Conservation Genetics

, Volume 18, Issue 2, pp 453–466 | Cite as

Temporal shifts in the saltmarsh–Nelson’s sparrow hybrid zone revealed by replicated demographic and genetic surveys

  • Jennifer WalshEmail author
  • W. Gregory Shriver
  • Maureen D. Correll
  • Brian J.  Olsen
  • Chris S. Elphick
  • Thomas P.  Hodgman
  • Rebecca J.  Rowe
  • Kathleen M. O’Brien
  • Adrienme I. Kovach
Research Article


Conservation of threatened or endangered species in a hybrid zone requires a comprehensive understanding of interspecific dynamics over time and space. We evaluated changes in location and composition of a hybrid zone over a 15-year period (with replicated sampling in 1997–2000 and 2011–2013) for saltmarsh (Ammodramus caudacutus) and Nelson’s (A. nelsoni) sparrows, two tidal marsh specialists of high conservation priority in the northeastern United States. We combined genetic analyses using microsatellite and mitochondrial markers with species distribution patterns. In both time periods, replicate genetic sampling (n = 85; five sites) and field population surveys (93 sites) were conducted. We compared the distribution of parental species and hybrids and estimates for hybrid zone width and center between the two time periods. An increase in the relative proportion of Nelson’s sparrows in sympatric marshes and an approximate doubling of hybrid zone width provides evidence for expansion. Introgression rates increased over time for neutral loci but declined for a mitochondrial gene and two gene-associated loci under the influence of selection, as expected under a speciation model with barriers to gene flow. On average, the center of the hybrid zone shifted 60 km southward over the 15 years. We placed our findings within a policy framework to evaluate management options for hybrids. We conclude that despite increasing rates of introgression, hybridization poses a substantially lesser threat to parental populations than the imminent consequences of sea-level rise and habitat degradation. Based on our current knowledge of hybrid zone dynamics in this system, we conclude that the conservation of hybrids is warranted along with parental species at this time.


Saltmarsh sparrow Nelson’s sparrow Hybrid zone Temporal stability Range expansion Hybrid conservation 



Funding for this project was provided by the United States Fish and Wildlife Service through its Region 5, Division of Natural Resources, National Wildlife Refuge System, State Wildlife Grant # U2-5-R-1, and the Northeast Regional Conservation Needs Grant Program, by the New Hampshire Agricultural Experiment Station, through a USDA National Institute of Food and Agriculture McIntire-Stennis Project # 225575, and by the National Science Foundation Grant # DEB-1340008. This is Scientific Contribution Number 2702 of the New Hampshire Agricultural Experiment Station. Sampling was conducted in accordance with the Institutional Animal Care and Use Committee of the University of New Hampshire (100605, 130604). The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Supplementary material

10592_2016_920_MOESM1_ESM.pdf (464 kb)
Supplementary material 1 (PDF 464 KB)


