Insularity and the evolution of melanism,sexual dichromatism and body size in the worldwide‐distributed barn owl

Island biogeography has provided fundamental hypotheses in population genetics, ecology and evolutionary biology. Insular populations usually face different feeding conditions, predation pressure, intraspecific and interspecific competition than continental populations. This so‐called island syndrome can promote the evolution of specific phenotypes like a small (or large) body size and a light (or dark) colouration as well as influence the evolution of sexual dimorphism. To examine whether insularity leads to phenotypic differentiation in a consistent way in a worldwide‐distributed nonmigratory species, we compared body size, body shape and colouration between insular and continental barn owl (Tyto alba) populations by controlling indirectly for phylogeny. This species is suitable because it varies in pheomelanin‐based colouration from reddish‐brown to white, and it displays eumelanic black spots for which the number and size vary between individuals, populations and species. Females are on average darker pheomelanic and display more and larger eumelanic spots than males. Our results show that on islands barn owls exhibited smaller and fewer eumelanic spots and lighter pheomelanic colouration, and shorter wings than on continents. Sexual dimorphism in pheomelanin‐based colouration was less pronounced on islands than continents (i.e. on islands males tended to be as pheomelanic as females), and on small islands owls were redder pheomelanic and smaller in size than owls living on larger islands. Sexual dimorphism in the size of eumelanic spots was more pronounced (i.e. females displayed much larger spots than males) in barn owls living on islands located further away from a continent. Our study indicates that insular conditions drive the evolution towards a lower degree of eumelanism, smaller body size and affects the evolution of sexual dichromatism in melanin‐based colour traits. The effect of insularity was more pronounced on body size and shape than on melanic traits.     

Darker eumelanic barn owls better withstand food depletion through resistance to food deprivation and lower appetite

The intensity of selection exerted on ornaments typically varies between environments. Reaction norms may help to identify the conditions under which ornamented individuals have a selective advantage over drab conspecifics. It has been recently hypothesized that in vertebrates eumelanin-based coloration reflects the ability to regulate the balance between energy intake and expenditure. We tested two predictions of this hypothesis in barn owl nestlings, namely that darker eumelanic individuals have a lower appetite and lose less weight when food-deprived. We found that individuals fed ad libitum during 24 h consumed less food when their plumage was marked with larger black spots. When food-deprived for 24 h nestlings displaying larger black spots lost less weight. Thus, in the barn owl the degree of eumelanin-based coloration reflects the ability to withstand periods of food depletion through lower appetite and resistance to food restriction. Eumelanic coloration may therefore be associated with adaptations to environments where the risk of food depletion is high.     

Sex‐linked inheritance,genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

Theory states that genes on the sex chromosomes have stronger effects on sexual dimorphism than genes on the autosomes. Although empirical data are not necessarily consistent with this theory, this situation may prevail because the relative role of sex‐linked and autosomally inherited genes on sexual dimorphism has rarely been evaluated. We estimated the quantitative genetics of three sexually dimorphic melanin‐based traits in the barn owl (Tyto alba), in which females are on average darker reddish pheomelanic and display more and larger black eumelanic feather spots than males. The plumage traits with higher sex‐linked inheritance showed lower heritability and genetic correlations, but contrary to prediction, these traits showed less pronounced sexual dimorphism. Strong offspring sexual dimorphism primarily resulted from daughters not expressing malelike melanin‐based traits and from sons expressing femalelike traits to similar degrees as their sisters. We conclude that in the barn owl, polymorphism at autosomal genes rather than at sex‐linked genes generate variation in sexual dimorphism in melanin‐based traits.     

Age‐related change in melanin‐based coloration of Barn owls (Tyto alba): females that become more female‐like and males that become more male‐like perform better

Ornament expression fluctuates with age in many organisms. Whether these changes are adaptively plastic is poorly known. In order to understand the ultimate function of melanin‐based ornaments, we studied their within‐individual fluctuations and their covariation with fitness‐related traits. In barn owls (Tyto alba), individuals vary from reddish‐brown pheomelanic to white, and from immaculate to marked with black eumelanic spots, with males being less reddish and less spotted than females. During the first molt, both sexes became less pheomelanic, females displayed larger spots and males fewer spots, but the extent of these changes was not associated with reproduction. At subsequent molts, intra‐individual changes in melanin‐based traits covaried with simultaneous reproduction changes. Adult females bred earlier in the season and laid larger eggs when they became scattered with larger spots, whereas adults of both sexes produced larger broods when they became whiter. These results suggest that the production of melanin pigments and fitness‐related life‐history traits are concomitantly regulated in a sex‐specific way. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 689–704.     

