This passerine family occurs across Eurasia and contains two genera, Phylloscopus and Seicercus. Hybridization has only been documented in the former genus.
The Chiffchaff (P. collybita) complex is composed of several subspecies of which some are in secondary contact (Helbig et al., 1996, Rakovic et al., 2019). In Sweden, P. c. collybita is expanding north and engaging in hybridization with P. c. abientinus (Hansson et al., 2000) and in the Southern Urals, P. c. tristis and P. c. abientinus are interbreeding (Marova et al., 2009; Marova et al., 2017; Shipilina et al., 2017). A genomic analysis of these species revealed a handful of candidate regions that might be important for trait variation between the two species (Talla et al. 2017).
The most studied hybrid zone in this complex involves P. c. collybita and P. c. brehmii in the Pyrenees. It was first described based on morphological and vocal characteristics (Salomon, 1989; Salomon & Hemim, 1992; Salomon et al., 1997). Genetic analyses indicated extensive hybridization (Bensch et al., 2002b). However, gene flow was mostly restricted to nuclear alleles, possibly by means of hybrid males, while mitochondrial gene flow was inhibited by sterile hybrid females (Helbig et al., 2001). Both species also differ in flight-related morphology due to different migration patterns. Hybrids might be maladapted in terms of migration strategies (Perez-Tris et al., 2003).
Subspecies of the Willow Warbler (P. trochilus) form a migratory divide in Sweden, confirmed by isotope analyses (Chamberlain et al., 2000) and experiments (Ilieva et al., 2012). The subspecies are clearly separated morphologically and behaviourally, but there is little genetic differentiation (Bensch et al., 1999; Bensch et al., 2002a). However, three genomic regions – on chromosomes 1, 3 and 5 – are highly differentiated and house putative ‘migration genes’ (Lundberg, et al. 2017). Possibly there is strong selection on hybrid migration strategies, because premating isolation is weak (Liedvogel et al., 2014). In addition, the circular distribution of this species around the Baltic Sea might make it an example of a ring (sub)species (Bensch et al., 2009).
Another likely example of a ring species is the Greenish Warbler (P. trochiloides), which extends around the Tibetan Plateau. The two terminal populations of this ring (viridamus and plumbeitarsus) meet, but do not interbreed (Irwin et al., 2001a; Irwin et al., 2001b). These populations sing different song and do not recognize each other’s song (Irwin, 2000; Irwin et al., 2001a). Song divergence is mainly driven by male competition. In the south, population density is higher, leading to more interactions between the males and consequently strong selection for shorter songs. In the north, competition between males is weaker and there is a stronger selection by females for longer, complex songs (Scordato, 2018). Genetic analysis using AFLPs demonstrated gene flow between the connected populations (Irwin et al., 2005). But recent studies are questioning the validity of the Greenish Warbler as a classical ring species. Morphology and song seem to be converging in sympatry (Kovylov et al., 2012), and a genomic analyses showed that there have been occasional geographic breaks during the development of the ring (Alcaide et al., 2014).
Hybridization between Western Bonelli’s Warbler (P. bonelli) and Wood Warbler (P. sibilatrix) has been confirmed genetically (Dietzen et al., 2007).
Description of the Pallas’ Warbler (P. proregulus) complex indicates the existence of contact zones and possible hybridization between certain races (Martens et al., 2004).
Alstrom et al. (2010) describe a new species, Limestone Leaf Warbler (P. calciatilis) in Vietnam, that might be interbreeding with Sulphur-breasted Warbler (P. richetti).
Alcaide, M., Scordato, E. S., Price, T. D. & Irwin, D. E. (2014). Genomic divergence in a ring species complex. Nature.
Alstrom, P., Davidson, P., Duckworth, J. W., Eames, J. C., Le, T. T., Nguyen, C., Olsson, U., Robson, C. & Timmins, R. (2010). Description of a new species of Phylloscopus warbler from Vietnam and Laos. Ibis 152, 145-168.
Bensch, S., Andersson, T. & Akesson, S. (1999). Morphological and molecular variation across a migratory divide in willow warblers, Phylloscopus trochilus. Evolution 53, 1925-1935.
Bensch, S., Akesson, S. & Irwin, D. E. (2002a). The use of AFLP to find an informative SNP: genetic differences across a migratory divide in willow warblers. Molecular Ecology 11, 2359-2366.
Bensch, S., Helbig, A. J., Salomon, M. & Siebold, I. (2002b). Amplified fragment length polymorphism analysis identifies hybrids between two subspecies of warblers. Molecular Ecology 11, 473-481.
Bensch, S., Grahn, M., Muller, N., Gay, L. & Akesson, S. (2009). Genetic, morphological, and feather isotope variation of migratory willow warblers show gradual divergence in a ring. Molecular Ecology 18, 3087-3096.
Chamberlain, C. P., Bensch, S., Feng, X., Akesson, S. & Andersson, T. (2000). Stable isotopes examined across a migratory divide in Scandinavian willow warblers (Phylloscopus trochilus trochilus and Phylloscopus trochilus acredula) reflect their African winter quarters. Proceedings of the Royal Society B-Biological Sciences 267, 43-48.
Dietzen, C., Hackenberg, C., Heyne, K. H., Sauer-Gurth, H., Staudter, H. & Wink, M. (2007). Genetically confirmed interbreeding between western Bonelli’s warbler (Phylloscopus bonelli) and wood warbler (P-sibilatrix). Journal of Ornithology 148, 85-90.
