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

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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.

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.

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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.

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Authors and Affiliations

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

    Scott A. Taylor & Vicki L. Friesen

  2. Graduate School of Environmental Studies, Nagoya University, Sonoyama House 105, Sonoyama-cho 2-21-1, Chikusa-ku, Nagoya, 464-0812, Japan

    Carlos B. Zavalaga

  3. Universidad Católica del Norte, Centro de Estudios Avanzados en Zonas Áridas CEAZA, Larrondo 1281, Coquimbo, Chile

    Guillermo Luna-Jorquera

  4. Facultad de Ecologia y Recursos Naturales, Departamento de Ecologia y Biodiversidad, Universidad Andres Bello, Republica 470, Santiago, Chile

    Alejandro Simeone

  5. Department of Biology, Wake Forest University, Winston-Salem, NC, 27109, USA

    David J. Anderson

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  1. Scott A. Taylor
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  2. Carlos B. Zavalaga
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  3. Guillermo Luna-Jorquera
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  6. Vicki L. Friesen
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Correspondence to Scott A. Taylor.

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Communicated by M. Wink.

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Taylor, S.A., Zavalaga, C.B., Luna-Jorquera, G. et al. Panmixia and high genetic diversity in a Humboldt Current endemic, the Peruvian Booby (Sula variegata). J Ornithol 152, 623–630 (2011). https://doi.org/10.1007/s10336-010-0628-3

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