Regulation of stress response is heritable and functionally linked to melanin‐based coloration

Sexual selection theory posits that ornaments can signal the genetic quality of an individual. Eumelanin‐based coloration is such an ornament and can signal the ability to cope with a physiological stress response because the melanocortin system regulates eumelanogenesis as well as physiological stress responses. In the present article, we experimentally investigated whether the stronger stress sensitivity of light than dark eumelanic individuals stems from differential regulation of stress hormones. Our study shows that darker eumelanic barn owl nestlings have a lower corticosterone release after a stressful event, an association, which was also inherited from the mother (but not the father) to the offspring. Additionally, nestlings sired by darker eumelanic mothers more quickly reduced experimentally elevated corticosterone levels. This provides a solution as to how ornamented individuals can be more resistant to various sources of stress than drab conspecifics. Our study suggests that eumelanin‐based coloration can be a sexually selected signal of resistance to stressful events.     

Temporal variation in glucocorticoid levels during the resting phase is associated in opposite way with maternal and paternal melanic coloration

Sex‐dependent selection can help maintain sexual dimorphism. When the magnitude of selection exerted on a heritable sex trait differs between the sexes, it may prevent each sex to reach its phenotypic optimum. As a consequence, the benefit of expressing a sex trait to a given value may differ between males and females favouring sex‐specific adaptations associated with different values of a sex trait. The level of metabolites regulated by genes that are under sex‐dependent selection may therefore covary with the degree of ornamentation differently in the two sexes. We investigated this prediction in the barn owl, a species in which females display on average larger black spots on the plumage than males, a heritable ornament. This melanin‐based colour trait is strongly selected in females and weakly counter‐selected in males indicating sex‐dependent selection. In nestling barn owls, we found that daily variation in baseline corticosterone levels, a key hormone that mediates life history trade‐offs, covaries with spot diameter displayed by their biological parents. When their mother displayed larger spots, nestlings had lower corticosterone levels in the morning and higher levels in the evening, whereas the opposite pattern was found with the size of paternal spots. Our study suggests a link between daily regulation of glucocorticoids and sex‐dependent selection exerted on sexually dimorphic melanin‐based ornaments.     

Coloration signals the ability to cope with elevated stress hormones: effects of corticosterone on growth of barn owls are associated with melanism

Stressful situations during development can shape the phenotype for life by provoking a trade-off between development and survival. Stress hormones, mainly glucocorticoids, play an important orchestrating role in this trade-off. Hence, how stress sensitive an animal is critically determines the phenotype and ultimately fitness. In several species, darker eumelanic individuals are less sensitive to stressful conditions than less eumelanic conspecifics, which may be due to the pleiotropic effects of genes affecting both coloration and physiological traits. We experimentally tested whether the degree of melanin-based coloration is associated with the sensitivity to an endocrine response to stressful situations in the barn owl. We artificially administered the mediator of a hormonal stress response, corticosterone, to nestlings to examine the prediction that corticosterone-induced reduction in growth rate is more pronounced in light eumelanic nestlings than in darker nest mates. To examine whether such an effect may be genetically determined, we swapped hatchlings between randomly chosen pairs of nests. We first showed that corticosterone affects growth and, thus, shapes the phenotype. Second, we found that under corticosterone administration, nestlings with large black spots grew better than nestlings with small black spots. As in the barn owl the expression of eumelanin-based coloration is heritable and not sensitive to environmental conditions, it is therefore a reliable, genetically based sign of the ability to cope with an increase in blood corticosterone level.     

