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A major aim of evolutionary biology is to understand why patterns of genomic diversity vary within taxa and space. Large-scale genomic studies of widespread species are useful for studying how environment and demography shape patterns of genomic divergence. Here, we describe one of the most geographically comprehensive surveys of genomic variation in a wild vertebrate to date; the great tit (Parus major) HapMap project. We screened ca 500,000 SNP markers across 647 individuals from 29 populations, spanning ~30 degrees of latitude and 40 degrees of longitude - almost the entire geographical range of the European subspecies. Genome-wide variation was consistent with a recent colonisation across Europe from a South-East European refugium, with bottlenecks and reduced genetic diversity in island populations. Differentiation across the genome was highly heterogeneous, with clear 'islands of differentiation', even among populations with very low levels of genome-wide differentiation. Low local recombination rates were a strong predictor of high local genomic differentiation (F ST ), especially in island and peripheral mainland populations, suggesting that the interplay between genetic drift and recombination causes highly heterogeneous differentiation landscapes. We also detected genomic outlier regions that were confined to one or more peripheral great tit populations, probably as a result of recent directional selection at the species' range edges. Haplotype-based measures of selection were related to recombination rate, albeit less strongly, and highlighted population-specific sweeps that likely resulted from positive selection. Our study highlights how comprehensive screens of genomic variation in wild organisms can provide unique insights into spatio-temporal evolutionary dynamics., (© 2024 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.)

The great reed warbler has two genetically distinguishable haplogroups: "Clade A" occurs in higher proportions in Western Europe and Kazakhstan, and colonised Europe and Asia from a refugium in South-West Europe; and "Clade B", which is more common in Eastern Europe, and colonised parts of Europe from a refugium in the Middle East. Our aims were (i) to analyse the rate of differentiation in Hungarian breeding populations in order to see whether European-scale pattern is visible or not on as a small scale as the territory of Hungary and (ii) to compare the results obtained with mtDNA sequencing and microsatellite markers. To analyse the genetic differentiation, the mtDNA control region II was sequenced in 68 adult breeding birds, and 51 were fingerprinted at 11 microsatellite loci, while both analyses were performed on 36 birds (a total of 83 birds). The microsatellite data gave a better resolution and represented the fine-scale pattern of the suspected recolonisation. The lack of genetic differentiation among the breeding populations based on mitochondrial data seems to support this finding, because the admixture of the clades in this particular geographic region obliterates differentiation. Accordingly, the F st values from different branches are significantly based on microsatellite data only. The mtDNA methods only give reliable results when a geographic and ecological factor plays a role in the population subdivision, but in the case of an intermixing population larger-scale studies are needed., (© 2022. Akadémiai Kiadó Zrt.)

The Mediterranean Basin represents a Global Biodiversity Hotspot where many organisms show high inter- and intraspecific differentiation. Extant phylogeographic patterns of terrestrial circum-Mediterranean faunas were mainly shaped through Pleistocene range shifts and range fragmentations due to retreat into different glacial refugia. Thus, several extant Mediterranean bird species have diversified by surviving glaciations in different hospitable refugia and subsequently expanded their distribution ranges during the Holocene. Such a scenario was also suggested for the Eurasian Wren (Nannus troglodytes) despite the lack of genetic data for most Mediterranean subspecies. Our phylogenetic multi-locus analysis comprised 18 out of 28 currently accepted subspecies of N. troglodytes, including all but one subspecies which are present in the Mediterranean Basin. The resulting phylogenetic reconstruction dated the onset of the entire Holarctic radiation of three Nannus species to the early Pleistocene. In the Eurasian Wren, two North African subspecies represented separate basal lineages from the Maghreb (N. t. kabylorum) and from the Libyan Cyrenaica (N. t. juniperi), being only distantly related to other Mediterranean populations. Although N. troglodytes appeared to be paraphyletic with respect to the Nearctic Winter Wren (N. hiemalis), respective nodes did not receive strong statistical support. In contrast, paraphyly of the Ibero-Maghrebian taxon N. t. kabylorum was strongly supported. Southern Iberian populations of N. t. kabylorum did not clade with Maghrebian populations of the same subspecies but formed a sister clade to a highly diverse European clade (including nominate N. t. troglodytes and eight further taxa). In accordance with a pattern also found in other birds, Eurasian populations were split into a western clade (Europe, Caucasus) and an eastern clade (Central Asia, Sino-Himalayas, East Asia). This complex phylogeographic pattern revealed cryptic diversification in N. troglodytes, especially in the Iberio-Maghrebian region., Competing Interests: The authors have declared that no competing interests exist.

