Paridae

The Tits, Chickadees and Titmice a large passerine family which occurs across the Northern Hemisphere and in Africa. Hybridization has been observed in most genera.

 

Baeolophus

Oak Titmouse (B. inornatus) and Juniper Titmouse (B. ridgwayi) interbreed across northern California. Patterns of molecular variation are congruent with morphological and bioclimatic data. Oak Titmouse is able to expand into the range of Juniper Titmouse, which results in asymmetric introgression (Cicero, 2004).

In Texas and south-western Oklahoma Black-crested Titmouse (B. atricristatus) and Tufted Titmouse (B. bicolor) hybridize (Braun, Kitto & Braun, 1984; Dixon, 1955; Dixon, 1990). Morphological analysis of this hybrid zone indicates selection against hybrids (Curry & Patten, 2014).

Black-crested Titmouse (Baeolophus atricristatus) and Tufted Titmouse (B. bicolor)

 

Parus

The Great Tit (P. major) complex is divided into five groups, each containing several subspecies (Song et al., 2020). Mitochondrial DNA analysis showed that these groups are monophyletic and that hybridization between members of these groups are thus the result of secondary contact (Kvist et al., 2003a). The Great Tit complex is not a ring species, a conclusion that was further supported by new genetic data and song analysis (Packert et al., 2005). The hybrid zone between Great Tit and Japanese Tit (P. minor) has been well studied (Fedorov et al., 2006; Fedorov et al., 2009; Kvist & Rytkonen, 2006; Nazarenko, Valchuk & Martens, 1999) and even led to the discovery of paternal leakage of mtDNA (Kvist et al., 2003b).

Gene flow between island and mainland populations of Great Tits has led to differences in clutch sizes. Immigrants bring in genes for bigger clutch sizes. When gene flow is low (due to low immigration rates and selection against immigrants) clutch sizes are small, an adaptation to the island environment. In other areas, where gene flow is higher, clutch sizes are also bigger (Postma & van Noordwijk, 2005).

A cross-fostering experiment led to heterospecific pairings between Great Tit and Blue Tit (P. caeruleus), although all fledgling were Blue Tits (Slagsvold et al., 2002).

French populations of Blue Tit exhibit a mitochondrial polymorphism that could be the result of hybridization with Azure Tit (P. cyaneus) (Taberlet, Meyer & Bouvet, 1992).

Hybridization between Siberian Tit (P. cinctus) and Willow Tit (P. montanus) has been documented on multiple occasions (Järvinen, Ylimaunu & Hannila, 1985; Järvinen, 1987; Järvinen, 1989; Järvinen, 1997).

Great Tit (Parus major)

 

Periparus

A genetic study of the European Coal Tit (P. ater) indicated that German populations are a mixture of northern and southern populations, extending over a broad zone of intergradation (Tritsch et al. 2018).

Coal Tit (Periparus ater)

 

Poecile

Morphological and ecological similarities between Black-capped Chickadee (P. atricapillus) and Carolina Chickadee (P. carolensis) raised the suspicion that these species might be interbreeding (Brewer, 1963; Tanner, 1952). Hybridization was later confirmed by morphological (Johnston, 1971; Rising, 1968; Robbins, Braun & Tobey, 1986) and genetic analyses (Braun & Robbins, 1986; Sattler & Braun, 2000). Hybrids showed decreased reproductive success, indicating endogenous selection (Bronson, Grubb & Braun, 2003a; Bronson et al., 2005). The situation was summarized by Curry (2005). Hybridization has led to introgression, which was lower at highly divergent loci that might be involved in reproductive isolation (Taylor et al., 2014a). One population of Black-capped Chickadees is isolated in the Appalachian Mountains and has experienced less introgression compared to other populations near the hybrid zone (Davidson et al., 2013).

