Corvidae

These oscine birds can be found all over the world. The family contains crows, ravens, rooks, jackdaws, jays, magpies, treepies, choughs and nutcrackers. Numerous genera exhibit hybridization, namely Cyanolyca, Cyanocorax, Psilorhinus, Calocitta, Cyanocitta, Aphelocoma, Pica, Pyrrhocorax, Coloeus and Corvus. The phylogeography of several corvid species has been nicely summarized by Alexey Kryukov (2019).

Intergeneric hybrids have also been documented, for instance a hybrid between White-throated Magpie Jay (Calocitta formosa) and Brown Jay (Psilorhinus mexicanus) in Mexico (Pitelka, Selander & Del Toro, 1956).

Aphelocoma

Hybridization dynamics in this genus have been complicated by several taxonomic revisions. In 2011, the AOU decided to split the Mexican Jay into two species, one retaining the common name and the other called Transvolcanic Jay. Several genetic studies showed that these species exchanged genes in the past (McCormack & Venkatraman, 2013; Zarza et al., 2016). Currently there are six species recognized:

• Uncoloured Jay (A. unicolor)
• Mexican or Gray-breasted Jay (A. wollweberi)
• Transvolcanic Jay (A. ultramarina)
• Island Scrub Jay (A. insularis)
• Western Scrub Jay (A. californica)
• Florida Scrub Jay (A. caerulescens)

There is evidence for recent (but probably not ongoing) gene flow between allopatric lineages of the Mexican Jay, suggesting a reticulate history and possible speciation-with-bouts-of-gene-flow (Zarza et al., 2016).

The hybrid zone between two subspecies of Western Scrub Jay (californica and woodhouseii) was first described by Pitelka (1951). A morphological study on museum specimens indicated possible gene flow between the subspecies (Peterson, 1991). This hypothesis was later confirmed using molecular techniques (Gowen et al., 2014). Furthermore, gene flow was stronger in nuclear DNA compared to mtDNA, in accordance with Haldane’s Rule. This led the authors to propose lifting the subspecies up to species level.

A morphological study of museum specimens suggests that there might also be a hybrid zone between Woodhouse’s (A. w. grisea and A. w. cyanotis) and Sumichrast’s Scrub-Jay (A. w. sumichrasti and A. w. remota) in Mexico (DeRaad et al., 2019).

Two subspecies of Western Scrub Jay (A. c. californica and A. c. woodhouseii)

Mexican Jay populations show similarities with Western Scrub Jays, such as a rattle call and spotted eggs. This observation might be explained by recent hybridization and subsequent introgression (Brown & Li, 1995). However, genetic analyses based on mtDNA (Rice, Martinez-Meyer & Peterson, 2003) and several molecular markers (Bhagabati, Brown & Bowen, 2004) contradicted this idea, instead the similarities are probably due to convergence or ancient introgression.

Mexican Scrub Jay (A. californica)

Corvus

The hybrid zone between Carrion Crow (C. corone corone) and Hooded Crow (C. c. cornix) extends from Scotland, through Denmark, Germany, the Czech Republic and Hungary, to Italy (Mayr, 1963; Meise, 1928; Picozzi, 1976). The Scottish part may have shifted due to climatic changes (Cook, 1975). The hybrid zone also moved in Denmark and Germany compared to the study by Meise (1928), but the width remained stable (Haas & Brodin, 2005). Interestingly, there is a similar hybrid zone in Siberia (Kryukov & Blinov, 1994; Kryukov, Uphyrkina & Chelomina, 1992; Spiridonova & Kryukov, 2004).

The location of the hybrid zone was thus quickly established, but Nicola Saino was the first one to investigate what mechanisms determine the location and stability of the hybrid zone. Behavioural studies showed that these (sub)species prefer different habitats (Randler, 2007b; Rolando & Laiolo, 1994; Saino, 1992) and produce different calls (Palestrini & Rolando, 1996), which could both contribute to premating isolation. Indeed, assortative mating has been observed in several locations along the hybrid zone (Haas, Knape & Brodin, 2010; Randler, 2007a; Risch & Andersen, 1998; Rolando, 1993; Saino & Villa, 1992). Although there are no big differences in reproductive success, hybrids do seem to be at a disadvantage (Saino, 1990; Saino & Bolzern, 1992). Crows could engage in extra-pair copulations to avoid the costs of hybridization, but there was no strong support for this strategy (Knief et al., 2020).

Other studies looked at aggression (Saino & Scatizzi, 1991) and risk assessment (Randler, 2008) between the species, but their results contributed little to our understandings of the dynamics in the hybrid zone. Possible mechanisms for the formation and maintenance of the hybrid zone have also been simulated (Brodin & Haas, 2006; Brodin & Haas, 2009; Brodin, Haas & Hansson, 2013).

