Behavioral Ecology and Sociobiology

, Volume 70, Issue 8, pp 1171–1186 | Cite as

Shadow of a doubt: premating and postmating isolating barriers in a temporally complex songbird (Passeriformes: Paridae) hybrid zone

Original Article


Hybrid zones, where populations with incomplete reproductive isolation interact, are particularly good systems in which to study how isolating barriers evolve during speciation. Examining a hybrid zone over time or with contacts of different ages allows us to understand the relative roles of and interactions between different isolating barriers (such as selection against hybrids, innate preferences for hybrid, or parental types) and how they change with continued contact between the interacting populations. One such temporally complex hybrid zone is that of two oscine songbirds, the black-crested (Baeolophus atricristatus) and tufted (B. bicolor) titmice (family Paridae). In one region, the two populations have been interbreeding for several thousands of years; elsewhere, populations of the two species have contacted within the past century. We tested (1) if males treat other populations as potential competition; (2) if females show preferences for male phenotype; and (3) if there are reproductive consequences to hybridization. We found that older zone males responded most strongly to conspecifics, whereas younger zone discrimination is weaker; moreover, females responded most strongly to tufted song and plumage. Intrinsic postmating isolation appears to be absent even in the older part of this system. Future studies should focus on potential ecological or behavioral postmating barriers preventing expansion of the hybridization.

Significance statement

Hybrid zones, areas where populations with distinct differences meet and interbreed, are excellent for studying speciation. Because hybridizing populations can interbreed but do not fully merge, they allow us to understand what behaviors and intrinsic incompatibilities keep populations apart. Hybrid zones that contain different ages of contact can be particularly useful because we can see how such behaviors change with continued interaction. We found differences between behaviors in the younger and older contact zones in one such complex hybrid zone between songbirds, indicating behaviors evolve with continued interaction. Few studies as yet have examined behavior directly in a temporally complex zone as we did here, so our study provide new insights into how behavior evolves during the divergence of new species.


Reproductive isolation Speciation Female choice Preference Song playback Baeolophus 


