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Matrilineal evidence for demographic expansion, low diversity and lack of phylogeographic structure in the Atlantic forest endemic Greenish Schiffornis Schiffornis virescens (Aves: Tityridae)

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Abstract

Studies of Atlantic forest (AF) organisms suggest that the historical dynamics of the forest cover produced demographically stable populations in its central region and unstable populations in the southern regions. We studied the mitochondrial phylogeographic structure of an AF passerine, the Greenish Schiffornis Schiffornis virescens (Tityridae), and evaluated questions related to the history of the AF. We analyzed cytochrome b and control region sequences of the mitochondrial genome by traditional phylogenetic and population genetic methods based on summary statistics. In addition, we used coalescent simulations to evaluate specific models of evolution of the populations of S. virescens. The results did not support phylogeographic partitions of the genetic variability of S. virescens. The overall Φst was = 0.32 and gene flow between regions was moderate to high. The analyses suggested that the total population of S. virescens suffered a bottleneck followed by a demographic expansion in the late Pleistocene. The bottleneck might have contributed to the extinction of intraspecific lineages, and hence to the observed lack of a strong phylogeographic pattern and low genetic diversity. Our results suggest that some AF taxa have had all their populations similarly affected by the recent history of the biome, contrary to what has been revealed from most of the other phylogeographic studies in the region and as suggested by a model of AF refuges (the Carnaval–Moritz model). We suggest that the response of organisms to common histories may be idiosyncratic, and predictions about the history of the biome should take into account ecological characteristics and distribution of each specific taxa.

Zusammenfassung

Matrilineare Hinweise auf demografische Expansion, geringe genetische Diversität und fehlende phylogeografische Struktur bei der Olivtrauerkotinga Schiffornis virescens (Aves: Tityridae), einer endemischen Vogelart der Mata Atlantica

Untersuchungen an Organismen der Mata Atlantica deuten darauf hin, dass die historische Dynamik der Waldbedeckung dort demografisch stabile Populationen in den inneren Bereichen und instabile Populationen in den südlichen Regionen hervorgebracht hat. Wir betrachteten die mitochondriale phylogeografische Struktur bei der Olivtrauerkotinga S. virescens (Tityridae), einem Sperlingsvogel der Mata Atlantica, und untersuchten Fragen im Zusammenhang mit der Geschichte dieses atlantischen Waldes. Wir analysierten Sequenzen von Cytochrom b und von Kontrollregionen des mitochondrialen Genoms unter Anwendung der gebräuchlichen phylogenetischen und populationsgenetischen Methoden auf der Grundlage statistischer Parameter. Zusätzlich verwendeten wir Coalescent Simulations, um spezifische Evolutionsmodelle für die Populationen von S. virescens zu testen. Die Ergebnisse konnten keine phylogeografischen Untereinheiten in der genetischen Variabilität von S. virescens belegen. Der Gesamtwert für Φst betrug 0,32 und der Genfluss zwischen den Regionen war mäßig bis hoch. Die Analysen deuten an, dass die gesamte Population von S. virescens zunächst durch einen genetischen Flaschenhals ging, worauf anschließend im Oberen Pleistozän eine demografische Expansion erfolgte. Dieser Flaschenhals könnte zum Aussterben intraspezifischer Abstammungslinien und somit zum beobachteten Mangel an deutlichen phylogeografischen Mustern und zu der geringen genetischen Diversität beigetragen haben. Unsere Ergebnisse legen nahe, dass bei manchen Taxa der Mata Atlantica alle Populationen durch die jüngere Geschichte dieses Bioms ähnlich beeinflusst wurden. Dies steht im Gegensatz zu den Erkenntnissen der meisten anderen phylogeografischen Studien aus dieser Region und zu einem Modell atlantischer Waldrefugien (Carnaval–Moritz-Modell). Wir vermuten, dass verschiedene Organismen selbst auf eine gemeinsame Geschichte in ihrer ganz eigenen Weise reagieren. Prognosen über die Geschichte des Bioms sollten daher immer auch die ökologischen Eigenschaften und die Verbreitung jedes einzelnen Taxons berücksichtigen.

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Acknowledgments

We thank R.G. Lima, A. Martensen, M. Marini, A. Uezu and J.P. Metzger for providing us with some tissue samples. We also thank IBAMA, Instituto Florestal (SP, Brazil), Instituto Estadual de Florestas (MG, Brazil) and the Ministerio de Ecología de Misiones (Argentina) for the appropriate permits. We are also grateful to Conservación Argentina (G. Zurita and D. Varela), J. Albuquerque, F. d′Horta, R. Pessoa, F. Nodari and T. Matsumoto for assistance during fieldwork. V.A. Ellis, L. Calderon and L. Campagna provided useful comments that improved an early version of the manuscript. Finally, we thank J. Fjeldså and the Associate Editor F. Bairlein for the revision and comments that helped to improve the manuscript. This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Brazil), Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina, grant PIP 276), Agencia Nacional de Promoción Científica y Tecnológica (Argentina, grant PICT 805), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (Brazil), Fundação de Amparo à Pesquisa do Estado de São Paulo (Brazil) and WWF (USA). All experiments comply with the current laws of the country in which they were performed. The authors declare that they have no conflict of interest.

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  1. Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-090, Brazil

    G. S. Cabanne, D. Meyer & C. Y. Miyaki

  2. CONICET, Av. Rivadavia 1917, C1033AAJ, Ciudad de Buenos Aires, Argentina

    G. S. Cabanne

  3. División de Ornitología, Museo Argentino de Ciencias Naturales “B. Rivadavia”, Ángel Gallardo 470, C1405DJR, Ciudad de Buenos Aires, Argentina

    G. S. Cabanne

  4. Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Belo Horizonte, MG, 31270-901, Brazil

    E. H. R. Sari & F. R. Santos

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Appendix 1

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Table 4 Schiffornis virescens and S. turdina sampling localities and sample information used in the present study
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Appendix 2

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Table 5 Nucleotide diversity of cytochrome b (mtDNA) from studies of Atlantic forest passerines
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Cabanne, G.S., Sari, E.H.R., Meyer, D. et al. Matrilineal evidence for demographic expansion, low diversity and lack of phylogeographic structure in the Atlantic forest endemic Greenish Schiffornis Schiffornis virescens (Aves: Tityridae). J Ornithol 154, 371–384 (2013). https://doi.org/10.1007/s10336-012-0901-8

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