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Multilocus test of the absence of mtDNA phylogeographic structure in a widespread wader, the Common Sandpiper (Actitis hypoleucos)

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Abstract

Although geographically structured mitochondrial DNA (mtDNA) trees often present straightforward evidence for independently evolving lineages, unstructured mtDNA trees are often interpreted as inconclusive or even misleading inferences of phylogeographic history. Some authors believe that stochastic coalescent processes or natural selection can result in mtDNA-based gene trees that fail to capture existing geographic structure. In this study, we sequenced four introns and one exon to test a published mtDNA tree that showed a lack of phylogeographic structure in the Common Sandpiper (Actitis hypoleucos). Neither individual nuclear gene trees nor analyses based on the five genes combined showed geographic structure in this widespread Palearctic wader. Multilocus neutrality tests suggested that the unstructured mtDNA tree was not biased by natural selection although the variation pattern at the exon, Mc1r, was not neutral. Coalescence-based analyses showed that this species experienced a recent population expansion, which could explain the lack of population structure. Overall, the mtDNA results were consistent with those based on nuclear loci in suggesting a lack of strong population structure and a recent population increase. However, multiple genes are needed to quantify demographic history such as timing and extent of effective population size change.

Zusammenfassung

Ein Multilocus-Test auf das Fehlen einer phylogeografischen Strukturierung der mtDNA beim Flussuferläufer Actitis hypoleucos, einer weitverbreiteten Watvogelart

Obwohl geografisch strukturierte Stammbäume auf der Basis von mitochondrialer DNA (mtDNA) häufig klare Belege für sich unabhängig entwickelnde Stammeslinien liefern, werden unstrukturierte mtDNA-Stammbäume oft als uneindeutige oder sogar irreführende Rückschlüsse auf die phylogeografische Geschichte angesehen. Manche Autoren sind der Ansicht, dass stochastische Durchmischungsprozesse oder natürliche Selektion zu mtDNA-basierten Stammbäumen führen können, welche die bestehende geografische Strukturierung nicht richtig abbilden. Für diese Studie sequenzierten wir vier Introns und ein Exon, um einen mtDNA-Stammbaum aus der Literatur zu überprüfen, der auf das Fehlen einer geografischen Strukturierung beim Flussuferläufer Actitis hypoleucos deutete. Weder Stammbäume auf der Basis einzelner Kerngene noch kombinierte Analysen der fünf Gene zeigten eine geografische Strukturierung dieser weitverbreiteten paläarktischen Watvogelart. Tests auf Multilocus-Neutralität deuteten darauf hin, dass der unstrukturierte mtDNA-Stammbaum nicht durch natürliche Selektion verzerrt wurde, obgleich das Variationsmuster des Exons Mc1r sich nicht neutral verhielt. Durchmischungsbasierte Analysen zeigten, dass diese Art in jüngerer Zeit eine Populationsausweitung zu verzeichnen hatte, welche die mangelnde Populationsstrukturierung erklären könnte. Insgesamt deckten sich die anhand der mt-DNA gewonnen Ergebnisse mit denen auf der Grundlage nukleärer Loci und wiesen auf das Fehlen einer deutlichen Populationsstrukturierung und auf einen kürzlich erfolgten Populationsanstieg hin. Allerdings bedarf es der Analyse mehrerer Gene, um historische demografische Ereignisse wie zum Beispiel Zeitpunkt und Ausmaß effektiver Änderungen der Populationsgröße zu quantifizieren.

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Acknowledgments

We thank M. Westberg for laboratory assistance. We are grateful to the Burke Museum and S. Rohwer for access to tissue and DNA samples. We also thank A. Jones, B. Barber, Yu. Lohman, A. Banin, A. Andreev, V. Masterov, R. Faucett, V. Rohwer, I. Fadeev, E. Nesterov, I. Karagodin, E. Koblik, and Ya. Red’kin for collecting specimens. Support came from NSF (DEB 9707496, 0212832 and 0919494).

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Correspondence to Chih-Ming Hung.

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Hung, CM., Drovetski, S.V. & Zink, R.M. Multilocus test of the absence of mtDNA phylogeographic structure in a widespread wader, the Common Sandpiper (Actitis hypoleucos). J Ornithol 154, 1105–1113 (2013). https://doi.org/10.1007/s10336-013-0980-1

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