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Evidence of a genetic bottleneck in an El Niño affected population of South American fur seals, Arctocephalus australis

Published online by Cambridge University Press:  14 August 2009

Larissa Rosa de Oliveira ,
Diogo Meyer ,
Joseph Hoffman ,
Patricia Majluf  and
João S. Morgante
Larissa Rosa de Oliveira*
Affiliation:
Laboratório de Biologia Evolutiva e Conservação de Vertebrados (LABEC), Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, São Paulo, SP, 05508-090, Brazil Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS), Rua Felipe Néri 382/203, Porto Alegre, RS, 90550-140, Brazil Centro para la Sostenibilidad Ambiental, Universidad Peruana Cayetano Heredia (UPCH), Armendáriz 445, Miraflores, Lima 18, Peru
Diogo Meyer
Affiliation:
Laboratório de Biologia Evolutiva e Conservação de Vertebrados (LABEC), Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, São Paulo, SP, 05508-090, Brazil
Joseph Hoffman
Affiliation:
Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK
Patricia Majluf
Affiliation:
Centro para la Sostenibilidad Ambiental, Universidad Peruana Cayetano Heredia (UPCH), Armendáriz 445, Miraflores, Lima 18, Peru
João S. Morgante
Affiliation:
Laboratório de Biologia Evolutiva e Conservação de Vertebrados (LABEC), Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, Cidade Universitária, São Paulo, SP, 05508-090, Brazil
*
Correspondence should be addressed to: L.R. de Oliveira, Laboratório de Biologia Evolutiva e Conservação de Vertebrados – LABEC-USP, Universidade de São Paulo, Departado Biologia (Genética), Rua do Matão 277, Cidade Universitária, 05508-900 – São Paulo – SP, Brazil email: [email protected]
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Abstract

The South American fur seal, Arctocephalus australis, was one of the earliest otariid seals to be exploited by humans: at least 6000 years ago on the Atlantic coast and 4000 on the Pacific coast of South America. More than 750,000 fur seals were killed in Uruguay until 1991. However, a climatological phenomenon—the severe 1997–1998 El Niño Southern Oscillation (ENSO)—was responsible for the decline of 72% of the Peruvian fur seal population due to starvation as a consequence of warming of sea-surface temperatures and primary productivity reduction. Currently, there is no precise information on global population size or on the species' conservation status. The present study includes the first bottleneck test for the Pacific and Atlantic populations of A. australis based on the analysis of seven microsatellite loci. Genetic bottleneck compromises the evolutionary potential of a population to respond to environmental changes. The perspective becomes even more alarming due to current global warming models that predict stronger and more frequent ENSO events in the future. Our analysis found moderate support for deviation from neutrality–equilibrium for the Pacific population of fur seals and none for the Atlantic population. This difference among population reflects different demographic histories, and is consistent with a greater reduction in population size in the Pacific. Such an event could be a result of the synergic effects of recurrent ENSO events and the anthropogenic impact (sealing and prey overfishing) on this population.

