Conservation Genetics

, Volume 15, Issue 3, pp 509–520 | Cite as

Interspecific hybridization contributes to high genetic diversity and apparent effective population size in an endemic population of mottled ducks (Anas fulvigula maculosa)

  • Jeffrey L. Peters
  • Sarah A. Sonsthagen
  • Philip Lavretsky
  • Michael Rezsutek
  • William P. Johnson
  • Kevin G. McCracken
Research Article

Abstract

Under drift-mutation equilibrium, genetic diversity is expected to be correlated with effective population size (Ne). Changes in population size and gene flow are two important processes that can cause populations to deviate from this expected relationship. In this study, we used DNA sequences from six independent loci to examine the influence of these processes on standing genetic diversity in endemic mottled ducks (Anas fulvigula) and geographically widespread mallards (A. platyrhynchos), two species known to hybridize. Mottled ducks have an estimated census size that is about two orders-of-magnitude smaller than that of mallards, yet these two species have similar levels of genetic diversity, especially at nuclear DNA. Coalescent analyses suggest that a population expansion in the mallard at least partly explains this discrepancy, but the mottled duck harbors higher genetic diversity and apparent Ne than expected for its census size even after accounting for a population decline. Incorporating gene flow into the model, however, reduced the estimated Ne of mottled ducks to 33 % of the equilibrium Ne and yielded an estimated Ne consistent with census size. We also examined the utility of these loci to distinguish among mallards, mottled ducks, and their hybrids. Most putatively pure individuals were correctly assigned to species, but the power for detecting hybrids was low. Although hybridization with mallards potentially poses a conservation threat to mottled ducks by creating a risk of extinction by hybridization, introgression of mallard alleles has helped maintain high genetic diversity in mottled ducks and might be important for the adaptability and survival of this species.

Keywords

Coalescent Phenotype Introgression Population structure Multilocus phylogeography mtDNA Introns 

Supplementary material

10592_2013_557_MOESM1_ESM.docx (18 kb)
Supplementary material 1 (DOCX 18 kb)

