The Tanagers comprise one of the largest bird families. They have an American distribution. Hybridization has been recorded in several genera.
Sympatric populations of Tree Finches were genetically more similar compared to allopatric ones. This can be explained by hybridization and/or sympatric origin (Grant, Grant & Petren, 2005). Indirect evidence for hybridization was provided by an analysis of historical and recent samples of Small Tree Finch (C. parvulus), Medium Tree Finch (C. pauper) and Large Tree Finch (C. psittacula). The historical sample (1852-1906) showed three morphological clusters, while the recent samples showed two clusters and an increasing amount of hybridization (19% in 2005 and 41% in 2010) (Kleindorfer et al., 2014). Gene flow is asymmetric, from Medium into Small Tree Finch, probably driven by female choice (Peters et al. 2017). From 2005 to 2013, the foraging behaviour of the parental species changed, but that of the hybrids did not (Peters & Kleindorfer, 2015). In an acoustical survey on Floreana Island, song differed significantly between Medium Tree Finch and Small Tree Finch, but it was not possible to discriminate between the song of Small Tree Finch and hybrids (Peters & Kleindorfer, 2017).
The Mangrove Finch (C. heliobates) is critically endangered and currently restricted to one small population on Isabela Island (Galapagos Islands). A genetic study found that a number of individuals have hybridized with the closely related Woodpecker Finch (C. pallidus). Possibly, there is a breakdown of reproductive isolation between these species because the Mangrove Finches cannot find a mate due to the low population size (Lawson et al., 2016).
The Warbler Finch (C. olivacea) comprises two distinct genetic lineages that are paraphyletic. This pattern can be explained by incomplete lineage sorting and hybridization (Freeland & Boag, 1999b).
Several Darwin’s Finches interbreed (Farrington et al., 2014; Grant, 1999), but a few cases have been studied in great detail. Lamichhaney et al. (2015) give phylogenetic evidence of hybridization having occurred throughout the radiation (see also perspective by Almen et al. (2016)). The findings of this study have been placed into a greater perspective of introgressive hybridization by Palmer and Kronforst (2015).
On the small island Daphne Major, three species coexist, Medium Ground Finch (G. fortis), Common Cactus Finch (G. scandens) and Small Ground Finch (G. fuliginosa). They all interbreed at low frequencies (Freeland & Boag, 1999a; Grant, 1993). Hybridization is caused by occasional errors of imprinting on parental songs that are inherited culturally (Grant & Grant, 1996a; Grant & Grant, 1997b; Grant & Grant, 1997c). Hybrids showed high fitness under certain ecological circumstances (Grant & Grant, 1992b), they are morphologically intermediate which enables them to occupy intermediate ecological niches (Grant & Grant, 1996b; Grant & Grant, 1994). For example, the El Nino effect on the island created the opportunity for Medium Ground Finch hybrids to proliferate (Grant & Grant, 1993).
Hybridization led to the exchange of genetic material between species (Grant et al., 2005), which enhances genetic diversity of populations (Grant & Grant, 1992a; Grant & Grant, 2010), counteracts inbreeding depression (Grant et al., 2003) and creates new evolutionary tracks (Grant & Grant, 1996c). Hybridization can also lead to convergence of species (Grant et al., 2004). So, the balance between selection and hybridization will ultimately result in fission-fusion dynamics of species (Grant & Grant, 2008; Grant & Grant, 2006). These studies have uncovered the important role hybridization may fulfil in speciation (Grant, 2003; Grant & Grant, 1997a). An overview of this system has been nicely summarized (Grant & Grant, 2014), including the case of a hybrid Medium Ground Finch that reached the island and is behaving like a new lineage (Grant & Grant, 2009). Genomic analyses of this lineage indicated that it concerns the founders were a female Medium Ground Finch and male Large Cactus Finch (G. conirostris). Their offspring were reproductively isolated from the parental species and have been breeding amongst each other for several generations, resulting in the origin of a hybrid species (Lamichhaney, et al. 2017).
On Genovesa. Large Cactus Finch (G. conirostris) hybridizes occasionally with Sharp-beaked Ground Finch (G. difficilis) and Large Ground Finch (G. magnirostris) (Grant & Grant, 1989).
On Santa Cruz, there is positive assortative mating between large and small morphs of the Medium Ground Finch (Huber et al., 2007). Genetic analyses showed that this might be an example of divergence with gene flow (de Leon et al., 2010).
Mckay and Zink (2015) provide a different perspective on the Geospiza ground finches. They argue that these populations are cycling between stages of differentiation and will never attain species status, a process referred to as Sisyphean evolution. Although an interesting idea, how can you scientifically test a never-ending process (Peter Grant, personal communication)?
On Inaccessible Island, Wilkin’s Finch (N. wilkinsi) and Inaccessible Island Finch (N. acunhae) are interbreeding (Ryan, Moloney & Hudon, 1994). Hybrids are generally intermediate in size (Ryan, 2001) and egg size (Ryan & Moloney, 2002).
