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Evolution within the nuthatches (Sittidae: Aves, Passeriformes): molecular phylogeny, biogeography, and ecological perspectives

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Abstract

A comprehensive phylogeny of the nuthatches, genus Sitta, is proposed based on 21 of the 24–28 species recognized in the genus and three genes, two mitochondrial (cytochrome b and cytochrome oxidase subunit I) and one nuclear (RAG1). This phylogeny is well resolved and reveals several major clades within nuthatches. Przevalski’s Nuthatch Sitta przewalskii is sister to all other nuthatches, without any close relatives in our sampling. The larger species S. carolinensis and S. magna, despite their disjunct distributions, are sister taxa at the base of the tree. The next clade comprises the europaea group, which is sister to the two rock nuthatches (S. tephronota and S. neumayer), and to the Beautiful Nuthatch Sitta formosa of southeast Asia, although with less support. All these species use plastering to reduce the entrance of their hole or to build their nest with mud on rocks, but their ecologies are not as specialized as those of the rock nuthatches. The Asian small species (represented by S. azurea, S. frontalis and S. oenochlamys) form a well-supported clade. We confirm a single origin for the canadensis group that also includes the Yunnan nuthatch Sitta yunnanensis. Both are sister group to the two sibling species of North America (S. pygmaea and S. pusilla); all these species dig their own nest in trunks and are closely associated with coniferous forest. A biogeographical analysis supports the hypothesis of Asia being the center of diversification for nuthatches, with several independent dispersal events to North America.

Zusammenfassung

Evolution innerhalb der Kleiber (Sittidae: Aves, Passeriformes): molekulare Phylogenie, Biogeographie und ökologische Gegebenheiten

Auf der Grundlage von 21 der 24–28 derzeit anerkannten Kleiberaten schlagen wir eine umfassende Phylogenie der Gattung Sitta vor. Zwei Mitochondriengene (Cytochrom-b, COI) und ein Kerngen (RAG1) wurden herangezogen; die Phylogenie ist gut aufgelöst und weist mehrere größere Äste innerhalb der Kleiberverwandtschaft aus. Der chinesische Przhewalski-Kleiber (S. przhewalskii) ist Schwesterart zu allen anderen Kleibern und weist innerhalb der einbezogenen Taxa keine nahen Verwandten aus. Die größeren Arten S. carolinensis und S. magna sind trotz ihrer weit disjunkten Verbreitung in Nordamerika und Südostasien Geschwisterarten und stehen als nächster Ast nahe der Basis des genetischen Baumes. Der weitere Baum ist in zwei Hauptäste gegliedert. Einer umfasst die europaea-Artengruppe, in die auch der Himalayakleiber (S. himalayana) einbezogen ist, zusätzlich Felsenkleiber (S. tephronota), Klippenkleiber (S. neumayer) und der südostasiatische Prachtkleiber (S. formosa). Alle diese Arten verkleben die Höhleneingänge oder bauen die Nester gänzlich aus Lehm an Felsen; das Nestbauverhalten von Felsen- und Klippenkleiber ist am höchsten spezialisiert. Die asiatischen kleinen Arten, die hier von S. azurea, S. frontalis und S. oenochlamys repräsentiert sind, stellen einen Teil das anderen gut unterstützten phylogenetischen Hauptastes dar. Ihm gegenüber steht ein vielfältig strukturierter Ast mit acht Arten, die in oftmals winzigen Reliktarealen in der Westpaläarktis leben (S. whiteheadi, S. ledenti, S. krueperi), teils in China (S. yunnanensis, S. villosa) oder in Nordamerika (S. pusilla, S. pygmaea, S. canadensis). Wir bestätigen einen gemeinsamen Ursprung der canadensis-Gruppe, die auch den Yunnankleiber (S. yunnanensis) umfasst. Der gesamte Ast ist Schwestergruppe zu den kleinen nordamerikanischen Geschwisterarten S. pygmaea und S. pusilla. Alle diese Arten hacken ihre Nesthöhle eigenständig in Baumstämme und sind eng an Nadelbäume gebunden. Eine biogeografische Analyse unterstützt die Hypothese, dass Asien das Diversifikationszentrum der Kleiber darstellt. Von dort brachten mehrere voneinander unabhängige Ausbreitungsereignisse Gattungsvertreter nach Nordamerika.

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Acknowledgments

J. Martens thanks Feldbausch Stiftung and Wagner Stiftung, both at Fachbereich Biologie of Mainz University, and Research commission of Deutsche Ornithologen-Gesellschaft (East Asia Grants to J. Martens, A. Gebauer and M. Kaiser) for travel grants. J. Martens is most thankful to Sun YueHua for his generous hospitality especially during field trips in numerous provinces of China and in the Lianhua Shan Nature Reserve. A. Cibois and E. Pasquet thank Han Lian Xian for his kind help during field work in Yunnan. A. Cibois and E. Pasquet thank the Service de Systématique Moléculaire in MNHN, Paris for help during laboratory work. Two anonymous reviewers provided helpful comments on the manuscript. We also thank all colleagues and institutions who provided samples: M. Baloutch (Iran); Zhao Zhongying (North Korea); Joel Cracraft and Paul Sweet, AMNH (American Museum of Natural History), New York, USA; John Bates and David Willard, FMNH (Field Museum of Natural History), Chicago, USA; Frederick Sheldon and Diana Reynolds, LSUMNS (Louisiana State University Museum of Natural Science), Baton Rouge, USA; Robert Prys-Jones and Mark Adams, NHM (Natural History Museum), Tring, UK; Sharon Birks (University of Washington, Burke Museum), Washington, USA.

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Authors and Affiliations

  1. UMR7205 CNRS « OMSI », Muséum National d’Histoire Naturelle, 57 Rue Cuvier, Case Postale 51, 75231, Paris Cedex 05, France

    Eric Pasquet

  2. Department of Ecology, Evolution and Behavior and Bell Museum of Natural History, University of Minnesota, 100 Ecology Building, 1987 Upper Buford, Circle, St. Paul, MN, 55108, USA

    F. Keith Barker

  3. Institut für Zoologie, Saarstraße 21, 55099, Mainz, Germany

    Jochen Martens

  4. UMS2700 CNRS « OMSI », Muséum National D’Histoire Naturelle, 57 Rue Cuvier, Case Postale 26, 75231, Paris Cedex 05, France

    Eric Pasquet & Annie Tillier

  5. Institut de Génomique, CEA, 2 Rue Gaston Crémieux, 91057, Évry Cedex, France

    Corinne Cruaud

  6. Department of Mammalogy and Ornithology, Natural History Museum of Geneva, CP 6434, 1211, Geneva 6, Switzerland

    Alice Cibois

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  1. Eric Pasquet
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Correspondence to Eric Pasquet.

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Fig. S1

Bayesian chronogram for the Sittidae inferred using BEAST and a rate-based calibration. Time scale in Ma. Error bars represent 95 % HPD intervals (PDF 145 kb)

Table S1

List of samples and Genbank accession numbers (DOC 61 kb)

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Pasquet, E., Barker, F.K., Martens, J. et al. Evolution within the nuthatches (Sittidae: Aves, Passeriformes): molecular phylogeny, biogeography, and ecological perspectives. J Ornithol 155, 755–765 (2014). https://doi.org/10.1007/s10336-014-1063-7

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