  1. Abbott R et al (2013) Hybridization and speciation. J Evol Biol 26:229–246.CrossRefPubMedGoogle Scholar
  2. Agapow PM, Bininda-Emonds OR, Crandall KA, Gittleman JL, Mace GM, Marshall JC, Purvis A (2004) The impact of species concept on biodiversity studies. Q Rev Biol 79:161–179CrossRefPubMedGoogle Scholar
  3. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622CrossRefGoogle Scholar
  4. Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229PubMedPubMedCentralGoogle Scholar
  5. Bayard TS, Elphick CS (2011) Planning for sea level rise: quantifying patterns of saltmarsh sparrow (Ammodramus caudacutus) nest flooding under current sea level conditions. Auk 128:393–403CrossRefGoogle Scholar
  6. Beaumont M, Barratt EM, Gottelli D, Kitchener AC, Daniels MJ, Pritchard JK, Bruford MW (2001) Genetic diversity and introgression in the Scottish wildcat. Mol Ecol 10:319–336CrossRefPubMedGoogle Scholar
  7. Bierne N, Borsa P, Daguin C, Jollivet D, Viard F, Bonhomme F, David P (2003) Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis. Mol Ecol 12:447–461CrossRefPubMedGoogle Scholar
  8. Birdlife International (2016). Species factsheet: Ammodramus caudacutus. Accessed 01 Jul 2016
  9. Bohling JH, Waits LP (2011) Assessing the prevalence of hybridization between sympatric Canis species surrounding the red wolf (Canis rufus) recovery area in North Carolina. Mol Ecol 20(10):2142–2156CrossRefPubMedGoogle Scholar
  10. Bronson CL, Grubb TC, Sattler GD, Braun MJ (2003) Mate preference: a possible causal mechanism for a moving hybrid zone. Anim Behav 65:489–500CrossRefGoogle Scholar
  11. Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity 99:301–312CrossRefPubMedGoogle Scholar
  12. Bulgin NL, Gibbs HL, Vickery P, Baker AJ (2003) Ancestral polymorphism in genetic markers obscure detection of evolutionarily distinct populations in the endangered Florida grasshopper sparrow (Ammodramus savannarum floridanus). Mol Ecol 12:831–844CrossRefPubMedGoogle Scholar
  13. Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52CrossRefPubMedGoogle Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  15. Carson EW, Tobler M, Minckley WL, Ainsworth RJ, Dowling TE (2012) Relationships between spatio-temporal environmental and genetic variation reveal an important influence of exogenous selection in a pupfish hybrid zone. Mol Ecol 21:1209–1222CrossRefPubMedGoogle Scholar
  16. Correll MD, Wiest WA, Hodgman TP, Shriver WG, Elphick CS, McGill GJ, Obrien KM, Olsen BJ (2016) Predictors of specialist avifaunal decline in coastal marshes. Cons Bio doi: 10.1111/cobi.12797 Google Scholar
  17. Daguin C, Bonhomme F, Borsa P (2001) The zone of sympatry and hybridization of Mytilus edulis and M. galloprovincialis, as described by intron length polymorphism at locus mac-1. Heredity 86:342–354CrossRefPubMedGoogle Scholar
  18. Dasmahapatra KK, Blum MJ, Aiello A, Hackwell S, Davies N, Bermingham EP, Mallet J (2002) Inferences from a rapidly moving hybrid zone. Evolution 56:741–753CrossRefPubMedGoogle Scholar
  19. Den Hartog PM, Den Boer-Visser AM, Ten Cate C (2010) Unidirectional hybridization and introgression in an avian contact zone: evidence from genetic markers, morphology, and comparisons with laboratory-raised F1 hybrids. Auk 127:605–616CrossRefGoogle Scholar
  20. Derryberry EP, Derryberry GE, Maley JM, Brumfield RT (2013) HZAR: hybrid zone analysis using an R software package. Mol Ecol Res 14:652–663CrossRefGoogle Scholar
  21. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Con Gen Res 4:359–361CrossRefGoogle Scholar
  22. Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475CrossRefPubMedGoogle Scholar
  23. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  24. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedPubMedCentralGoogle Scholar
  25. Field et al. Accepted to Ecography (in press)Google Scholar
  26. Fitzpatrick BM, Ryan ME, Johnson JR, Corush J, Carter ET (2015) Hybridization and the species problem in conservation. Curr Zol 6:206–216CrossRefGoogle Scholar
  27. Gjerdrum C, Elphick CS, Rubega M (2005) Nest site selection and nesting success in salt marsh breeding sparrows: the importance of nest habitat, timing, and study site differences. Condor 107:849–862CrossRefGoogle Scholar
  28. 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
  29. Gompert Z, Buerkle CA (2010) INTROGRESS: a software package for mapping components of isolation in hybrids. Mol Ecol Res 10:378–384CrossRefGoogle Scholar
  30. Goudet J (1995) FSTAT: a computer program to calculate F-statistics. J Hered 86:485–486CrossRefGoogle Scholar
