Body size, developmental instability, and climate change.

Development is often temperature-dependent. We hypothesized smaller size and larger asymmetry with increasing temperatures. However, we also predicted associations with asymmetry to differ among traits that differ in their degree of functional importance (especially the functional wings in migratory birds were predicted to be more canalized), timing of development (skeletal [femur, tarsus, and humerus] vs. feather [wing and tail traits]). We analyzed a large dataset of which we included species with at least 20 specimens resulting in 5533 asymmetry values in 1593 individuals from 66 species. There was a consistent significant decrease in size with temperature across all traits. Fluctuating asymmetry (FA) for wings and femur was on average lower, suggesting higher canalization, and it decreased with migration distance, however that was not the case for the other traits. FA increased with increasing temperature for wings, but not for the other characters, where the different responses of different characters to temperature were significant. Because there was no significant three-way interaction between temperature, migration distance, and character, the asymmetry-temperature response was similar in migratory and resident species. These findings imply that climate warming reduces size of all traits and decreases developmental instability of wings in birds.

Breakdown of brain-body allometry and the encephalization of birds and mammals.

The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.

Brain size in birds is related to traffic accidents.

Estimates suggest that perhaps a quarter of a billion birds are killed by traffic annually across the world. This is surprising because birds have been shown to learn speed limits. Birds have also been shown to adapt to the direction of traffic and lane use, and this apparently results in reduced risks of fatal traffic accidents. Such behavioural differences suggest that individual birds that are not killed in traffic should have larger brains for their body size. We analysed the link between being killed by traffic and relative brain mass in 3521 birds belonging to 251 species brought to a taxidermist. Birds that were killed in traffic indeed had relatively smaller brains, while there was no similar difference for liver mass, heart mass or lung mass. These findings suggest that birds learn the behaviour of car drivers, and that they use their brains to adjust behaviour in an attempt to avoid mortality caused by rapidly and predictably moving objects.

Brain size and the risk of getting shot.

Hunting kills hundreds of millions of animals annually, potentially constituting an important selection pressure on hunted species. We hypothesized that hunted individuals differing from survivors by having better ability to distinguish between dangerous humans and other human beings would be at a selective advantage. We tested whether shot individual birds had smaller brains than survivors, under the assumption that individuals with larger brains had superior escape ability. We used a large database on birds from Denmark to test whether getting shot was predicted by brain mass, while controlling statistically for the potentially confounding effects of age, sex, body mass and body condition. Analyses based on all species, or only species that were hunted, while controlling for differences in sampling effort in random effects models, showed consistently that shot individuals had smaller brains than survivors.

Long lifespans have evolved with long and monounsaturated fatty acids in birds.

The evolution of lifespan is a central question in evolutionary biology, begging the question why there is so large variation among taxa. Specifically, a central quest is to unravel proximate causes of ageing. Here, we show that the degree of unsaturation of liver fatty acids predicts maximum lifespan in 107 bird species. In these birds, the degree of fatty acid unsaturation is positively related to maximum lifespan across species. This is due to a positive effect of monounsaturated fatty acid content, while polyunsaturated fatty acid content negatively correlates with maximum lifespan. Furthermore, fatty acid chain length unsuspectedly increases with maximum lifespan independently of degree of unsaturation. These findings tune theories on the proximate causes of ageing while providing evidence that the evolution of lifespan in birds occurs in association with fatty acid profiles. This suggests that studies of proximate and ultimate questions may facilitate our understanding of these central evolutionary questions.

High levels of liver antioxidants are associated with life-history strategies characteristic of slow growth and high survival rates in birds.

Antioxidants have a large potential to coevolve with life-histories because of their capacity to counteract the negative effects of free radicals on fitness. However, only a few studies have explored the association between antioxidant levels and life-history strategies comparing a large number of species. Here we used an extensive dataset of 125 species of birds to investigate the association between concentrations of antioxidants (carotenoids and vitamin E) in the liver, which is the main storage organ for fat-soluble antioxidants, and life-history and morphology. We found that high liver antioxidant concentrations were associated with life-history strategies characterized by "live slow, die old", in clear contrast to previous studies reporting a relationship between high plasma antioxidants and life-histories characterized by "live fast, die young". Thus, high carotenoid concentrations were present in species with large body, brain and egg sizes, high absolute metabolic rate and a resident lifestyle, while high vitamin E concentrations were present in species with large brain size and long life span and incubation period. Our results indicate that antioxidants and life-histories coevolve, and that this may be mediated by positive fitness consequences of the accumulation of liver antioxidants, as species with higher antioxidant levels live longer.

High prevalence of cataracts in birds with pheomelanin-based colouration.

