Abstract
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.
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References
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York
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 105:516–528
Bacon BR (1987) A hanging cylinder funnel trap. N Am Bird Bander 12:46–47
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 128:491–498
Baldauf SA, Kullmann H, Bakker TCM (2008) Technical restrictions of computer-manipulated visual stimuli and display units for studying animal behaviour. Ethology 114:737–751
Barton NH (1992) On the spread of new gene combinations in the third phase of Wright’s shifting-balance. Evolution 46:551–557
Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148
Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package, http://CRAN.R-project.org/package=lme4
Bracewell RR, Pfrender ME, Mock KE, Bentz BJ (2011) Cryptic postzygotic isolation in an eruptive species of bark beetle (Dendroctonus ponderosae). Evolution 65:961–975
Braun D, Kitto GB, Braun MJ (1984) Molecular population genetics of tufted and black-crested forms of Parus bicolor. Auk 101:170–173
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 122:759–772
Callahan PH (2002) Progress from grassland to shrubland: woody encroachment in North American grasslands. MSc thesis, University of Oklahoma
Campbell DR, Waser NM, Aldridge G, Wu CA (2008) Lifetime fitness in two generations of Ipomopsis hybrids. Evolution 62:2616–2627
Carling MD, Zuckerberg B (2011) Spatio-temporal changes in the genetic structure of the Passerina bunting hybrid zone. Mol Ecol 20:1166–1175
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 68:67–82
Cohen J (1992) A power primer. Psychol Bull 112:155–159
Coldren CL (1992) A comparison of the songs of the tufted and black-crested titmice in Texas. MSc thesis, Texas A&M University
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Inc., Sunderland
Curé C, Aubin T, Mathevon N (2010) Intra-sex vocal interactions in two hybridizing seabird species (Puffinus sp.). Behav Ecol Sociobiol 64:1823–1837
Curry CM (2014) The evolution of reproductive isolation in a temporally complex passerine hybrid zone. PhD dissertation, University of Oklahoma
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 171:271–300
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 178:53–63
Davidson BS, Sattler GD, Via S, Braun MJ (2013) Reproductive isolation and cryptic introgression in a sky island enclave of Appalachian birds. Ecol Evol 3:2485–2496
Del Re AC (2012) Compute.es: compute effect sizes. R package, http://cran.r-project.org/web/packages/compute.es
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 64:3537–3548
Dixon KL (1955) An ecological analysis of the inter-breeding of crested titmice in Texas. Univ Calif Publ Zool 54:125–206
Dixon KL (1978) A distributional history of the black-crested titmouse. Am Midl Nat 100:29–42
Dixon KL (1990) Constancy of margins of the hybrid zone in titmice of the Parus bicolor complex in coastal Texas. Auk 107:184–188
Dopman EB, Robbins PS, Seaman A (2010) Components of reproductive isolation between North American strains of the European corn borer. Evolution 64:881–902
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 24:2217–2229
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 130–144
Fotheringham JB, Ratcliffe L (1995) Song degradation and estimation of acoustic distance in black-capped chickadees (Parus atricapillus). Can J Zool 73:858–868
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks
Gill FB, Slikas B (1992) Patterns of mitochondrial DNA divergence in North American crested titmice. Condor 94:20–28
Gill FB, Mostrom AM, Mack AL (1993) Speciation in North American chickadees: I. Patterns of mtDNA genetic divergence. Evolution 47:195–212
Gompert Z, Buerkle CA (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol Ecol 18:1207–1224
Grant BR, Grant PR (1993) Evolution of Darwin’s finches caused by a rare climatic event. Proc R Soc Lond B 251:111–117
Grant PR, Grant BR (1997) Hybridization, sexual imprinting, and mate choice. Am Nat 149:1–28
Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282
Guerra MA, Ron SR (2008) Mate choice and courtship signal differentiation promotes speciation in an Amazonian frog. Behav Ecol 19:1128–1135
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 17:227–237
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 68:501–513
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 3–12
Hothorn T, Bretz F, Westfal P (2012) Multcomp: simultaneous inference in general parametric models. R package, http://multcomp.r-forge.r-project.org/
Hudson EJ, Price TD (2014) Pervasive reinforcement and the role of sexual selection in biological speciation. J Hered 105:812–833
Hughes JM, Toon A, Mather PB, Lange CL (2011) Maintenance of a hybrid zone: the role of female mate choice. Auk 128:688–695
Kim Y-K, Phillips DR, Tao Y (2013) Evidence for no sexual isolation between Drosophila albomicans and D. nasuta. Ecol Evol 3:2061–2074
Klicka J, Zink RM (1997) The importance of recent Ice Ages in speciation: a failed paradigm. Science 277:1666–1669
Kozak GM, Boughman JW (2009) Learned conspecific mate preference in a species pair of sticklebacks. Behav Ecol 20:1282–1288
Lepais O, Petit RJ, Guichoux E, Lavabre JE, Alberto F, Kremer A (2009) Species relative abundance and direction of introgression in oaks. Mol Ecol 18:2228–2242
Matsubayashi KW, Katakura H (2009) Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution 63:2563–2580
Matute DR, Coyne JA (2010) Intrinsic reproductive isolation between two sister species of Drosophila. Evolution 64:903–920
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 32:57
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 65:1489–1500
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 18:3256–3267
Moore WS (1977) An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52:263–277
Moravec ML, Striedter GF, Burley NT (2010) “Virtual parrots” confirm mating preferences of female budgerigars. Ethology 116:961–971
Moriarty Lemmon E, Lemmon AR (2010) Reinforcement in chorus frogs: lifetime fitness estimates including intrinsic natural and sexual selection against hybrids. Evolution 64:1748–1761
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 20:1000–1006
