Flycatcher song in allopatry and sympatry--convergence, divergence and reinforcement

The theory of reinforcement predicts that natural selection against the production of unfit hybrids favours traits that increase assortative mating. Whether culturally inherited traits, such as bird song, can increase assortative mating by reinforcement is largely unknown. We compared songs of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) from two hybrid zones of different ages with songs from allopatric populations. Previously, a character divergence in male plumage traits has been shown to reinforce premating isolation in sympatric flycatchers. In contrast, we find that the song of the pied flycatcher has converged towards that of the collared flycatcher (mixed singing). However, a corresponding divergence in the collared flycatcher shows that the species differences in song characters are maintained in sympatry. Genetic analyses suggest that mixed song is not caused by introgression from the collared flycatcher, but rather due to heterospecific copying. Circumstantial evidence suggests that mixed song may increase the rate of maladaptive hybridization. In the oldest hybrid zone where reinforcement on plumage traits is most pronounced, the frequency of mixed singing and hybridization is also lowest. Thus, we suggest that reinforcement has reduced the frequency of mixed singing in the pied flycatcher and caused a divergence in the song of the collared flycatcher. Whether a culturally inherited trait promotes or opposes speciation in sympatry may depend on its plasticity. The degree of plasticity may be genetically determined and accordingly under selection by reinforcement.     

Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.     

Reproductive character displacement of female,but not male song discrimination in an avian hybrid zone

Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co‐occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of Öland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on Öland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co‐occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.     

Combined effects of interspecific competition and hybridization impede local coexistence of Ficedula flycatchers

At secondary contact closely related species may both compete over similar resources and/or hybridize. Simulation models suggest that hybridization increases the risk of extinction beyond the risk resulting from interspecific competition alone, but such combined effects are rarely studied empirically. Here, we use detailed records on pairing patterns, breeding success, local recruitment and immigration collected during 8?years (2002–2009) to investigate the underlying mechanism of the rapid displacement of pied flycatchers by collared flycatchers on the Swedish island of ?land. We found no differences in average reproductive success or reproductive lifespan between the two species. However, we show that young male pied flycatchers failed to establish new territories as the density of male collared flycatchers increased. In addition, as the relative frequency of collared flycatchers increased, the risk of hybridization dramatically increased for female pied flycatchers, which speeds up the exclusion process since there is a high fitness cost associated with hybridization between the two species. In a nearby control area, within the same island, where pied flycatchers breed in the absence of collared flycatchers, no decline in the number of breeding pairs was observed during the same period of time. Our results demonstrate the crucial importance of studying the combined effects of various types of heterospecific interactions to understand and predict the ecological and evolutionary implications of secondary contact between congeneric species. These findings are particularly interesting in the light of recent climate change since the expected range shifts of many taxa will increase competitive and sexual interactions between previously separated species.     

Vocal Plasticity – are Pied Flycatchers,Ficedula Hypoleuca,Open‐Ended Learners?

In some songbird species, large song repertoires are advantageous in female attraction, whereas song sharing with neighbours may give an advantage in male–male competition. Open‐ended learners, with the ability to memorize new song elements throughout their lives, may learn from territorial neighbours and thus benefit from increasing both repertoire size and song sharing. A distinction needs to be made between true adult song learning, i.e. memorization of novel song elements, and vocal plasticity resulting in changes in the use of previously memorized elements, such as the use of hidden repertoires or increased production of previously rare syllable types. We assessed the ability of adult pied flycatcher Ficedula hypoleuca males to learn previously unheard song elements and to change their song production in response to playback of unfamiliar, conspecific song, emulating a singing neighbour. After a 1‐week playback treatment, three out of 20 subjects had learned foreign song elements, providing evidence from the wild that pied flycatchers are true open‐ended learners. However, the syllable sharing with the playback stimulus repertoires had not changed, and the males’ repertoires had decreased rather than increased. Hence, we did not find support for increased syllable sharing with neighbours or increased repertoire size as functions of adult song learning in pied flycatchers. Because pied flycatcher song seems to serve mainly for mate attraction, copying of attractive syllable types is a possible alternative function of adult song learning in this species.     