Hansson, M. C., Bensch, S. & Brannstrom, O. (2000). Range expansion and the possibility of an emerging contact zone between two subspecies of Chiffchaff Phylloscopus collybita ssp. Journal of Avian Biology 31, 548-558.
Helbig, A. J., Martens, J., Seibold, I., Henning, F., Schottler, B. & Wink, M. (1996). Phylogeny and species limits in the Palaearctic chiffchaff Phylloscopus collybita complex: Mitochondrial genetic differentiation and bioacoustic evidence. Ibis 138, 650-666.
Helbig, A. J., Salomon, M., Bensch, S. & Seibold, I. (2001). Male-biased gene flow across an avian hybrid zone: evidence from mitochondrial and microsatellite DNA. Journal of Evolutionary Biology 14, 277-287.
Ilieva, M., Toews, D. P. L., Bensch, S., Sjoholm, C. & Akesson, S. (2012). Autumn migratory orientation and displacement responses of two willow warbler subspecies (Phylloscopus trochilus trochilus and P. t. acredula) in South Sweden. Behavioural Processes 91, 253-261.
Irwin, D. E. (2000). Song variation in an avian ring species. Evolution 54, 998-1010.
Irwin, D. E., Bensch, S. & Price, T. D. (2001a). Speciation in a ring. Nature 409, 333-337.
Irwin, D. E., Irwin, J. H. & Price, T. D. (2001b). Ring species as bridges between microevolution and speciation. Genetica 112, 223-243.
Irwin, D. E., Bensch, S., Irwin, J. H. & Price, T. D. (2005). Speciation by distance in a ring species. Science 307, 414-416.
Kovylov, N., Marova, I. & Ivanitskii, V. (2012). Variation of song and plumage in the western (Phylloscopus trochiloides viridanus) and eastern (Phylloscopus trochiloides plumbeitarsus) forms of the greenish warbler in a sympatry zone: Is the hypothesis of ring speciation true? Biology Bulletin 39, 729-740.
Liedvogel, M., Larson, K. W., Lundberg, M., Gursoy, A., Wassenaar, L. I., Hobson, K. A., Bensch, S. & Akesson, S. (2014). No evidence for assortative mating within a willow warbler migratory divide. Frontiers in Zoology 11.
Lundberg M., Liedvogel M., Larson K., Sigeman H., Grahn M., Wright A., Åkesson S., Bensch S. (2017). Genetic differences between willow warbler migratory phenotypes are few and cluster in large haplotype blocks. Evolution Letters 1: 155-168.
Marova, I., Fedorov, V., Shipilina, D. & Alekseev, V. (2009). Genetic and vocal differentiation in hybrid zones of passerine birds: Siberian and European chiffchaffs (Phylloscopus [collybita] tristis and Ph.[c.] abietinus) in the southern Urals. In Doklady Biological Sciences, vol. 427, pp. 384-386. Springer.
Marova, I., Shipilina, D., Fedorov, V., Alekseev, V., Ivanitskii, V. (2017) Interaction between Common and Siberian Chiffchaff in a contact zone. Ornis Fennica 94, 66-81.
Martens, J., Tietze, D. T., Eck, S. & Veith, M. (2004). Radiation and species limits in the Asian Pallas’s warbler complex (Phylloscopus proregulus s.l.). Journal of Ornithology 145, 206-222.
Rakovic, M., Neto, J.M., Lopes, R.J., Koblik, E.A., Fadeev, I.V., Lohman, Y.V., Aghayan, S.A., Boano, G., Pavia, M., Periman, Y., Kiat, Y., Ben Dov, A., Collinson, J.M., Voelker, G. & Drovetski, S.V. (2019) Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’. PLoS One 14(1):e0210268.
Perez-Tris, J., Ramirez, A. & Telleria, J. L. (2003). Are Iberian Chiffchaffs Phylloscopus (collybita) brehmii long-distance migrants? An analysis of flight-related morphology. Bird Study 50, 146-152.
Salomon, M. (1989). Song as a Possible Reproductive Isolating Mechanism between 2 Parapatric Forms – the Case of the Chiffchaffs Phylloscopus-Collybita-Collyb. And Phylloscopus-Collybita-Brehmii in the Western Pyrenees. Behaviour 111, 270-290.
Salomon, M. & Hemim, Y. (1992). Song Variation in the Chiffchaffs (Phylloscopus-Collybita) of the Western Pyrenees – the Contact Zone between the Collybita and Brehmii Forms. Ethology 92, 265-282.
Salomon, M., Bried, J., Helbig, A. J. & Riofrio, J. (1997). Morphometric differentiation between male common chiffchaffs, Phylloscopus [c] collybita Vieillot, 1817, and Iberian chiffchaffs, P [c] brehmii Homeyer, 1871, in a secondary contact zone (Aves: Sylviidae). Zoologischer Anzeiger 236, 25-36.
Scordato, E. (2018) Male competition drives song divergence along an ecological gradient in an avian ring species. Evolution 72(11):2360-2377.
Shipilina, D., Serbyn, M., Ivanitskii, V., Marova, I. & Backström, N. (2017). Patterns of genetic, phenotypic, and acoustic variation across a chiffchaff (Phylloscopus collybita abietinus/tristis) hybrid zone. Ecology and Evolution.
Talla, V., Kalsoom, F., Shipilina, D., Marova, I. & Backström, N. (2017) Heterogeneous Patterns of Genetic Diversity and Differentiation in European and Siberian Chiffchaff (Phylloscopus collybita abietinus/P. tristis). G3: Genes, Genomes, Genetics 7(12), 3983-3998.