  31. Greenlaw JS (1993) Behavioral and morphological diversification in sharp-tailed sparrows (Ammodramus caudacutus) of the Atlantic Coast. Auk 110:286–303Google Scholar
  32. Haig SM, Mullins TD, Forsman ED, Trail PW, Wennerberg L (2004) Genetic identification of spotted owls, barred owls, and their hybrids: legal implications of hybrid identity. Cons Biol 18:1347–1357.CrossRefGoogle Scholar
  33. Haldane, JBS (1922) Sex ratio and unisexual sterility in animal hybrids. J Genet 12:101–109CrossRefGoogle Scholar
  34. Hamilton JA, Lexer C, Aitken SN (2013) Genomic and phenotypic architecture of a spruce hybrid zone (Picea sitchensis x P. glauca). Mol Ecol 22:827–841CrossRefPubMedGoogle Scholar
  35. Hill CE, Tomko S, Hagen C, Schable NA, Glenn TC (2008) Novel microsatellite markers for the saltmarsh sharp-tailed sparrow, Ammodramus caudacutus (Aves: Passeriformes). Mol Ecol Res 8:113–115CrossRefGoogle Scholar
  36. Hodgman TP, Shriver WG, Vickery PD (2002) Redefining range overlap between the sharp-tailed sparrows of coastal New England. Wilson Bull 114:38–43CrossRefGoogle Scholar
  37. Jackiw RN, Mandil G, Hager HA (2015) A framework to guide the conservation of species hybrids based on ethical and ecological considerations. Con Biol DOI: 10.1111/cobi.12526 Google Scholar
  38. Kalinowski ST (2005) HP-RARE 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  39. Kovach AI, Walsh J, Ramsdell J, Thomas K (2015) Development of diagnostic microsatellite markers from whole genome sequences of Ammodramus sparrows for assessing admixture in a hybrid zone. Ecol Evol 5:2267–2283CrossRefPubMedPubMedCentralGoogle Scholar
  40. Latch EK, Kierepka EM, Heffelfinger JR, Rhodes OE (2011) Hybrid swarm between divergent lineages of mule deer (Odocoileus hemionus). Mol Ecol 20(24):5265–5279CrossRefPubMedGoogle Scholar
  41. Milne RI, Abbott RJ (2008) Reproductive isolation among two infertile Rhododendron species: low frequency of post-F1 genotypes in alpine hybrid zones. Mol Ecol 17:1108–1121CrossRefPubMedGoogle Scholar
  42. Montagna W (1942) The Sharp-tailed sparrows of the Atlantic coast. Wilson Bull 54:107–121Google Scholar
  43. Nicotra AB, Beever EA, Roberson AL, Hofmann GE, O’Leary J (2015) Assessing the components of adaptive capacity to improve conservation and management efforts under global change. Con Biol 29:1268–1278CrossRefGoogle Scholar
  44. Nocera JJ, Fitzgerald TM, Hanson AR, Milton GR (2007) Differential habitat use by acadian nelson’s sharp-tailed sparrows: implications for regional conservation. J Field Ornithol 78:50–55CrossRefGoogle Scholar
  45. Oliveira R, Godinho R, Randi E, Ferrand N, Alves PC (2008) Molecular analysis of hybridisation between wild and domestic cats (Felis silvestris) in Portugal: implications for conservation. Conserv Genet 9(1):1–11CrossRefGoogle Scholar
  46. Payseur BA (2010) Using differential introgression in hybrid zones to identify genomic regions involved in speciation. Mol. Ecol Res 10:806–820CrossRefGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  48. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Randi E (2008) Detecting hybridization between wild species and their domesticated relatives. Mol Ecol 17:285–293CrossRefPubMedGoogle Scholar
  50. Raymond M, Rousset F (1995) GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  51. Reullier J, Pérez-Tris J, Bensch S, Secondi J (2006) Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone. Mol Ecol 15:753–763CrossRefPubMedGoogle Scholar
  52. Rheindt FE, Edwards SV (2011) Genetic introgression: an integral but neglected component of speciation in birds. Auk 128:620–632CrossRefGoogle Scholar
  53. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Evol S 27:83–109.CrossRefGoogle Scholar
  54. Rising JD, Avise JC (1993) The application of genealogical concordance principles to the taxonomy and evolutionary history of the sharp-tailed sparrow (Ammodramus caudacutus). Auk 110:844–856CrossRefGoogle Scholar
  55. Rohwer S, Bermingham E, Wood C (2001) Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55:405–422CrossRefPubMedGoogle Scholar
  56. Ruskin KJ, Etterson MA, Hodgman TP, Borowske AC, Cohen JB, Elphick CS, Field CR, Kern RA, Kocek AR, Kovach AI, O’Brien KM, Pau N, Shriver WG, Walsh J, Olsen BJ (2016) Seasonal fecundity is not related to geographic position across a species’ global range despite a central peak in abundance. Oecologia. Doi:  10.1007/s00442-016-3745-8 PubMedGoogle Scholar