Keywords

South American fur sealArctocephalus australisbottleneckmicrosatelliteEl Niño Southern Oscillation (ENSO)
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 8 , December 2009 , pp. 1717 - 1725
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Allen, P.J., Amos, W., Pomery, P.P. and Twiss, S.D. (1995) Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between 2 British breeding colonies. Molecular Ecology 4, 653–662.CrossRefGoogle Scholar
Arias-Schreiber, M. (2000) Distribución, tamaño y estructura de las poblaciones de lobos marinos Arctocephalus australis y Otaria byronia en el litoral Peruano durante 1999. Informe Anual 1999. Informe Interno del Instituto del Mar del Perú.Google Scholar
Arias-Schreiber, M. and Rivas, C. (1998) Distribución, tamaño y estructura de las poblaciones de lobos marinos Arctocephalus australis y Otaria byronia en el litoral Peruano, en Noviembre 1996 y Marzo 1997. Informe Progresivo del Instituto del Mar del Perú 73. Callao, Peru, pp. 17–32.Google Scholar
Bonavia, D. (1982) Los gavilanes (precerámico peruano), mar, desierto y oasis en la historia del hombre. Lima: Editorial Ausonia.Google Scholar
Brookfield, J.F.Y. (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Molecular Ecology 5, 453–455.CrossRefGoogle ScholarPubMed
Cane, M.A. (1983) Oceanographic events during El Niño. Science 222, 1189–1195.CrossRefGoogle ScholarPubMed
Coltman, D.W., Bowen, W.D. and Wright, J.M. (1996) PCR primers for harbour seal (Phoca vitulina concolor) microsatellites amplify polymorphic loci in other species. Molecular Ecology 5, 161–163.CrossRefGoogle Scholar
Cornuet, J.M. and Luikart, G. (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 2001–2014.CrossRefGoogle ScholarPubMed
Cushing, D.H. (1982) Climate and fisheries. London: Academic Press.Google Scholar
De Vries, T.J. (1987) A review of geological evidence for ancient El Niño activity in Peru. Journal of Geophysical Research 92, 14471–14479.CrossRefGoogle Scholar
Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. and Freimer, N.B. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences USA 91, 3166–3170.CrossRefGoogle ScholarPubMed
Fabiani, A., Hoelzel, A.R., Galimberti, F. and Muelbert, M.M.C. (2003) Long-range paternal gene flow in the southern elephant seal. Science 299, 676.CrossRefGoogle ScholarPubMed
Frankel, O.H. and Soulé, M.E. (1981) Conservation and evolution. Cambridge: Cambridge University Press.Google Scholar
Frankham, R. (1995) Inbreeding depression: a threshold effect. Conservation Biology 9, 792–799.CrossRefGoogle Scholar
Garza, J.C. and Williamson, E.G. (2001) Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10, 305–318.CrossRefGoogle ScholarPubMed
Glantz, M.H. (1996) Currents of change—El Niño's impact on climate and society. Cambridge: Cambridge University Press.Google Scholar
Goodman, S.J. (1997) Development of PCR primers derived from the European harbour seal (Phoca vitulina vitulina) which amplify microsatellite loci in diverse pinnipeds species. Animal Genetics 28, 310–311.Google Scholar
Goodnight, C.J. (1987) On the effect of founder events on epistatic genetic variance. Evolution 41, 80–91.CrossRefGoogle ScholarPubMed
Hedrick, P.W. and Miller, P.S. (1992) Conservation genetics: techniques and fundamentals. Ecological Applications 2, 30–46.CrossRefGoogle ScholarPubMed
Hoelzel, A.R., LeBouef, B.J., Campagna, C. and Reiter, J. (1999) Alpha male paternity in elephant seals. Behavioral Ecology and Sociobiology 46, 298–306.CrossRefGoogle Scholar
Hoffman, J.I., Boyd, I.L. and Amos, W. (2003) Male reproductive strategy and the importance of maternal status in the Antarctic fur seal Arctocephalus gazella. Evolution 57, 1917–1930.Google ScholarPubMed
Idyll, C.P. (1973) The anchovy crisis. Scientific American 228, 22–29.CrossRefGoogle Scholar
Kimura, M. and Crow, J.F. (1964) The number of alleles that can be maintained in a finite population. Genetics 49, 728–738.CrossRefGoogle Scholar
Lande, R. (1988) Genetics and demography in biological conservation. Science 241, 1455–1459.CrossRefGoogle ScholarPubMed
Leberg, P.L. (1990) Influence of genetic variability on population growth: implications for conservation. Journal of Fish Biology 37, 193–195.CrossRefGoogle Scholar
Luikart, G. and Cornuet, J.M. (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology 12, 228–237.CrossRefGoogle Scholar
Majluf, P. (1987) South American fur seal, Arctocephalus australis, in Peru. In Croxall, J.P. and Gentry, R.L. (eds) Proceedings of an International Symposium and Workshop. University of Cambridge, 23–27 April 1984. Status, biology and ecology of fur seals, Cambridge, pp. 23–27.Google Scholar
Majluf, P. (1992) Timing of births and juvenile mortality in the South American fur seal in Peru. Journal of Zoology, London 227, 367–383.CrossRefGoogle Scholar
Majluf, P. and Apaza, M. (1998) Effects of the 1997/1998 El Niño on pinnipeds in Peru. In Anais da 8a Reunião de Trabalhos de Especialistas em Mamíferos Aquáticos da América do Sul e 2° Congresso da Sociedade Latinoamericana de Especialistas em Mamíferos Aquáticos de América do Sul, 25–29 October 1998, Olinda, p. 120.Google Scholar
Majluf, P. and Trillmich, F. (1981) Distribution and abundance of sea lions (Otaria byronia) and fur seals (Arctocephalus australis in Peru. Zeitschriften für Saügetierkunde 46, 384–393.Google Scholar