  1. Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New YorkGoogle Scholar
  2. Avise JC, Zink RM (1988) Molecular genetic divergence between avian sibling species: king and clapper rails, long-billed and short-billed dowitchers, boat-tailed and great-tailed grackles, and tufted and black-crested titmice. Auk 105:516–528Google Scholar
  3. Bacon BR (1987) A hanging cylinder funnel trap. N Am Bird Bander 12:46–47Google Scholar
  4. Baker MC, Bjerke TK, Lampe H, Espmark Y (1986) Sexual response of female great tits to variation in size of males’ song repertoires. Am Nat 128:491–498CrossRefGoogle Scholar
  5. Baldauf SA, Kullmann H, Bakker TCM (2008) Technical restrictions of computer-manipulated visual stimuli and display units for studying animal behaviour. Ethology 114:737–751CrossRefGoogle Scholar
  6. Barton NH (1992) On the spread of new gene combinations in the third phase of Wright’s shifting-balance. Evolution 46:551–557CrossRefGoogle Scholar
  7. Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148CrossRefGoogle Scholar
  8. Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package,
  9. Bracewell RR, Pfrender ME, Mock KE, Bentz BJ (2011) Cryptic postzygotic isolation in an eruptive species of bark beetle (Dendroctonus ponderosae). Evolution 65:961–975CrossRefPubMedGoogle Scholar
  10. Braun D, Kitto GB, Braun MJ (1984) Molecular population genetics of tufted and black-crested forms of Parus bicolor. Auk 101:170–173Google Scholar
  11. Bronson CL, Grubb TC, Sattler GD, Braun MJ (2005) Reproductive success across the black-capped chickadee (Poecile atricapillus) and Carolina chickadee (P. carolinensis) hybrid zone in Ohio. Auk 122:759–772CrossRefGoogle Scholar
  12. Callahan PH (2002) Progress from grassland to shrubland: woody encroachment in North American grasslands. MSc thesis, University of OklahomaGoogle Scholar
  13. Campbell DR, Waser NM, Aldridge G, Wu CA (2008) Lifetime fitness in two generations of Ipomopsis hybrids. Evolution 62:2616–2627CrossRefPubMedGoogle Scholar
  14. Carling MD, Zuckerberg B (2011) Spatio-temporal changes in the genetic structure of the Passerina bunting hybrid zone. Mol Ecol 20:1166–1175CrossRefPubMedGoogle Scholar
  15. Carmody G, Diaz Collazo A, Dobzhansky T, Ehrman L, Jaffrey IS, Kimball S, Obrebski S, Silagi S, Tidwell T, Ullrich R (1962) Mating preferences and sexual isolation within and between the incipient species of Drosophila paulistorum. Am Midl Nat 68:67–82CrossRefGoogle Scholar
  16. Cohen J (1992) A power primer. Psychol Bull 112:155–159CrossRefPubMedGoogle Scholar
  17. Coldren CL (1992) A comparison of the songs of the tufted and black-crested titmice in Texas. MSc thesis, Texas A&M UniversityGoogle Scholar
  18. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Inc., SunderlandGoogle Scholar
  19. Curé C, Aubin T, Mathevon N (2010) Intra-sex vocal interactions in two hybridizing seabird species (Puffinus sp.). Behav Ecol Sociobiol 64:1823–1837CrossRefGoogle Scholar
  20. Curry CM (2014) The evolution of reproductive isolation in a temporally complex passerine hybrid zone. PhD dissertation, University of OklahomaGoogle Scholar
  21. Curry CM, Patten MA (2014) Current and historical extent of phenotypic variation in the tufted and black-crested titmouse (Paridae) hybrid zone in the southern Great Plains. Am Midl Nat 171:271–300CrossRefGoogle Scholar
  22. Danner JE, Danner RM, Bonier F, Martin PR, Small TW, Moore IT (2011) Female, but not male, tropical sparrows respond more strongly to the local song dialect: implications for population divergence. Am Nat 178:53–63CrossRefPubMedGoogle Scholar
  23. Davidson BS, Sattler GD, Via S, Braun MJ (2013) Reproductive isolation and cryptic introgression in a sky island enclave of Appalachian birds. Ecol Evol 3:2485–2496CrossRefGoogle Scholar
  24. Del Re AC (2012) compute effect sizes. R package,
  25. Dingle C, Poelstra JW, Halfwerk W, Brinkhuizen DM, Slabbekoorn H (2010) Asymmetric response patterns to subspecies-specific song differences in allopatry and parapatry in the gray-breasted wood-wren. Evolution 64:3537–3548CrossRefPubMedGoogle Scholar