Hooded Crow (Corvus corone cornix) and Carrion Crow  (C. c. corone)

Geographical variation in morphology, such as sexual dimorphism, is correlated with ecological gradients (Saino & Debernardi, 1994) and shows a clinal pattern (Saino, Wuster & Thorpe, 1998) that is consistent with allozymic markers (Saino et al., 1992). Further genetic analyses (using microsatellites) failed to find differentiation between phenotypes in the hybrid zone (Haas et al., 2009). However, this result might be explained by differential gene expression (Wolf et al., 2010). Based on this study, several candidate pigmentation genes were selected for further analysis, but they did not yield any conclusive results (Poelstra, Ellegren & Wolf, 2013, but see Wu et al., 2019). A genome-wide introgression study, on the other hand, found a genomic region that was immune to introgression and harboured several genes involved in pigmentation and visual perception (de Knijff, 2014; Poelstra et al., 2014). So, this genomic island in an ocean of introgression might account for the observed phenotypic divergence. A subset of these genomic regions showed up in a genome association study, linking genetic variants with plumage color (Knief et al., 2019). Epistatic interaction of the gene NDP and a factor on chromosome 18 account for most of the phenotypic variation. Considering differential expression in the melanogensis pathway (Poelstra et al., 2015), it is conceivable that both of these contribute to regulation of the transcription factor MITF which seems to a crucial genetic switch during the development of feathers (Wu et al., 2019). Moreover, the lower expression of NDP in Hooded Crows seems to be related to a LTR retrotransposon insertion about 20kb upstream of the gene (Weissensteiner et al, 2020).

Comparing the genomic underpinnings of this hybrid zones with a similar zone in Siberia, where Hooded Crow interbreeds with Eastern Carrion Crow (C. orientalis), revealed that different genomic regions are under selection in the different hybrids zones. In other words, selection seems to be context-dependent (Vijay, Bossu et al. 2016).

American Crow (C. brachyrhynchos) and Northwestern Crow (C. caurinus) interbreed in a 900 kilometre-wide cryptic hybrid zone along west coast of North America (Slager et al., 2020).

In North America, the Common Raven (C. corax) includes two deeply divergent mtDNA lineages. Mate pairing between these lineages are random and there is no difference in reproductive success. Hence, there is no reproductive isolation and these lineage might represent an example of speciation in reverse (Webb, Marzluff & Omland, 2011). Further analyses confirmed this idea. Common Ravens have admixed genomes from two non-sister lineages (Holarctic and California) that diverged about 1.5 million years ago (Kearns et al., 2018).

Calocitta

Williams and Wheat (1971) describe a hybrid between Blue Jay (C. cristata) and Steller’s Jay (C. stelleri) in Colorado.

Blue Jay (Calocitta cristata)

Cyanocorax

Analyses of museum specimens uncovered hybrids between the Plush-crested Jay (Cyanocorax chrysops) and the White-naped Jay (C. cynanopogon) in Brazil (Apolinario & Silveira, 2019).

A Plush-crested Jay in Argentina © Tim Sackton | Flickr

Pyrrhocorax

The Alpenzoo Innsbruck housed hybrids between Cough (P. pyrrhocorax) and Alpine Chough (P. graculus). Vocal analyses of these birds and their hybrids, in combination with field observations, revealed that hybrids are bilingual (Sitasuwan & Thaler, 1985).

Alpine Cough (Pyrrhocorax graculus) and Cough (P. pyrrhocorax)

References

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Bhagabati, N. K., Brown, J. L. & Bowen, B. S. (2004). Geographic variation in Mexican jays (Aphelocoma ultramarina): local differentiation, polyphyly or hybridization? Molecular Ecology 13, 2721-2734.

Brodin, A. & Haas, F. (2006). Speciation by perception. Animal Behaviour 72, 139-146.

Brodin, A. & Haas, F. (2009). Hybrid zone maintenance by non-adaptive mate choice. Evolutionary Ecology 23, 17-29.

Brodin, A., Haas, F. & Hansson, B. (2013). Gene-flow across the European crow hybrid zone – a spatial simulation. Journal of Avian Biology 44, 281-287.

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de Knijff, P. (2014). How carrion and hooded crows defeat Linnaeus’s curse. Science 344, 1345-1346.

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Kryukov, A. P. (2019). Phylogeography and hybridization of corvid birds in the Palearctic Region. Journal of Genetics and Breeding, 23(2), 232-238.

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Wu, C., Klaesson, A., Buskas, J., Ranefall, P., Mirzazadeh, R., Söderberg, O. & Wolf, J.B.W. (2019) In situ quantification of individual mRNA transcripts in melanocytes discloses gene regulation of relevance to speciation. The Journal of Experimental Biology, 222: jeb194431.

Zarza, E., Faircloth, B. C., Tsai, W. L., Bryson, R. W., Jr., Klicka, J. & McCormack, J. E. (2016). Hidden histories of gene flow in highland birds revealed with genomic markers. Molecular Ecology 25, 5144-5157.

* Corvus section has been reviewed by Jochen Wolf (University of Munich, Germany)