Ecological character displacement in the face of gene flow: Evidence from two species of nightingales

<p>Abstract</p> <p>Background</p> <p>Ecological character displacement is a process of phenotypic differentiation of sympatric populations caused by interspecific competition. Such differentiation could facilitate speciation by enhancing reproductive isolation between incipient species, although empirical evidence for it at early stages of divergence when gene flow still occurs between the species is relatively scarce. Here we studied patterns of morphological variation in sympatric and allopatric populations of two hybridizing species of birds, the Common Nightingale (<it>Luscinia megarhynchos</it>) and the Thrush Nightingale (<it>L. luscinia</it>).</p> <p>Results</p> <p>We conducted principal component (PC) analysis of morphological traits and found that nightingale species converged in overall body size (PC1) and diverged in relative bill size (PC3) in sympatry. Closer analysis of morphological variation along geographical gradients revealed that the convergence in body size can be attributed largely to increasing body size with increasing latitude, a phenomenon known as Bergmann's rule. In contrast, interspecific interactions contributed significantly to the observed divergence in relative bill size, even after controlling for the effects of geographical gradients. We suggest that the divergence in bill size most likely reflects segregation of feeding niches between the species in sympatry.</p> <p>Conclusions</p> <p>Our results suggest that interspecific competition for food resources can drive species divergence even in the face of ongoing hybridization. Such divergence may enhance reproductive isolation between the species and thus contribute to speciation.</p

Vocal Communications and the Maintenance of Population Specific Songs in a Contact Zone

Bird song has been hypothesized to play a role in several important aspects of the biology of songbirds, including the generation of taxonomic diversity by speciation; however, the role that song plays in speciation within this group may be dependent upon the ability of populations to maintain population specific songs or calls in the face of gene flow and external cultural influences. Here, in an exploratory study, we construct a spatially explicit model of population movement to examine the consequences of secondary contact of populations singing distinct songs. We concentrate on two broad questions: 1) will population specific songs be maintained in a contact zone or will they be replaced by shared song, and 2) what spatial patterns in the distribution of songs may result from contact? We examine the effects of multiple factors including song-based mating preferences and movement probabilities, oblique versus paternal learning of song, and both cultural and genetic mutations. We find a variety of conditions under which population specific songs can be maintained, particularly when females have preferences for their population specific songs, and we document many distinct patterns of song distribution within the contact zone, including clines, banding, and mosaics

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

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

Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers

Interbreeding between species (hybridization) typically produces unfit offspring. Reduced hybridization should therefore be favored by natural selection. However, this is difficult to accomplish because hybridization also sets the stage for genetic recombination to dissociate species-specific traits from the preferences for them. Here we show that this association is maintained by physical linkage (on the same chromosome) in two hybridizing Ficedula flycatchers. By analyzing the mating patterns of female hybrids and cross-fostered offspring, we demonstrate that species recognition is inherited on the Z chromosome, which is also the known location of species-specific male plumage traits and genes causing low hybrid fitness. Limited recombination on the Z chromosome maintains associations of Z-linked genes despite hybridization, suggesting that the sex chromosomes may be a hotspot for adaptive speciation.

Sex chromosome-linked species recognition and evolution of reproductive isolation in flycatchers

Interbreeding between species (hybridization) typically produces unfit offspring. Reduced hybridization should therefore be favored by natural selection. However, this is difficult to accomplish because hybridization also sets the stage for genetic recombination to dissociate species-specific traits from the preferences for them. Here we show that this association is maintained by physical linkage (on the same chromosome) in two hybridizing Ficedula flycatchers. By analyzing the mating patterns of female hybrids and cross-fostered offspring, we demonstrate that species recognition is inherited on the Z chromosome, which is also the known location of species-specific male plumage traits and genes causing low hybrid fitness. Limited recombination on the Z chromosome maintains associations of Z-linked genes despite hybridization, suggesting that the sex chromosomes may be a hotspot for adaptive speciation