References

  1. Alleaume-Benharira M, Pen IR, Ronce O (2006) Geographical patterns of adaptation within a species’ range: interactions between drift and gene flow. J Evol Biol 19:203–215PubMedCrossRefGoogle Scholar
  2. Bielefeld RR, Brasher MG, Moorman TE, Gray PN (2010) Mottled duck (Anas fulvigula). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, IthacaGoogle Scholar
  3. Bottema CDK, Sarkar G, Cassady JD, Ii S, Dutton CM, Sommer SS, Wu R (1993) Polymerase chain reaction amplification of specific alleles: a general method of detection of mutations, polymorphisms, and haplotypes. Methods Enzymol 218:388–402PubMedCrossRefGoogle Scholar
  4. Bradbury IR, Hubert S, Higgins B, Bowman S, Borza T, Paterson IG, Snelgrove PVR, Morris CJ, Gregory RS, Hardie D, Hutchings JA, Ruzzante DE, Taggart CT, Bentzen P (2013) Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evol Appl 6:450–461PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bulgarella M, Sorenson MD, Peters JL, Wilson RE, McCracken KG (2010) Phylogenetic relationships of Amazonetta, Speculanas, Lophonetta, and Tachyeres: four morphologically divergent duck genera endemic to South America. J Avian Biol 41:186–199CrossRefGoogle Scholar
  6. Carney SM (1992) Species, age and sex identification of ducks using wing plumage. US Department of the Interior & US Fish and Wildlife Service, Washington, D.C.Google Scholar
  7. Cutter AD, Payseur BA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14:262–274PubMedCrossRefGoogle Scholar
  8. Delany S, Scott D (2006) Waterbird population estimates, 4th edn. Wetlands International, the NetherlandsGoogle Scholar
  9. Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  10. Ellegren H, Smeds L, Burri R, Olason PI, Backstrom N, Kawakami T, Kunstner A, Makinen H, Nadachowska-Brzyska K, Qvarnstrom A, Uebbing S, Wolf JBW (2012) The genomic landscape of species divergence in Ficedula flycatchers. Nature 491:756–760PubMedGoogle Scholar
  11. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  12. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  13. Eyre-Walker A, Keightley P, Smith N, Gaffney D (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19:2142–2149PubMedCrossRefGoogle Scholar
  14. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  15. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  16. Frankham R (2012) How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination. Heredity 108:167–178PubMedCentralPubMedCrossRefGoogle Scholar
  17. Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443CrossRefGoogle Scholar
  18. Grand JB (1992) Breeding chronology of mottled ducks in a Texas coastal marsh. J Field Ornithol 63:195–202Google Scholar
  19. Hemmer-Hansen J, Nielsen EE, Therkildsen NO, Taylor MI, Ogden R, Geffen AJ, Bekkevold D, Helyar S, Pampoulie C, Johansen T, Carvalho GR, Fishpoptrace Consortium (2013) A genomic island linked to ecotype divergence in Atlantic cod. Mol Ecol 22:2653–2667PubMedCrossRefGoogle Scholar
  20. Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCentralPubMedCrossRefGoogle Scholar
  21. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6:e1000862PubMedCentralPubMedCrossRefGoogle Scholar
  22. Hughes A (2005) Evidence for abundant slightly deleterious polymorphisms in bacterial populations. Genetics 169:533–538PubMedCentralPubMedCrossRefGoogle Scholar
  23. Johnson KP, Sorenson MD (1999) Phylogeny and biogeography of dabbling ducks (Genus: Anas): a comparison of molecular and morphological evidence. Auk 116:792–805CrossRefGoogle Scholar
  24. Johnson WP, Holbrook RS, Rohwer FC (2002) Nesting chronology, clutch size and egg size of the mottled duck. Wildfowl 53:155–166Google Scholar
  25. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol  Ecol Notes 5:187–189Google Scholar
  26. Kirby RE, Reed A, Dupuis P, Obrecht III HH, Quist WJ (2000) Description and identification of American black duck, mallard, and hybrid wing plumage. US Geological Survey, Biological Resources Division, Biological Science Report USGS/BRD/BSR-2000-0002:1-26Google Scholar
  27. Kraus R, Zeddeman A, van Hooft P, Sartakov D, Soloviev S, Ydenberg R, Prins H (2011) Evolution and connectivity in the world-wide migration system of the mallard: inferences from mitochondrial DNA. BMC Genet 12:99PubMedCentralPubMedCrossRefGoogle Scholar
  28. Kraus RHS, van Hooft P, Megens H, Tsvey A, Fokin SY, Ydenberg RC, Prins HHT (2013) Global lack of flyway structure in a cosmopolitan bird revealed by a genome wide survey of single nucleotide polymorphisms. Mol Ecol 22:41–55PubMedCrossRefGoogle Scholar
  29. Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429–434PubMedCentralPubMedGoogle Scholar
  30. Kulikova IV, Zhuravlev YN, McCracken KG (2004) Asymmetric hybridization and sex-biased gene flow between Eastern spot-billed ducks (Anas zonorhyncha) and mallards (A. platyrhynchos) in the Russian Far East. Auk 121:930–949CrossRefGoogle Scholar
  31. Kulikova IV, Drovetski SV, Gibson DD, Harrigan RJ, Rohwer S, Sorenson MD, Winker K, Zhuravlev YN, McCracken KG (2005) Phylogeography of the mallard (Anas platyrhynchos): hybridization, dispersal, and lineage sorting contribute to complex geographic structure. Auk 122:949–965CrossRefGoogle Scholar
  32. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158CrossRefGoogle Scholar
  33. Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791CrossRefGoogle Scholar
  34. Lavretsky P, McCracken KG, Peters JL (2014) Phylogenetics of a recent radiation in the mallards and allies (genus Anas): inferences from a genomic transect and the multispecies coalescent. Mol Phylogenet Evol 70:402–411PubMedCrossRefGoogle Scholar
  35. Leffler EM, Bullaughey K, Matute DR, Meyer WK, Segurel L, Venkat A, Andolfatto P, Przeworski M (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10:e1001388PubMedCentralPubMedCrossRefGoogle Scholar
  36. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189CrossRefGoogle Scholar
