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Demographic history of the Magellanic Penguin (Spheniscus magellanicus) on the Pacific and Atlantic coasts of South America

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Abstract

Spatial subdivision, local extinction and recolonization influence the genetic variation of natural populations. Different levels of population structure can be identified in nature, from panmictic populations, in which high gene flow homogenizes diversity across localities, to metapopulations, where combinations of moderate to high levels of population differentiation and source-sink population dynamics are expected. Gene flow, dispersal and recolonization can be affected by changes in ecological conditions such as climate and resource distribution. Evaluating demographic history is crucial for understanding current population dynamics. We assessed a mitchondrial DNA (mtDNA) control region and microsatellite data for 210 Magellanic Penguins (Spheniscus magellanicus) from 13 breeding colonies on the coastlines of Chile and Argentina, covering a great portion of the species’ distribution. We found high levels of genetic diversity and detected two genetic-geographic regions, Pacific and Atlantic, probably due to interruption of the connection between the oceans during the Last Glacial Maximum (LGM), when several parts of the Magellanic Channel were connected to the continent. The Atlantic ocean colonies showed a slight differentiation between the northern and southern colonies, and the Falkand/Malvinas one seems to be a mix of northern, southern and Pacific colonies. Magellanic Penguins showed intense gene flown among colonies, and exhibited low levels of genetic differentiation in each region. Furthermore, our findings indicate that the Magellanic Penguin experienced a population expansion around 17,500 years ago, which is in agreement with the timing of a decreased sea level and the exposure of the continental shelf along the coast of Argentina and the Falkland/Malvinas Islands at the end of the LGM. Thus, our results suggest that climate changes that affect the sea level in South America can play important roles in the migration of Magellanic Penguins.

Zusammenfassung

Die demografische Geschichte des Magellanpinguins ( Spheniscus magellanicus ) an den pazifischen und atlantischen Küsten Südamerikas

Räumliche Trennung sowie lokale Aussterbe- und Wiederbesiedlungsereignisse beeinflussen die genetische Variation natürlicher Populationen. In der Natur lassen sich verschiedene Ebenen der Populationsstruktur unterscheiden—von panmiktischen Populationen, bei denen starker Genfluss die Diversität zwischen den Örtlichkeiten ausgleicht, bis hin zu Metapopulationen, bei denen eine Kombination aus mäßigen bis hohen Graden der Populationsdifferenzierung und einer Source-Sink-Populationsdynamik zu erwarten ist. Genfluss, Dismigration und Wiederbesiedlung können durch Veränderungen der ökologischen Bedingungen, wie zum Beispiel Klima und Ressourcenverteilung, beeinflusst werden. Eine Analyse der demografischen Geschichte ist für das Verständnis der aktuellen Populationsdynamik daher von fundamentaler Bedeutung. Wir untersuchten mtDNA aus der Kontrollregion und Mikrosatelliten-DNA-Daten von 210 Magellanpinguinen (Spheniscus magellanicus) aus 13 Brutkolonien entlang der Küsten von Chile und Argentinien, was einen Großteil des Verbreitungsgebietes der Art abdeckt. Wir stellten ein hohes Maß an genetischer Diversität fest und ermittelten zwei genetisch-geografische Regionen, eine pazifische und eine atlantische, vermutlich aufgrund einer Unterbrechung der Verbindung zwischen den Ozeanen während des letzteiszeitlichen Maximums (Last Glacial Maximum, LGM), als verschiedene Abschnitte der Magellanstraße mit dem Kontinent verbunden waren. Am Atlantik zeigten sich leichte Unterschiede zwischen nördlichen und südlichen Küstenkolonien; auf den Falklandinseln/Malwinen scheint es sich um eine Mischung aus nördlichen, südlichen und pazifischen Kolonien zu handeln. Die Magellanpinguine zeigten einen starken Genfluss zwischen den Kolonien, aber ein geringes Maß an genetischer Differenzierung in der jeweiligen Region. Des Weiteren deuten unsere Ergebnisse an, dass es bei den Magellanpinguinen vor etwa 17.500 Jahren zu einer Populationsausdehnung kam, was im Einklang mit einer Periode abgesenkten Meeresspiegels und freiliegender Kontinentalschelfe entlang der Küsten Argentiniens und der Falklandinseln/Malwinen am Ende des letzteiszeitlichen Maximums steht. Daher legen unsere Ergebnisse nahe, dass Klimaveränderungen in Südamerika, welche den Meeresspiegel beeinflussen, eine wichtige Rolle für die Ausbreitungsbewegungen der Magellanpinguine spielen können.

