A.B. Kerimov

Immune challenge affects basal metabolic activity in wintering great tits.

The costs of exploiting an organisms immune function are expected to form the basis of many life–history trade–offs. However, there has been debate about whether such costs can be paid in energetic and nutritional terms. We addressed this question in a study of wintering, free–living, male great tits by injecting them with a novel, non–pathogenic antigen (sheep red blood cells) and measuring the changes in their basal metabolic rates and various condition indices subsequent to immune challenge. The experiment showed that activation of the immune system altered the metabolic activity and profile of immune cells in birds during the week subsequent to antigen injection: individuals mounting an immune response had nearly 9% higher basal metabolic rates, 8% lower plasma albumin levels and 37% higher heterophile–to–lymphocyte ratios (leucocytic stress indices) than sham–injected control birds. They also lost nearly 3% (0.5 g) of their body mass subsequent to the immune challenge. Individuals that mounted stronger antibody responses lost more mass during the immune challenge. These results suggest that energetic expenditures to immune response may have a non–trivial impact upon an individuals condition.

Geographical variation in egg mass and egg content in a passerine bird.

Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.

Evolutionary signals of selection on cognition from the great tit genome and methylome

For over 50 years, the great tit (Parus major) has been a model species for research in evolutionary, ecological and behavioural research; in particular, learning and cognition have been intensively studied. Here, to provide further insight into the molecular mechanisms behind these important traits, we de novo assemble a great tit reference genome and whole-genome re-sequence another 29 individuals from across Europe. We show an overrepresentation of genes related to neuronal functions, learning and cognition in regions under positive selection, as well as increased CpG methylation in these regions. In addition, great tit neuronal non-CpG methylation patterns are very similar to those observed in mammals, suggesting a universal role in neuronal epigenetic regulation which can affect learning-, memory- and experience-induced plasticity. The high-quality great tit genome assembly will play an instrumental role in furthering the integration of ecological, evolutionary, behavioural and genomic approaches in this model species.

Estimation of heritability and repeatability of resting metabolic rate in birds by the example of free-living pied flycatchers Ficedula hypoleuca (Aves: Passeriformes)

Repeatability of a trait estimated over long time intervals and its heritability make it possible to assess whether it can serve as an individual characteristic and be subject to selection. Heritability and repeatability of energetic traits are still poorly studied in birds. The most important physiological characteristic of the homoiotherms is the minimal level of energy expenditure, referred to as the resting metabolic rate (RMR), which, in the absence of the expenditure for biomass growth, does not exceed the basal metabolic rate (BMR). We have estimated the BMR repeatability in adult free-living pied flycatchers in Moscow-region (55°44′ N, 36°51′ E; 1992–2008) and Tomsk (56°20′ N, 84°56′ E; 2008–2009) populations over intervals of 40 days to 3 years. In the Moscow-region pied flycatcher population, the BMR repeatability recorded during the same period of the reproductive season was τ = 0.34 ± 0.10 for a 1-year interval (n = 80), τ = 0.60 ± 0.15 for a 2-year interval (n = 19), and τ = 0.85 ± 0.13 for a 3-year interval (n = 6). In the Tomsk population, the BMR repeatability for the 1-year interval was τ = 0.49 ± 0.11 (n = 50). The repeatability of a trait is a measure of its constancy in time and specifies the upper limit of its heritability. RMR heritability was assessed in cross-fostering experiments in the Moscow-region free-living pied flycatcher population in 2003–2005. The RMRs of chicks and BMRs of their biological fathers displayed a positive correlation, whereas no correlation was found between the RMRs of chicks and their foster fathers. The RMR heritability value was h2 = 0.43 ± 0.17 (n = 210). The obtained estimates for repeatability and heritability of fundamental energetic traits in pied fly-catcher are rather high for a physiological trait and suggest the existence of evolutionary stable diversity of the avian population in the BMR.