  26. Dixon KL (1955) An ecological analysis of the inter-breeding of crested titmice in Texas. Univ Calif Publ Zool 54:125–206Google Scholar
  27. Dixon KL (1978) A distributional history of the black-crested titmouse. Am Midl Nat 100:29–42CrossRefGoogle Scholar
  28. Dixon KL (1990) Constancy of margins of the hybrid zone in titmice of the Parus bicolor complex in coastal Texas. Auk 107:184–188Google Scholar
  29. Dopman EB, Robbins PS, Seaman A (2010) Components of reproductive isolation between North American strains of the European corn borer. Evolution 64:881–902CrossRefPubMedGoogle Scholar
  30. Egan SP, Janson EM, Brown CG, Funk DJ (2011) Postmating isolation and genetically variable host use in ecologically divergent host forms of Neochlamisus bebbianae leaf beetles. J Evol Biol 24:2217–2229CrossRefPubMedGoogle Scholar
  31. Feder JL (1998) The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 130–144Google Scholar
  32. Fotheringham JB, Ratcliffe L (1995) Song degradation and estimation of acoustic distance in black-capped chickadees (Parus atricapillus). Can J Zool 73:858–868CrossRefGoogle Scholar
  33. Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand OaksGoogle Scholar
  34. Gill FB, Slikas B (1992) Patterns of mitochondrial DNA divergence in North American crested titmice. Condor 94:20–28CrossRefGoogle Scholar
  35. Gill FB, Mostrom AM, Mack AL (1993) Speciation in North American chickadees: I. Patterns of mtDNA genetic divergence. Evolution 47:195–212CrossRefGoogle Scholar
  36. Gompert Z, Buerkle CA (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol Ecol 18:1207–1224CrossRefPubMedGoogle Scholar
  37. Grant BR, Grant PR (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proc R Soc Lond B 251:111–117CrossRefGoogle Scholar
  38. Grant PR, Grant BR (1997) Hybridization, sexual imprinting, and mate choice. Am Nat 149:1–28CrossRefGoogle Scholar
  39. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075CrossRefPubMedGoogle Scholar
  40. Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282CrossRefPubMedGoogle Scholar
  41. Guerra MA, Ron SR (2008) Mate choice and courtship signal differentiation promotes speciation in an Amazonian frog. Behav Ecol 19:1128–1135CrossRefGoogle Scholar
  42. Haavie J, Borge T, Bureš S, Garamszegi LZ, Lampe HM, Moreno J, Qvarnström A, Török J, Sætre G-P (2004) Flycatcher song in allopatry and sympatry—convergence, divergence and reinforcement. J Evol Biol 17:227–237CrossRefPubMedGoogle Scholar
  43. Harris RB, Carling MD, Lovette IJ (2014) The influence of sampling design on species tree inference: a new relationship for the new world chickadees (Aves: Poecile). Evolution 68:501–513CrossRefPubMedGoogle Scholar
  44. Harrison RG (1993) Hybrids and hybrid zones: historical perspective. In: Harrison RG (ed) Hybrid zones and the evolutionary process. Oxford University Press, New York, pp 3–12Google Scholar
  45. Hothorn T, Bretz F, Westfal P (2012) Multcomp: simultaneous inference in general parametric models. R package,
  46. Hudson EJ, Price TD (2014) Pervasive reinforcement and the role of sexual selection in biological speciation. J Hered 105:812–833CrossRefGoogle Scholar
  47. Hughes JM, Toon A, Mather PB, Lange CL (2011) Maintenance of a hybrid zone: the role of female mate choice. Auk 128:688–695CrossRefGoogle Scholar
  48. Kim Y-K, Phillips DR, Tao Y (2013) Evidence for no sexual isolation between Drosophila albomicans and D. nasuta. Ecol Evol 3:2061–2074CrossRefPubMedPubMedCentralGoogle Scholar
  49. Klicka J, Zink RM (1997) The importance of recent Ice Ages in speciation: a failed paradigm. Science 277:1666–1669CrossRefGoogle Scholar
  50. Kozak GM, Boughman JW (2009) Learned conspecific mate preference in a species pair of sticklebacks. Behav Ecol 20:1282–1288CrossRefGoogle Scholar
  51. Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kremer A (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242CrossRefPubMedGoogle Scholar