Other genetic studies showed that the hybrid zone is moving north and becoming wider (Reudink et al., 2007), suggesting a selective advantage for the Caroline Chickadee. Indeed, experimental work confirmed that females have a preference for Carolina-like birds (Bronson et al., 2003b) and patterns of extrapair paternity (EPP) led to a similar conclusion (Reudink, Mech & Curry, 2006). The precise characteristics that provide Caroline Chickadees were unknown. Sexual selection might be involved, but song turned out to be a poor indicator for hybridization (Enstrom & Bollinger, 2009; Sattler, Sawaya & Braun, 2007). However, winter temperatures seem to limit the distribution of Caroline Chickadees. The northward expansion (and subsequent hybridization) may be connected to recent climate change (Taylor et al., 2014b), although another study did not find a significant relation between lower air temperatures and basal metabolic rates (BMR) of Carolina Chickadees (Olson et al., 2010). Hybrids perform worse on associative learning and problem-solving tasks. This lower intelligence could act as a postzygotic isolation mechanisms (McQuillan et al., 2018). Genomic work supported a role for metabolism and learning in postzygotic isolation (Wagner et al., 2020).

Experiments shows that Black-capped Chickadee and Carolina Chickadee can discriminate between species using olfactory cues. Possible, odor can promote premating reproductive isolation (Van Huynh & Rice, 2019).

Black-capped Chickadees also hybridize with Boreal Chickadee (P. hudsonicus) (Lait, Lauff & Burg, 2012) and Mountain Chickadee (P. gambeli) (Grava et al., 2012). In the latter case, hybridization might have led to character displacement in song (Grava et al., 2013). Populations of Mountain Chickadee that have been diverging since the Pleistocene exhibit different rates of gene flow among each other (Spellman, Riddle & Klicka, 2007). While southern populations continue to diverge, northern populations might converge and form a “hybrid” species (Manthey, Klicka & Spellman, 2012). Although there are phenotypic differences along an altitudinal gradient, there is no genetic differentiation between high and low elevation populations. Phenotypic variation might be maintained by strong selection despite gene flow (Branch et al. 2017).

Black-capped Chickadee (Poecile atricapillus) and Carolina Chickadee (P. carolensis)

 

Pseudopodoces

In the Ground Tit (P. humilis), genomic analyses revealed an incipient speciation with unidirectional gene flow from the edge to platform populations on the Qinghai-Tibet Plateau. This suggests that both refugial isolation and the subsequent habitat differentiation and morphological divergence have contributed and maintained the incipient speciation pattern between the platform and edge populations of this species (Jiang et al., 2019).

A pair of Ground Tits near Hongyuan (Tibetan Plateau), Sichuan, China. © Ulrich Weber | Oriental Bird Images.

 

References

Branch C.L., Jahner J.P., Kozlovsky D.Y., Parchman T.L., Pravosudov V.V. (2017) Absence of population structure across elevational gradients despite large phenotypic variation in mountain chickadees( Poecile gambeli).Royal Society Open Science 4, 170057.

Braun, D., Kitto, G. & Braun, M. (1984). Molecular population genetics of tufted and black-crested forms of Parus bicolor. The Auk, 170-173.

Braun, M. J. & Robbins, M. B. (1986). Extensive Protein Similarity of the Hybridizing Chickadees Parus-Atricapillus and Parus-Carolinensis. Auk 103, 667-675.

Brewer, R. (1963). Ecological and reproductive relationships of Black-capped and Carolina chickadees. The Auk, 9-47.

Bronson, C. L., Grubb, T. C. & Braun, M. J. (2003a). A test of the endogenous and exogenous selection hypotheses for the maintenance of a narrow avian hybrid zone. Evolution 57, 630-637.

Bronson, C. L., Grubb, T. C., Sattler, G. D. & Braun, M. J. (2003b). Mate preference: a possible causal mechanism for a moving hybrid zone. Animal Behaviour 65, 489-500.

Bronson, C. L., Grubb, T. C., Sattler, G. D. & Braun, M. J. (2005). Reproductive success across the black-capped Chickadee (Poecile atricapillus) and Carolina Chickadee (P-Carolinensis) hybrid zone in Ohio. Auk 122, 759-772.

Cicero, C. (2004). Barriers to sympatry between avian sibling species (Paridae : Baeolophus) in local secondary contact. Evolution 58, 1573-1587.

Curry, C. M. & Patten, M. A. (2014). Current and Historical Extent of Phenotypic Variation in the Tufted and Black-crested Titmouse (Paridae) Hybrid Zone in the Southern Great Plains. American Midland Naturalist 171, 271-300.

Curry, R. L. (2005). Hybridization in Chickadees: Much to learn from familiar birds. Auk 122, 747-758.

Davidson, B. S., Sattler, G. D., Via, S. & Braun, M. J. (2013). Reproductive isolation and cryptic introgression in a sky island enclave of Appalachian birds. Ecology and Evolution 3, 2485-2496.