In Colombia, habitat modifications have led to secondary contact between two subspecies of Flame-rumped Tanager (R. flammigerus). Morphological analyses confirmed hybridization is occurring, probably accompanied by genetic introgression (Bedoya & Murillo, 2012).
A study of an adaptive radiation comprising 11 species found marked phenotypic differences despite a lack of mtDNA monophyly. This pattern can be explained by incomplete lineage sorting, introgressive hybridization and demographic expansions (Campagna et al., 2012; Campagna et al., 2013). A genomic analysis on this radiation found no evidence for gene flow between five sympatric species (S. hypoxantha, S. melanogaster, S. palustris, S. pileata, S. ruficollis), likely due to recent divergence and the fact that a high number of shared ancestral polymorphisms reduces the power of tests for finding signatures of gene flow (Campagna et al., 2015).
Two studies tested whether a certain taxon was of hybrid origin (S. zelechi and a variant of S. hypoxantha), but in both cases it turned out to be a colour morph (Areta, 2008; Areta & Repenning, 2011).
Almen, M. S., Lamichhaney, S., Berglund, J., Grant, B. R., Grant, P. R., Webster, M. T. & Andersson, L. (2016). Adaptive radiation of Darwin’s finches revisited using whole genome sequencing. Bioessays 38, 14-20.
Areta, J. I. (2008). Entre Rios Seedeater (Sporophila zelichi): a species that never was. Journal of Field Ornithology 79, 352-363.
Areta, J. I. & Repenning, M. (2011). Systematics of the Tawny-Bellied Seedeater (Sporophila Hypoxantha). Ii. Taxonomy and Evolutionary Implications of the Existence of a New Tawny Morph. Condor 113, 678-690.
Bedoya, M. J. & Murillo, O. E. (2012). Morphological evidence of hybridization between Ramphocelus flammigerus subspecies (Passeriformes: Thraupidae) in Colombia. Revista De Biologia Tropical 60, 75-85.
Campagna, L., Gronau, I., Silveira, L. F., Siepel, A. & Lovette, I. J. (2015). Distinguishing noise from signal in patterns of genomic divergence in a highly polymorphic avian radiation. Molecular Ecology 24, 4238-4251.
Campagna, L., Benites, P., Lougheed, S. C., Lijtmaer, D. A., Di Giacomo, A. S., Eaton, M. D. & Tubaro, P. L. (2012). Rapid phenotypic evolution during incipient speciation in a continental avian radiation. Proceedings of the Royal Society B-Biological Sciences 279, 1847-1856.
Campagna, L., Silveira, L. F., Tubaro, P. L. & Lougheed, S. C. (2013). Identifying the Sister Species to the Rapid Capuchino Seedeater Radiation (Passeriformes: Sporophila). Auk 130, 645-655.
de Leon, L. F., Bermingham, E., Podos, J. & Hendry, A. P. (2010). Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin’s finches. Philosophical Transactions of the Royal Society B-Biological Sciences 365, 1041-1052.
Farrington, H. L., Lawson, L. P., Clark, C. M. & Petren, K. (2014). The Evolutionary History of Darwin’s Finches: Speciation, Gene Flow, and Introgression in a Fragmented Landscape. Evolution 68, 2932-2944.
Freeland, J. R. & Boag, P. T. (1999a). The mitochondrial and nuclear genetic homogeneity of the phenotypically diverse Darwin’s ground finches. Evolution 53, 1553-1563.
Freeland, J. R. & Boag, P. T. (1999b). Phylogenetics of Darwin’s finches: Paraphyly in the tree-finches, and two divergent lineages in the Warbler Finch. Auk 116, 577-588.
Grant, B. R. (2003). Evolution in Darwin’s finches: a review of a study on Isla Daphne Major in the Galapagos Archipelago. Zoology 106, 255-259.
Grant, B. R. & Grant, P. R. (1989). Evolutionary dynamics of a natural population: the large cactus finch of the Galápagos. University of Chicago Press.
Grant, B. R. & Grant, P. R. (1993). Evolution of Darwin Finches Caused by a Rare Climatic Event. Proceedings of the Royal Society B-Biological Sciences 251, 111-117.
Grant, B. R. & Grant, P. R. (1996a). Cultural inheritance of song and its role in the evolution of Darwin’s finches. Evolution 50, 2471-2487.
Grant, B. R. & Grant, P. R. (1996b). High survival of Darwin’s finch hybrids: Effects of beak morphology and diets. Ecology 77, 500-509.
Grant, B. R. & Grant, P. R. (2008). Fission and fusion of Darwin’s finches populations. Philosophical Transactions of the Royal Society B-Biological Sciences 363, 2821-2829.
Grant, P. R. (1993). Hybridization of Darwin Finches on Isla-Daphne-Major, Galapagos. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 340, 127-139.
Grant, P. R. (1999). Ecology and evolution of Darwin’s finches. Princeton University Press.
Grant, P. R. & Grant, B. R. (1992a). Demography and the Genetically Effective Sizes of 2 Populations of Darwin Finches. Ecology 73, 766-784.
Grant, P. R. & Grant, B. R. (1992b). Hybridization of Bird Species. Science 256, 193-197.