Detecting positive selection using genomic data is critical to understanding the role of adaptive evolution. Of particular interest in this context is sex chromosomes since they are thought to play a special role in local adaptation and speciation. We sought to circumvent the challenges associated with statistical phasing when using haplotype-based statistics in sweep scans by benefitting from that whole chromosome haplotypes of the sex chromosomes can be obtained by resequencing of individuals of the hemizygous sex. We analyzed whole Z chromosome haplotypes from 100 females from several populations of four black and white flycatcher species (in birds, females are ZW and males ZZ). Based on integrated haplotype score (iHS) and number of segregating sites by length (nSL) statistics, we found strong and frequent haplotype structure in several regions of the Z chromosome in each species. Most of these sweep signals were population-specific, with essentially no evidence for regions under selection shared among species. Some completed sweeps were revealed by the cross-population extended haplotype homozygosity (XP-EHH) statistic. Importantly, by using statistically phased Z chromosome data from resequencing of males, we failed to recover the signals of selection detected in analyses based on whole chromosome haplotypes from females; instead, what likely represent false signals of selection were frequently seen. This highlights the power issues in statistical phasing and cautions against conclusions from selection scans using such data. The detection of frequent selective sweeps on the avian Z chromosome supports a large role of sex chromosomes in adaptive evolution., (© 2019 The Authors. Molecular Ecology Published by John Wiley & Sons Ltd.)

Hewitt's paradigm for effects of Pleistocene glaciations on European populations assumes their isolation in peninsular refugia during glacial maxima, followed by re-colonization of broader Europe during interstadials. This paradigm is well supported by studies of poorly dispersing taxa, but highly dispersive birds have not been included. To test this paradigm, we use the dunnock ( Prunella modularis ), a Western Palaearctic endemic whose range includes all major European refugia. MtDNA gene tree, multilocus species tree and species delimitation analyses indicate the presence of three distinct lineages: one in the Iberian refugium, one in the Caucasus refugium, and one comprising the Italian and Balkan refugia and broader Europe. Our gene flow analysis suggests isolation of both the Iberian and Caucasus lineages but extensive exchange between Italy, the Balkans and broader Europe. Demographic stability could not be rejected for any refugial population, except the very recent expansion in the Caucasus. By contrast, northern European populations may have experienced two expansion periods. Iberia and Caucasus had much smaller historical populations than other populations. Although our results support the paradigm, in general, they also suggest that in highly dispersive taxa, isolation of neighbouring refugia was incomplete, resulting in large super-refugial populations., (© 2018 The Author(s).)

It is important to identify the factors that affect the evolutionary potential of populations to respond to environmental changes. Such processes are for example the ones affecting the amount of heritable phenotypic variation in a population. We examined factors explaining the wide phenotypic variation in the genetically determined black-brown dorsal colouration of male pied flycatchers (Ficedula hypoleuca) during a period of >50 years in a northern European breeding population. We demonstrate that the temperature-dependent relative breeding success of brown males predicts the inter-annual change in the proportion of the brown male phenotype. The proportion of brown males also appears to reflect immigration from Central Europe, where the brown type prevails due to local selection pressure. Warm springs in northern Central Europe had a positive effect on the proportion of the brown phenotype in the north in the early part of the study period, which suggests prolonged migration in favourable conditions. However, the association between warm springs and a high proportion of brown males has weakened from the 1950s to the present, which may explain why the proportion of the brown males in our study area decreased by a third during the period 1954 to 2008. This is likely a result of decreasing population size in Central Europe. These results demonstrate that temporal variation in environmental conditions is maintaining variation in the pied flycatcher male phenotype. They also indicate that climate warming has the potential to change the population composition both through temperature-dependent selection and environmental factors affecting long-distance immigration.

