Song similarity predicts hybridization in flycatchers.

Given that population divergence in sexual signals is an important prerequisite for reproductive isolation, a key prediction is that cases of signal convergence should lead to hybridization. However, empirical studies that quantitatively demonstrate links between phenotypic characters of individuals and their likelihood to hybridize are rare. Here we show that song convergence between sympatric pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) influence social and sexual interactions between the two species. In sympatry, the majority of male pied flycatchers (65%) include various parts of collared flycatcher song in their song repertoire (but not vice versa). Playback experiments on male interactions demonstrate that male collared flycatchers respond similarly to this 'mixed' song as to conspecific song. Long-term data on pairing patterns show that males singing a converged song attract females of the other species: female collared flycatchers only pair with male pied flycatchers if the males sing the mixed song type. From the perspective of a male pied flycatcher, singing a mixed song type is associated with 30% likelihood of hybridization. This result, combined with our estimates of the frequency of mixed singers, accurately predicts the observed occurrence of hybridization among male pied flycatchers in our study populations (20.45% of 484 pairs; predicted 19.5%). Our results support the suggestion that song functions as the most important prezygotic isolation mechanism in many birds.

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.

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.

Discrepancies in population differentiation at microsatellites, mitochondrial DNA and plumage colour in the pied flycatcher--inferring evolutionary processes.

Genetic differentiation between three populations of the pied flycatcher Ficedula hypoleuca (Norway, Czech Republic and Spain, respectively) was investigated at microsatellite loci and mitochondrial DNA (mtDNA) sequences and compared with the pattern of differentiation of male plumage colour. The Czech population lives sympatrically with the closely related collared flycatcher (F. albicollis) whereas the other two are allopatric. Allopatric populations are on average more conspicuously coloured than sympatric ones, a pattern that has been explained by sexual selection for conspicuous colour in allopatry and a character displacement on breeding plumage colour in sympatry that reduces the rate of hybridization with the collared flycatcher. The Czech population was genetically indistinguishable from the Norwegian population at microsatellite loci and mtDNA sequences. Recent isolation and/or gene flow may explain the lack of genetic differentiation. Accordingly, different selection on plumage colour in the two populations is either sufficiently strong so that gene flow has little impact on the pattern of colour variation, or differentiation of plumage colour occurred so recently that the (presumably) neutral, fast evolving markers employed here are unable to reflect the differentiation. Genetically, the Spanish population was significantly differentiated from the other populations, but the divergence was much more pronounced at mtDNA compared to microsatellites. This may reflect increased rate of differentiation by genetic drift at the mitochondrial, compared with the nuclear genome, caused by the smaller effective population size of the former genome. In accordance with this interpretation, a genetic pattern consistent with effects of small population size in the Spanish population (genetic drift and inbreeding) were also apparent at the microsatellites, namely reduced allelic diversity and heterozygous deficiency.