Amount of introgression in flycatcher hybrid zones reflects regional differences in pre and post-zygotic barriers to gene exchange

Introgression is the incorporation of alleles from one species or semispecies into the gene pool of another through hybridization and backcrossing. The rate at which this occurs depends on the frequency of hybridization and the fitness of hybrids and backcrosses compared to 'pure' individuals. The collared flycatcher (Ficedula albicollis) and the pied flycatcher (F. hypoleuca) co-exist and hybridize at low to moderate frequencies in a clinal hybrid zone in Central Europe and on the islands of Gotland and Oland off the Swedish east coast. Data on hatching success suggest that hybrids are less fertile in Central Europe compared to on the islands. Direct fitness estimates using molecular markers to infer paternity are consistent with the demographic data. Applying a tag-array-based minisequencing assay to genotype interspecific substitutions and single nucleotide polymorphisms we demonstrate that the amount of introgression from the pied to the collared flycatcher is higher in the two island populations (Gotland and Oland) than in two geographically distinct areas from the Central European hybrid zone (Czech Republic and Hungary). In all areas the amount of introgression from collared to pied flycatchers is very low or seemingly absent. The different patterns of introgression are consistent with regional differences in rates of hybridization and fitness of hybrids. We suggest that barriers to gene exchange may have been partly broken down on the islands due to asymmetric gene flow from allopatry. Alternatively, or in addition, more pronounced reinforcement of prezygotic isolation in Central Europe might have increased post-zygotic isolation through hitchhiking, since genes affecting pre and post-zygotic isolation are both sex-linked in these birds. One of our genetic markers appears to introgress from pied to collared flycatchers at a much higher rate than the other markers. We discuss the possibility that the introgressed marker may be linked to a gene which is under positive selection in the novel genetic background.     

Females discriminate against heterospecific sperm in a natural hybrid zone

When hybridization is maladaptive, species‐specific mate preferences are selectively favored, but low mate availability may constrain species‐assortative pairing. Females paired to heterospecifics may then benefit by copulating with multiple males and subsequently favoring sperm of conspecifics. Whether such mechanisms for biasing paternity toward conspecifics act as important reproductive barriers in socially monogamous vertebrate species remains to be determined. We use a combination of long‐term breeding records from a natural hybrid zone between collared and pied flycatchers (Ficedula albicollis and F. hypoleuca), and an in vitro experiment comparing conspecific and heterospecific sperm performance in female reproductive tract fluid, to evaluate the potential significance of female cryptic choice. We show that the females most at risk of hybridizing (pied flycatchers) frequently copulate with multiple males and are able to inhibit heterospecific sperm performance. The negative effect on heterospecific sperm performance was strongest in pied flycatcher females that were most likely to have been previously exposed to collared flycatcher sperm. We thus demonstrate that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate. While the evolutionary history of this barrier is unknown, our results imply that there is opportunity for it to be accentuated via a reinforcement‐like process.     

Malaria infections reinforce competitive asymmetry between two Ficedula flycatchers in a recent contact zone

Parasites may influence the outcome of interspecific competition between closely related host species through lower parasite virulence in the host with which they share the longer evolutionary history. We tested this idea by comparing the prevalence of avian malaria (Haemosporidia) lineages and their association with survival in pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breeding in a recent contact zone on the Swedish island of Öland. A nested PCR protocol amplifying haemosporidian fragments of mtDNA was used to screen the presence of malaria lineages in 1048 blood samples collected during 6 years. Competitively inferior pied flycatchers had a higher prevalence of blood parasites, including the lineages that were shared between the two flycatcher species. Multistate mark–recapture models revealed a lower survival of infected versus uninfected female pied flycatchers, while no such effects were detected in male pied flycatchers or in collared flycatchers of either sex. Our results show that a comparatively new host, the collared flycatcher, appears to be less susceptible to a local northern European malarial lineage where the collared flycatchers have recently expanded their distribution. Pied flycatchers experience strong reproductive interference from collared flycatchers, and the additional impact of species‐specific blood parasite effects adds to this competitive exclusion. These results support the idea that parasites can strongly influence the outcome of interspecific competition between closely related host species, but that the invading species need not necessarily be more susceptible to local parasites.     