Spatial variation in the temporal change of male and female melanic ornamentation in the barn owl

Because the magnitude of selection can vary between sexes and in space and time, sexually antagonistic selection is difficult to demonstrate. In a Swiss population of barn owls (Tyto alba), a heritable eumelanic colour trait (size of black spots on ventral feathers) was positively selected with respect to yearling survival only in females. It remains unclear whether the absence of negative selection in males is typical in this species. To tackle this issue indirectly, we measured the size of black spots in 1733 skin specimens collected by museums from 1816 to 2001 in seven European countries and in the Middle-East. The temporal change in spot size was sex- and country-specific. In males, spots became smaller particularly in three countries (Middle-East, Italy and Switzerland). In females, the size of spots increased significantly in two countries (UK and Spain) and decreased in two others (Germany and Switzerland). Because migration and phenotypic plasticity cannot explain these results, selection is the most likely cause. The weaker temporal change in spot size in females than males may be because of the combined effect of strong genetic correlation between the sexes and stronger negative selection in males than positive selection in females. We thus suggest that in the barn owl, spot size (or genetically correlated traits) is sexually antagonistically selected and that its pattern of selection may account for the maintenance of its variation and sexual dimorphism.     

Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba)

The hypothesis that extravagant ornaments signal parasite resistancehas received support in several species for ornamented malesbut more rarely for ornamented females. However, recent theorieshave proposed that females should often be under sexual selection,and therefore females may signal the heritable capacity toresist parasites. We investigated this hypothesis in the sociallymonogamous barn owl, Tyto alba, in which females exhibit on average more and larger black spots on the plumage than males,and in which males were suggested to choose a mate with respectto female plumage spottiness. We hypothesized that the proportionof the plumage surface covered by black spots signals parasiteresistance. In line with this hypothesis, we found that theectoparasitic fly, Carnus hemapterus, was less abundant onyoung raised by more heavily spotted females and those flieswere less fecund. In an experiment, where entire clutches werecross-fostered between nests, we found that the fecundity ofthe flies collected on nestlings was negatively correlatedwith the genetic mother's plumage spottiness. These resultssuggest that the ability to resist parasites covaries with theextent of female plumage spottiness. Among females collecteddead along roads, those with a lot of black spots had a smallbursa of Fabricius. Given that parasites trigger the developmentof this immune organ, this observation further suggests thatmore spotted females are usually less parasitized. The same analyses performed on male plumage spottiness all provided non-significant results. To our knowledge, this study is the first one showingthat a heritable secondary sexual characteristics displayedby females reflects parasite resistance.     

Body size clines in the European badger and the abundant centre hypothesis

Aim To test the abundant centre hypothesis by analysing the physical and climatic factors that influence body size variation in the European badger (Meles meles). Location Data were compiled from 35 locations across Europe. Methods We used body mass, body length and condylo‐basal length (CBL) as surrogates of size. We also compiled data on latitude, several climatic variables, habitat type and site position relative to the range edge. We collapsed all continuous climatic variables into independent vectors using principal components analysis (PCA), and used a general linear model to explain the morphometric variation in badger populations across the species’ range. Results Body mass and body length were nonlinearly and significantly related to latitude. In contrast, CBL was linearly related to latitude. Body mass changed nonlinearly along the temperature (PC1) gradient, with the highest values observed at mid‐range. Furthermore, body mass, body length and CBL differed significantly among habitats, with badgers showing larger size in temperate habitats and core areas relative to peripheral zones. Main conclusions Our analysis supports the nonlinear pattern predicted by the abundant centre hypothesis only for body mass and body length. These results imply that individuals are largest and heaviest at the centre of the climatic range of badger distribution. Variation of CBL with latitude follows a linear trend, consistent with Bergmann’s rule. Our results provide mixed support for the abundant centre hypothesis, and suggest food availability/quality to be the main mechanism underlying body size clines in this species.     

