Vitamin E improves growth of collared flycatcher Ficedula albicollis young: a supplementation experiment

In altricial birds, the quantity and quality of food provided by parents is a crucial determinant of nestling performance. Vitamin E is an important micronutrient with various physiological functions, including a positive role in the antioxidant system. Sufficient intake of vitamin E has been shown to condition normal avian development in poultry, yet, our knowledge of the role of vitamin E in free‐living birds is limited. Thus, we experimentally examined the effects of vitamin E on nestling development in the collared flycatcher Ficedula albicollis. We supplemented nestlings with vitamin E and evaluated their growth and survival till fledging. Increased availability of vitamin E did not affect body mass, wing length or survival, but improved tarsus growth. The effect of supplementation on tarsus length changed over season and with initial body mass. Supplemented nestlings that were smaller at hatching and those that hatched later in the season grew longer tarsi compared to the control. Our results suggest that 1) vitamin E may be limiting for the development of collared flycatcher nestlings, 2) seasonal changes of vitamin E availability may affect breeding success of collared flycatchers, and 3) increased income of vitamin E may improve growth of nestlings with bad start in life.     

Lack of evidence for improved immune response of extra‐pair nestlings in collared flycatcher Ficedula albicollis

Extra‐pair paternity is common in many socially monogamous bird species. Increasing evidence suggests that extra‐pair copulations are female‐driven, but benefits for females mating outside social pair‐bonds are still poorly understood. The most influential explanation, “good genes” hypothesis, states that females mated socially with low quality males, engage in extra‐pair copulations to obtain genetic benefits for their progeny. According to this model, enhanced performance of extra‐pair offspring is expected. Here, based on 4‐year study of collared flycatcher Ficedula albicollis, we compared the condition of extra‐pair and within‐pair young. We found no difference in immune response and body size between maternal half‐siblings raised in the same nests. Additionally sex ratio was not biased among extra‐pair nestlings, and paternity was not associated with hatching rank. Our results failed to reveal “good genes” effects in the studied population. These effects might be hard to detect, but other hypotheses should also be studied more thoroughly in the future.     

High individual repeatability and population differentiation in stable isotope ratios in winter-grown collared flycatcher Ficedula albicollis feathers

For migrants, we often lack complete information of their spatial distribution year round. Here, we used stable carbon, nitrogen and hydrogen isotope ratios extracted from feathers grown at the wintering sites of the long-distance migratory collared flycatcher Ficedula albicollis , to study how individuals from different breeding populations are distributed at the wintering sites. A sub-sample of birds was also sampled in two consecutive years to test for the repeatability of isotope ratios. Birds from the same breeding populations had more similar isotope ratios compared to birds from other nearby populations (10–100 km apart). Furthermore, isotope repeatability within individuals was high, implying that the observed pattern of isotope variation is consistent between years. We put forward two hypotheses for these patterns; 1) strong wintering site philopatry and migratory connectivity, suggesting that migratory connectivity may potentially be found on a much smaller spatial scale than previously considered, and 2) consistent interpopulation differentiation of feeding ecology at their wintering site.     

Low genetic variance in the duration of the incubation period in a collared flycatcher (Ficedula albicollis) population

The avian incubation period is associated with high energetic costs and mortality risks suggesting that there should be strong selection to reduce the duration to the minimum required for normal offspring development. Although there is much variation in the duration of the incubation period across species, there is also variation within species. It is necessary to estimate to what extent this variation is genetically determined if we want to predict the evolutionary potential of this trait. Here we use a long-term study of collared flycatchers to examine the genetic basis of variation in incubation duration. We demonstrate limited genetic variance as reflected in the low and nonsignificant additive genetic variance, with a corresponding heritability of 0.04 and coefficient of additive genetic variance of 2.16. Any selection acting on incubation duration will therefore be inefficient. To our knowledge, this is the first time heritability of incubation duration has been estimated in a natural bird population.     