Dixon, K. L. (1955). An ecological analysis of the interbreeding of crested titmice in Texas. University of California Press.

Dixon, K. L. (1990). Constancy of margins of the hybrid zone in titmice of the Parus bicolor complex in coastal Texas. The Auk, 184-188.

Enstrom, P. C. & Bollinger, E. K. (2009). Stability in Distributions of Black-Capped, Carolina, and Aberrant Chickadee Song Types in Illinois. Wilson Journal of Ornithology 121, 265-272.

Fedorov, V., Formozov, N., Kerimov, A., Surin, V. & Val’chuk, O. (2006). Genetic consequences of hybridization between Parus major and P. minor in the Middle Amur river basin. Зоологический журнал 85.

Fedorov, V. V., Surin, V. L., Valchuk, O. P., Kapitonova, L. V., Kerimov, A. B. & Formozov, N. A. (2009). Maintaining morphological specificity and genetic introgression in populations of the great tit Parus major and the Japanese tit P. minor in the middle Amur region. Russian Journal of Genetics 45, 771-780.

Grava, A., Grava, T., Didier, R., Lait, L. A., Dosso, J., Koran, E., Burg, T. M. & Otter, K. A. (2012). Interspecific dominance relationships and hybridization between black-capped and mountain chickadees. Behavioral Ecology 23, 566-572.

Grava, A., Otter, K. A., Grava, T., LaZerte, S. E., Poesel, A. & Rush, A. C. (2013). Character displacement in dawn chorusing behaviour of sympatric mountain and black-capped chickadees. Animal Behaviour 86, 177-187.

Järvinen, A. (1987). A successful mixed breeding between Parus cinctus and Parus montanus in Finnish Lapland. Ornis Fennica 64, 158-159.

Järvinen, A. (1997). Interspecific hybridization between the Siberian Tit Parus cinctus and the Willow Tit Parus montanus produces fertile offspring. Ornis Fennica 74, 149-152.

Järvinen, A. (1989). More mixed breedings between Parus cinctus and P. montanus in Finnish Lapland. Ornis Fennica  66(3):123.

Järvinen, A., Ylimaunu, J. & Hannila, J. (1985). A mixed nesting pair Parus montanus and P. cinctus in Finnish Lapland. Ornis Fennica 62, 25-26.

Jiang, Z.Y., Gao, B., Lei, F.M. & Qu, Y.H. (2019) Population genomics reveals that refugial isolation and habitat change lead to incipient speciation in the Ground tit. Zoologica Scripta.

Johnston, D. W. (1971). Ecological Aspects of Hybridizing Chickadees (Parus) in Virginia. American Midland Naturalist 85, 124-134.

Kvist, L., Martens, J., Higuchi, H., Nazarenko, A. A., Valchuk, O. P. & Orell, M. (2003a). Evolution and genetic structure of the great tit (Parus major) complex. Proceedings of the Royal Society B-Biological Sciences 270, 1447-1454.

Kvist, L., Martens, J., Nazarenko, A. A. & Orell, M. (2003b). Paternal leakage of mitochondrial DNA in the great tit (Parus major). Molecular Biology and Evolution 20, 243-247.

Kvist, L. & Rytkonen, S. (2006). Characterization of a secondary contact zone of the Great Tit Parus major and the Japanese Tit P-minor (Aves : Passeriformes) in Far Eastern Siberia with DNA markers. Zootaxa, 55-73.

Lait, L. A., Lauff, R. F. & Burg, T. M. (2012). Genetic Evidence Supports Boreal Chickadee (Poecile hudsonicus) x Black-capped Chickadee (Poecile atricapillus) Hybridization in Atlantic Canada. Canadian Field-Naturalist 126, 143-147.

Manthey, J. D., Klicka, J. & Spellman, G. M. (2012). Is Gene Flow Promoting the Reversal of Pleistocene Divergence in the Mountain Chickadee (Poecile gambeli)? Plos One 7.

McQuillan, M., Roth II, T.C., Huynh, A.V. & Rice, A.M. (2018) Hybrid chickadees are deficient in learning and memory. Evolution

Nazarenko, A., Valchuk, O. & Martens, J. (1999). Secondary contact and overlap of Parus major and Parus minor populations in the middle Amur river basin. Zoologichesky Zhurnal 78, 372-381.