Exploring the adjustment to parasite pressure hypothesis: differences in uropygial gland volume and haemosporidian infection in palearctic and neotropical birds

Parasites are globally widespread pathogenic organisms, which impose important selective forces upon their hosts. Thus, in accordance with the Adjustment to parasite pressure hypothesis, it is expected that defenses among hosts vary relative to the selective pressure imposed by parasites. According to the latitudinal gradient in diversity, species richness and abundance of parasites peak near the equator. The uropygial gland is an important defensive exocrine gland against pathogens in birds. Size of the uropygial gland has been proposed to vary among species of birds because of divergent selection by pathogens on their hosts. Therefore, we should expect that bird species from the tropics should have relatively larger uropygial glands for their body size than species from higher latitudes. However, this hypothesis has not yet been explored. Here, we analyze the size of the uropygial gland of 1719 individual birds belonging to 36 bird species from 3 Neotropical (Peru) and 3 temperate areas (Spain). Relative uropygial gland volume was 12.52% larger in bird species from the tropics than from temperate areas. This finding is consistent with the relative size of this defensive organ being driven by selective pressures imposed by parasites. We also explored the potential role of this gland as a means of avoiding haemosporidian infection, showing that species with large uropygial glands for their body size tend to have lower mean prevalence of haemosporidian infection, regardless of their geographical origin. This result provides additional support for the assumption that secretions from the uropygial gland reduce the likelihood of becoming infected with haemosporidians.     

Sexually dimorphic melanin‐based colour polymorphism,feather melanin content,and wing feather structure in the barn owl (Tyto alba)

Feathers confer protection against biophysical agents and determine flying ability. The geometry and arrangement of the barbs, together with the keratin and pigments deposited in the feathers, determine the mechanical stability of the vane, and its stiffness and resistance to abrasive agents. In colour‐polymorphic species, individuals display alternative colour morphs, which can be associated with different foraging strategies. Each morph may therefore require specific flying abilities, and their feathers may be exposed to different abrasive agents. Feathers of differently coloured individuals may thus have a specific structure, and colour pigments may help resist abrasive agents and improve stiffness. We examined these predictions in the barn owl (Tyto alba), a species for which the ventral body side varies from white to dark reddish pheomelanic, and in the number and size of black spots located at the tip of the feathers. White and reddish birds show different foraging strategies, and the size of black feather spots is associated with several phenotypic attributes. We found that birds displaying a darker reddish coloration on the ventral body side deposit more melanin pigments in their remiges, which also have fewer barbs. This suggests that wear resistance increases with darkness, whereas feathers of lighter coloured birds may bend less easily. Accordingly, individuals displaying a lighter reddish coloration on the ventral body side, and those displaying larger black spots, displayed more black transverse bars on their remiges: as larger‐spotted individuals are heavier and longer‐winged birds also have more transverse bars, these bars may reduce feather bending when flying. We conclude that differently coloured individuals produce wing feathers of different strengths to adopt alternative behavioural and life history strategies. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 562–573.     

Melanin‐Based Coloration in Juvenile Kestrels ( Falco tinnunculus) Covaries with Anti‐Predatory Personality Traits

Recent studies have shown that melanin‐based coloration is associated with the ability to cope with stressful environments, potentially explaining why coloration covaries with anti‐predator behaviours, boldness and docility. To investigate whether these relationships are consistent across species, we performed a study in the European kestrel ( Falco tinnunculus). Similar to our results found previously in the barn owl ( Tyto alba), nestling kestrels displaying a larger sub‐terminal black tail band stayed on their back longer (tonic immobility test) and breathed at a lower rate than individuals with a smaller black band when handled. However, in contrast to barn owls, nestling kestrels with a larger black tail band were more aggressive and more agitated. Our results strengthen the hypothesis that melanin coloration is related to stress response and in turn to the reaction to predators, a very important personality trait (i.e. boldness).     

Evolutionary trade‐off between naturally‐ and sexually‐selected melanin‐based colour traits in worldwide barn owls and allies