Eggshell coloration in relation to male ornamentation, female condition and egg quality in the collared flycatcher Ficedula albicollis

The blue-green eggshell pigment biliverdin is an efficient antioxidant, the deposition of which may be costly and act as a handicap to the female's antioxidant capacity. Thus, it is hypothesized that there exists a positive correlation between the degree of eggshell coloration and the condition and health state of the mother. In this study, we measured the blue-green chroma of collared flycatcher Ficedula albicollis eggs, and investigated the associations between egg colour and parental characteristics, laying date, clutch size and laying order. We also analysed the possible correlations between egg size, yolk carotenoid and antibody levels and eggshell pigmentation. Our results revealed no significant relationships between egg colour and female age, morphological and serological variables. Blue-green colour intensity of eggs increased throughout the breeding season, which could be the result of either a proximate constraint or an adaptive strategy. We found a positive association between egg colour saturation and yolk lutein concentration. This relationship could be the result of the seasonal improvement of caterpillar supply, which could influence the deposition of both components into the egg. Furthermore, we found that females mated to lower-quality males produced eggs with higher biliverdin pigmentation. It is possible that deposition of biliverdin is correlated to some unmeasured aspect of egg quality that could enhance the viability of offspring of lower-quality fathers. We found that intensity of blue-green coloration increased with laying order between the first and fifth eggs.     

Sex-dependent risk taking in the collared flycatcher, Ficedula albicollis, when exposed to a predator at the nestling stage

An increased mortality rate is a cost of parental care, and can be high during the provisioning phase of altricial nestlings. When a parent stops feeding the nestlings temporarily after seeing a predator, it can reduce its own predation risk, but the suspension of parental care may also reduce its offspring's chances of surviving. We modelled this situation by exposing a stuffed sparrowhawk near collared flycatcher nests and removing it when both parents had seen it. We measured the time (return time) between the removal and when each parent entered the nestbox. The parents' risk taking and the return time are assumed to be inversely related. We studied which brood variables the parents take into account when deciding how much risk they are willing to take during the provisioning period. Males took more risk for older and better-quality nestlings and earlier broods. The females' behaviour was opposite to that of the males: they took significantly less risk for older and better-quality offspring and visited the nestbox later for earlier broods. The males' behaviour supported the reproductive value hypothesis, that risk taking is related to brood value and survival chances, whereas the females' behaviour supported the harm to offspring hypothesis, that risk taking is related to the broods' vulnerability. Copyright 2000 The Association for the Study of Animal Behaviour.     

Severe inbreeding depression in collared flycatchers (Ficedula albicollis)

The causes and magnitude of inbreeding depression are of considerable importance for a wide range of issues in evolutionary and conservation biology, but we have only a limited understanding of inbreeding depression in natural populations. Here, we present a study of inbreeding in a large wild population of collared flycatchers (Ficedula albicollis). Inbreeding was rare, to the extent that we detected only 1.04% of 2139 matings over 18 years that resulted in offspring with a non-zero inbreeding coefficient, f > 0. When it did occur, inbreeding caused a significant reduction in the egg-hatching rate, in fledgling skeletal size and in post-fledging juvenile survival, with the number of offspring being recruited to the breeding population from a nest of f = 0.25 being reduced by 94% relative to a non-inbred nest. A maximum-likelihood estimate of the number of lethal equivalents per gamete was very high at B = 7.47, indicating a substantial genetic load in this population. There was also a non-significant tendency for inbreeding depression to increase with the strength of selection on a trait. The probability of mating between close relatives (f = 0.25) increased throughout the breeding season, possibly reflecting increased costs of inbreeding avoidance. Our results illustrate how severe inbreeding depression and considerable genetic load may exist in natural populations, but detecting them may require extensive long-term datasets.     

Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome

Properly estimating genetic diversity in populations of nonmodel species requires a basic understanding of how diversity is distributed across the genome and among individuals. To this end, we analysed whole‐genome resequencing data from 20 collared flycatchers (genome size ≈1.1 Gb; 10.13 million single nucleotide polymorphisms detected). Genomewide nucleotide diversity was almost identical among individuals (mean = 0.00394, range = 0.00384–0.00401), but diversity levels varied extensively across the genome (95% confidence interval for 200‐kb windows = 0.0013–0.0053). Diversity was related to selective constraint such that in comparison with intergenic DNA, diversity at fourfold degenerate sites was reduced to 85%, 3′ UTRs to 82%, 5′ UTRs to 70% and nondegenerate sites to 12%. There was a strong positive correlation between diversity and chromosome size, probably driven by a higher density of targets for selection on smaller chromosomes increasing the diversity‐reducing effect of linked selection. Simulations exploring the ability of sequence data from a small number of genetic markers to capture the observed diversity clearly demonstrated that diversity estimation from finite sampling of such data is bound to be associated with large confidence intervals. Nevertheless, we show that precision in diversity estimation in large outbred population benefits from increasing the number of loci rather than the number of individuals. Simulations mimicking RAD sequencing showed that this approach gives accurate estimates of genomewide diversity. Based on the patterns of observed diversity and the performed simulations, we provide broad recommendations for how genetic diversity should be estimated in natural populations.     

Moderate heritability and low evolvability of sperm morphology in a species with high risk of sperm competition,the collared flycatcher Ficedula albicollis

Spermatozoa represent the morphologically most diverse type of animal cells and show remarkable variation in size across and also within species. To understand the evolution of this diversity, it is important to reveal to what degree this variation is genetic or environmental in origin and whether this depends on species’ life histories. Here we applied quantitative genetic methods to a pedigreed multigenerational data set of the collared flycatcher Ficedula albicollis, a passerine bird with high levels of extra‐pair paternity, to partition genetic and environmental sources of phenotypic variation in sperm dimensions for the first time in a natural population. Narrow‐sense heritability (h²) of total sperm length amounted to 0.44 ± 0.14 SE, whereas the corresponding figure for evolvability (estimated as coefficient of additive genetic variation, CV_a) was 0.02 ± 0.003 SE. We also found an increase in total sperm length within individual males between the arrival and nestling period. This seasonal variation may reflect constraints in the production of fully elongated spermatozoa shortly after arrival at the breeding grounds. There was no evidence of an effect of male age on sperm dimensions. In many previous studies on laboratory populations of several insect, mammal and avian species, heritabilities of sperm morphology were higher, whereas evolvabilities were similar. Explanations for the differences in heritability may include variation in the environment (laboratory vs. wild), intensity of sexual selection via sperm competition (high vs. low) and genetic architecture that involves unusual linkage disequilibrium coupled with overdominance in one of the studied species.     

Triparental care in the collared flycatcher (Ficedula albicollis): Cooperation of two females with a cuckolded male in rearing a brood

Certain predominant forms of mating and parental care systems are assumed in several model species among birds, but the opportunistic and apparently infrequent variations of “family structures” may often remain hidden due to methodological limitations with regard to genetic or behavioral observations. One of the intensively studied model species, the collared flycatcher (Ficedula albicollis), is usually characterized by social monogamy with polyterritorial, facultative social polygyny, and frequent extrapair mating and extrapair paternity. During a brood‐size manipulation experiment, we observed two females and a male delivering food at an enlarged brood. A combination of breeding phenology data (egg laying and hatching date), behavioral data (feeding rates) from video recordings at 10 days of nestling age, and microsatellite genotyping for maternity and paternity suggests a situation of an unrelated female helping a pair in chick rearing. Such observations highlight the relevance of using traditional techniques and genetic analyses together to assess the parental roles within a population, which becomes more important where individuals may dynamically switch from their main and presupposed roles according to the actual environmental conditions.     