  37. McCracken KG, Johnson WP, Sheldon FH (2001) Molecular population genetics, phylogeography, and conservation biology of the mottled duck (Anas fulvigula). Conserv Genet 2:87–102CrossRefGoogle Scholar
  38. McCracken KG, Bulgarella M, Johnson KP, Kuhner MK, Trucco J, Valqui TH, Wilson RE, Peters JL (2009) Gene flow in the face of countervailing selection: adaptation to high-altitude hypoxia in the beta A hemoglobin subunit of yellow-billed pintails in the Andes. Mol Biol Evol 26:815–827PubMedCrossRefGoogle Scholar
  39. Nadeau NJ, Whibley A, Jones RT, Davey JW, Dasmahapatra KK, Baxter SW, Quail MA, Joron M, Ffrench-Constant RH, Blaxter ML, Mallet J, Jiggins CD (2012) Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philos Trans R Soc B 367:343–353CrossRefGoogle Scholar
  40. Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166CrossRefGoogle Scholar
  41. North American Waterfowl Management Plan, Plan Committee (2004) North American Waterfowl Management Plan 2004. Implementation Framework: Strengthening the Biological Foundation. Canadian Wildlife Service, US Fish and Wildlife Service, Secretaria de Medio Ambiente y Recursos NaturalesGoogle Scholar
  42. Omland K (1997) Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling ducks (Anatini). Evolution 51:1636–1646CrossRefGoogle Scholar
  43. Paulus S (1988) Social behavior and pairing chronology of mottled ducks during autumn and winter in Louisiana. In: Weller M (ed) Waterfowl in Winter. University of Minnesota Press, Minneapolis, pp 59–70Google Scholar
  44. Peters JL, Zhuravlev Y, Fefelov I, Logie A, Omland KE (2007) Nuclear loci and coalescent methods support ancient hybridization as cause of mitochondrial paraphyly between gadwall and falcated duck (Anas spp.). Evolution 61:1992–2006PubMedCrossRefGoogle Scholar
  45. Peters JL, Zhuravlev YN, Fefelov I, Humphries EM, Omland KE (2008) Multilocus phylogeography of a holarctic duck: colonization of North America from Eurasia by gadwall (Anas strepera). Evolution 62:1469–1483PubMedCrossRefGoogle Scholar
  46. Peters JL, McCracken KG, Pruett CL, Rohwer S, Drovetski SV, Zhuravlev YN, Kulikova I, Gibson DD, Winker K (2012) A parapatric propensity for breeding precludes the completion of speciation in common teal (Anas crecca, sensu lato). Mol Ecol 21:4563–4577PubMedCrossRefGoogle Scholar
  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  48. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  49. Renaut S, Maillet N, Normandeau E, Sauvage C, Derome N, Rogers SM, Bernatchez L (2012) Genome-wide patterns of divergence during speciation: the lake whitefish case study. Philos Trans R Soc B 367:354–363CrossRefGoogle Scholar
  50. Rhymer J, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  51. Rieseberg L, Burke J (2001) A genic view of species integration—commentary. J Evol Biol 14:883–886CrossRefGoogle Scholar
  52. Smith BT, Klicka J (2013) Examining the role of effective population size on mitochondrial and multilocus divergence time discordance in a songbird. PLoS ONE 8:e55161PubMedCentralPubMedCrossRefGoogle Scholar
  53. Sousa VC, Grelaud A, Hey J (2011) On the nonidentifiability of migration time estimates in isolation with migration models. Mol Ecol 20:3956–3962PubMedCentralPubMedCrossRefGoogle Scholar
  54. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989PubMedCentralPubMedCrossRefGoogle Scholar
  55. Strasburg JL, Rieseberg LH (2011) Interpreting the estimated timing of migration events between hybridizing species. Mol Ecol 20:2353–2366PubMedCrossRefGoogle Scholar
  56. USFWS (2013) 2013 Western Gulf Coast mottled duck survey. USFWS Division of Migratory Bird Management, Branch of Population and Habitat Assessment, LaurelGoogle Scholar
  57. Vucetich JA, Waite TA, Nunney L (1997) Fluctuating population size and the ratio of effective to census population size. Evolution 51:2017–2021CrossRefGoogle Scholar
  58. Williams CL, Brust RC, Fendley TT, Tiller GR Jr, Rhodes OE Jr (2005a) A comparison of hybridization between mottled ducks (Anas fulvigula) and mallards (A. platyrhynchos) in Florida and South Carolina using microsatellite DNA analysis. Conserv Genet 6:445–453CrossRefGoogle Scholar
  59. Williams CL, Fedynich AM, Pence DB, Rhodes OE (2005b) Evaluation of allozyme and microsatellite variation in Texas and Florida mottled ducks. Condor 107:155–161CrossRefGoogle Scholar
  60. Woerner AE, Cox MP, Hammer MF (2007) Recombination-filtered genomic datasets by information maximization. Bioinformatics 23:1851–1853PubMedCrossRefGoogle Scholar
  61. Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053CrossRefGoogle Scholar
  62. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedCentralPubMedGoogle Scholar
  63. Wright S (1938) Size of population and breeding structure in relation to evolution. Science 87:430–431Google Scholar
  64. Wu C (2001) The genic view of the process of speciation. J Evol Biol 14:851–865CrossRefGoogle Scholar
  65. Wu C, Ting C (2004) Genes and speciation. Nat Rev Genet 5:114–122PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Jeffrey L. Peters
    • 1
    • 2
  • Sarah A. Sonsthagen
    • 2
    • 3
  • Philip Lavretsky
    • 1
  • Michael Rezsutek
    • 4
  • William P. Johnson
    • 5
    • 6
  • Kevin G. McCracken
    • 2
    • 7
  1. 1.Department of Biological SciencesWright State UniversityDaytonUSA
  2. 2.Institute of Arctic BiologyUniversity of Alaska FairbanksFairbanksUSA
  3. 3.United States Geological Survey, Alaska Science CenterAnchorageUSA
  4. 4.Texas Parks and Wildlife DepartmentPort ArthurUSA
  5. 5.Texas Parks and Wildlife DepartmentCanyonUSA
  6. 6.U.S. Fish and Wildlife Service, National Wildlife Refuge System, Division of Biological SciencesWest Texas A&M UniversityCanyonUSA
  7. 7.Department of Biology and Rosenstiel School of Marine and Atmospheric SciencesUniversity of MiamiCoral GablesUSA

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