  52. Matsubayashi KW, Katakura H (2009) Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution 63:2563–2580CrossRefPubMedGoogle Scholar
  53. Matute DR, Coyne JA (2010) Intrinsic reproductive isolation between two sister species of Drosophila. Evolution 64:903–920CrossRefPubMedGoogle Scholar
  54. Mayr E (1946) Experiments on sexual isolation in Drosophila: VI. Isolation between Drosophila pseudoobscura and Drosophila persimilis and their hybrids. Proc Natl Acad Sci U S A 32:57CrossRefPubMedPubMedCentralGoogle Scholar
  55. Merrill RM, Gompert Z, Dembeck LM, Kronforst MR, McMillan WO, Jiggins CD (2011) Mate preference across the speciation continuum in a clade of mimetic butterflies. Evolution 65:1489–1500CrossRefPubMedGoogle Scholar
  56. Mettler RD, Spellman GM (2009) A hybrid zone revisited: molecular and morphological analysis of the maintenance, movement, and evolution of a Great Plains avian (Cardinalidae: Pheucticus) hybrid zone. Mol Ecol 18:3256–3267CrossRefPubMedPubMedCentralGoogle Scholar
  57. Moore WS (1977) An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–277CrossRefGoogle Scholar
  58. Moravec ML, Striedter GF, Burley NT (2010) “Virtual parrots” confirm mating preferences of female budgerigars. Ethology 116:961–971CrossRefGoogle Scholar
  59. Moriarty Lemmon E, Lemmon AR (2010) Reinforcement in chorus frogs: lifetime fitness estimates including intrinsic natural and sexual selection against hybrids. Evolution 64:1748–1761CrossRefGoogle Scholar
  60. Murphy TG, Hernandez-Mucino D, Osorio-Beristain M, Montgomerie R, Omland KE (2009a) Carotenoid-based status signaling by females in the tropical streak-backed oriole. Behav Ecol 20:1000–1006CrossRefGoogle Scholar
  61. Murphy TG, Rosenthal MF, Montgomerie R, Tarvin KA (2009b) Female American goldfinches use carotenoid-based bill coloration to signal status. Behav Ecol 20:1348–1355CrossRefGoogle Scholar
  62. Nolte AW, Gompert Z, Buerkle CA (2009) Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations. Mol Ecol 18:2615–2627CrossRefPubMedGoogle Scholar
  63. O’Loghlen AL, Rothstein SI (2010) It’s not just the song: male visual displays enhance female sexual responses to song in brown-headed cowbirds. Condor 112:615–621CrossRefGoogle Scholar
  64. Otter K, Ratcliffe L, Michaud D, Boag PT (1998) Do female black-capped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol 42:25–36CrossRefGoogle Scholar
  65. Palumbi SR, Metz EC (1991) Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol 8:227–239PubMedGoogle Scholar
  66. Patten MA, Smith-Patten BD (2008) Black-crested titmouse (Baeolophus atricristatus). In: Poole A (ed) The birds of North America, No 717. Cornell Laboratory of Ornithology, Ithaca, NYGoogle Scholar
  67. Patten MA, Rotenberry JT, Zuk M (2004) Habitat selection, acoustic adaptation, and the evolution of reproductive isolation. Evolution 58:2144–2155CrossRefPubMedGoogle Scholar
  68. Powell THQ, Cha DH, Linn CE, Feder JL (2012) On the scent of standing variation for speciation: behavioral evidence for native sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae) in the southern United States. Evolution 66:2739–2756CrossRefPubMedGoogle Scholar
  69. Pravosudova EV, Parker PG, Gaunt AS (2002) Genetic evidence for extrapair paternity in the tufted titmouse. Wilson Bull 114:279–281CrossRefGoogle Scholar
  70. Price TD (2008) Speciation in birds. Roberts and Company, Greenwood VillageGoogle Scholar
  71. Price TD, Bouvier MM (2002) The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083–2089CrossRefPubMedGoogle Scholar
  72. Pulich WM (1988) Birds of north-central Texas. Texas A&M University Press, College StationGoogle Scholar
  73. Pyron RA, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev 90:1248–1262CrossRefPubMedGoogle Scholar
  74. Quinn TP, Unwin MJ, Kinnison MT (2000) Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced chinook salmon populations. Evolution 54:1372–1385CrossRefPubMedGoogle Scholar
  75. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  76. Reudink MW, Mech SG, Curry RL (2006) Extrapair paternity and mate choice in a chickadee hybrid zone. Behav Ecol Sociobiol 17:56–62CrossRefGoogle Scholar