Geographical trends in the yolk carotenoid composition of the pied flycatcher (Ficedula hypoleuca)

Carotenoids in the egg yolks of birds are considered to be important antioxidants and immune stimulants during the rapid growth of embryos. Yolk carotenoid composition is strongly affected by the carotenoid composition of the female’s diet at the time of egg formation. Spatial and temporal differences in carotenoid availability may thus be reflected in yolk concentrations. To assess whether yolk carotenoid concentrations or carotenoid profiles show any large-scale geographical trends or differences among habitats, we collected yolk samples from 16 European populations of the pied flycatcher, Ficedula hypoleuca. We found that the concentrations and proportions of lutein and some other xanthophylls in the egg yolks decreased from Central Europe northwards. The most southern population (which is also the one found at the highest altitude) also showed relatively low carotenoid levels. Concentrations of β-carotene and zeaxanthin did not show any obvious geographical gradients. Egg yolks also contained proportionally more lutein and other xanthophylls in deciduous than in mixed or coniferous habitats. We suggest that latitudinal gradients in lutein and xanthophylls reflect the lower availability of lutein-rich food items in the northern F. hypoleuca populations and in montane southern populations, which start egg-laying earlier relative to tree phenology than the Central European populations. Similarly, among-habitat variation is likely to reflect the better availability of lutein-rich food in deciduous forests. Our study is the first to indicate that the concentration and profile of yolk carotenoids may show large-scale spatial variation among populations in different parts of the species’ geographical range. Further studies are needed to test the fitness effects of this geographical variation.

Specific immunity and polymorphism of breeding plumage in pied flycatcher (Ficedula hypoleuca) males (Aves: Passeriformes)

The relationship between the type of melanin-based plumage colouration and the strength of experimentally induced immune response was studied using as an example a pied flycatcher population from the Moscow region. The breeding plumage of pied flycatcher males exhibits the full spectrum of transitions from contrasting black-and-white to cryptic brownish, the latter being very similar to the colouration of females. In spite of numerous studies, the nature of this polymorphism still remains vague. Unlike many other avian species with monocyclic breeding, a considerable fraction of pied flycatchers overlaps two energy-consuming productive processes, breeding and moult, over the whole species range. During the main experimental treatment we activated the humoral immunity of free-living males in chick-rearing period by injection of nonpathogenic multifactorial antigen (sheep red blood cells, SRBC) and estimated the strength of the immune responses after repeated captures in 6–8 days. In addition, after each capture we evaluated the numbers of leucocytes (WBC), heterophil to lymphocyte ratios (H/L) and measured night time basal metabolic rates (BMR). Non-moulting males of different colour types showed the same immune responses. Among moulting birds, the strength of the immune response was significantly higher in pale males (morphs 4–7 by Drost’s scale) than in bright males with rich melanin-based colouration (morphs 2–3). This difference resulted from two opposite processes. During moulting, pale males heightened the antibody titer after immunization, while bright males tended to reduce the strength of immune response. Possibly such an asymmetry in immunocompetence at the first stage of moult reflects the different life strategies of pied flycatcher males—conspicuous birds less commonly overlap breeding with moult than cryptic ones.

Male Colour Type and Lifetime Breeding Success in the Pied Flycatcher Ficedula hypoleuca

Abstract. The lifetime breeding success of male Pied Flycatchers was evaluated over a period of nine years (1991–99). The breeding success of males recorded in at least two breeding seasons, and nesting at least once in the study area, was analysed. The lifespan number of offspring was positively and significantly correlated with longevity. The reproductive investment in the first year of life did not correspond with longevity, and hence nonbreeding males in the first year did not compensate for the losses in fecundity. There were no differences in longevity between dark, intermediate and female-like coloured males. Darker males were less successful in their breeding attempts in the first year than paler birds. Breeding in the first year of life positively influenced the future number of fledglings, and the greater investment in reproduction in this year positively affected future brood size in dark males. Among males successfully breeding in the study area from their first season, dark males reared significantly more offspring during their lifetime, and in the first year of life, than paler ones. Nevertheless, in the total sample, lifetime brood size did not vary between differently coloured males, perhaps because dark males are more vulnerable to predators. The general difference between differently coloured males lay in how breeding efforts were distributed during life. Dark males can maximise reproductive investment from the first breeding year, while paler males increased average brood size in the following years of life only.