Background: Inference of population and species histories and population stratification using genetic data is important for discriminating between different speciation scenarios and for correct interpretation of genome scans for signs of adaptive evolution and trait association. Here we use data from 24 intronic loci re-sequenced in population samples of two closely related species, the pied flycatcher and the collared flycatcher., Results: We applied Isolation-Migration models, assignment analyses and estimated the genetic differentiation and diversity between species and between populations within species. The data indicate a divergence time between the species of <1 million years, significantly shorter than previous estimates using mtDNA, point to a scenario with unidirectional gene-flow from the pied flycatcher into the collared flycatcher and imply that barriers to hybridisation are still permeable in a recently established hybrid zone. Furthermore, we detect significant population stratification, predominantly between the Spanish population and other pied flycatcher populations., Conclusions: Our results provide further evidence for a divergence process where different genomic regions may be at different stages of speciation. We also conclude that forthcoming analyses of genotype-phenotype relations in these ecological model species should be designed to take population stratification into account.

Our understanding of species phylogeography in much of the Palearctic is incomplete. In addition, many existing studies based solely on mitochondrial DNA (mtDNA) can provide a biased view of phylogeographic history because of the effects of lineage sorting, natural selection, or hybridization. We analyzed 13 introns to assess a mtDNA study of the Eurasian nuthatch (Sitta europaea) that suggested a seemingly contemporaneous origin of distinct taxa in the Caucasus, Europe, and Asia. Neutrality tests showed no evidence of selection on either the mtDNA or nuclear sequences. Most nuclear gene trees, except for Z-linked ones, did not recover the three lineages, which we attribute to recent splitting. Analyses of the 13 introns combined revealed the same three groups as did the mtDNA and suggested that nuthatches experienced a trichotomous (or two indistinguishable) split(s) 1-2 million years ago (Mya) and have remained isolated with trifling if not zero gene flow since then, and the Asian group increased in population size. This result demonstrates the usefulness of mtDNA in discovering phylogeographic patterns. The use of multiple nuclear loci facilitated detection of an introgressed individual and improved estimates of process parameters such as divergence time and population expansion. We recommend that phylogeographic studies should be based on both mtDNA and nuclear genes., (© 2012 The Author(s). Evolution© 2012 The Society for the Study of Evolution.)

The role of natural selection in shaping adaptive trait differentiation in natural populations has long been recognized. Determining its molecular basis, however, remains a challenge. Here, we search for signals of selection in candidate genes for colour and its perception in a passerine bird. Pied flycatcher plumage varies geographically in both its structural and pigment-based properties. Both characteristics appear to be shaped by selection. A single-locus outlier test revealed 2 of 14 loci to show significantly elevated signals of divergence. The first of these, the follistatin gene, is expressed in the developing feather bud and is found in pathways with genes that determine the structure of feathers and may thus be important in generating variation in structural colouration. The second is a gene potentially underlying the ability to detect this variation: SWS1 opsin. These two loci were most differentiated in two Spanish pied flycatcher populations, which are also among the populations that have the highest UV reflectance. The follistatin and SWS1 opsin genes thus provide strong candidates for future investigations on the molecular basis of adaptively significant traits and their co-evolution.

