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Journal of Ornithology

, Volume 152, Issue 3, pp 623–630 | Cite as

Panmixia and high genetic diversity in a Humboldt Current endemic, the Peruvian Booby (Sula variegata)

  • Scott A. Taylor
  • Carlos B. Zavalaga
  • Guillermo Luna-Jorquera
  • Alejandro Simeone
  • David J. Anderson
  • Vicki L. Friesen
Original Article

Abstract

Marine ecosystems and their inhabitants are increasingly under threat from climate change, competition with humans for resources, and pollution. Species that are endemic to particular currents or regions of the world’s oceans have the potential to be at higher risk due to localized overfishing, pollution, or locally severe impacts of climate change such as more intense, or longer, El Niño Southern Oscillation events. Understanding patterns of population differentiation in endemic marine organisms may be particularly important for their conservation and persistence. Peruvian Boobies (Sula variegata) are endemic to the Humboldt Current upwelling system and have experienced population fluctuations throughout their evolutionary history due to both dramatic reduction of food supplies, and anthropogenic influence over the last ~150 years. Recent research on other members of the Sulidae indicates that populations of these primarily tropical seabirds show a high degree of genetic differentiation; however, the sister species of the Peruvian Booby, the Blue-footed Booby (S. nebouxii), exhibits only weak range-wide population genetic structure. We characterized population genetic differentiation and diversity in 153 Peruvian Boobies using sequence variation of 540 base pairs of the mitochondrial control region and seven microsatellite loci. Although we found evidence of panmixia, a signature of isolation by distance appears to exist between the five sampled colonies. We also found unexpectedly high genetic diversity given this species’ recent population decline. Our results are similar to those for the Humboldt Penguin (Spheniscus humboldti), another endemic of the Humboldt Current upwelling system.

Keywords

Humboldt current Marine ecosystems Dispersal Sulid Population genetics 

Zusammenfassung

Marine Ökosysteme und ihre Bewohner sind zunehmend bedroht durch den Klimawandel, den Wettbewerb mit Menschen um Ressourcen und durch Umweltverschmutzung. Arten, die endemisch in bestimmten Meeresströmungen oder Regionen vorkommen, sind hierbei potentiell stärker bedroht durch lokale Überfischung, Umweltverschmutzung oder lokal stark ausgeprägte Auswirkungen des Klimawandels wie z. B. intensivere oder länger andauernde El Niño Südliche Oszilllation-Ereignisse. Das Verständnis von Mustern der Populationsdifferenzierung endemischer mariner Organsimen kann von besonderer Bedeutung für ihren Schutz und ihr Weiterbestehen sein. Guanotölpel (Sula variegata) sind endemisch im Auftriebsgebiet der Humboldtströmung und haben Populationsschwankungen über ihre evolutionäre Vergangenheit auf Grund von dramatischen Reduktionen von verfügbarer Nahrung als auch durch anthropogene Einflüsse der letzten etwa 150 Jahre erfahren. Neuere Forschung an weiteren Arten der Sulidae weist auf eine hochgradige genetische Populationsdifferenzierung dieser primär tropischen Seevögel hin. Dem entgegen steht jedoch eine nur schwache genetische Populationsstruktur der Schwesterart des Guanotölpels, dem Blaufußtölpel (S. nebouxii), über dessen Verbreitungsgebiet. Wir beschreiben die genetische Populationsdifferenzierung und Diversität von 153 Guanotölpeln an Hand der Sequenzvariation einer 540 Basenpaaren langen Sequenz der mitochondrialen Kontrollregion und von sieben Mikrosatellitenmarkern. Obwohl wir Hinweise gefunden haben die auf Panmixie hinweisen, scheint ein Muster der Isolation durch Distanz zwischen den fünf beprobten Kolonien vorzuherrschen. Außerdem haben wir eine unerwartet hohe genetische Diversität gefunden, obwohl diese Art kürzlich einen Populationsrückgang erfahren hat. Unsere Ergebnisse ähneln denen die für den Humboldtpinguin (Spheniscus humboldti) gefunden wurden, einer weiteren endemischen Art des Auftriebsgebietes der Humboldtströmung.