Basal metabolic rate in free-living tropical birds: the influence of phylogenetic, behavioral, and ecological factors

Abstract The majority of our knowledge of avian energetics is based on studies of birds from temperate and high latitudes. Using the largest existing sample of wild-caught Old World tropical species, we showed that birds from Southern Vietnam had lower basal metabolic rate (BMR) than temperate species. The strongest dissimilarity between tropical and temperate species was the low scaling exponent in the allometric relation between BMR and body mass in tropical birds (the regression slope was 0.573). The passerine migrants to temperate and high latitudes had higher BMR than tropical sedentary passerines. Body mass alone accounted for 93% of the variation in BMR (body mass ranged from 5 to 252 g). Contrary to some other studies, we did not find evidence besides the above mentioned that phylogeny, taxonomy, behavior, or ecology have a significant influence on BMR variation among tropical birds.

The role of a social factor in exploration of a novel environment in great tits (Parus major) under conditions of limited space

Sequential tests in an open field (OF) and in an aviary were performed to study the exploration behavior of great tits, Parus major Each aviary of 2×2×2 m included a standard set of objects: trees, feeder, and shelters. Twenty-four aviaries included a single individual, and 49 aviaries included two heterosexual individuals. During the 15-min observation, a number of explored objects, the latent exploration period of each object (the time period from the start of observation to the first visit of each object), and the time period to the onset of feeding were recorded. The exploration rate of each individual was characterized by the sum of all latent periods (CLP). No association between the cumulative locomotor activities in OF and in an aviary was found. Probably, in the complex environment of an aviary, the frequency of directed actions increases, competing with the movement activity. Faster individuals in OF showed a shorter CLP; i.e., they were fast explorers. The exploration rate of a novel environment in the presence of socid partner was unrelated to exploration scores in OF. Interrelations of birds combined in an aviary were dependent on combinations of personality characteristics identified in OF.

Melanin-based coloration and immunity in polymorphic population of pied flycatcher, Ficedula hypoleuca

A specific interest in the persistence of color polymorphism in some populations of birds and other vertebrates is often linked to ideas about the signaling honesty of bright coloration. The evolution of conspicuous ornamentation could be associated with physiological costs including limitations of the immune system. The study of this process is crucial for an understanding of the maintenance of polymorphic coloration. Here we summarized the results of a study of a pied flycatcher population from the Moscow region (Russia) in 2010–2013. We experimentally induced antibody production by injecting sheep red blood cells (SRBC) and inflammatory swelling by injecting phytohaemagglutinin (PHA) after which we estimated the immune response in breeding males. We used leucocytes-to-erythrocytes and heterophils-to-lymphocytes (H/L) ratios as indicators of infectious, inflammatory processes and stress. The results showed that the feeding rates of males treated with SRBC decreased and negatively related to the intensity of their immune responses. Non-molting males of different color types did not significantly differ in antibody production. Among molting breeders, the immune response to SRBC was significantly higher in pale males than in bright ones with rich melanin-based coloration. In contrast to non-molting males, molting pale males had an increased antibody titer after immunization. The lower humoral immune response was associated with the higher H/L stress index before immunization. The change in H/L after immunization positively correlated with the intensity of the humoral immune response. As opposed to humoral immunity, we did not find any significant predictors, including coloration, molt, or their two-way interaction, to explain the variation in cutaneous inflammatory response to PHA. The results suggest that the apparent advantage of a cryptic male phenotype over a conspicuous phenotype occurring in one of two types of immune response has an impact on the maintenance of color polymorphism in the pied flycatcher.