Male-biased sex ratio among unhatched eggs in great tit Parus major, blue tit P. caeruleus and collared flycatcher Ficedula albicollis

An increasing number of studies have demonstrated that brood sex ratios are frequently unequal, but the proximate mechanisms underlying this deviation are largely unknown. In the current study we analysed deviation from expected 1:1 sex ratio among dead embryos from unhatched eggs collected from partially unhatched clutches of three passerine bird species. We showed that male embryos were significantly overrepresented among unhatched eggs of great tit Parus major , blue tit P. caeruleus and collared flycatcher Ficedula albicollis . Moreover, the bias in sex ratio differed among species and tended to differ among study years. We discuss several hypotheses to explain the observed male bias among unhatched eggs. We conclude that sex specific embryo mortality may contribute to explain the observed variation in sex ratios in several species of wild birds and that sexing unhatched eggs is important in studies of sex ratio allocation.     

Developmental plasticity in a passerine bird: an experiment with collared flycatchers Ficedula albicollis

Young birds often face poor food supply, which reduces their growth and development. However, if the shortage of resources is only temporary, there is a possibility to adjust the growth trajectory of morphological traits after the end of the short-term limitation period. The two main ways of compensatory growth are delayed development (parallel growth) and growth acceleration (catch-up growth). Parallel growth has been widely demonstrated in birds, but the presence of catch-up growth in altricial species has been questioned. However, most experiments have been conducted in laboratory conditions. We manipulated the food supply of nestling collared flycatchers Ficedula albicollis in the wild by removing the male parent for three days at 4–7 days of chick age. We performed early partial swapping to control for origin effects on growth, and total swapping after the period of food limitation to ensure similar late growth environment for deprived and control chicks. Both body mass and tarsus length of deprived chicks was negatively affected by the food scarcity. Body mass showed efficient catch-up growth, but this compensation was absent in skeletal size. Body mass is an important determinant of postfledging survival in this long-distance migrant. Further studies are needed in a variety of species to examine developmental plasticity in relation to age at food scarcity and the allocation hierarchy of various morphological traits.     

Inheritance of size and shape in a natural population of collared flycatchers,Ficedula albicollis

Four external skeletal and three feather dimensions were measured on adult collared flycatchers (Ficedula albicollis) and their adult offspring. By using mid-offspring-midparent regressions, all traits were found to be heritable with an arithmetic mean heritability of 0.46. Heritability estimates from full-sib analyses were about 1.5 times higher (mean 0.67), indicating that variation in traits was affected by shared nest environment among full-sibs. The overall body size as measured by principal component one (PC1) was found to be heritable (h² = 0.40). However, this multivariate measure of heritability was not significant in offspring-father comparison, while highly so in offspring-mother comparison (h² = 0.60). Low offspring-father resemblance was evident also in univariate estimates of heritability. Possible causes of this (extra-pair copulations, maternal effects, sex-linked variance) are discussed. Genetic correlations among seven traits were estimated to be low (mean 0.22), and of similar magnitude or higher than phenotypic correlations (mean 0.18). All genetic correlations were positive. Genetic and phenotypic correlations as well as covariances were fairly similar to each other (r = 0.85 and r = 0.87, respectively). Environmental correlations did not follow the pattern of genetic correlations (r = 0.11), but were more similar to phenotypic correlations (r = 0.60). Given the low genetic correlations and moderate heritabilities, the overall conclusion is that the external morphology of collared flycatchers is largely under additive genetic control and that there is a strong potential for evolutionary change in morphology even under complex multivariate selection.     

A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution

By taking advantage of a recently developed reference marker set for avian genome analysis we have constructed a gene-based genetic map of the collared flycatcher, an important "ecological model" for studies of life-history evolution, sexual selection, speciation, and quantitative genetics. A pedigree of 322 birds from a natural population was genotyped for 384 single nucleotide polymorphisms (SNPs) from 170 protein-coding genes and 71 microsatellites. Altogether, 147 gene markers and 64 microsatellites form 33 linkage groups with a total genetic distance of 1787 cM. Male recombination rates are, on average, 22% higher than female rates (total distance 1982 vs. 1627 cM). The ability to anchor the collared flycatcher map with the chicken genome via the gene-based SNPs revealed an extraordinary degree of both synteny and gene-order conservation during avian evolution. The great majority of chicken chromosomes correspond to a single linkage group in collared flycatchers, with only a few cases of inter- and intrachromosomal rearrangements. The rate of chromosomal diversification, fissions/fusions, and inversions combined is thus considerably lower in birds (0.05/MY) than in mammals (0.6-2.0/MY). A dearth of repeat elements, known to promote chromosomal breakage, in avian genomes may contribute to their stability. The degree of genome stability is likely to have important consequences for general evolutionary patterns and may explain, for example, the comparatively slow rate by which genetic incompatibility among lineages of birds evolves.     