Notes

Acknowledgments

We are grateful to the wardens of the Peruvian islands, especially to R.J. Balbín and A.T. Nieto, who provided accommodation and lodging on Lobos de Tierra and Lobos de Afuera, and to Giacomo Dell’Omo for his help in blood collection on Peruvian Islands. We would like to thank L.L. Baglietto who obtained the permits to work on the islands in Peru and to export the blood samples to Canada. We also thank T.P. Birt, Z. Sun, G.A. Ibarguchi, J.A. Morris-Pocock, and P. Deane for help with laboratory work and discussion about the manuscript. Funds for this research were provided by the National Geographic Society (Grant #8331-07) to D.J. Anderson, an NSERC Discovery grant to V.L. Friesen, and NSERC postgraduate scholarships (PGS-M, PGS-D) to S.A. Taylor. PROABONOS provided permission to work on the islands in Peru (CARTA N 186-2007-AG-PROABONOS-GO/DE). Collection and exportation of Peruvian Booby blood was possible with permits issued by the Peruvian Institute of Natural Resources, Ministry of Agriculture-INRENA (011352-AG-INRENA and 143-2007-INRENA-IFFS-DCB). The Servicio Agrícola y Ganadero (SAG) provided permission to work on the islands in Chile as well as to collect and to export the Peruvian Booby blood (Resol. No. 6813, 12 Diciembre 2008, SAG, Ministerio de Agricultura). The experiments conducted here comply with Canadian law.

Supplementary material

10336_2010_628_MOESM1_ESM.doc (259 kb)
Supplementary 1 (DOCX 259 kb)