Murphy TG, Rosenthal MF, Montgomerie R, Tarvin KA (2009b) Female American goldfinches use carotenoid-based bill coloration to signal status. Behav Ecol 20:1348–1355
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 18:2615–2627
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 112:615–621
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 42:25–36
Palumbi SR, Metz EC (1991) Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol 8:227–239
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, NY
Patten MA, Rotenberry JT, Zuk M (2004) Habitat selection, acoustic adaptation, and the evolution of reproductive isolation. Evolution 58:2144–2155
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 66:2739–2756
Pravosudova EV, Parker PG, Gaunt AS (2002) Genetic evidence for extrapair paternity in the tufted titmouse. Wilson Bull 114:279–281
Price TD (2008) Speciation in birds. Roberts and Company, Greenwood Village
Price TD, Bouvier MM (2002) The evolution of F1 postzygotic incompatibilities in birds. Evolution 56:2083–2089
Pulich WM (1988) Birds of north-central Texas. Texas A&M University Press, College Station
Pyron RA, Costa GC, Patten MA, Burbrink FT (2015) Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev 90:1248–1262
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 54:1372–1385
R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reudink MW, Mech SG, Curry RL (2006) Extrapair paternity and mate choice in a chickadee hybrid zone. Behav Ecol Sociobiol 17:56–62
Rising JD (1983) The Great Plains hybrid zones. Curr Ornithol 1:131–157
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 51:1838–1847
Roy J-S, O’Connor D, Green DM (2012) Oscillation of an anuran hybrid zone: morphological evidence spanning 50 years. PLoS One 7:e52819
Sætre G-P, Sæther SA (2010) Ecology and genetics of speciation in Ficedula flycatchers. Mol Ecol 19:1091–1106
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 247:53–64
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 66:690–707
Sasa MM, Chippindale PT, Johnson NA (1998) Patterns of post-zygotic isolation in frogs. Evolution 52:1811–1820
Schlupp I (2000) Are there lessons from negative results in studies using video playback? Acta Ethol 3:9–13
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 175–189
Searcy WA, Brenowitz EA (1988) Sexual differences in species recognition of avian song. Nature 332:152–154
Searcy WA, Nowicki S, Hughes M (1997) The response of male and female song sparrows to geographic variation in song. Condor 99:651–657
Shaffer TL (2004) A unified approach to analyzing nest success. Auk 121:526–540
Shonfield J, Taylor RW, Boutin S, Humphries MM, McAdam AG (2012) Territorial defence behavior in red squirrels is influenced by local density. Behaviour 149:369–390
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 122:94–107
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 67:3442–3454
Stelkens RB, Young KA, Seehausen O (2010) The accumulation of reproductive incompatabilities in African cichlid fish. Evolution 64:617–633
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 154:439–443
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 136–179
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 66:1167–1179
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Ward JL, McLennan DA (2009) Mate choice based on complex visual signals in the brook stickleback, Culaea inconstans. Behav Ecol 20:1323–1333
Acknowledgments
We are grateful to the following landowners and site managers who provided access to their land: J. and W. Erickson, S. Osborne, U.S. Fish and Wildlife Service, Texas Parks and Wildlife Department, Texas Historical Commission, The City of Graham, Oklahoma Department of Wildlife Conservation, Oklahoma Department of Tourism and Recreation, Quartz Mountain Nature Park, Oklahoma Biological Survey, and the U.S. Forest Service. We thank the volunteers who collected the nesting data for this study through The Cornell Laboratory of Ornithology’s Nest Box Network, The Birdhouse Network, NestWatch, the Smithsonian Migratory Bird Research Center’s Neighborhood NestWatch, and various state nest monitoring projects that have contributed their historic data. T. Murphy, B. Sandercock, and J.M. Martin discussed several aspects of this paper with us; J.M. Martin also facilitated access to the NestWatch dataset. A. Ainsworth and S.H. Stuart aided with bird care and fieldwork. J. Kelly, R. Broughton, W. Elisens, B. Hoagland, G. Wellborn, E. Bridge, A. Harris, T. Steil, R. Madding, D. Hough, J. Helms, M. Herzog, T. Yuri, B. Freeman, R. Kostecke, D. Bryant, A.J. Contina, D. Roeder, W.T. Honeycutt, M. Curry, and J. Curry provided additional logistical support and comments. T. D. Price and three anonymous reviewers provided comments that greatly improved this manuscript.
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CMC was supported by a Department of Education Graduate Assistance in Areas of National Need Fellowship and a University of Oklahoma (OU) Graduate College Alumni Fellowship. Funding for field and lab work was provided by the George Miksch Sutton Scholarship in Ornithology, American Museum of Natural History, Sigma Xi, Oklahoma Ornithological Society, M. Blanche and M. Frances Adams Summer Research and Academic Year Scholarships, and the OU Graduate Student Senate and Graduate College.
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All applicable international, national, and institutional guidelines for the care and use of animals were followed. All procedures performed were in accordance with the ethical standards of the institution at which the studies were conducted. These studies were conducted under Federal Bird Banding Permit 23215H, Federal Fish and Wildlife Permit MB148195-2, Oklahoma Department of Wildlife Conservation Scientific Collecting Permits 4716, 4955, 5210, and 5507; Texas Parks and Wildlife Department Scientific Collecting Permit SPR-0310-019; and University of Oklahoma Institutional Animal Care and Use Committee protocols R09-004 and R12-009.
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Curry, C.M., Patten, M.A. Shadow of a doubt: premating and postmating isolating barriers in a temporally complex songbird (Passeriformes: Paridae) hybrid zone. Behav Ecol Sociobiol 70, 1171–1186 (2016). https://doi.org/10.1007/s00265-016-2126-y
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DOI: https://doi.org/10.1007/s00265-016-2126-y