Grant, P. R. & Grant, B. R. (1994). Phenotypic and Genetic-Effects of Hybridization in Darwins Finches. Evolution 48, 297-316.
Grant, P. R. & Grant, B. R. (1996c). Speciation and hybridization in island birds. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 351, 765-772.
Grant, P. R. & Grant, B. R. (1997a). Genetics and the origin of bird species. Proceedings of the National Academy of Sciences of the United States of America 94, 7768-7775.
Grant, P. R. & Grant, B. R. (1997b). Hybridization, sexual imprinting, and mate choice. American Naturalist 149, 1-28.
Grant, P. R. & Grant, B. R. (1997c). Mating patterns of Darwin’s finch hybrids determined by song and morphology. Biological Journal of the Linnean Society 60, 317-343.
Grant, P. R. & Grant, B. R. (2006). Species before speciation is complete. Annals of the Missouri Botanical Garden 93, 94-102.
Grant, P. R. & Grant, B. R. (2009). The secondary contact phase of allopatric speciation in Darwin’s finches. Proceedings of the National Academy of Sciences of the United States of America 106, 20141-20148.
Grant, P. R. & Grant, B. R. (2010). Conspecific versus heterospecific gene exchange between populations of Darwin’s finches. Philosophical Transactions of the Royal Society B-Biological Sciences 365, 1065-1076.
Grant, P. R. & Grant, B. R. (2014). Synergism of Natural Selection and Introgression in the Origin of a New Species*. American Naturalist 183, 671-681.
Grant, P. R., Grant, B. R., Keller, L. F., Markert, J. A. & Petren, K. (2003). Inbreeding and interbreeding in Darwin’s finches. Evolution 57, 2911-2916.
Grant, P. R., Grant, B. R., Markert, J. A., Keller, L. F. & Petren, K. (2004). Convergent evolution of Darwin’s finches caused by introgressive hybridization and selection. Evolution 58, 1588-1599.
Grant, P. R., Grant, B. R. & Petren, K. (2005). Hybridization in the recent past. American Naturalist 166, 56-67.
Huber, S. K., De Leon, L. F., Hendry, A. P., Bermingham, E. & Podos, J. (2007). Reproductive isolation of sympatric morphs in a population of Darwin’s finches. Proceedings of the Royal Society B-Biological Sciences 274, 1709-1714.
Kleindorfer, S., O’Connor, J. A., Dudaniec, R. Y., Myers, S. A., Robertson, J. & Sulloway, F. J. (2014). Species Collapse via Hybridization in Darwin’s Tree Finches. American Naturalist 183, 325-341.
Lamichhaney, S., Berglund, J., Almen, M. S., Maqbool, K., Grabherr, M., Martinez-Barrio, A., Promerova, M., Rubin, C. J., Wang, C., Zamani, N., Grant, B. R., Grant, P. R., Webster, M. T. & Andersson, L. (2015). Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518.
Lamichhaney S, Han F, Webster MT, Andersson L, Grant BR, Grant PR. (2017). Rapid hybrid speciation in Darwin’s finches. Science:eaao4593.
Lawson, L. P., Fessl, B., Vargas, F. H., Farrington, H. L., Cunninghame, H. F., Mueller, J. C., Nemeth, E., Sevilla, P. C. & Petren, K. (2016). Slow motion extinction: inbreeding, introgression, and loss in the critically endangered mangrove finch (Camarhynchus heliobates). Conservation Genetics, 1-12.
Mckay, B. D. & Zink, R. M. (2015). Sisyphean evolution in Darwin’s finches. Biological Reviews 90, 689-698.
Palmer, D. H. & Kronforst, M. R. (2015). Divergence and gene flow among Darwin’s finches: A genome-wide view of adaptive radiation driven by interspecies allele sharing. Bioessays 37, 968-974.
Peters, K. J. & Kleindorfer, S. (2015). Divergent foraging behavior in a hybrid zone: Darwin’s tree finches (Camarhynchus spp.) on Floreana Island. Current Zoology 61, 181-190.
Peters, K. J. & Kleindorfer, S. (2017). Avian population trends in Scalesia forest on Floreana Island (2004-2013): Acoustical surveys cannot detect hybrids of Darwin’s tree finches Camarhynchus spp. Bird Conservation International, 1-17.
Peters, K.J., Myers S.A., Dudaniec R.Y., O’Connor J.A., Kleindorfer, S. (2017). Females drive asymmetrical introgression from rare to common species in Darwin’s tree finches. Journal of Evolutionary Biology, 30, 1940-1952.
Ryan, P. G. (2001). Morphological heritability in a hybrid bunting complex: Nesospiza at inaccessible island. Condor 103, 429-438.
Ryan, P. G. & Moloney, C. L. (2002). Breeding behaviour, clutch size and egg dimensions of Neospiza buntings at Inaccessible island, Tristan da Cunha. (vol 73, pg 52, 2002). Ostrich 73, 165-165.
Ryan, P. G., Moloney, C. L. & Hudon, J. (1994). Color Variation and Hybridization among Nesospiza Buntings on Inaccessible Island, Tristan-Da-Cunha. Auk 111, 314-327.