Majluf, P., Riveros, J.C. and Parlane, S. (1996) Cool spots as ‘hot spots’: the evolution of lekking in the South American fur seal. In Croxall, J.P. and R.L. Gentry, R.L. (eds) International Symposium and workshop on Otariid reproductive strategies and conservation. 12–16 April 1996, Washington, EUA, p. 26.Google Scholar
Majluf, P., Boness, D., Insley, S. and Paredes, R. (2000) Determinantes de la estructura del sistema social en el lobo fino sudamericano Arctocephalus australis—resultados de un experimento natural. In Anales de la 9a Reunión de Trabajo de Especialistas en Mamíferos Acuáticos de América del Sur y 3° Congreso de la Sociedad Latinoamericana de Especialistas en Mamíferos Acuáticos de América del Sur, 30 October–3 November 2000, Buenos Aires, Argentina, p. 81.Google Scholar
NCDC–NOOA 2007. The top 10 El Niño Events of the 20th Century. Available from: http://www.ncdc.noaa.gov/oa/climate/research/1998/enso/10elnino.html (accessed March 2007).Google Scholar
Oliveira, L.R. (2004) Variação geográfica do lobo-marinho sul-americano, Arctocephalus australis (Zimmermann, 1783) com base em dados morfológicos e moleculares. PhD thesis. Universidade de São Paulo, São Paulo, Brazil.Google Scholar
Oliveira, L.R., Hingst-Zaher, E. and Morgante, J.S. (2005) Size and shape sexual dimorphism in the skull of the South American fur seal, Arctocephalus australis (Zimmermann, 1783) (Carnivora: Otariidae). Latin American Journal of Aquatic Mammals 4, 27–40.CrossRefGoogle Scholar
Oliveira, L.R., Arias-Schreiber, M., Meyer, D. and Morgante, J.S. (2006) Effective population size in a bottlenecked fur seal population. Biological Conservation 131, 505–509.CrossRefGoogle Scholar
Oliveira, L.R., Hoffman, J.I., Hingst-Zaher, E., Majluf, P., Muelbert, M.M.C., Morgante, J.S. and Amos, W. (2008) Morphological and genetic evidence for two evolutionarily significant units (ESUS) in the South American fur seal, Arctocephalus australis. Conservation Genetics 9, 1451–1466.CrossRefGoogle Scholar
Otha, T. and Kimura, M. (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genetics Research, Cambridge 22, 201–204.Google Scholar
Pauly, D. and Tsukayama, I. (1987) On the implementation of management-oriented fishery research: the case of the Peruvian Anchoveta. In Pauly, D. and Tsukayama, I. (eds) The Peruvian Anchoveta and its upwelling ecosystem: three decades of change. ICLARM Studies and Reviews 15, 351 p. Instituto del Mar del Perú (IMARPE), Callao, Perú; Deutsche Gesellschaft für Technische Zusammenarbeit (GTZ), GMBH, Eschborn, República Federal Alemana; e International Center for Living Aquatic Resources Management (ICLARM), Manila, Filipinas. pp. 1–13.Google Scholar
Pimm, S.L., Gittleman, J.L., McCracken, G.F. and Gilpin, M.E. (1989) Plausible alternatives to bottlenecks to explain reduced genetic diversity. Trends in Ecology and Evolution 4, 176–178.CrossRefGoogle ScholarPubMed
Piry, S., Alapetite, A., Cornuet, J.-M., Paetkau, D., Baudouin, L. and Estoup, A. (1999) GeneClass2: a software for genetic assignment and first generation migrants detection. Available from http://www.montpellier.inra.fr/CBGP/softwaresGoogle Scholar
Quinn, W.H., Neal, V.T. and Antuñez de Mayolo, S.E. (1987) El Niño occurrences over the past four and half centuries. Journal of Geophysical Research 92, 14449–14461.CrossRefGoogle Scholar
Reed, D.H., Grady, J.J.O., Brook, B.W., Ballou, J.D. and Frankham, R. (2003) Estimates of minimum viable population sizes for vertebrates and factors influencing those estimates. Biological Conservation 113, 23–24.CrossRefGoogle Scholar
Reeves, R.R., Stwart, B.S. and Leatherwood, S. (1992) The Sierra Club handbook of seals and sirenians. San Francisco: Sierra Club Books.Google Scholar
Rousset, M. and Raymond, F. (1995) An exact test for population differentiation. Evolution 49, 1280–1283.Google Scholar
Sandweiss, D.H., Richardson, J.B. III, Reitz, E.J., Rollins, H.B. and Maasch, K.A. (1996) Geoarchaeological evidence from Peru for a 5000 years BC onset of El Niño. Science 273, 1531–1533.CrossRefGoogle Scholar
Schiavini, A.C.M. (1987) Una aproximación a la predación de los aborígenes prehistóricos del Canal de Beagle sobre los pinípedos. In Anais da 2a. Reunião de Trabalho de Especialistas em Mamíferos Aquáticos da América do Sul, 4–8 January 1986, Abstracts, Rio de Janeiro, Brazil, pp. 81–82.Google Scholar
Seal Conservation Society (SCS) (2007) South American fur seal. Available from http://www.pinnipeds.org/species/samfursl.htm (accessed March 2007).Google Scholar
Stevens, M.A. and Boness, D.J. (2003) Influences of habitat features and human disturbance on use of breeding sites by a declining population of southern fur seals (Arctocephalus australis). Journal Zoology, London 260, 154–152.CrossRefGoogle Scholar
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. and Shipley, P. (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.CrossRefGoogle Scholar
Weber, D.S., Stwart, B.S. and Lehman, N. (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). Journal of Heredity 95, 144–153.CrossRefGoogle ScholarPubMed
Williamson-Natesan, E.G. (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conservation Genetics 6, 551–562.CrossRefGoogle Scholar
Worthington-Wilmer, J., Allen, P.J., Pomeroy, P.P., Twiss, S.D. and Amos, W. (1999) Where have all the fathers gone? An extensive microsatellite analysis of paternity in the grey seal (Halichoerus grypus). Molecular Ecology 8, 1417–1429.CrossRefGoogle ScholarPubMed
Ximenez, I.M. and Langguth, E. (2002) Isla de Lobos. Graphis ed.Google Scholar