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).
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.
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.
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). 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).
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).
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).
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).
Williams and Wheat (1971) describe a hybrid between Blue Jay (C. cristata) and Steller’s Jay (C. stelleri) in Colorado.
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).
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.
Brown, J. L. & Li, S. H. (1995). Phylogeny of social behavior in Aphelocoma jays: A role for hybridization? Auk 112, 464-472.
Cook, A. (1975). Changes in Carrion-Hooded Crow Hybrid Zone and Possible Importance of Climate. Bird Study 22, 165-168.
de Knijff, P. (2014). How carrion and hooded crows defeat Linnaeus’s curse. Science 344, 1345-1346.
Gowen, F. C., Maley, J. M., Cicero, C., Peterson, A. T., Faircloth, B. C., Warr, T. C. & McCormack, J. E. (2014). Speciation in Western Scrub-Jays, Haldane’s rule, and genetic clines in secondary contact. Bmc Evolutionary Biology 14.
Haas, F. & Brodin, A. (2005). The crow Corvus corone hybrid zone in southern Denmark and northern Germany. Ibis 147, 649-656.
Haas, F., Knape, J. & Brodin, A. (2010). Habitat preferences and positive assortative mating in an avian hybrid zone. Journal of Avian Biology 41, 237-247.
Haas, F., Pointer, M. A., Saino, N., Brodin, A., Mundy, N. I. & Hansson, B. (2009). An analysis of population genetic differentiation and genotype-phenotype association across the hybrid zone of carrion and hooded crows using microsatellites and MC1R. Molecular Ecology 18, 294-305.
Kearns, A.M., Restani, M., Szabo, I., Schrøder-Nielsen, A., Kim, J.A., Richardson, H.M., Marzluff, J.M., Fleischer, R.C., Johnsen, A. & Omland, K. E. (2018). Genomic evidence of speciation reversal in ravens. Nature communications, 9(1), 906.
Knief, U., Bossu, C.M., Saino, N., Hansson, B., Poelstra, J., Vijay, N., Weissensteiner, M. & Wolf, J.B.W. (2019) Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone. Nature Ecology & Evolution, 3:570-576.
Kryukov, A. & Blinov, V. (1994). Hybrid zone of hooded and carrion crows in Siberia. Journal of Ornithology 135, 147.
Kryukov, A., Uphyrkina, O. & Chelomina, G. (1992). Analysis of crow genomes (Corvidae, Passeriformes) from the zone of overlapping areas of habitation and hybridization. Genetika 28, 136-140.
Kryukov, A. P. (2019). Phylogeography and hybridization of corvid birds in the Palearctic Region. Journal of Genetics and Breeding, 23(2), 232-238.
Mayr, E. (1963). Animal species and evolution. Belknap Press of Harvard University Press, Cambridge,.
McCormack, J. E. & Venkatraman, M. X. (2013). A Distinctive Genetic Footprint of Ancient Hybridization. Auk 130, 469-475.
Meise, W. (1928). Die Verbreitung der Aaskrähe (Formenkreis Corvus corone L.). Dornblüth.
Palestrini, C. & Rolando, A. (1996). Differential calls by Carrion and Hooded Crows (Corvus corone corone and C-c-cornix) in the Alpine hybrid zone. Bird Study 43, 364-370.
Peterson, A. T. (1991). Gene Flow in Scrub Jays – Frequency and Direction of Movement. Condor 93, 926-934.
Picozzi, N. (1976). Hybridization of Carrion and Hooded Crows Corvus-C-Corone and Corvus-C-Cornix, in Northeastern Scotland. Ibis 118, 254-257.
Pitelka, F. A. (1951). Speciation and ecologic distribution in American jays of the genus Aphelocoma. University of California Press.
Pitelka, F. A., Selander, R. K. & Del Toro, M. A. (1956). A hybrid jay from Chiapas, Mexico. Condor, 98-106.
Poelstra, J. W., Ellegren, H. & Wolf, J. B. W. (2013). An extensive candidate gene approach to speciation: diversity, divergence and linkage disequilibrium in candidate pigmentation genes across the European crow hybrid zone. Heredity 111, 467-473.
Poelstra, J. W., Vijay, N., Bossu, C. M., Lantz, H., Ryll, B., Muller, I., Baglione, V., Unneberg, P., Wikelski, M., Grabherr, M. G. & Wolf, J. B. W. (2014). The genomic landscape underlying phenotypic integrity in the face of gene flow in crows. Science 344, 1410-1414.