Natural selection typically constrains the evolution of sexually‐selected characters. The evolution of naturally‐ and sexually‐selected traits can be intertwined if they share part of their genetic machinery or if sex traits impair foraging success or increase the risk of depredation. The present study investigated phenotypic correlations between naturally‐ and sexually‐selected plumage traits in the Tytonidae (barn owls, grass owls, and masked owls). Phenotypic correlations indicate the extent to which selection on one trait will indirectly influence the evolution of another trait. In this group of birds, the ventral body side varies from white to dark reddish, a naturally‐selected pheomelanin‐based colour trait with important roles in predator–prey interactions. Owls also exhibit eumelanin‐based black spots, for which number and size signal different aspects of individual quality and are used in mate choice. These three plumage traits are strongly heritable and sexually dimorphic, with females being on average darker reddish and more spotted than males. Phenotypic correlations were measured between these three plumage traits in 3958 free‐living barn owls in Switzerland and 10 670 skin specimens from 34 Tyto taxa preserved in museums. Across Tyto taxa, the sexually‐selected plumage spottiness was positively correlated with the naturally‐selected reddish coloration, with redder birds being more heavily spotted. This suggests that they are genetically constrained or that natural and sexual selection are not antagonistically exerted on plumage traits. In a large sample of Swiss nestlings and within 34 Tyto taxa, the three plumage traits were positively correlated. The production of melanin pigments for one plumage trait is therefore not traded off against the production of melanin pigments for another plumage trait. Only in the most heavily‐spotted Tyto taxa do larger‐spotted individuals display fewer spots. This indicates that, at some threshold value, the evolution of many spots constrains the evolution of large spots. These analyses raise the possibility that different combinations of melanin‐based plumage traits may not be selectively equivalent.     

The relationship between intra–guild diet overlap and breeding in owls in Israel

Even though intra-guild predators frequently prey on the same species, it is unclear whether diet overlap between two predators is a source of interspecific competition or whether predators simply use the same abundant prey resource. We measured the extent to which the diets of barn owls (Tyto alba) and long-eared owls (Asio otus) in Israel overlap and examined whether yearly differences in diet overlap correlate with barn owl breeding success. Pianka’s index of niche overlap was positively related to barn owl population size but not to its breeding success. The number of breeding barn owls was higher when long-eared owls consumed more rodents, suggesting that diet overlap most likely increased when rodents became more abundant. Therefore, in Israel, when these two owl species prey more often on rodents, their diets are more similar and interspecific competition is reduced. Unlike sympatric populations in Europe, in years when rodents are less abundant in Israel long-eared owls switch to hunting alternative prey (e.g., birds), perhaps to avoid competition with barn owls.     

Haemosporidian parasites depress breeding success and plumage coloration in female barn swallows Hirundo rustica

Parasites are major effectors of natural selection and also play a role in sexual selection processes. Haemosporidian blood parasites are common in vertebrates and have been shown to vary in their effects depending on both the parasite and host species, on the host trait investigated as well as on host condition and stage of infection. Here we investigated infection of adult barn swallows Hirundo rustica by Plasmodium, Leucocytozoon and Haemoproteus species during the chronic stage of infection and the consequences for host fitness traits. Prevalence was higher than 10% only for Plasmodium. Chronic stage infection by Plasmodium was associated with reduced female breeding success, but did not affect breeding dates. Infection did not affect the expression of male secondary sexual traits (tail length and melanin‐based plumage coloration), but was associated with paler coloration of females. Finally, we found a negative effect of infection by Plasmodium on feather growth rate in older but not in yearling individuals. Because feathers are moulted during wintering in sub‐Saharan Africa where infection of barn swallows by Plasmodium occurs, our results suggest that male secondary sexual traits have little potential to reveal acute‐stage infection whereas plumage coloration of females may advertise their infection status. In addition, these results suggest that infection by Plasmodium can influence the course of plumage moult. Thus, our results add to the observations of negative effects of haemosporidian infection on fitness traits in birds and provides evidence that these effects can vary among traits and in relation to age and sex.     

Geographic variation in sexual dimorphism in the barn owl Tyto alba: a role for direct selection or genetic correlation?

Geographic variation in sexually selected traits is commonly attributed to geographic variation in the net benefit accrued from bearing such traits. Although natural and sexual selection are potentially important in shaping geographic variation, genetic constraints may also play a role. Although a genetic correlation between two traits may itself be the outcome of natural or sexual selection, it may indirectly reinforce the establishment and maintenance of cline variation with respect to one particular trait when across the cline different values of other traits are selected. Using the barn owl Tyto alba, a species in which the plumage of females is more reddish‐brown and more marked with black spots than that of males, I report results that are consistent with the hypothesis that both direct selection and genetic constraints may help establish and maintain cline variation in sexual dichromatism. In this species, inter‐individual variation in plumage coloration and spottiness has a genetic basis, and these traits are not sensitive to the environment. Data, based on the measurement of skin specimens, is consistent with the hypothesis that the stronger European cline variation in male spottiness than in female spottiness depends on the combined effects of (1) the similar cline variation in male and female plumage coloration and (2) the more intense phenotypic correlation between plumage coloration and spottiness in males (darker birds are more heavily spotted in the two sexes, but especially males) which is a general feature among the globally distributed barn owls. In northern Europe, male and female T. a. guttata are reddish‐brown and heavily spotted, and in southern Europe male and female T. a. alba are white, but only females display many spots. Here, I discuss the relative importance of direct selection, genetic correlation and the post‐ice age invasion of Europe by T. alba, in generating sex‐specific cline variation in plumage spottiness and non‐sex‐specific cline variation in plumage coloration.     

Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta‐analysis

Sexual selection arises from competition among individuals for access to mates, resulting in the evolution of conspicuous sexually selected traits, especially when inter‐sexual competition is mediated by mate choice. Different sexual selection regimes may occur among populations/subspecies within the same species. This is particularly the case when mate choice is based on multiple sexually selected traits. However, empirical evidence supporting this hypothesis at the among‐populations level is scarce. We conducted a meta‐analysis of the intensity of sexual selection on the largest database to date for a single species, the barn swallow (Hirundo rustica), relying on quantitative estimates of sexual selection. The intensity of sexual selection was expressed as the strength (effect size) of the relationships between six plumage ornaments (tail length, tail asymmetry, size of white spots on tail, ventral plumage colour, throat plumage colour and throat patch size) and several fitness proxies related to reproduction, parental care, offspring quality, arrival date from spring migration, and survival. The data were gathered for four geographically separated subspecies (H. r. rustica, H. r. erythrogaster, H. r. gutturalis, H. r. transitiva). The overall mean effect size (Z_r = 0.214; 95% confidence interval = 0.175–0.254; N = 329) was of intermediate magnitude, with intensity of sexual selection being stronger in males than in females. Effect sizes varied during the breeding cycle, being larger before egg deposition, when competition for access to mates reaches its maximum (i.e. in the promiscuous part of the breeding cycle), and decreasing thereafter. In addition, effect sizes from experiments were not significantly larger than those from correlative studies. Finally, sexual selection on different sexually dimorphic traits varied among subspecies. This last result suggests that morphological divergence among populations has partly arisen from divergent sexual selection, which may eventually lead to speciation.     

Microsatellite markers characterized in the barn owl (Tyto alba) and of high utility in other owls (Strigiformes: AVES)

We have identified 15 polymorphic microsatellite loci for the barn owl (Tyto alba), five from testing published owl loci and 10 from testing non‐owl loci, including loci known to be of high utility in passerines and shorebirds. All 15 loci were sequenced in barn owl, and new primer sets were designed for eight loci. The 15 polymorphic loci displayed two to 26 alleles in 56–58 barn owls. When tested in 10 other owl species (n = 1–6 individuals), between four and nine loci were polymorphic per species. These loci are suitable for studies of population structure and parentage in owls.     

Condition‐dependent expression of carotenoid‐ and melanin‐based plumage colour of northern flicker nestlings revealed by manipulation of brood size

Carotenoid‐based colouration in feathers is widely accepted to be a reliable signal of the health of an individual, but the condition‐dependence of melanin‐based plumage ornaments has been highly debated. Using broods that were manipulated in size, we tested whether nutritional stress during rearing affected the carotenoid pigmentation in secondary feathers and the size, shape, and symmetry of melanin spots on breast plumage of northern flicker Colaptes auratus nestlings. Two measures of carotenoid colour (chroma and brightness) of secondary flight feathers did not vary according to brood size treatment, but in a larger dataset from the population, carotenoid chroma was positively associated with nestling mass. Nestlings from experimentally enlarged broods had smaller melanin spots than those from reduced broods, which is some of the first experimental evidence that melanin ornament size in growing nestlings is condition‐dependent. However, the shape and symmetry of the melanin breast spots was not associated with nestling mass. Sexual dimorphism was apparent in both types of pigmentation and future studies should investigate whether there are any trade‐offs for nestlings between investing in carotenoid colouration and melanisation and whether trade‐offs differ between the sexes.