Olson, J. R., Cooper, S. J., Swanson, D. L., Braun, M. J. & Williams, J. B. (2010). The Relationship of Metabolic Performance and Distribution in Black-Capped and Carolina Chickadees. Physiological and Biochemical Zoology 83, 263-275.

Packert, M., Martens, J., Eck, S., Nazarenko, A. A., Valchuk, O. P., Petri, B. & Veith, M. (2005). The great tit (Parus major) – a misclassified ring species. Biological Journal of the Linnean Society 86, 153-174.

Postma, E. & van Noordwijk, A. J. (2005). Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature 433, 65-68.

Reudink, M. W., Mech, S. G. & Curry, R. L. (2006). Extrapair paternity and mate choice in a chickadee hybrid zone. Behavioral Ecology 17, 56-62.

Reudink, M. W., Mech, S. G., Mullen, S. P. & Curry, R. L. (2007). Structure and dynamics of the hybrid zone between black-capped chickadee (Poecile atricapillus) and Carolina chickadee (P-carolinensis) in southeastern Pennsylvania. Auk 124, 463-478.

Rising, J. D. (1968). A multivariate assessment of interbreeding between the chickadees, Parus atricapillus and P. carolinensis. Systematic Biology 17, 160-169.

Robbins, M. B., Braun, M. J. & Tobey, E. A. (1986). Morphological and vocal variation across a contact zone between the chickadees Parus atricapillus and P. carolinensis. The Auk, 655-666.

Sattler, G. D. & Braun, M. J. (2000). Morphometric variation as an indicator of genetic interactions between Black-capped and Carolina chickadees at a contact zone in the Appalachian mountains. Auk 117, 427-444.

Sattler, G. D., Sawaya, P. & Braun, M. J. (2007). An assessment of song admixture as an indicator of hybridization in Black-capped Chickadees (Poecile atricapillus) and Carolina Chickadees (P-carolinensis). Auk 124, 926-944.

Slagsvold, T., Hansen, B. T., Johannessen, L. E. & Lifjeld, J. T. (2002). Mate choice and imprinting in birds studied by cross-fostering in the wild. Proceedings of the Royal Society B-Biological Sciences 269, 1449-1455.

Spellman, G. M., Riddle, B. & Klicka, J. (2007). Phylogeography of the mountain chickadee (Poecile gambeli): diversification, introgression, and expansion in response to Quaternary climate change. Molecular Ecology 16, 1055-1068.

Song, G. et al. (2020). Great journey of Great Tits (Parus major group): Origin, diversification and historical demographics of a broadly distributed bird lineage. Journal of Biogeography.

Taberlet, P., Meyer, A. & Bouvet, J. (1992). Unusual mitochondrial DNA polymorphism in two local populations of blue tit Parus caeruleus. Molecular Ecology 1, 27-36.

Tanner, J. T. (1952). Black-capped and Carolina chickadees in the southern Appalachian Mountains. The Auk, 407-424.

Taylor, S. A., Curry, R. L., White, T. A., Ferretti, V. & Lovette, I. (2014a). Spatiotemporally consistent genomic signatures of reproductive isolation in a moving hybrid zone. Evolution 68, 3066-3081.

Taylor, S. A., White, T. A., Hochachka, W. M., Ferretti, V., Curry, R. L. & Lovette, I. (2014b). Climate-Mediated Movement of an Avian Hybrid Zone. Current Biology 24, 671-676.

Tritsch, C., Stuckas, H., Martens, J., Pentzold, S., Kvist, L., Lo Valvo, M., Giacalone, G., Tietze, D.T., Nazarenko, A.A. & Päckert, M. (2018) Gene flow in the European coal tit, Periparus ater (Aves: Passeriformes): low among Mediterranean populations but high in a continental contact zone. Biological Journal of the Linnean Society, 124(3):319-338.

Van Huynh, A., & Rice, A. M. (2019). Conspecific olfactory preferences and interspecific divergence in odor cues in a chickadee hybrid zone. Ecology and Evolution.

Wagner, D. N., Curry, R. L., Chen, N., Lovette, I. J., & Taylor, S. A. (2020). Genomic regions underlying metabolic and neuronal signaling pathways are temporally consistent in a moving avian hybrid zone. Evolution.