Skip to main content
Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Under drift-mutation equilibrium, genetic diversity is expected to be correlated with effective population size (N e ). 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 N e than expected for its census size even after accounting for a population decline. Incorporating gene flow into the model, however, reduced the estimated N e of mottled ducks to 33 % of the equilibrium N e and yielded an estimated N e 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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 19:203–215

    Article  CAS  PubMed  Google Scholar 

  • 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, Ithaca

    Google Scholar 

  • 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 218:388–402

    Article  CAS  PubMed  Google Scholar 

  • 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 6:450–461

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 41:186–199

    Article  Google Scholar 

  • 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 

  • Cutter AD, Payseur BA (2013) Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet 14:262–274

    Article  CAS  PubMed  Google Scholar 

  • Delany S, Scott D (2006) Waterbird population estimates, 4th edn. Wetlands International, the Netherlands

    Google Scholar 

  • Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • 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 491:756–760

    CAS  PubMed  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • 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 10:564–567

    Article  PubMed  Google Scholar 

  • Eyre-Walker A, Keightley P, Smith N, Gaffney D (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19:2142–2149

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • 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 108:167–178

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443

    Article  Google Scholar 

  • Grand JB (1992) Breeding chronology of mottled ducks in a Texas coastal marsh. J Field Ornithol 63:195–202

    Google Scholar 

  • 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 22:2653–2667

    Article  PubMed  Google Scholar 

  • 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 167:747–760

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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:e1000862

    Article  PubMed Central  PubMed  Google Scholar 

  • Hughes A (2005) Evidence for abundant slightly deleterious polymorphisms in bacterial populations. Genetics 169:533–538

    Article  PubMed Central  PubMed  Google Scholar 

  • Johnson KP, Sorenson MD (1999) Phylogeny and biogeography of dabbling ducks (Genus: Anas): a comparison of molecular and morphological evidence. Auk 116:792–805

    Article  Google Scholar 

  • Johnson WP, Holbrook RS, Rohwer FC (2002) Nesting chronology, clutch size and egg size of the mottled duck. Wildfowl 53:155–166

    Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol  Ecol Notes 5:187–189

  • 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-2000-0002:1-26

  • 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 12:99

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 22:41–55

    Article  CAS  PubMed  Google Scholar 

  • Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429–434

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 121:930–949

    Article  Google Scholar 

  • 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 122:949–965

    Article  Google Scholar 

  • Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158

    Article  Google Scholar 

  • Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791

    Article  Google Scholar 

  • 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 70:402–411

    Article  PubMed  Google Scholar 

  • 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:e1001388

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  • McCracken KG, Johnson WP, Sheldon FH (2001) Molecular population genetics, phylogeography, and conservation biology of the mottled duck (Anas fulvigula). Conserv Genet 2:87–102

    Article  CAS  Google Scholar 

  • 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 26:815–827

    Article  CAS  PubMed  Google Scholar 

  • 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 367:343–353

    Article  CAS  Google Scholar 

  • Newton I (2006) Can conditions experienced during migration limit the population levels of birds? J Ornithol 147:146–166

    Article  Google Scholar 

  • 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 Naturales

  • Omland K (1997) Examining two standard assumptions of ancestral reconstructions: repeated loss of dichromatism in dabbling ducks (Anatini). Evolution 51:1636–1646

    Article  Google Scholar 

  • 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 59–70

    Google Scholar 

  • 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 61:1992–2006

    Article  CAS  PubMed  Google Scholar 

  • 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 62:1469–1483

    Article  CAS  PubMed  Google Scholar 

  • 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 21:4563–4577

    Article  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • 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 367:354–363

    Article  CAS  Google Scholar 

  • Rhymer J, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109

    Article  Google Scholar 

  • Rieseberg L, Burke J (2001) A genic view of species integration—commentary. J Evol Biol 14:883–886

    Article  Google Scholar 

  • 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:e55161

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sousa VC, Grelaud A, Hey J (2011) On the nonidentifiability of migration time estimates in isolation with migration models. Mol Ecol 20:3956–3962

    Article  PubMed Central  PubMed  Google Scholar 

  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Strasburg JL, Rieseberg LH (2011) Interpreting the estimated timing of migration events between hybridizing species. Mol Ecol 20:2353–2366

    Article  PubMed  Google Scholar 

  • USFWS (2013) 2013 Western Gulf Coast mottled duck survey. USFWS Division of Migratory Bird Management, Branch of Population and Habitat Assessment, Laurel

    Google Scholar 

  • Vucetich JA, Waite TA, Nunney L (1997) Fluctuating population size and the ratio of effective to census population size. Evolution 51:2017–2021

    Article  Google Scholar 

  • 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 6:445–453

    Article  CAS  Google Scholar 

  • Williams CL, Fedynich AM, Pence DB, Rhodes OE (2005b) Evaluation of allozyme and microsatellite variation in Texas and Florida mottled ducks. Condor 107:155–161

    Article  Google Scholar 

  • Woerner AE, Cox MP, Hammer MF (2007) Recombination-filtered genomic datasets by information maximization. Bioinformatics 23:1851–1853

    Article  CAS  PubMed  Google Scholar 

  • Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wright S (1938) Size of population and breeding structure in relation to evolution. Science 87:430–431

    Google Scholar 

  • Wu C (2001) The genic view of the process of speciation. J Evol Biol 14:851–865

    Article  Google Scholar 

  • Wu C, Ting C (2004) Genes and speciation. Nat Rev Genet 5:114–122

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Shawn Houston provided high-performance computing through the University of Alaska’s Life Science Informatics Portal. Funding was provided by the National Science Foundation (Alaska EPSCoR EPS-0346770) and the Texas Parks and Wildlife Department. J Pearce and two anonymous reviewers provided valuable comments on drafts of this manuscript. Any use of trade names is for descriptive purposes only and does not imply endorsement of the US Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey L. Peters.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peters, J.L., Sonsthagen, S.A., Lavretsky, P. et al. Interspecific hybridization contributes to high genetic diversity and apparent effective population size in an endemic population of mottled ducks (Anas fulvigula maculosa). Conserv Genet 15, 509–520 (2014). https://doi.org/10.1007/s10592-013-0557-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0557-9

Keywords

Navigation