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Genetic distinctiveness of brown pelicans (Pelecanus occidentalis) from the Galápagos Islands compared to continental North America - Conservation Genetics

  • ️Friesen, Vicki
  • ️Sat Dec 23 2017

Abstract

We examined population differentiation across a substantial portion of the range of the brown pelican (Pelecanus occidentalis) to assess (1) the genetic distinctness of the Galápagos subspecies (P. o. urinator) and (2) genetic differentiation between subspecies that inhabit the coasts of North and Central America (P. o. californicus and P. o. carolinensis). Birds were sampled from coastal California, coastal Florida, and the Galápagos Islands. Using a 957 bp (bp) fragment of the NADH dehydrogenase subunit 2 (ND2) gene, 661 bp of the mitochondrial control region, and eleven microsatellite loci we characterize population genetic differentiation among 158 brown pelicans. The Galápagos subspecies is genetically distinct from the sampled continental subspecies, possessing a unique ND2 haplotype and unique mitochondrial control region haplotypes. Samples from the two continental subspecies all possessed the same ND2 haplotype and shared four mitochondrial control region haplotypes. Bayesian clustering in STRUCTURE placed the Galápagos subspecies in a distinct genetic group with high probability, but could not differentiate the continental subspecies from one another. Estimates of migration rates from BayesAss indicated substantial migration between continental subspecies, but no migration between the Galápagos subspecies and either continental subspecies. There are clearly two Evolutionarily Significant Units within the range of the brown pelican, which warrants conservation attention. Further investigation should determine how the un-sampled subspecies (P. o. murphyi and P. o. occidentalis) fit into the broader picture.

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References

  • Ainley DG, Carter HR, Anderson DW, Briggs KT, Coulter MC. (1988) Effects of the 1982–83 El Niño-southern oscillation on Pacific Ocean bird populations. Acta XIX Congr Intl Ornithol 19:1747–1758

    Google Scholar 

  • Barry JE (2001) Charles Darwin Foundation Annual Report

  • Cai W, Borlace S, Lengaigne M, Rensch P, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden MJ, Wu L, England MH, Wang G, Guilyardi E, Jin FF (2014) Increasing frequency of extreme El Nino events due to greenhouse warming. Nat Clim Change 4:111–116

    Article  CAS  Google Scholar 

  • Castoe TA, Poole AW, de Koning APJ, Jones KL, Tomback DF, Oyler-McCance SJ, Fike JA, Lance SL, Streicher JW, Smith EN, Pollock DD (2012) Rapid microsatellite identification from Illumina paired-end genomic sequencing in two birds and a snake. PLoS ONE 7:e30953

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cepeda F, Cruz JB (1994) Status and management of seabirds on the Galapagos Islands, Ecuador. In: Nettleship DN, Burger J, Gochfeld M (eds) Seabirds on islands: threats, case studies and action plans. BirdLife Conserv. Ser. no. 1, BirdLife Int, Cambridge, pp 268–278

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1695

    Article  PubMed  CAS  Google Scholar 

  • Crandall K, Bininda-Emonds O, Mace G, Wayne R (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  CAS  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. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformat Online 1:47–50

    CAS  Google Scholar 

  • FCD (Fundación Charles Darwin) and WWF (1999) Visión para la biodiversidad de las islas Galápagos. In: Bensted-Smith R (ed) FCD, Galápagos, p. 152

    Google Scholar 

  • Friesen VL (2015) Speciation in seabirds: why are there so many species…and why aren’t there more? J Ornithol 156:27–39. https://doi.org/10.1007/s10336-015-1235-0

    Article  Google Scholar 

  • Friesen VL, Burg TM, McCoy KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785. https://doi.org/10.1111/j.1365-294X.2006.03197.x

    Article  PubMed  CAS  Google Scholar 

  • Gifford EW (1913) The birds of the Galápagos Islands, with observations on the birds of Cocos and Clipperton Islands (Columbiformes to Pelicaniformes). Expedition of the California Academy of Science, 1905–1906. Part VIII. Proc Calif Acad Sci 2(1):1–132

    Google Scholar 

  • González-Jaramillo M, Rocha-Olivares A (2011) Barriers acting on the genetic structure of a highly aerial seabird: the magnificent frigatebird. Biochem Syst Ecol 39:392–396