Hybridization cost of delayed maturation of secondary sexual traits in the collared flycatcher

In many species, individuals do not attain their full adult coloration until one or several years after reaching sexual maturity, and this signaling of juvenile status is thought to enable young individuals to avoid aggression from older, dominant conspecifics. We propose that hybridization may be one of several costs and benefits associated with such delayed maturation. We tested this idea in a hybrid zone of collared (Ficedula albicollis) and pied (F. hypoleuca) flycatchers on the Baltic islands of Oland and Gotland. One-year-old (subadult) male collared flycatchers differed from older birds in many plumage traits, and approached male pied flycatchers in phenotype. On both islands, subadult male collared flycatchers hybridized at a higher rate than adults. Mate-choice experiments in aviaries suggest that this difference is at least partly due to female pied flycatchers having a preference for subadults when constrained to choose a heterospecific mate. Because novel morphologies are often derived from changes in ontology, juvenile forms may resemble adults of closely related taxa. When such juveniles are reproductively mature, their phenotypic similarity to the adults of closely related species may increase their risk of hybridization.     

Heterospecific female mimicry in Ficedula flycatchers

Mimicry is a widespread phenomenon. Vertebrate visual mimicry often operates in an intraspecific sexual context, with some males resembling conspecific females. Pied flycatcher (Ficedula hypoleuca) dorsal plumage varies from the ancestral black to female‐like brown. Experimental studies have shown that conspecific and heterospecific (collared flycatcher, F. albicollis) individuals of both sexes respond, at least initially, to brown individuals as if they were female. We quantified the perceptual and biochemical differences between brown feathers and found that brown pied flycatcher males are indistinguishable from heterospecific, but not from conspecific, females in both aspects. To our knowledge, this is the first evidence of a visual mimetic signalling system in a sexual context where the model is heterospecific to the mimic. By only mimicking heterospecific females, brown pied flycatcher males can establish territories next to the more dominant collared flycatcher in sympatry, suffer less aggression by darker conspecifics in allopatry and preserve within‐species sexual recognition throughout the breeding range. A closer look at the evolutionary history and ecology of these two species illustrates how such a mimetic system can evolve. Although likely rare, this phenomenon might not be unique to Ficedula flycatchers.     

Can environmental fluctuation prevent competitive exclusion in sympatric flycatchers?

Ecology has been characterized by a central controversy for decades: namely, whether the distribution and abundance of organisms are determined by species interactions, such as competitive exclusion, or by environmental conditions. In part, this is because competitive exclusion has not been convincingly demonstrated in open, natural systems. In addition, traditional theoretical models cannot predict the outcome of competitive interactions in the presence of environmental variability. In this paper we document the limiting influence of strong interspecific competition on population dynamics and nestling mortality in a mixed population of pied flycatchers (Ficedula hypoleuca) and collared flycatchers (F. albicollis in a narrow zone of sympatry. Whereas the former species was limited mainly by interspecific competition, the latter species was limited by the concerted influences of intraspecific competition and climate. The analysis suggests a march towards competitive exclusion of the pied flycatcher during warm periods. However, competitive exclusion is apparently prohibited on a local scale because intraspecific competition among individual collared flycatchers intensifies when they are forced to cope with severe environmental conditions, promoting the temporary and local presence of pied flycatchers.     

POPULATION DIVERGENCE IN SEXUAL ORNAMENTS: THE WHITE FOREHEAD PATCH OF NORWEGIAN PIED FLYCATCHERS IS SMALL AND UNSEXY

Models of sexual selection suggest that populations may easily diverge in male secondary sexual characters. Studies of a Spanish population of the pied flycatcher, Ficedula hypoleuca, and a Swedish population of the closely related collared flycatcher, F. albicollis, have indicated that the white forehead patch of males is a sexually selected trait. We studied the white forehead patch of male pied flycatchers (n = 487) in a Norwegian population over seven years. Males with large forehead patches were in general more brightly colored, but patch height was not correlated to body mass, body size, or parasite loads. Conditions during the nestling period did not seem to influence patch height as an adult. Patch height increased slightly from the first to the second year as adults, but then remained relatively constant at higher ages. Patch height was not related to survival. Year-to-year changes showed that males who increased in patch height also increased in body mass, suggesting that expression of the forehead patch may be partly condition dependent. However, changes in body mass explained only a small proportion of the variance in patch height between males. Thus, patch height would not be a good indicator of male quality. Furthermore, patch size was also not related to male ability to feed nestlings, indicating that females would not obtain direct benefits by choosing males with large patches. However, patch height could be a Fisher trait, but this requires heritability and there was no significant father-son resemblance in patch height. Comparisons of the males visited by each female during the mate sampling period indicated that chosen males did not have larger forehead patches than rejected males. Experimental manipulation of patch height did not affect male mating success. These results indicate that females do not use patch size as a mate choice cue. Finally, patch height did not predict the outcome of male contests for nestboxes, suggesting that the forehead patch is not an intrasexually selected cue of status. Norwegian pied flycatchers have smaller forehead patches than both Spanish pied flycatchers and Swedish collared flycatchers. We suggest that this pattern may be explained by the lack of sexual selection on the forehead patch in the Norwegian population as compared to the other populations, where the patch is apparently sexually selected. We discuss possible reasons for these population divergences, such as female choice on an alternative secondary sexual character (general plumage color) and speciation among Ficedula flycatchers.     

Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species

In geographic areas where pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breed in sympatry, hybridization occurs, leading to gene flow (introgression) between the two recently diverged species. Notably, while such introgression is observable at autosomal loci it is apparently absent at the Z chromosome, suggesting an important role for genes on the Z chromosome in creating reproductive isolation during speciation. To further understand the role of Z-linked loci in the formation of new species, we studied genetic variation of the two species from regions where they live in allopatry. We analyzed patterns of polymorphism and divergence in introns from 9 Z-linked and 23 autosomal genes in pied and collared flycatcher males. Average variation on the Z chromosome is greatly reduced compared to neutral expectations based on autosomal diversity in both species. We also observe significant heterogeneity between patterns of polymorphism and divergence at Z-linked loci and a relative absence of polymorphisms that are shared by the two species on the Z chromosome compared to the autosomes. We suggest that these observations may indicate the action of recurrent selective sweeps on the Z chromosome during the evolution of the two species, which may be caused by sexual selection acting on Z-linked genes. Alternatively, reduced variation on the Z chromosome could result from substantially higher levels of introgression at autosomal than at Z-linked loci or from a complex demographic history, such as a population bottleneck.     

Natural and sexual selection against hybrid flycatchers

While sexual selection is generally assumed to quickly cause or strengthen prezygotic barriers between sister species, its role in causing postzygotic isolation, through the unattractiveness of intermediate hybrids, is less often examined. Combining 24 years of pedigree data and recently developed species-specific molecular markers from collared (Ficedula albicollis) and pied (Ficedula hypoleuca) flycatchers and their hybrids, we were able to quantify all key components of fitness. To disentangle the relative role of natural and sexual selection acting on F1 hybrid flycatchers, we estimated various fitness components, which when combined represent the total lifetime reproductive success of F1 hybrids, and then compared the different fitness components of F1 hybrids to that of collared flycatchers. Female hybrid flycatchers are sterile, with natural selection being the selective force involved, but male hybrids mainly experienced a reduction in fitness through sexual selection (decreased pairing success and increased rate of being cuckolded). To disentangle the role of sexual selection against male hybrids from a possible effect of genetic incompatibility (on the rate of being cuckolded), we compared male hybrids with pure-bred males expressing intermediate plumage characters. Given that sexual selection against male hybrids is a result of their intermediate plumage, we expect these two groups of males to have a similar fitness reduction. Alternatively, hybrids have reduced fitness owing to genetic incompatibility, in which case their fitness should be lower than that of the intermediate pure-bred males. We conclude that sexual selection against male hybrids accounts for approximately 75% of the reduction in their fitness. We discuss how natural and sexual selection against hybrids may have different implications for speciation and conclude that reinforcement of reproductive barriers may be more likely when there is sexual selection against hybrids.     

A HIGH‐DENSITY SCAN OF THE Z CHROMOSOME IN FICEDULA FLYCATCHERS REVEALS CANDIDATE LOCI FOR DIVERSIFYING SELECTION

Theoretical and empirical data suggest that genes located on sex chromosomes may play an important role both for sexually selected traits and for traits involved in the build‐up of hybrid incompatibilities. We investigated patterns of genetic variation in 73 genes located on the Z chromosomes of two species of the flycatcher genus Ficedula, the pied flycatcher and the collared flycatcher. Sequence data were evaluated for signs of selection potentially related to genomic differentiation in these young sister species, which hybridize despite reduced fitness of hybrids. Seven loci were significantly more divergent between the two species than expected under neutrality and they also displayed reduced nucleotide diversity, consistent with having been influenced by directional selection. Two of the detected candidate regions contain genes that are associated with plumage coloration in birds. Plumage characteristics play an important role in species recognition in these flycatchers suggesting that the detected genes may have been involved in the evolution of sexual isolation between the species.     