Poelstra, J. W., Vijay, N., Hoeppner, M. P., & Wolf, J. B. W. (2015). Transcriptomics of colour patterning and coloration shifts in crows. Molecular Ecology, 24(18), 4617–4628
Randler, C. (2007a). Assortative mating of Carrion Corvus corone and Hooded Crows C. cornix in the hybrid zone in eastern Germany. Ardea 95, 143-149.
Randler, C. (2007b). Habitat use by Carrion Crows Corvus corone corone and Hooded Crows C c cornix and their hybrids in eastern Germany. Acta Ornithologica 42, 191-194.
Randler, C. (2008). Risk assessment by crow phenotypes in a hybrid zone. Journal of Ethology 26, 309-316.
Rice, N. H., Martinez-Meyer, E. & Peterson, A. T. (2003). Ecological niche differentiation in the Aphelocoma jays: a phylogenetic perspective. Biological Journal of the Linnean Society 80, 369-383.
Risch, M. & Andersen, L. (1998). Non-random mating of crows (Corvus corone) in a hybrid zone of carrion crow (C. c. corone) and hooded crow (C. c. cornix). Journal fur Ornithologie 139, 173-178.
Rolando, A. (1993). A study on the hybridization between carrion and hooded crow in Northwestern Italy. Ornis Scandinavica, 80-83.
Rolando, A. & Laiolo, P. (1994). Habitat selection of Hooded and Carrion Crows in the Alpine hybrid zone. Ardea 82, 193-193.
Saino, N. (1990). Low reproductive success of the Carrion Crow Corvus corone corone-Hooded Crow Corvus c. cornix hybrids. Avocetta 14, 103-109.
Saino, N. (1992). Selection of Foraging Habitat and Flocking by Crow Corvus-Corone Phenotypes in a Hybrid Zone. Ornis Scandinavica 23, 111-120.
Saino, N. & Bolzern, A. M. (1992). Egg Volume, Chick Growth and Survival across a Carrion Hooded Crow Hybrid Zone. Bollettino Di Zoologia 59, 407-415.
Saino, N. & Debernardi, F. (1994). Geographic-Variation in Size and Sexual Dimorphism across a Hybrid Zone between Carrion Crows (Corvus Corone Corone) and Hooded Crows (C-C-Cornix). Canadian Journal of Zoology-Revue Canadienne De Zoologie 72, 1543-1550.
Saino, N., Lorenzini, R., Fusco, G. & Randi, E. (1992). Genetic-Variability in a Hybrid Zone between Carrion and Hooded Crows (Corvus-Corone-Corone and Cc Cornix, Passeriformes, Aves) in North-Western Italy. Biochemical Systematics and Ecology 20, 605-613.
Saino, N. & Scatizzi, L. (1991). Selective Aggressiveness and Dominance among Carrion Crows, Hooded Crows and Hybrids. Bollettino Di Zoologia 58, 255-260.
Saino, N. & Villa, S. (1992). Pair Composition and Reproductive Success across a Hybrid Zone of Carrion Crows and Hooded Crows. Auk 109, 543-555.
Saino, N., Wuster, W. & Thorpe, R. S. (1998). Congruence between morphological variation and altitudinal gradient across a hybrid zone between carrion and hooded crows. Italian Journal of Zoology 65, 407-412.
Sitasuwan, N. & Thaler, E. (1985). Vocal Inventory and Communication in the Chough (Pyrrhocorax-Pyrrhocorax), in the Alpine Chough (Pyrrhocorax-Graculus) and Their Hybrids. Journal Fur Ornithologie 126, 181-193.
Spiridonova, L. & Kryukov, A. (2004). Genetic Variability of Carrion and Hooded Crows and Their Hybrids According to RAPD-PCR Data. Cytology and Genetics 38, 27-35.
Vijay, N., C. M. Bossu, J. W. Poelstra, M. H. Weissensteiner, A. Suh, A. P. Kryukov and J. B. Wolf (2016). Evolution of heterogeneous genome differentiation across multiple contact zones in a crow species complex. Nature communications 7: 13195.
Webb, W. C., Marzluff, J. M. & Omland, K. E. (2011). Random interbreeding between cryptic lineages of the Common Raven: evidence for speciation in reverse. Molecular Ecology 20, 2390-2402.
Williams, O. & Wheat, P. (1971). Hybrid Jays in Colorado. Wilson Bulletin 83, 343-&.
Wolf, J. B. W., Bayer, T., Haubold, B., Schilhabel, M., Rosenstiel, P. & Tautz, D. (2010). Nucleotide divergence vs. gene expression differentiation: comparative transcriptome sequencing in natural isolates from the carrion crow and its hybrid zone with the hooded crow. Molecular Ecology 19, 162-175.
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)