Patterns of natural selection on morphology of male and female collared flycatchers (Ficedula albicollis)

Natural selection may act in different directions among years, life stages, or classes of individuals. Fluctuating selection of this kind is potentially an important mechanism by which additive genetic variation for quantitative traits is maintained, and can prevent populations reaching local adaptive peaks. We analysed natural selection acting on three morphological traits of male and female collared flycatchers via both fecundity and survival, using 15 years' data from a large isolated population on Godand, Sweden. We particularly investigated variation in the direction and magnitude of selection acting: (1) among years over the study period; (2) on different life stages and (3) the consistency of observed patterns of selection with sexual size dimorphism (SSD) in this population. We found little evidence of natural selection on these traits over the study period. Evidence for directional, stabilizing and disruptive selection was found for some year-trait combinations, but these patterns were inconsistent with respect to both the magnitude and form of selection found. Consequently, our results, based on the detailed analysis of natural selection in a large wild population over a period of 15 years, provide evidence for the common assumption that forces of selection acting on quantitative traits are generally weak. They are also consistent with the suggestion that environmental stability is an important determinant of the degree to which organisms fit their environment.     

A sexual conflict in collared flycatchers,Ficedula albicollis: early male moult reduces female fitness

A sexual conflict over levels of parental care occurs in most animals with biparental care, and studies of sexual differences in levels of parental care have usually focused on its intra-annual fitness consequences. We investigated inter-annual fitness consequences of a sexual difference in timing of feather replacement (moult) in collared flycatchers (Ficedula albicollis). In this study, males overlapped reproduction and moult more often than females, they also initiated their moult at an earlier stage of breeding than females. Females mated to males with a moult-breeding overlap had significantly lowered survival chances than females mated with males initiating moult after breeding. Furthermore, females mated with moulting males risked a lowered future fecundity in terms of a delayed start to breeding in the following season. However, early moulting males achieved a similar reproductive success as males initiating moult after breeding. Likewise, male survival probability to the following breeding season did not differ between early and late moulting individuals, nor was there any evidence that males gained or lost in future mating advantages by moulting early. These results show not only that a sexual conflict over timing of moult may operate, but also that it can impose severe fitness consequences, in terms of reduced future fecundity and survival probability, upon the ''losing'' sex.     

Male-male competition and parental care in collared flycatchers (Ficedula albicollis): an experiment controlling for differences in territory quality

Females are known to benefit from mate choice in several different ways but the relationship between these benefits has received little attention. The quality of resources provided by males, such as nest sites, and paternal care are often assumed to covary positively However, because the location of the nest affects the cost of parental care, these two benefits from mate choice can easily be confounded. To investigate the provisioning ability of successful competitors while controlling for differences in territory quality we removed early-settled pairs of collared flycatchers (Ficedula albicollis) and allowed replacement by later-arriving males or floaters (i.e.'poor competitors'). A control group of early-settled males (i.e. 'good competitors') had their females removed. Females paired to good competitors enjoyed a significantly higher reproductive success and tended to receive more parental assistance from their mates compared with females mated to poor competitors. Thus, some males seem able not only to compete successfully over resources but also to feed their offspring at a relatively higher rate. An alternative explanation, that poor competitors invested less in offspring quality in response to a lower share of paternity, could be rejected. The rate of extra-pair paternity did not differ between the two treatment groups. Our results suggest that male- male competition can sometimes facilitate female choice of superior care-givers. Thus, a female's benefit from choosing a competitive male may not be restricted to the quality of the resource he defends but can also include superior paternal care.