References

  1. Aid CS, Montgomery GG, Mock DW (1985) Range extension of the Peruvian booby to Panama during the 1983 El Niño. Colon. Waterbird 8:67–68CrossRefGoogle Scholar
  2. Allendorf FW, Luikart G (2006) Conservation and the genetics of populations. Wiley-Blackwell, MaldenGoogle Scholar
  3. Avise JC (2000) Phylogeography, the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  4. Birdlife International (2008) Birdlife International American Bird Conservancy workshop on seabirds and seabird-fishery interactions in Peru. RSPB, SandyGoogle Scholar
  5. Brown JW, Van Coeverden De Groot PJ, Birt TP, Seutin G, Boag PT, Friesen VL (2007) Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrines. Mol Ecol 16:327–343PubMedCrossRefGoogle Scholar
  6. Burton RS (2009) Molecular markers, natural history, and conservation of marine animals. Bioscience 59:831–840CrossRefGoogle Scholar
  7. Cassens I, Van Waerebeek K, Best PB, Tzika A, Van Helden AL, Crespo EA, Milinkovitch MC (2005) Evidence for male dispersal along the coasts but no migration in pelagic waters in dusky dolphins (Lagenorhynchus obscurus). Mol Ecol 14:107–121PubMedCrossRefGoogle Scholar
  8. Chakraborty R (1990) Mitochondrial DNA polymorphism reveals hidden heterogeneity within some Asian populations. Am J Hum Genet 47:87–94PubMedGoogle Scholar
  9. Chavez FP, Messié M (2009) A comparison of Eastern Boundary Upwelling Ecosystems. Prog Oceanogr 83:80–96Google Scholar
  10. Clement M, Posada D, Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659Google Scholar
  11. Coker RE (1908) Regarding the future of the guano industry and the guano-producing birds of Peru. Science 28:58–64PubMedCrossRefGoogle Scholar
  12. Coker RE (1920) Peru’s wealth-producing birds. National Geographic Magazine, June 1920, pp 537–566Google Scholar
  13. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  14. Couceiro L, Barrerio R, Ruiz JM, Sotka EE (2007) Genetic isolation by distance among populations of the netted dog whelk Nassarius reticulates (L.) along the European Atlantic coastline. Heredity 98:603–610CrossRefGoogle Scholar
  15. Cushman GT (2005) “The most valuable birds in the world”: international conservation science and the revival of Peru’s guano industry, 1909–1965. Environ Hist 10:477–509CrossRefGoogle Scholar
  16. Duffy DC (1983a) The foraging ecology of Peruvian seabirds. Auk 100:800–810Google Scholar
  17. Duffy DC (1983b) The ecology of tick parasitism on densely nesting Peruvian seabirds. Ecology 64:110–119CrossRefGoogle Scholar
  18. Duffy DC (1983c) Environmental uncertainty and commercial fishing: effects on Peruvian guano birds. Biol Conserv 26:227–238CrossRefGoogle Scholar
  19. Duffy DC (1994) The guano islands of Peru: the once and future management of a renewable resource. Birdlife Conserv Ser 1:68–76Google Scholar
  20. Ewens WJ (1972) Sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112PubMedCrossRefGoogle Scholar
  21. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  22. Friesen VL, Anderson DJ (1997) Phylogeny and evolution of the Sulidae (Aves: Pelecaniformes): a test of alternative modes of speciation. Mol Phylogenet Evol 7:252–260PubMedCrossRefGoogle Scholar
  23. Goya E (2000) Abundancia de aves guaneras y su relación con la pesquería de anchoveta peruana 1953 a 1999. Bol. Ins. del Mar del Perú 19(1–2):125–131Google Scholar
  24. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  25. Huyvaert KP, Anderson DJ (2004) Limited dispersal by Nazca boobies Sula granti. J Avian Biol 35:46–53CrossRefGoogle Scholar
  26. Jahncke J (1998) Las poblaciones de aves guaneras y sus relaciones con la abundancia de anchoveta y la ocurrencia de eventos El Niño en el mar peruano. Bol Inst Mar Perú 17:1–13Google Scholar
  27. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  28. Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics. 149:429–434PubMedGoogle Scholar
  29. LaValle JA (1918) Estudio sobre los factores que influyen sobre la distribuci6n de los nidos de las aves productores del guano. Mem Comp Ad-mora Guano 9:207–213Google Scholar
  30. Luna-Jorquera G, Simeone A, Aguilar R (2003) Ecofisiología de animales endodermos en un desierto cálido y un mar frío: el caso de las aves marinas de la corriente de Humboldt. In: Bozinovic F (ed) Fisiología Ecológica y Evolutiva: 297–316. Ediciones Universidad Católica de Chile, SantiagoGoogle Scholar
  31. Maes GE, Volckaert FAM (2002) Clinal genetic variation and isolation by distance in the European eel Anguilla anguilla (L.). Biol J Linn Soc 77:509–521CrossRefGoogle Scholar
  32. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  33. Mills LS (2007) Conservation of wildlife populations: demography, genetics, and management. Blackwell, MaldenGoogle Scholar
  34. Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518CrossRefGoogle Scholar
  35. Morris-Pocock JA, Steeves TE, Estela FA, Anderson DJ, Friesen VL (2010a) Comparative phylogeography of brown (Sula leucogaster) and red-footed boobies (S. sula): the influence of physical barriers and habitat preference on gene flow in pelagic seabirds. Mol Phylogenet Evol 54:883–896PubMedCrossRefGoogle Scholar