In order to describe the influence of Pleistocene glaciations on the genetic structure and demography of a highly mobile, but specialized, passerine, the Savi's Warbler (Locustella luscinioides), mitochondrial DNA sequences (ND2) and microsatellites were analysed in c.330 individuals of 17 breeding and two wintering populations. Phylogenetic, population genetics and coalescent methods were used to describe the genetic structure, determine the timing of the major splits and model the demography of populations. Savi's Warblers split from its sister species c.8 million years ago and have two major haplotype groups that diverged in the early/middle Pleistocene. One of these clades originated in the Balkans and is currently widespread, showing strong evidence for population expansion; whereas the other is restricted to Iberia and remained stable. Microsatellites agreed with a genetic break around the Pyrenees, but showed considerable introgression and a weaker genetic structure. Both genetic markers showed an isolation-by-distance pattern associated with the population expansion of the eastern clade. Breeding populations seem to be segregated at the wintering sites, but results on migratory connectivity are preliminary. Savi's Warbler is the only known migratory bird species in which Iberian birds did not expand beyond the Pyrenees after the last glaciation. Despite the long period of independent evolution of western and eastern populations, complete introgression occurred when these groups met in Iberia. Mitochondrial sequences indicated the existence of refugia-within-refugia in the Iberian Peninsula during the last glacial period, which is surprising given the high dispersal capacity of this species. Plumage differences of eastern subspecies seemed to have evolved recently through natural selection, in agreement with the glacial expansion hypothesis. This study supports the great importance of the Iberian Peninsula and its role for the conservation of genetic variation.

Background: The Old World warbler genus Sylvia has been used extensively as a model system in a variety of ecological, genetic, and morphological studies. The genus is comprised of about 25 species, and 70% of these species have distributions at or near the Mediterranean Sea. This distribution pattern suggests a possible role for the Messinian Salinity Crisis (from 5.96-5.33 Ma) as a driving force in lineage diversification. Other species distributions suggest that Late Miocene to Pliocene Afro-tropical forest dynamics have also been important in the evolution of Sylvia lineages. Using a molecular phylogenetic hypothesis and other methods, we seek to develop a biogeographic hypothesis for Sylvia and to explicitly assess the roles of these climate-driven events., Results: We present the first strongly supported molecular phylogeny for Sylvia. With one exception, species fall into one of three strongly supported clades: one small clade of species distributed mainly in Africa and Europe, one large clade of species distributed mainly in Africa and Asia, and another large clade with primarily a circum-Mediterranean distribution. Asia is reconstructed as the ancestral area for Sylvia. Long-distance migration is reconstructed as the ancestral character state for the genus, and sedentary behavior subsequently evolved seven times., Conclusion: Molecular clock calibration suggests that Sylvia arose in the early Miocene and diverged into three main clades by 12.6 Ma. Divergence estimates indicate that the Messinian Salinity Crisis had a minor impact on Sylvia. Instead, over-water dispersals, repeated loss of long-distance migration, and palaeo-climatic events in Africa played primary roles in Sylvia divergence and distribution.

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., (© 2010 The Author(s). Evolution© 2010 The Society for the Study of Evolution.)

Birds have for long been popular study objects in speciation research. Being easy to observe in the field, they have traditionally been particularly important in studies of behavioural and ecological factors in speciation, whereas the genetic aspects of the process have been studied in other organisms, such as Drosophila. More recently, however, a stronger genetic focus has been placed on speciation research also in birds. Here, we review ecological, behavioural and genetic studies on speciation in the pied flycatcher (Ficedula hypoleuca) and the collared flycatcher (Ficedula albicollis). These well-studied birds provide among the few proposed examples of the process of reinforcement of premating isolation, and the evidence for reinforcement is strong. They are further characterized by having strong intrinsic postzygotic barriers (female hybrid sterility), yet the two species appear to be very similar ecologically. This is in stark contrast to another well-studied bird complex, Darwin's finches, in which the species differ vastly in ecologically important traits but have no developmental problems arising from genetic incompatibilities, and where no evidence for reinforcement is found. In the flycatchers, sex chromosome linkage of genes affecting traits associated with both pre- and postzygotic barriers to gene exchange is likely to facilitate reinforcement. We discuss whether such sex-linkage may be common in birds. The contrast between flycatchers and Darwin's finches indicate that speciation in birds cannot always be understood mainly as a result of divergent natural selection ('ecological speciation'), and generalizations from one system may lead us astray. We discuss to what extent insight from research on the flycatchers may point to fruitful avenues for future research on bird speciation and specifically call for a more systematic effort to simultaneously investigate ecology, behaviour and genetics of birds caught in the process of speciation.

