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Late Pleistocene climate change shapes population divergence of an Atlantic Forest passerine: a model-based phylogeographic hypothesis test

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Abstract

Several evolutionary processes seem to have influenced the Atlantic Forest (AF) biogeographic history, as suggested by phylogeographic studies that have shown a multitude of patterns. Here, we use approximate Bayesian computation to test alternative historical hypotheses to investigate the phylogeographic pattern, historical demography, and palaeodistribution of the Grey-hooded Flycatcher Mionectes rufiventris, an endemic AF bird, distributed mainly in southern areas of the biome. Our goal was to integrate molecular and ecological data to test diversification hypotheses available for the AF. Our investigation revealed two mitochondrial phylogroups, geographically structured around the Doce River. Coalescence analyses revealed that these groups shared a common ancestor in the Late Pleistocene, between 200,000 and 300,000 years ago, and that divergence was probably associated with climatic fluctuations during this period. Demographic analyses suggested recent demographic expansion in both groups. Ecological niche modelling suggested larger ranges during the Last Glacial Maximum (LGM) than in the present, not in agreement with the genetic pattern recovered. We simulated alternative historical models to test these competing scenarios. Our findings support the existence of small populations during the LGM which expanded afterwards from putative refuges. Thus, these results suggest that the Pleistocene climate shaped patterns of diversification and demographic history of this species in accordance with the classical forest refuge hypothesis.

Zusammenfassung

Klimaänderungen im späten Pleistozän prägten die Populationsdivergenz eines Singvogels der Mata Atlantica: ein modellbasierter Test phylogeografischer Hypothesen

Mehrere evolutionäre Prozesse scheinen die biogeografische Geschichte der Mata Atlantica (engl.: Atlantic Forest, AF) beeinflusst zu haben, wie phylogeografische Studien nahelegen, welche eine Unzahl von Mustern aufgedeckt haben. Mittels Bayes’scher Näherungsrechnung (engl.: Approximate Bayesian Computation, ABC) prüften wir alternative historische Hypothesen, um die phylogeografischen Muster, die historische Demografie sowie die paläologische Verbreitung des Graukopf-Pipratyrann Mionectes rufiventris zu untersuchen, einer für den AF endemischen Vogelart, welche überwiegend in den südlichen Bereichen dieses Biomes verbreitet ist. Unser Ziel war es, unter Einbeziehung molekularer und ökologischer Daten die für den AF verfügbaren Diversifikationshypothesen zu prüfen. Unsere Multilokus-Untersuchung ließ zwei phylogenetische Gruppen erkennen, die geografisch um den Rio Doce angeordnet waren. Koalenszenzanalysen zeigten, dass diese Gruppen einen gemeinsamen Vorfahren im späten Pleistozän (vor 200.000-300.000 Jahren) besaßen und dass die Divergenz vermutlich mit Klimafluktuationen während dieser Periode zusammenhing. Demografische Analysen deuteten auf eine vor kurzem erfolgte demografische Expansion in beiden Gruppen hin. Die ökologische Nischenmodellierung ließ vermuten, dass die Verbreitungsgebiete während des Letzteiszeitlichen Maximums (engl.: Last Glacial Maximum, LGM) größer waren als heute, was nicht mit dem beobachteten genetischen Muster in Einklang steht. Zur Prüfung dieser konkurrierenden Szenarien führten wir Simulationen alternativer historischer Modelle durch. Unsere Befunde sprechen für die Existenz kleiner Populationen während des LGM, die sich anschließend ausgehend von angenommenen Refugien ausbreiteten. Diese Ergebnisse deuten somit darauf hin, dass das Klima im Pleistozän die Diversitätsmuster und die demografische Geschichte dieser Vogelart gemäß der klassischen Waldrefugien-Hypothese gestaltet hat.

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Acknowledgements

The authors thank the Rede de Plataformas Tecnológicas for use of its sequencing facility in FIOCRUZ-Bahia, and the organizations which provided funds for this study: FAPESB (RED0045/2014; JCB0026/2016), CNPq (for scientific initiation grant and through project 443249/2014-8), CAPES, PROPCI/UFBA (PRODOC-2013/5813), FAPESP (2009/12989-1, BIOTA 2013/50297-0), NSF (DOB 1343578), and NASA. This work was developed in the Research Center on Biodiversity and Computing (BioComp) of the Universidade de São Paulo (USP), supported by the USP Provost’s Office for Research. We also thank the Laboratório de Biodiversidade e Evolução Molecular (LBEM) of the Universidade Federal de Minas Gerais, and Museu Nacional do Rio de Janeiro of the Universidade Federal do Rio de Janeiro for providing tissue samples for this study. We are grateful to Marcelo Vasconcelos for discussions and comments on previous versions of this manuscript. We thank two anonymous reviewers and the Editor Franz Bairlein for their comments.

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Authors and Affiliations

  1. Instituto de Biologia, Universidade Federal da Bahia, Salvador, BA, 40170-115, Brazil

    Rilquer Mascarenhas, Ricardo Dobrovolski & Henrique Batalha-Filho

  2. National Institute of Science and Technology in Interdisciplinary and Transdisciplinary Studies in Ecology and Evolution (INCT IN-TREE), Instituto de Biologia, Universidade Federal da Bahia, Salvador, BA, 40170-115, Brazil

    Rilquer Mascarenhas & Henrique Batalha-Filho

  3. Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, 05508-090, Brazil

    Cristina Yumi Miyaki

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  1. Rilquer Mascarenhas
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Correspondence to Rilquer Mascarenhas.

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Sequence data have been submitted to GenBank: accession numbers cytb (MK610041-MK610097), G3PDH (MK671363-MK671418), TGFB2 (MK671419-MK671472).

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Mascarenhas, R., Miyaki, C.Y., Dobrovolski, R. et al. Late Pleistocene climate change shapes population divergence of an Atlantic Forest passerine: a model-based phylogeographic hypothesis test. J Ornithol 160, 733–748 (2019). https://doi.org/10.1007/s10336-019-01650-1

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