    Article  CAS  Google Scholar 

  • Hailer F, Schreiber EA, Miller JM et al (2011) Long-term isolation of a highly mobile seabird on the Galapagos. Proc R Soc B 278:817–825. https://doi.org/10.1038/nature01090

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Huyvaert K, Anderson J D (2004) Limited dispersal by Nazca boobies Sula granti. J Avian Biol 35:46–53. https://doi.org/10.1111/j.0908-8857.2004.03131.x

    Article  Google Scholar 

  • Jeyasingham WS, Taylor SA, Zavalaga CB, Simeone A, Friesen VL (2013) Specialization to cold-water upwellings may facilitate gene flow in seabirds: new evidence from the Peruvian pelican Pelecanus thagus (Pelecaniformes: Pelecanidae). J Avian Biol 44:297–304

    Article  Google Scholar 

  • Kennedy M, Taylor SA, Nádvornik P, Spencer HG (2013) The phylogenetic relationships of the extant pelicans inferred from DNA sequence data. Mol Phylogenet Evol 66:215–222

    Article  PubMed  Google Scholar 

  • Koressaar T, Remm M (2007) Enhancements and modifications of primer design program Primer3. Bioinformatics 23:1289–1291

    Article  PubMed  CAS  Google Scholar 

  • Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Res 14:726–733

    Article  Google Scholar 

  • Milot E, Weimerskirch H, Bernatchez L (2008) The seabird paradox: dispersal, genetic structure and population dynamics in a highly mobile, but philopatric albatross species. Mol Ecol 17:1658–1673

    Article  PubMed  CAS  Google Scholar 

  • Moritz C (1994) Defining “evolutionarily significant units” for conservation. Trends Ecol Evol 9:373–375

    Article  PubMed  CAS  Google Scholar 

  • Morris-Pocock JA, Taylor SA, Birt TP, Friesen VL (2010) Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evol Biol 10:14

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morris-Pocock JA, Anderson DJ, Friesen VL (2011) Mechanisms of global diversification in the brown booby (Sula leucogaster) revealed by uniting statistical phylogeographic and multilocus phylogenetic methods. Mol Ecol 20:2835–2850. https://doi.org/10.1111/j.1365-294X.2011.05132.x

    Article  PubMed  CAS  Google Scholar 

  • Nelson JB (2005) Pelicans, cormorants, and their relatives. Oxford University Press, New York

    Google Scholar 

  • Nylander JA (2004) MrModeltest v2.—Program distributed by the author. Evolutionary Biology Centre, Uppsala Univ, Uppsala

    Google Scholar 

  • Oomen RA, Reudink MW, Nocera JJ, Somers CM, Green MC, Kyle CJ (2011) Mitochondrial evidence for panmixia despite perceived barriers to gene flow in a widely distributed waterbird. J Hered 102:584–592

    Article  PubMed  CAS  Google Scholar 

  • Pritchard JK, Wen W (2004) Documentation for STRUCTURE software: Version 1.2, University of Chicago, Chicago

    Google Scholar 

  • Reudink MW, Kyle CJ, Nocera JJ, Oomen RA, Green MC, Somers CM (2011) Panmixia on a continental scale in a widely distributed colonial waterbird. Biol J Lin Soc 102:583–592

    Article  Google Scholar 

  • Sambrook J, Russell DW (2005) The condensed protocols from molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Pres. Cold Spring Harbor, New York

    Google Scholar 

  • Sgro CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol App 2:326–337

    Article  Google Scholar 

  • Shields M (2002) Brown Pelican (Pelecanus occidentalis). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  • Steeves TE, Anderson DJ, Friesen VL (2005) The Isthmus of Panama: a major physical barrier to gene flow in a highly mobile pantropical seabird. J Evol Biol 18:1000–1008

    Article  PubMed  CAS  Google Scholar 

  • Sullivan BL et al (2014) The eBird enterprise: an integrated approach to development and application of citizen science. Biol Cons 169:31–40

    Article  Google Scholar 

  • Taylor SA, Maclagan L, Anderson DJ, Friesen VL (2011a) Could specialization to cold-water upwelling systems influence gene flow and population differentiation in marine organisms? A case study using the blue-footed booby, Sula nebouxii. J Biogeog 38:883–893. https://doi.org/10.1111/j.1365-2699.2010.02445.x