Speciation, introgressive hybridization and nonlinear rate of molecular evolution in flycatchers

Evolutionary history of Muscicapidae flycatchers is inferred from nuclear and mitochondrial DNA (mtDNA) sequence comparisons and population genetic analysis of nuclear and mtDNA markers. Phylogenetic reconstruction based on sequences from the two genomes yielded similar trees with respect to the order at which the species split off. However, the genetic distances fitted a nonlinear, polynomial model reflecting diminishing divergence rate of the mtDNA sequences compared to the nuclear DNA sequences. This could be explained by Haldane's rule because genetic isolation might evolve more rapidly on the mitochondrial rather than the nuclear genome in birds. This is because hybrid sterility of the heterogametic sex (females) would predate that of the homogametic sex (males), leading to sex biased introgression of nuclear genes. Analyses of present hybrid zones of pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) may indicate a slight sexual bias in rate of introgression, but the introgression rates were too low to allow proper statistical analyses. It is suggested, however, that the observed deviation from linearity can be explained by a more rapid mutational saturation of the mtDNA sequences than of the nuclear DNA sequences, as supported by analyses of third codon position transversions at two protein coding mtDNA genes. A phylogeographic scenario for the black and white flycatcher species is suggested based on interpretation of the genetic data obtained. Four species appear to have diverged from a common ancestor relatively simultaneously during the Pleistocene. After the last glaciation period, pied and collared flycatchers expanded their breeding ranges and eventually came into secondary contact in Central and Eastern Europe and on the Baltic Isles.     

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 Q _ST ( P _ST)– F _ST 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 ( P _ST) and neutral genetic distances ( F _ST) 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.     

Age-Dependent Expression of Song in the Collared Flycatcher, Ficedula albicollis

Theory suggests that male ornaments should be reliable signals of age, with more elaborated ornaments reflecting superior quality in terms of experience and/or viability. Bird song is immensely involved in sexual selection, thus not‐surprisingly, it usually shows age‐dependent variation. Although the collared flycatcher Ficedula albicollis has been intensively studied for its sexual traits, and female preference for male age is expected to be strong, there is no quantitative information on age‐dependent expression of song in this species. Here, we fill this gap and, based on phenotypic correlations, we report the relationship between age and several song features. Repertoire size was consistently smaller in yearlings than in older males, but it also tended to increase after the second year of breeding. In a meta‐analysis of effect sizes using data from the literature, we found that the strength of the relationship between age and repertoire size in the collared flycatcher is similar to patterns observed in other passerines. Song rate was inversely related to age, as yearlings sang at higher rates than older males. Generally, effect sizes for the relationship between age and other song traits were of medium level on average, and had broad confidence intervals. Song traits covaried with survival in a direction suggesting that differences in song between age categories are unlikely to result from phenotype dependent survival. Our results generally support the hypothesis that song holds the potential to function as a reliable indicator of male age in the collared flycatcher. However, it seems that not all song traits are unambiguously more expressed in older males than in yearlings.     

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 (P_ST) was higher than that in neutral genetic markers (F_ST), 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.     

Difference in plasticity of resting metabolic rate – the proximate explanation to different niche breadth in sympatric Ficedula flycatchers

Variation in relative fitness of competing recently formed species across heterogeneous environments promotes coexistence. However, the physiological traits mediating such variation in relative fitness have rarely been identified. Resting metabolic rate (RMR) is tightly associated with life history strategies, thermoregulation, diet use, and inhabited latitude and could therefore moderate differences in fitness responses to fluctuations in local environments, particularly when species have adapted to different climates in allopatry. We work in a long‐term study of collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca) in a recent hybrid zone located on the Swedish island of Öland in the Baltic Sea. Here, we explore whether differences in RMR match changes in relative performance of growing flycatcher nestlings across environmental conditions using an experimental approach. The fitness of pied flycatchers has previously been shown to be less sensitive to the mismatch between the peak in food abundance and nestling growth among late breeders. Here, we find that pied flycatcher nestlings have lower RMR in response to higher ambient temperatures (associated with low food availability). We also find that experimentally relaxed nestling competition is associated with an increased RMR in this species. In contrast, collared flycatcher nestlings did not vary their RMR in response to these environmental factors. Our results suggest that a more flexible nestling RMR in pied flycatchers is responsible for the better adaptation of pied flycatchers to the typical seasonal changes in food availability experienced in this hybrid zone. Generally, subtle physiological differences that have evolved when species were in allopatry may play an important role to patterns of competition, coexistence, or displacements between closely related species in secondary contact.