The crystalline lens of the eyes of vertebrates focuses light on the retina. Therefore, maintaining the lens clear is necessary for proper visual function. However, oxidative damage to proteins of the lens leads to opacification and lens dysfunction, termed cataract. Antioxidants thus have a role in avoiding the development of cataracts through their reduction of oxidative stress, and glutathione (GSH), a key intracellular antioxidant, belongs to the primary antioxidant defence mechanism of the lens. Other physiological mechanisms that require GSH may compete with the antioxidant mechanism of the eye. Pheomelanin is a main type of melanin, the most common pigment in vertebrates, and its synthesis consumes GSH. Here, we use data on 81 bird species to test the hypothesis that species producing large amounts of pheomelanin should have diminished capacity to use GSH to protect their eyes and, as a consequence, higher prevalence of cataracts. As predicted, the proportion of pheomelanic plumage was positively associated with the proportion of individuals with cataracts across species, suggesting that production of pheomelanin may have profound fitness consequences, as birds with cataracts have limited ability to perform vital activities. This constitutes the first comparative study of cataracts in wild animals.

A behavioral ecology approach to traffic accidents: interspecific variation in causes of traffic casualties among birds.

Birds and other animals are frequently killed by cars, causing the death of many million individuals per year. Why some species are killed more often than others has never been investigated. In this work hypothesized that risk taking behavior may affect the probability of certain kinds of individuals being killed disproportionately often. Furthermore, behavior of individuals on roads, abundance, habitat preferences, breeding sociality, and health status may all potentially affect the risk of being killed on roads. We used information on the abundance of road kills and the abundance in the surrounding environment of 50 species of birds obtained during regular censuses in 2001-2006 in a rural site in Denmark to test these predictions. The frequency of road kills increased linearly with abundance, while the proportion of individuals sitting on the road or flying low across the road only explained little additional variation in frequency of road casualties. After having accounted for abundance, we found that species with a short flight distance and hence taking greater risks when approached by a potential cause of danger were killed disproportionately often. In addition, solitary species, species with a high prevalence of Plasmodium infection, and species with a large bursa of Fabricius for their body size had a high susceptibility to being killed by cars. These findings suggest that a range of different factors indicative of risk-taking behavior, visual acuity and health status cause certain bird species to be susceptible to casualties due to cars.

Ectoparasites, uropygial glands and hatching success in birds.

The uropygial gland of birds secretes wax that is applied to the plumage, where the secretions are hypothesized to eliminate fungi and bacteria, thereby potentially providing important benefits in terms of plumage maintenance. We analyzed variation in size of the uropygial gland in 212 species of birds to determine the function and the ecological correlates of variation in gland size. Bird species with larger uropygial glands had more genera of chewing lice of the sub-order Amblycera, but not of the sub-order Ischnocera, and more feather mites. There was a fitness advantage associated with relatively large uropygial glands because such species had higher hatching success. These findings are consistent with the hypothesis that the uropygial gland functions to manage the community of microorganisms, and that certain taxa of chewing lice have diverged as a consequence of these defenses.

Levels of antioxidants in rural and urban birds and their consequences.

Numerous animals have successfully invaded urban habitats, although the factors associated with invasion success remain poorly understood. Urban areas are characterized by warmer microclimates, higher levels of primary productivity, longer breeding seasons and higher levels of pollutants. All these factors should cause oxidative stress, favoring invasion by species that have access to high levels of antioxidants. We analyzed concentrations of two categories of dietary, fat-soluble antioxidants (total carotenoids, total vitamin E) in the liver, the main storage organ in birds. Individuals killed by cats had lower levels of vitamin E than individuals that died for other reasons, showing natural selection on stored antioxidants. Bird species that had successfully colonized urban areas had significantly higher levels of vitamin E and total carotenoids than species that did not succeed, and rural populations had higher concentrations of vitamin E and total carotenoids than urban populations of the same species. Interspecific differences in concentrations of fat-soluble antioxidants, and differences between rural and urban populations of the same species, were accounted for by diet, but also by time since urbanization and number of generations since urbanization. These findings suggest that antioxidants, and by implication the ability to cope with oxidative stress, have contributed to successful invasion of urban areas by birds, and that the concentration of these antioxidants has changed in response to the urban environment.

Sperm competition and sexually size dimorphic brains in birds.

Natural selection may favour sexually similar brain size owing to similar selection pressures in males and females, while sexual selection may lead to sexually dimorphic brains. For example, sperm competition involves clear-cut sex differences in behaviour, as males display, mate guard and copulate with females, while females choose among males, and solicit or reject copulations. These behaviours may require fundamentally different neural government in the two sexes leading to sex-dependent brain evolution. Using two phylogenetic approaches in a comparative study, we tested for roles of both natural and sexual-selection pressures on brain size evolution of birds. In accordance with the natural-selection theory, relative brain size of males coevolved with that of females, which may be the result of adaptation to similar environmental constraints such as feeding innovation. However, the mode of brain size evolution differed between the sexes, and factors associated with sperm competition as reflected by extra-pair paternity may give rise to sexually size dimorphic brains. Specifically, species in which females have larger brains than males were found to have a higher degree of extra-pair paternity independently of potentially confounding factors, whereas species in which males have relatively larger brains than females appeared to have lower rates of extra-pair paternity. Hence, the evolution of sperm competition may select for complex behaviours together with the associated neural substrates in the sex that has a higher potential to control extra-pair copulations at the observed levels. Brain function may thus be affected differently in males and females by sexual selection.