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Acknowledgements

This study was financed by the National Counsel of Technological and Scientific Development, Brazil (CNPq 490403/2008-5); the São Paulo Research Foundation (FAPESP 2009/08624-8); FAPESP-CONICET (the National Research Council of Argentina) (10/525908), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior of Brazil (CAPES), the Fondo Nacional de Desarollo Cientifico y Tecnologico del Chile (FONDECYT 11110060; 1010250; 1100695; 1150517); Sea World and Busch Gardens Conservation Fund, PICT 2110. Samples were obtained under Subpesca CONAF, DGFFS-minag, IBAMA, and Secretaria de Ambiente y Desarrollo Sustentable of Argentina (permits 011187/2010). Permits were granted from the Dirección de Fauna y Flora Silvestre and the Secretaría de Turismo y Areas Protegidas de la Provincia de Chubut. We thank Sarah Crofts, Micky Reeves, and Jonathan Handley from Falklands Conservation for their contribution to the sampling. The study was approved by the Ethics Committee of Pontificia Universidad Catolica de Minas Gerais, Brazil. All samples were collected with the Subpesca permit no. 110, CITES permit (Brazil, 10BR005149/DF; Chile, 0524984; Argentina, 011187).

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Contributions

G. P. M. D. is interested in phylogeography and population genetics as a background to conservation, and she contributed to the design of the study, the sampling, data analysis, and the text. F. R. S., L. R. .O and J. S. M. are interested in evolutionary biology, phylogeography and conservation biology and contributed to writing the draft of the manuscript. D. G. A., E. C., E. F. and A. M. are interested in ornithology including penguins and other Antarctic organisms, and contributed to the sampling. J. A. V. is interested in phylogeography and conservation genetics, and contributed to sampling, data analysis and writing the text. G. C. M., A. C. M. M., L. T. C. and V. S. A. were responsible for the laboratory procedures.

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Correspondence to Gisele Pires Mendonça Dantas.

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Communicated by C. Barbraud.

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10336_2018_1538_MOESM1_ESM.tif

S1 Haplotype network for the D-loop region of Magellanic Penguin sequences. Colors correspond to haplotype source: light grey Chiloé, dark grey Magdalena, black Cabo Virgines, light green San Julian, dark green Falklands/Malvinas, light blue San Lorenzo, blue Isla Moreno, dark blue Cabo Bahía, yellow Cabo Blanco, orange Quiroga/Chaffer, pink Pinguino, brown Cb Guardian, red median vectors or hypothetical states inferred by maximum parsimony. Node size corresponds to haplotype frequency. (TIFF 261 kb)

10336_2018_1538_MOESM2_ESM.jpg

S2 Bayesian analysis of population structure from Magellanic Penguin sequences (D-loop region), considering clustering of individuals with spatial models, with mixture and admixture analysis, considering K1–13 and 100,000 interactions. (JPEG 30 kb)

10336_2018_1538_MOESM3_ESM.tif

S3 Comparison of STRUCTURE classification of Magellanic Penguin based on ten microsatellite loci admixture model, with K = 3 for 13 colonies with a total of 210 individuals with LOCPRIOR, 13 colonies with a total of 210 individuals without LOCPRIOR. y-axis shows individual probabilities of assignment. (TIFF 350 kb)

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Dantas, G.P.M., Maria, G.C., Marasco, A.C.M. et al. Demographic history of the Magellanic Penguin (Spheniscus magellanicus) on the Pacific and Atlantic coasts of South America. J Ornithol 159, 643–655 (2018). https://doi.org/10.1007/s10336-018-1538-z

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