    Article  Google Scholar 

  • Taylor SA, Zavalaga CB, Luna-Jorquera G, Simeone A, Anderson DJ, Friesen VL (2011b) Panmixia and high genetic diversity in a Humboldt Current endemic, the Peruvian booby (Sula variegata). J Ornithol 152:623–630

    Article  Google Scholar 

  • USFWS. 2011. Breton National Wildlife Refuge. http://www.fws.gov/breton/index.html

  • Valle CA, Cruz F, Cruz JB, Merlen G, Coulter MC (1987) The impact of the 1982–1983 El Niño-Southern Oscillation on seabirds in the Galapagos Islands Ecuador. J Geophys Res 92(C13):14437–14444

    Article  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Willis DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Res 4:535–538

    Google Scholar 

  • Wallace SJ, Wolf SG, Bradley RW et al (2015) The influence of biogeographical barriers on the population genetic structure and gene flow in a coastal Pacific seabird. J Biogeog 42:390–400. https://doi.org/10.1111/jbi.12404

    Article  Google Scholar 

  • Wetmore A (1945) A Review of the forms of the brown pelican. Auk 62:577–586

    Article  Google Scholar 

  • Wiedenfeld DA (2006) Aves, the Galapagos Islands, Ecuador. Checklist 2:1–27

    Article  Google Scholar 

Download references

Acknowledgements

Thanks to Dan Anderson, B. Ploger and P. Boag for sample collection; to the Galápagos National Park Directorate (GNPD) for permission to work in the Park; to the Charles Darwin Foundation (CDF) and TAME Airline for logistical support; and to the Zhengxin Sun for microsatellite analyses, Genome Quebec Innovation Center for sequencing, and Savanah River Ecology Laboratory (S. Lance) for microsatellite development. Thanks to W. Hochachka, J. Morris-Pocock, S. Wallace, E. Chown, and C. Eckert for lab and data analysis help and project discussion. Thanks to the rangers from the GNPD and the assistants from CDF who helped in the field in Galápagos. Thanks to the USNM for the Panama specimen tissue loan. This work was funded by an NSERC Discovery grant (VLF), an NSERC PGSD (SAT), and Queen’s University Summer Work Experience Program. This material is based upon work supported by the National Science Foundation under Grant No. DEB 0842199 to DJA. This publication is a contribution of the Charles Darwin Foundation for the Galápagos Islands.

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Author notes

  1. Scott A. Taylor

    Present address: Department of Ecology and Evolutionary Biology, University of Colorado Boulder, 1300 Pleasant Street, Boulder, CO, 80302, USA

Authors and Affiliations

  1. Department of Biology, Queen’s University, Kingston, ON, Canada

    Scott A. Taylor, Melissa Jenkins, Meera Manghani, Tim Birt & Vicki Friesen

  2. Department of Biology, Wake Forest University, Winston-Salem, NC, USA

    David J. Anderson

  3. Charles Darwin Research Station, Puerto Ayora, Isla Santa Cruz, Galápagos, Ecuador

    Gustavo Jiménez-Uzcátegui

Authors

  1. Scott A. Taylor

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  2. Melissa Jenkins

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  3. Meera Manghani

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  4. Tim Birt

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  5. David J. Anderson

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  6. Gustavo Jiménez-Uzcátegui

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  7. Vicki Friesen

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Contributions

SAT and VLF conceived the ideas; SAT, MJ, MM, TB, GJU and DJA collected the data; SAT, MJ, and MM analyzed the data; VLF and DJA funded the project; and SAT led the writing with the help of all authors.

Corresponding author

Correspondence to Scott A. Taylor.

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This research was conducted in compliance with the Guidelines to the use of Wild Birds in Research and adhering to V. L. Friesen’s Animal Care Protocol.

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Taylor, S.A., Jenkins, M., Manghani, M. et al. Genetic distinctiveness of brown pelicans (Pelecanus occidentalis) from the Galápagos Islands compared to continental North America. Conserv Genet 19, 629–636 (2018). https://doi.org/10.1007/s10592-017-1041-8

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  • Received: 16 June 2017

  • Accepted: 18 December 2017

  • Published: 23 December 2017

  • Issue Date: June 2018

  • DOI: https://doi.org/10.1007/s10592-017-1041-8

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