Climate, body condition and spleen size in birds.

Climatic conditions may impact on the body condition of animals and thereby affect their survival prospects. However, climate may also impact directly on the survival prospects of animals by affecting the size of immune defence organs that are used for defence against parasites. We used a large long-term database on body condition and size of the spleen in birds to test for immediate and delayed relationships between climatic conditions as indexed by the North Atlantic Oscillation (NAO) and body condition and spleen mass, respectively. Across 14 species of birds, spleen mass was significantly positively correlated with the NAO index, while the delayed effect of NAO on spleen mass was not significant. Spleen mass was positively related to body condition, but body condition did not depend significantly on NAO or delayed NAO effects. Bird species with a strong positive effect of NAO on spleen mass tended to have small spleens for their body size, while species with a strong negative effect of NAO on spleen mass tended to have relatively large spleens. Since bird species with relatively large spleen have been shown to suffer more from the negative effects of parasites, we can infer that the effects of climate as indexed by NAO on the size of the spleen depends on the importance of parasite-mediated natural selection.

The evolution of immune defense and song complexity in birds.

There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.

Seasonal changes in immune response and parasite impact on hosts.

Seasonal changes in the impact of parasites on hosts should result in seasonal changes in immune function. Since both ectoparasites and endoparasites time their reproduction to that of their hosts, we can predict that hosts have been selected to show an annual peak in their ability to raise an immune response during the reproductive season. We found large seasonal changes in immune function between the breeding and the nonbreeding season for a sample of temperate bird species. These changes amounted to a decrease in spleen mass from the breeding to the nonbreeding season by on average 18% across 71 species and a seasonal decrease in T-cell-mediated immunity by on average 33% across 13 species. These seasonal changes in immune function differed significantly among species. The condition dependence of immune function also differed between the breeding and the nonbreeding season, with individuals in prime condition particularly having greater immune responses during breeding. Analyses of ecological factors associated with interspecific differences in seasonal change of immune function revealed that hole-nesting species had a larger increase in immune function during the breeding season than did open nesters. Since hole nesters suffer greater reduction in breeding success because of virulent parasites than do open nesters, this seasonal change in immune function is suggested to have arisen as a response to the increased virulence of parasites attacking hole-nesting birds.

Coevolving avian eye size and brain size in relation to prey capture and nocturnality.

Behavioural adaptation to ecological conditions can lead to brain size evolution. Structures involved in behavioural visual information processing are expected to coevolve with enlargement of the brain. Because birds are mainly vision-oriented animals, we tested the predictions that adaptation to different foraging constraints can result in eye size evolution, and that species with large eyes have evolved large brains to cope with the increased amount of visual input. Using a comparative approach, we investigated the relationship between eye size and brain size, and the effect of prey capture technique and nocturnality on these traits. After controlling for allometric effects, there was a significant, positive correlation between relative brain size and relative eye size. Variation in relative eye and brain size were significantly and positively related to prey capture technique and nocturnality when a potentially confounding variable, aquatic feeding, was controlled statistically in multiple regression of independent linear contrasts. Applying a less robust, brunching approach, these patterns also emerged, with the exception that relative brain size did not vary with prey capture technique. Our findings suggest that relative eye size and brain size have coevolved in birds in response to nocturnal activity and, at least partly, to capture of mobile prey.

PARASITE VIRULENCE AND HOST IMMUNE DEFENSE: HOST IMMUNE RESPONSE IS RELATED TO NEST REUSE IN BIRDS.

The evolution of parasite virulence has been hypothesized to be related to the mode of parasite transmission; horizontally transmitted parasites can afford to damage their hosts more than vertically transmitted parasites because increased virulence does not reduce the probability of transmission to new hosts. This relationship between mode of transmission and virulence would particularly select for improved immune defense in hosts that are subject to horizontally transmitted parasites. Among avian hosts, hole nesters and colonial nesters frequently reuse nest sites because of nest-site limitation, and this results in an increased frequency of horizontal transmission. Comparison of the size of two organs involved in the immune defense between pairs of bird species being either hole or open nesters, or colonially or solitarily nesting birds, respectively, revealed that the size of the bursa of Fabricius and the spleen were consistently larger in hole nesters than in open nesters, and similarly in colonially breeding bird species than in solitarily breeding species. These results support the hypothesis that mode of parasite transmission affects the evolution of immune defence in hosts.