  36. Morris-Pocock JA, Taylor SA, Birt TP, Friesen VL (2010b) Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evol Biol 10:14PubMedCrossRefGoogle Scholar
  37. Murphy RC (1923) The oceanography of the Peruvian littoral with reference to the abundance and distribution of marine life. Geogr Rev 13:64–85CrossRefGoogle Scholar
  38. Murphy RC (1925) Bird Islands of Peru: the record of a sojourn on the west coast. Putnam, New YorkGoogle Scholar
  39. Murphy RC (1936) Oceanic birds of South America. American Museum of Natural History, New YorkGoogle Scholar
  40. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Gen 7:783–787CrossRefGoogle Scholar
  41. Nelson BJ (1978) The Sulidae: gannets and boobies. Oxford University Press, AberdeenGoogle Scholar
  42. Palumbi SR, Sandifer PA, Allan JD, Beck MW, Fautin DG, Fogarty MJ, Halpern BS, Incze LS, Leong J, Norse E, Stachowicz JJ, Wall DH (2008) Managing for ocean biodiversity to sustain marine ecosystem services. Front Ecol Environ 7:204–211CrossRefGoogle Scholar
  43. Pauls SV, Theissinger K, Haase P (2009) Patterns of population structure in two closely related, partially sympatric caddisflies in Eastern Europe: historic introgression, limited dispersal and cryptic diversity. J North Am Benthol Soc 28:517–536CrossRefGoogle Scholar
  44. Pinsky ML, Newsome SD, Dickerson BR, Fang Y, van Tuinen M, Kennett DJ, Ream RR, Hadly EA (2010) Dispersal provided resilience to range collapse in a marine mammal: insights from the past to inform conservation biology. Mol Ecol. doi: 10.1111/j.1365-294X.2010.04671.x
  45. Polunin NCV (2009) Marine ‘genetic resources’ and the potential role of protected areas in conserving them. Environ Conserv 10:31–41CrossRefGoogle Scholar
  46. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  47. Schlosser JA, Dubach JM, Garner TWJ, Araya B, Bernal M, Simeone A, Smith KA, Wallace RS (2009) Evidence for gene flow differs from observed dispersal patterns in the Humboldt penguin, Spheniscus humboldti. Conserv Genet 10:839–849CrossRefGoogle Scholar
  48. Steeves TE, Anderson DJ, McNally H, Kim MC, Friesen VL (2003) Phylogeography of Sula: the role of physical barriers to gene flow in the diversification of tropical seabirds. J Avian Biol 34:217–223CrossRefGoogle Scholar
  49. Steeves TE, Anderson DJ, Friesen VL (2005a) The Isthmus of Panama: a major physical barrier to gene flow in a highly mobile pantropical seabird. J Evol Biol 18:1000–1008PubMedCrossRefGoogle Scholar
  50. Steeves TE, Anderson DJ, Friesen VL (2005b) A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the masked booby (Sula dactylatra). Mol Ecol 14:3877–3887PubMedCrossRefGoogle Scholar
  51. Taylor SA, Morris-Pocock JA, Sun Z, Friesen VL (2010) Isolation and characterization of ten microsatellite loci in blue-footed (Sula nebouxii) and Peruvian boobies (S. variegata). J Ornithol 151:525–528CrossRefGoogle Scholar
  52. Taylor SA, Maclagan L, Anderson DJ, Friesen VL (in press) Could specialization to cold water upwelling systems influence genetic diversity and gene flow in marine organisms? A case study using the blue-footed booby, Sula nebouxii. J BiogeogrGoogle Scholar
  53. Thatje S, Heilmayer O, Laudien J (2008) Climate variability and El Niño Southern Oscillation: implications for natural coastal resources and management. Helgoland Mar Res 62:5–14CrossRefGoogle Scholar
  54. Thompson JD (1999) Population differentiation in Mediterranean plants: insights into colonization history and the evolution and conservation of endemic species. Heredity 82:229–236PubMedCrossRefGoogle Scholar
  55. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  56. Tovar H, Galarza N (1983) Fluctuaciones mensuales de las poblaciones de aves guaneras durante el Niño de 1972. Inf Inst Mar Peru 83:1–38Google Scholar
  57. Wang M, Overland JE, Bond NA (2010) Climate projections for selected large marine ecosystems. J Mar Syst 79:258–266CrossRefGoogle Scholar
  58. Watterson GA (1978) Homozygosity test of neutrality. Genetics 88:405–417PubMedGoogle Scholar
  59. Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26:375–400CrossRefGoogle Scholar
  60. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedGoogle Scholar
  61. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
  62. Zavalaga CB, Taylor SA, Dell’Omo G, Anderson DJ, Friesen VL (2009) Male/female classification of the Peruvian booby. Wilson J Ornithol 121:739–744CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2010

Authors and Affiliations

  • Scott A. Taylor
    • 1
  • Carlos B. Zavalaga
    • 2
  • Guillermo Luna-Jorquera
    • 3
  • Alejandro Simeone
    • 4
  • David J. Anderson
    • 5
  • Vicki L. Friesen
    • 1
  1. 1.Department of BiologyQueen’s UniversityKingstonCanada
  2. 2.Graduate School of Environmental StudiesNagoya UniversityChikusa-ku, NagoyaJapan
  3. 3.Universidad Católica del Norte, Centro de Estudios Avanzados en Zonas Áridas CEAZACoquimboChile
  4. 4.Facultad de Ecologia y Recursos Naturales, Departamento de Ecologia y BiodiversidadUniversidad Andres BelloSantiagoChile
  5. 5.Department of BiologyWake Forest UniversityWinston-SalemUSA

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