The Old World Flycatchers are a large passerine family mostly restricted to Europe, Asia and Africa. Several genera display hybridization and some have been studied in greater detail.
The phylogeography of Magpie-robins (genera Copsychus and Trichixos) is well studied. On Borneo and Java, black-bellied and white-bellied populations of Oriental Magpie-robin (C. saularis) have come into contact and are interbreeding (Sheldon et al., 2009). A similar process can also be observed between subspecies of the White-rumped Shama (C. malabaricus) on Borneo (Lim et al., 2010).
Hybrids between Chorister Robin-Chat (C. dichroa) and Red-capped Robin-Chat (C. natalensis) have been recorded in South Africa (Davies et al., 2011).
Hybridization between Collared Flycatcher (F. albicollis) and Pied Flycatcher (F. hypoleuca) has been studied extensively on the Baltic Islands, Gotland and Öland (Alatalo, Gustafsson & Lundberg, 1982; Alerstam et al., 1978; Vallin et al., 2012a), and in a hybrid across Central Europe (Saetre et al., 1999). The results from these studies have been reviewed elsewhere (Qvarnstrom, Rice & Ellegren, 2010; Saetre & Saether, 2010), but I will nonetheless give an overview of the main findings.
Hybrids are perfectly viable and a translocation experiment found difference in survival between hybrids and pure nestlings (Vallin et al., 2013). Hybrid fertility follows Haldane’s Rule, females are sterile while males are able to reproduce (Gelter, Tegelstrom & Gustafsson, 1992). There is however sexual selection against males in combination with genetic incompatibilities (Svedin et al., 2008), which can disrupt spermatogenesis (Alund et al., 2013). The effects of postzygotic selection increase in later generations (Wiley et al., 2009a). There might be selection against hybrids if they follow intermediate migration routes, but isotope analyses showed that hybrids use the same wintering areas as their parental species with a preference for Pied Flycatcher (Veen et al., 2014; Veen et al., 2007). Hybrids might also suffer from reduced immune function, but the prevalence of haemosporidians was intermediate in hybrids (Wiley, Qvarnstrom & Gustafsson, 2009b).
Hybridization can sometimes be beneficial, which has been termed adaptive mate choice. Benefits include more male offspring and siring of offspring by other conspecifics (Veen et al., 2001), possible heterotic effects (Merila, Sheldon & Griffith, 2003), and access to better territories (Wiley et al., 2007).
On the island of Öland, both species have advanced their timing of breeding in response to increasing spring temperatures. However, Pied Flycatchers showed a slower response compared to Collared Flycatchers, possibly leading to the build-up of temporal isolation (Sirkiä et al., 2018). In addition, competition has led to habitat isolation. High quality habitats are associated with a high risk of hybridization for Pied Flycatchers, leading to a selection pressure for immigrants to settle in lower quality habitats (Rybinksi et al. 2016).
In allopatry, the songs of both species are different (Wallin, 1986). In sympatry, however, the songs converge (Gelter, 1987; Haavie et al., 2004). Males singing mixed songs (caused by heterospecific copying, not hybridization) attract more females, which increases the risk of hybridization (Qvarnstrom et al., 2006).
Flycatchers display female mimicry (males resemble females) due to delayed maturation (Wiley et al., 2005). If these males resemble heterospecifics, this might increase the risk of maladaptive hybridization. Based on this reasoning, Saetre et al. (1993) hypothesized that light plumage colour in sympatry is driven by reinforcement. But subsequent studies showed that the occurrence of light plumage can be attributed to interspecific effects, such as aggression avoidance (Alatalo, Gustafsson & Lundberg, 1994). Reinforcement does not explain the light plumage colour, it could nonetheless explain divergence in plumage colour (Saetre et al., 1997). However, it is also possible that divergent males are simply more successful (Vallin et al., 2012b). Several major plumage traits have diverged in sympatry, but increase gradually in conspicuousness with distance to the sympatric zone. This suggests a cline maintained by gene flow (Laaksonen et al., 2015).
Tegelstrom and Gelter (1990) compared divergence at mitochondrial and nuclear loci and discovered that mtDNA was highly divergent in contrast to nDNA. They explained this pattern by sex-biased gene flow. Fertile males mitigate gene flow of nDNA, while sterile females prevent gene flow of mtDNA. This pattern can also be explained by a rapid mutational saturation of mtDNA (Saetre et al., 2001). Further studies also indicated strong selection against gene flow on the sex chromosomes (especially Z-chromosome) and suggested that male plumage is sex-linked (Saetre et al., 2003). This suggestion led to intensive studies of the Z-chromosome. Borge et al. (2005) found reduced variation on the Z-chromosome, which can be attributed to recurrent selective sweeps (by sexual selection?) or complex demographic history, such as a population bottleneck. Cross-fostering experiments indicated that species recognition genes are inherited on the Z-chromosome, and probably physically linked to genes of male plumage traits and genes causing low hybrid fitness (Saether et al., 2007). A candidate gene approach uncovered seven divergent loci of which two were associated with plumage (Backstrom et al., 2010a). There is however no evidence for a role for rearrangements of the Z-chromosome in reproductive isolation (Backstrom et al., 2010b). The inclusion of more species and the availability of whole genome sequences confirmed that Z-chromosomes are more divergent than autosomal loci (Ellegren et al., 2012; Hogner et al., 2012b). In addition, the genomic landscape of Flycatchers consists of several “islands of divergence”, which indicates that different genomic regions are at different stages of speciation (Backstrom, Saetre & Ellegren, 2013). Linkage disequilibrium is also highest in these “genomic islands” (Kawakami et al., 2014). Genomic analyses also provided strong evidence for gene flow among the flycatcher species, with distinct patterns of reduced introgression on the Z chromosome (Nater et al., 2015).
