data from: The evolution of iris colour in relation to nocturnality in owls

data for dryads Raw data used for comparative analyses on eye colour in owlsBirds, due to their multiple colourful displays, constitute a classic paradigm for the study of colour evolution. Although avian eyes are remarkably coloured, the functional basis behind inter‐specific variability in iris colouration remains poorly understood. Owls are an ideal system to shed light on the role of ecology in promoting iris colour evolution as they show inter‐specific variation in iris colour and in niche specialization with some species being strictly nocturnal and others active during the day. Owls perching for hunting at night might be unnoticed by both predators and their prey if they had dark irises, which would predict that dark irises were more likely to evolve in strictly nocturnal species than in diurnal ones. Using phylogenetic comparative models, we tested the camouflage hypothesis for eye colour. Ancestral state reconstruction revealed that the owl ancestor of the family Strigidae was more likely bright‐irided whereas the ancestor of the family Tytonidae was more likely dark‐irided. We found that iris colour and activity rhythm have more likely evolved in concert than independently, and a non‐significant trend of dark eyes to evolve more easily in owl species presenting strictly nocturnal habits than in diurnal species. The transition from diurnality to nocturnality was a previous requisite for the evolution of dark irises in owls. Taken together our results are only partly consistent with the camouflage hypothesis suggesting that dark irises in owls have primarily evolved to enhance concealment in nocturnal conditions.Peer reviewe

data for dryads

Raw data used for comparative analyses on eye colour in owl

The evolution of iris colour in relation to nocturnality in owls

Birds, due to their multiple colourful displays, constitute a classic paradigm for the study of colour evolution. Although avian eyes are remarkably coloured, the functional basis behind inter-specific variability in iris colouration remains poorly understood. Owls are an ideal system to shed light on the role of ecology in promoting iris colour evolution as they show inter-specific variation in iris colour and in niche specialization with some species being strictly nocturnal and others active during the day. Owls perching for hunting at night might be unnoticed by both predators and their prey if they had dark irises, which would predict that dark irises were more likely to evolve in strictly nocturnal species than in diurnal ones. Using phylogenetic comparative models, we tested the camouflage hypothesis for eye colour. The proportion of dark-eyed owl species is higher among strictly nocturnal owls than among diurnal ones. Ancestral state reconstruction revealed that the owl ancestor of the family Strigidae was more likely bright-irided whereas the ancestor of the family Tytonidae was more likely dark-irided. Our results show robust support for the coevolution of iris coloration and nocturnality in the owls, and suggest that shifting to a nocturnal niche would be a prerequisite leading to the evolution of dark eyes in owls. The specific evolutionary pathway by which iris coloration and activity rhythm coevolve, however, remains to be investigated further as we have found only partial support for the idea that dark irises in birds might be an adaptive feature evolved due to the selective advantage of concealment from undesired visual receptors.Peer reviewe

Data from: The evolution of iris colour in relation to nocturnality in owls

Birds, due to their multiple colourful displays, constitute a classic paradigm for the study of colour evolution. Although avian eyes are remarkably coloured, the functional basis behind inter‐specific variability in iris colouration remains poorly understood. Owls are an ideal system to shed light on the role of ecology in promoting iris colour evolution as they show inter‐specific variation in iris colour and in niche specialization with some species being strictly nocturnal and others active during the day. Owls perching for hunting at night might be unnoticed by both predators and their prey if they had dark irises, which would predict that dark irises were more likely to evolve in strictly nocturnal species than in diurnal ones. Using phylogenetic comparative models, we tested the camouflage hypothesis for eye colour. Ancestral state reconstruction revealed that the owl ancestor of the family Strigidae was more likely bright‐irided whereas the ancestor of the family Tytonidae was more likely dark‐irided. We found that iris colour and activity rhythm have more likely evolved in concert than independently, and a non‐significant trend of dark eyes to evolve more easily in owl species presenting strictly nocturnal habits than in diurnal species. The transition from diurnality to nocturnality was a previous requisite for the evolution of dark irises in owls. Taken together our results are only partly consistent with the camouflage hypothesis suggesting that dark irises in owls have primarily evolved to enhance concealment in nocturnal conditions

Dear territory or dear partner? : Causes and consequences of breeding dispersal in a highly territorial bird of prey with a strong pair bond

Territorial species are unlikely to show extensive movements between breeding seasons. This is especially true for long-lived species, which often have strong pair bonding and can occupy the same territory for years. However, also in such species, individuals may face situations that can lead to a territory shift. Here, we use a comprehensive dataset documenting 40 years of breeding behavior in tawny owl (Strix aluco) - a long-lived species with high site tenacity and mate fidelity - to examine the factors affecting the decisions whether or not to move to another breeding territory and how far, as well as the fitness consequences thereof. We found that the likelihood and distance of movement in either sexes is strongly associated with a change of partner, indicating that mate loss may cause breeding dispersal. Moreover, mate change, not movement to a new territory, had negative effects on subsequent reproductive performance: individuals that changed partner were more likely to skip reproduction in the subsequent year and, in those cases they bred, they produced smaller clutches and raised fewer offspring. Our findings indicate that tawny owls change territory almost exclusively when searching for a new partner and that mate change has profound consequences on their subsequent breeding performance. Overall, our study provides evidence that in tawny owls territoriality and monogamy are associated and strongly linked to fitness, but mate fidelity may be more important than site fidelity, likely because sexes are involved in specific tasks and their cooperation ensures breeding success and, consequently, increases fitness. Significance statement Breeding dispersal, the movement of individuals between breeding sites, can entail high costs for animal fitness, especially for territorial species, which display strong site fidelity. We studied the factors associated with breeding dispersal and the consequences on breeding performances in tawny owl (Strix aluco), a highly territorial species. We found that tawny owls moved more frequently to another breeding territory when the mate died. Either sexes showed an equal probability to move, but the effect was stronger in females than in males after a mate change. Moreover, owls that changed partner showed delayed reproduction, smaller clutch and a higher probability to skip reproduction. Our findings show that in tawny owls territoriality and monogamy are associated and strongly linked to fitness, but mate fidelity may be more important than site fidelity, likely because sexes share the costs of holding the territory

Changes in over-winter prey availability, rather than winter climate, are associated with a long-term decline in a northern Tawny Owl population

Although the associations between climate, food conditions and reproduction in the wild has been the focus of numerous studies in recent years, we still know little about population level responses to climate and fluctuating food conditions in long-lived species and during longer periods of time. Here, we assessed the relative importance of the abundance of the main prey in winter (small mammals), and winter climate on population size and productivity in a Tawny Owl (Strix aluco) population in southern Finland during a 40-year period. We studied how population trends changed over time and in relation to winter weather and small mammal abundance on three levels: total estimated population size, proportion of breeders and population productivity. We identified declining trends in each population parameter over time, as well as directional changes in climate variables and prey abundance. Overall, small mammal abundance was the foremost predictor in explaining the variation in the number of active territorial pairs (population size). Moreover, both prey abundance and winter temperature significantly affected the proportion of territorial pairs that attempted to breed and thereby total offspring production, which reveals the relevance of winter weather conditions for population productivity. These results provide additional support to the view that changes in climate can modify predator-prey interactions leading to functional changes in the food web.Peer reviewe