Glenn-Peter Sætre

Hybridization and adaptive mate choice in flycatchers

Hybridization in natural populations is strongly selected against when hybrid offspring have reduced fitness. Here we show that, paradoxically, pairing with another species may offer the best fitness return for an individual, despite reduced fitness of hybrid offspring. Two mechanisms reduce the costs to female collared flycatchers of pairing with male pied flycatchers. A large proportion of young are sired by conspecific male collared flycatchers through extra-pair copulations, and there is a bias in favour of male offspring (which, unlike females, are fertile) within hybrid pairs. In combination with temporal variation in breeding success, these cost-reducing mechanisms yield quantitative predictions about when female collared flycatchers should accept a male pied flycatcher as a mate; empirical data agree with these predictions. Apparent hybridization may thus represent adaptive mate choice under some circumstances.

Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome.

As a case study for single‐nucleotide polymorphism (SNP) identification in species for which little or no sequence information is available, we investigated several approaches to identifying SNPs in two passerine bird species: pied and collared flycatchers (Ficedula hypoleuca and F. albicollis). All approaches were successful in identifying sequence polymorphism and over 50 candidate SNPs per species were identified from ≈ 9.1 kb of sequence. In addition, 17 sites were identified in which the frequency of alternative bases differed by > 50% between species (termed interspecific SNPs). Interestingly, polymorphism of microsatellite/intron loci in the source species appeared to be a positive predictor of nucleotide diversity in homologous flycatcher sequences. The overall nucleotide diversity of flycatchers was 2.3–2.7 × 10−3, which is ≈ 3–6 times higher than observed in recent studies of human SNPs. Higher nucleotide diversity in the avian genome could be due to the relatively older age of flycatcher populations, compared with humans, and/or a higher long‐term effective population size.

Sex chromosome evolution and speciation in Ficedula flycatchers

Speciation is the combination of evolutionary processes that leads to the reproductive isolation of different populations. We investigate the significance of sex-chromosome evolution on the development of post–and prezygotic isolation in two naturally hybridizing Ficedula flycatcher species. Applying a tag–array–based mini–sequencing assay to genotype single nucleotide polymorphisms (SNPs) and interspecific substitutions, we demonstrate rather extensive hybridization and backcrossing in sympatry. However, gene flow across the partial postzygotic barrier (introgression) is almost exclusively restricted to autosomal loci, suggesting strong selection against introgression of sex–linked genes. In addition to this partial postzygotic barrier, character displacement of male plumage characteristics has previously been shown to reinforce prezygotic isolation in these birds. We show that male plumage traits involved in reinforcing prezygotic isolation are sex linked. These results suggest a major role of sex–chromosome evolution in mediating post–and prezygotic barriers to gene flow and point to a causal link in the development of the two forms of reproductive isolation.

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.

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 Öland 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 Öland) 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.

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.

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.