The population genetic structure of Pied Flycatcher has also been mapped. Populations in Norway and Czech Republic are indistinguishable, possibly due to gene flow, while the Spanish birds are clearly divergent (Haavie, Saetre & Moum, 2000).
Common Nightingale (L. megarhynchos) and Thrush Nightingale (L. luscinia) interbreed regularly (Becker, 1995; Becker, 2007; Kverek, 1998; Kverek, 2002; Kverek et al., 2008; Nöhring, 1943; Reifová, Kverek & Reif, 2011). Several individuals have been documented that produce songs of both species (Lille, 1988; Sorjonen, 1986), but a genetic analysis showed that this need not be the result of hybridization; many mixed singers did not possess genetic material from the other species (Vokurkova et al., 2013). Cultural transmission of song it thus an important mechanism. In addition, mixed songs might facilitate the coexistence of these two species by establishing interspecific territoriality. This concept is known as convergent agonistic character displacement (Souriau et al., 2018).
Hybrids can be detected based on morphological characteristics (Kovats, Vegvari & Varga, 2013). But despite hybridization, these species still diverge in certain traits, such as bill size (Reifova et al., 2011). This is probably due to differences in habitat use that are driven by interspecific competition (Sottas et al. 2018).
Both species differ in sperm morphology. However, sperm morphology is more different in sympatry than in allopatry, which suggests reinforcement might be operating (Albrecht et al., 2018).
Genomic analysis showed reduced introgression on the Z-chromosome compared to autosomes (Storchova, Reif & Nachman, 2010), which supports the idea that the Z-chromosome plays an important role in reproductive isolation (female hybrids are sterile). Female sterility is probably due to incompatible genes involved in meiosis that are located in genomic islands of differentiation (Morkovsky et al. 2018). The gene flow patterns on the Z-chromosome can be explained by higher levels of genetic drift in the Common Nightingale, leading to faster accumulation of hybrid incompatibilities (Janoušek et al., 2018).
The distribution of two haplotypes in the Japanese Robin (L. akahige) can be best explained by past introgression (Seki, Nishiumi & Saitoh, 2012). As similar situation occurs in Russia, where a genetic analysis of the Siberian Rubythroat (L. calliope) revealed two haplotypes that are shared by certain populations. This may indicate the existence of a hybrid zone (Spiridonova et al., 2013).
Randler et al. (2012) evaluated the status of the Cyprus Wheatear (O. cypriaca), which is closely related to Pied Wheatear (O. pleschanka) and Black-eared Wheatear (O. hispanica). This close relationship can be explained if O. cypriaca is a young taxon or if there is ongoing hybridization among these three species. A genomic analysis of this species complex revealed that Cyprus wheatear is more closely related to Eastern Black-eared Wheatear, followed by Pied Wheatear and Western Black-eared Wheatear. Moreover, there is extensive gene flow between Pied and Eastern Black-eared Wheatear (Schweizer et al., 2019a; Schweizer et al., 2019b). Indeed, a hybrid zone between these species has been described (Grabovsky, Panov & Rubtsov, 1992; Panov, 1986). More detailed studies of this hybrid zone showed song convergence (Grabovsky & Panov, 1992) and no differences in survival between hybrids and pure males (Rubtsov, 1995).
Geographical variation in Eastern Pied Wheatear (O. pictata) can be explained by hybridization dynamics between three morphological races (pictata, opistholeuca and capistrata) (Panov, Grabovsky & Ljubustchenko, 1993).
Hybridization between Kurdish Wheatear (O. xanthoprymna) and Persian Wheatear (O. chrysopygia) has been documented based on morphological data and the occurrence of intermediate colour variants (Chamani et al., 2010).
European Common Redstart (P. phoenicurus) and Black Redstard (P. ochruros) interbreed (Landmann, 1987). Experimental work indicated no differences between these species and their hybrids in prey-handling time and efficiency (Grosch, 2003) and habitat selection (Grosch, 2004). However, in an urban environment both species do use different habitats and interact aggressively, this behaviour could act as a reproductive barrier (Sedlacek, Fuchs & Exnerova, 2004). Genetic analysis of Common Redstart revealed two divergent mitochondrial haplotypes that appear to coexist (Hogner et al., 2012a). Intergeneric hybridization between Common Redstart and Winchat (Saxicola rubetra) has been confirmed by molecular analysis (Hogner et al., 2015).
Different subspecies of captive-bred Stonechats (S. torquata) have been used extensively in experimental settings. In most cases, hybrids showed intermediate outcomes in parameters, such as moult schedule (Gwinner & Neusser, 1985; Helm & Gwinner, 1999), clutch size (Gwinner, Konig & Haley, 1995), growth (Starck, Konig & Gwinner, 1995), circannual behaviour (Helm, 2009; Helm, Schwabl & Gwinner, 2009). However, the regulation of Basal Metabolic Rate (BMR) is more complicated. Hybrids showed differential BMR, which suggests that mitochondrial and nuclear genes are involved (Tieleman et al., 2009; Versteegh et al., 2012). Also, environmental factors and phenotypic plasticity may play an important role. The same is true for immune function (Versteegh et al., 2014).
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* Ficedula text reviewed by Hans Ellegren (Uppsala Universitet, Sweden)
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