Eugen Belskii

Geographic patterns of genetic differentiation and plumage colour variation are different in the pied flycatcher (Ficedula hypoleuca)

The pied flycatcher is one of the most phenotypically variable bird species in Europe. The geographic variation in phenotypes has often been attributed to spatial variation in selection regimes that is associated with the presence or absence of the congeneric collared flycatcher. Spatial variation in phenotypes could however also be generated by spatially restricted gene flow and genetic drift. We examined the genetic population structure of pied flycatchers across the breeding range and applied the phenotypic QST (PST)–FST approach to detect indirect signals of divergent selection on dorsal plumage colouration in pied flycatcher males. Allelic frequencies at neutral markers were found to significantly differ among populations breeding in central and southern Europe whereas northerly breeding pied flycatchers were found to be one apparently panmictic group of individuals. Pairwise differences between phenotypic (PST) and neutral genetic distances (FST) were positively correlated after removing the most differentiated Spanish and Swiss populations from the analysis, suggesting that genetic drift may have contributed to the observed phenotypic differentiation in some parts of the pied flycatcher breeding range. Differentiation in dorsal plumage colouration however greatly exceeded that observed at neutral genetic markers, which indicates that the observed pattern of phenotypic differentiation is unlikely to be solely maintained by restricted gene flow and genetic drift.

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.

Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation

1. Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2. We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3. Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4. We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.

Candidate genes for colour and vision exhibit signals of selection across the pied flycatcher (Ficedula hypoleuca) breeding range

The role of natural selection in shaping adaptive trait differentiation in natural populations has long been recognized. Determining its molecular basis, however, remains a challenge. Here, we search for signals of selection in candidate genes for colour and its perception in a passerine bird. Pied flycatcher plumage varies geographically in both its structural and pigment-based properties. Both characteristics appear to be shaped by selection. A single-locus outlier test revealed 2 of 14 loci to show significantly elevated signals of divergence. The first of these, the follistatin gene, is expressed in the developing feather bud and is found in pathways with genes that determine the structure of feathers and may thus be important in generating variation in structural colouration. The second is a gene potentially underlying the ability to detect this variation: SWS1 opsin. These two loci were most differentiated in two Spanish pied flycatcher populations, which are also among the populations that have the highest UV reflectance. The follistatin and SWS1 opsin genes thus provide strong candidates for future investigations on the molecular basis of adaptively significant traits and their co-evolution.

Local survival of pied flycatcher males and females in a pollution gradient of a Cu smelter

Survival is one of the most central population measures when the effects of the pollution are studied in natural bird populations. However, only few studies have actually measured rigorous survival estimates on adult birds. In recent years there has been a methodological advance in survival analyses by mark-recapture models. We modelled local survival (including mortality and emigration) with the program MARK in a population of a small insectivorous passerine bird, the pied flycatcher (Ficedula hypoleuca), around a point source of heavy metals. The local survival of females in the polluted area was about 50% lower than in the other areas. Males, however, survived relatively well in the heavily polluted area, but showed somewhat lower survival in the moderately polluted area. Different pollution effects between two sexes might be due to pollution-related differences in reproductive effort in females and males, and/or more intensive uptake of heavy metals by laying females.

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.

Sympatric divergence and clinal variation in multiple coloration traits of Ficedula flycatchers

Geographic variation in phenotypes plays a key role in fundamental evolutionary processes such as local adaptation, population differentiation and speciation, but the selective forces behind it are rarely known. We found support for the hypothesis that geographic variation in plumage traits of the pied flycatcher Ficedula hypoleuca is explained by character displacement with the collared flycatcher Ficedula albicollis in the contact zone. The plumage traits of the pied flycatcher differed strongly from the more conspicuous collared flycatcher in a sympatric area but increased in conspicuousness with increasing distance to there. Phenotypic differentiation (PST) was higher than that in neutral genetic markers (FST), and the effect of geographic distance remained when statistically controlling for neutral genetic differentiation. This suggests that a cline created by character displacement and gene flow explains phenotypic variation across the distribution of this species. The different plumage traits of the pied flycatcher are strongly to moderately correlated, indicating that they evolve non‐independently from each other. The flycatchers provide an example of plumage patterns diverging in two species that differ in several aspects of appearance. The divergence in sympatry and convergence in allopatry in these birds provide a possibility to study the evolutionary mechanisms behind the highly divergent avian plumage patterns.

Diet composition as a cause of different contaminant exposure in two sympatric passerines in the Middle Urals, Russia.

Contaminant exposure can vary between species but primary causes of it are often unclear. In order to estimate heavy metal intake of two sympatric passerines - Ficedula hypoleuca Pall. and Parus ater L. - we studied nestling diet and metal concentrations in prey invertebrates, near the Middle Ural copper smelter and in an unpolluted area. Diet of P. ater contained more Cu, Cd and Zn compared to F. hypoleuca and the same amount of Pb. Contribution of different prey taxa to bird metal intake was not equal to their dietary proportion. Proportion of Cu, Zn, Pb and Cd provided to birds by spiders and molluscs, as well as Cd and Pb provided by ants and imagoes Diptera, exceeded their dietary fraction by several times. In contrast, the contribution of Lepidoptera and sawfly larvae to bird metal intake was less than their dietary proportion. Pollution-related changes in the diet modified bird contaminant exposure along with pollutant concentrations in preys.

Snail consumption and breeding performance of pied flycatchers (Ficedula hypoleuca) along a pollution gradient in the Middle Urals, Russia

During the years 1989-91, 1997-2003, and 2005-07, we studied how emissions from the Middle Urals copper smelter affect snail availability and reproduction of free-living pied flycatchers (Ficedula hypoleuca). We counted snail shells dropped in nests and analysed food samples of nestlings. Pied flycatchers brought to nestlings fewer shells in heavily polluted sites compared to background sites, resulting in reduced Ca intake. Species diversity of snails collected by birds decreased with decreasing distance from the pollution source. The pattern was the same both in deciduous and coniferous forests. In sites closest to the smelter, 20-50% of breeding females suffered from Ca deficiency, which resulted in an increased proportion of deserted clutches and clutches with defective eggshells. Number of fledglings per nest decreased in heavily polluted sites, especially in broods with decreased snail supply. This study demonstrated that pollution can cause both direct effect of toxicants to birds and indirect effects via reduced Ca availability.

Ant (Hymenoptera, Formicidae) diversity along a pollution gradient near the Middle Ural Copper Smelter, Russia

Ants are considered to be suitable indicators of ecological change and are widely used in land management and environmental monitoring. However, responses of ant communities to industrial pollution are less known so far. We studied pollution-related variations of ant diversity and abundance near the Middle Ural Copper Smelter (Russia) in 2009 and 2013, with pitfall traps set up at 10 sites in Picea obovata and Abies sibirica forest. This study provided evidences for humped pollution-induced dynamics of ant diversity and abundance. Species richness and diversity peaked in the habitat intermediate between slightly damaged and fully destroyed forest ecosystems. The total abundance of ants peaked in the middle of the pollution gradient and was determined mainly by the dominant species Formica aquilonia. The abundance of other species increased towards the smelter, but was less important for total abundance than that of red wood ants. Community dominants changed with increase of exposure; F. aquilonia, a typical species of mature forests, was replaced by species of open habitats, Lasius niger and Myrmica ruginodis. Habitat variables and competition between species seem to affect local ant communities more strongly than pollution exposure. Stand basal area and cover of the field layer were the main determinants of ant diversity and abundance of individual species.