We analysed mitochondrial DNA (mtDNA) sequences from 154 bluethroats (Luscinia svecica) sampled at 21 sites throughout much of their Eurasian range. A previously reported, single base-pair mtDNA difference between L. s. svecica and L. s. namnetum was inconsistent upon expanded geographical sampling. A significant FST value (0.29) and an isolation-by-distance effect show the existence of geographical differentiation. Phylogenetic analysis of haplotypes revealed northern and southern groups, although lineage sorting is incomplete. There was no geographical structure to the haplotype tree within groups, and currently recognized subspecies were not supported. A minimum evolution tree based on pairwise mtDNA genetic distances among average samples showed the same two broadly distributed northern and southern groups. These groups abut in the centre of the latitudinal range, and were possibly isolated by forest that developed and spread westward over the last 15 000 years. Pairwise FST values averaged 0.16 in the southern group, 0.04 in the northern group, and 0.42 between groups. Mismatch distributions suggested population growth in each group, with that in the south being more recent. In the northern group, the geographical pattern in tau suggested northward and eastward expansion. Analysis of nucleotide diversity suggested westward expansion in the southern group. The northern group had higher nucleotide diversity than the southern group, consistent with a larger current population size in the north. Given the significant FST, incompletely sorted haplotype tree, and broadly patterned minimum evolution tree, L. svevica appears to represent a species at an intermediate stage of differentiation between panmixia and reciprocal monophyly.

The great tit complex is divided into four groups, each containing several subspecies. Even though the groups are known to differ markedly on morphological, vocal and behavioural characters, some hybridization occurs in the regions where they meet. The great tit has often been referred to as an example of a ring species, although this has later been questioned. Here, we have studied the genetic structure and phylogenetic relationships of the subspecies groups to clarify the evolutionary history of the complex using control region sequences of the mitochondrial DNA. The subspecies groups were found to be monophyletic and clearly distinct in mitochondrial haplotypes, and therefore must have had long-independent evolutionary histories. This conflicts with the ring species assignment and supports the formation of secondary contact zones of previously temporarily isolated groups. According to the phylogenetic species concept, all the subspecies groups could be considered as separate species, but if the definition of the biological species concept is followed, none of the subspecies groups is a true species because hybridization still occurs.

We analyzed sequences from a 275-bp hypervariable region in the 5' end of the mitochondrial DNA control region in 190 common chaffinches (Fringilla coelebs) from 19 populations in Europe and North Africa, including new samples from Greece and Morocco. Coalescent techniques were applied to estimate the time to the most recent common ancestor (TMRCA) and divergence times of these populations. The first objective of this study was to infer the locations of refugia where chaffinches survived the last glacial episode, and this was achieved by estimating the TMRCA of populations in regions surrounding the Mediterranean that were unglaciated in the late Pleistocene. Although extant populations in Iberia, Corsica, Greece, and North Africa harbor haplotypes that are basal in a phylogenetic tree, this information alone cannot be used to infer that these localities served as refugia, because it is impossible to infer the ages of populations and their divergence times without also considering the population genetic processes of mutation, migration, and drift. Provided we assume the TMRCAs of populations are a reasonable estimate of a population's age, coalescent-based methods place resident populations in Iberia, Corsica, Greece, and North Africa during the time of the last glacial maximum, suggesting these regions served as refugia for the common chaffinch. The second objective was to determine when populations began diverging from each other and to use this as a baseline to estimate current levels of gene flow. Divergence time estimates suggest that European populations began diverging about 60,000 years before present. The relatively recent divergence of populations in North Africa, Italy, and Iberia may explain why classic migration estimates based on equilibrium assumptions are high for these populations. We compare these estimates with nonequilibrium-based estimates and show that the nonequilibrium estimates are consistently lower than the equilibrium estimates.

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.