  57. Secondi J, Faivre B, Bensch S (2006) Spreading introgression in the wake of a moving contact zone. Mol Ecol 15:2463–2475CrossRefPubMedGoogle Scholar
  58. Shapiro LH, Canterbury RA, Stover DM, Fleischer RC (2004) Reciprocal introgression between golden-winged warblers (Vermivora chrysoptera) and blue-winged warblers (V. pinus) in eastern North America. Auk 121:1019–1030CrossRefGoogle Scholar
  59. Shriver WG, Hodgman TP, Gibbs JP, Vickery PD (2004) Landscape context influences salt marsh bird diversity and area requirements in New England. Biol Conserv 119:545–553CrossRefGoogle Scholar
  60. Shriver WG, Gibbs JP, Vickery PD et al (2005) Concordance between morphological and molecular markers in assessing hybridization between sharp-tailed sparrows in New England. Auk 122:94–107CrossRefGoogle Scholar
  61. Shriver WG, O’Brien KM, Ducey MJ, Hodgman TP (2015) Population abundance and trends of saltmarsh (Ammodramus caudacutus) and Nelson’s (A. nelsoni) sparrows: influence of sea levels and precipitation. J Ornithol. DOI: 10.1007/s10336-015-1266-6 Google Scholar
  62. Smith KL, Hale JM, Gay L, Kearney MR, Austin JJ, Parris KM, Melville J (2012) Spatio-temporal changes in the structure of an Australian fog hybrid zone: a 40-year perspective. Evolution 67:3442–3454CrossRefGoogle Scholar
  63. Stronen AV, Paquet PC (2013) Perspectives on the conservation of wild hybrids. Biol Conserv 167:390–395CrossRefGoogle Scholar
  64. Taylor SA, White TA, Hochachka WM, Ferretti V, Curry RL, Lovette I (2014) Climate-mediated movement in an avian hybrid zone. Curr Biol 24:671–676CrossRefPubMedGoogle Scholar
  65. Therkildsen NO, Hemmer-Hansen J, Als TD, Swain DP, Morgan MJ, Trippel EA, Paumbi SR, Meldrup D, Nielsen EE (2013) Microevolution in time and space: SNP analysis of historical DNA reveals dynamic signatures of selection in Atlantic cod. Mol Ecol 22:2424–2440CrossRefPubMedGoogle Scholar
  66. U.S. Department of Interior (USDI), (2008) Birds of conservation concern 2008. USDI, Fish and Wildlife Service, Division of Migratory Bird Management, Arlington.
  67. Walsh J, Kovach AI, Lane OP, O’Brien KM, Babbitt KJ (2011) Genetic barcode RFLP analysis of the Nelson’s and saltmarsh sparrow hybrid zone. Wilson J Ornithol 123:316–322CrossRefGoogle Scholar
  68. Walsh J, Kovach AI, Babbitt KJ, O’Brien KM (2012) Fine-scale population structure and asymmetrical dispersal in an obligate salt-marsh passerine, the saltmarsh sparrow (Ammodramus caudacutus). Auk 129:247–258CrossRefGoogle Scholar
  69. Walsh J, Shriver WG, Olsen BJ, O’Brien KM, Kovach AI (2015a) Relationship of phenotypic variation and genetic admixture in the saltmarsh–Nelson’s sparrow hybrid zone. Auk 132:704–716Google Scholar
  70. Walsh J, Rowe RJ, Olsen BJ, Shriver WG, Kovach AI (2015b) Genotype-environment associations support a mosaic hybrid zone between two tidal marsh birds. Ecol Evol 6:279–294Google Scholar
  71. Walsh J, Shriver WG, Olsen BJ, Kovach AI (2016a) Differential introgression and the maintenance of species boundaries in an advanced generation avian hybrid zone. BMC Evol Biol 16:65Google Scholar
  72. Walsh, J, Olsen BJ, Ruskin KJ, Shriver WG, O’Brien KM, Kovach AI (2016b) Extrinsic and intrinsic factors influence fitness in an avian hybrid zone. Biol J Linn Soc. doi:  10.1111/bij.12837
  73. Wayne RK, Shaffer HB (2016) Hybridization and endangered species protection in the molecular era. Mol Ecol 25:2680–2689CrossRefPubMedGoogle Scholar
  74. Weist WA, Correll MD, Olsen BJ, Elphick CS, Hodgman TP, Curson DR, Shriver WG (2015) A regional monitoring framework for estimating the occurrence and abundance of tidal marsh birds in the Northeast USA. Condor. In pressGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Jennifer Walsh
    • 1
    Email author
  • W. Gregory Shriver
    • 2
  • Maureen D. Correll
    • 3
  • Brian J.  Olsen
    • 3
  • Chris S. Elphick
    • 4
  • Thomas P.  Hodgman
    • 5
  • Rebecca J.  Rowe
    • 1
  • Kathleen M. O’Brien
    • 6
  • Adrienme I. Kovach
    • 1
  1. 1.Department of Natural Resources & the EnvironmentUniversity of New HampshireDurhamUSA
  2. 2.Department of Entomology & Wildlife EcologyUniversity of DelawareNewarkUSA
  3. 3.School of Biology and EcologyUniversity of MaineOronoUSA
  4. 4.Ecology & Evolutionary Biology and Center for Conservation & BiodiversityUniversity of ConnecticutStorrsUSA
  5. 5.Maine Department of Inland Fish & WildlifeBangorUSA
  6. 6.U.S Fish and Wildlife ServiceRachel Carson National Wildlife RefugeWellsUSA

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