  77. Rising JD (1983) The Great Plains hybrid zones. Curr Ornithol 1:131–157CrossRefGoogle Scholar
  78. Rolán-Alvarez E, Johannesson K, Erlandsson J (1997) The maintenance of a cline in the marine snail Littorina saxatilis: the role of home site advantage and hybrid fitness. Evolution 51:1838–1847CrossRefGoogle Scholar
  79. Roy J-S, O’Connor D, Green DM (2012) Oscillation of an anuran hybrid zone: morphological evidence spanning 50 years. PLoS One 7:e52819CrossRefPubMedPubMedCentralGoogle Scholar
  80. Sætre G-P, Sæther SA (2010) Ecology and genetics of speciation in Ficedula flycatchers. Mol Ecol 19:1091–1106CrossRefPubMedGoogle Scholar
  81. Sætre G-P, Král K, Bureš S, Ims RA (1999) Dynamics of a clinal hybrid zone and a comparison with island hybrid zones of flycatchers (Ficedula hypoleuca and F. albicollis). J Zool 247:53–64CrossRefGoogle Scholar
  82. Sánchez-Guillén RA, Wullenreuther M, Cordero Rivera A (2012) Strong asymmetry in the relative strengths of prezygotic and postzygotic barriers between two damselfly sister species. Evolution 66:690–707CrossRefPubMedGoogle Scholar
  83. Sasa MM, Chippindale PT, Johnson NA (1998) Patterns of post-zygotic isolation in frogs. Evolution 52:1811–1820CrossRefGoogle Scholar
  84. Schlupp I (2000) Are there lessons from negative results in studies using video playback? Acta Ethol 3:9–13CrossRefGoogle Scholar
  85. Searcy WA (1992) Measuring responses of female birds to male song. In: McGregor PK (ed) Playback and studies of animal communication. Plenum Press, New York, pp 175–189CrossRefGoogle Scholar
  86. Searcy WA, Brenowitz EA (1988) Sexual differences in species recognition of avian song. Nature 332:152–154CrossRefGoogle Scholar
  87. Searcy WA, Nowicki S, Hughes M (1997) The response of male and female song sparrows to geographic variation in song. Condor 99:651–657CrossRefGoogle Scholar
  88. Shaffer TL (2004) A unified approach to analyzing nest success. Auk 121:526–540CrossRefGoogle Scholar
  89. Shonfield J, Taylor RW, Boutin S, Humphries MM, McAdam AG (2012) Territorial defence behavior in red squirrels is influenced by local density. Behaviour 149:369–390CrossRefGoogle Scholar
  90. Shriver WG, Gibbs JP, Vickery PD, Gibbs HL, Hodgman TP, Jones PT, Jacques C, Fleischer RC (2005) Concordance between morphological and molecular markers in assessing hybridization between sharp-tailed sparrows in New England. Auk 122:94–107CrossRefGoogle Scholar
  91. Smith KL, Hale JM, Gay L, Kearney M, Austin JJ, Parris KM, Melville J (2013) Spatio-temporal changes in the structure of an Australian frog hybrid zone: a 40-year perspective. Evolution 67:3442–3454CrossRefPubMedGoogle Scholar
  92. Stelkens RB, Young KA, Seehausen O (2010) The accumulation of reproductive incompatabilities in African cichlid fish. Evolution 64:617–633CrossRefPubMedGoogle Scholar
  93. Tarvin KA, Murphy TG (2012) It isn’t always sexy when both are bright and shiny: considering alternatives to sexual selection in elaborate monomorphic species. Ibis 154:439–443CrossRefGoogle Scholar
  94. Trivers RL (1972) Parental investment and sexual selection. In: Campbell BG (ed) Sexual selection and the descent of man 1871–1971. Aldine Publishing Company, Chicago, pp 136–179Google Scholar
  95. Vallin N, Rice AM, Bailey RI, Husby A, Qvarnström A (2012) Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone. Evolution 66:1167–1179CrossRefPubMedGoogle Scholar
  96. Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New YorkCrossRefGoogle Scholar
  97. Ward JL, McLennan DA (2009) Mate choice based on complex visual signals in the brook stickleback, Culaea inconstans. Behav Ecol 20:1323–1333CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Natural Resources InstituteUniversity of ManitobaWinnipegCanada
  2. 2.Oklahoma Biological SurveyUniversity of OklahomaNormanUSA
  3. 3.Ecology and Evolutionary Biology Program, Department of BiologyUniversity of OklahomaNormanUSA

Personalised recommendations