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Integrating phylogeography and ecological niche modelling to test diversification hypotheses using a Neotropical rodent

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Abstract

Several hypotheses have been used to explain diversification in the Neotropics. Integrating evolution with ecology extends the scope of testing the frameworks of these hypotheses. We test diversification hypotheses by integrating phylogeography and ecological niche models (ENMs) using the rodent Hylaeamys megacephalus (Azara’s broad-headed oryzomys or large headed rice rat) of the Amazon and dry forests, as a model. We estimated divergence times, ancestral areas, diversification events, historical demography, haplotype sharing, and genetic distances based on the mitochondrial cytochrome b gene. We generated ENMs and tested for niche divergence between lineages; integrated genetic data to predict gene flow corridors; and projected paleodistributions for comparison with historical demography. We found high structuring in northern Amazonia on the left bank of the Amazon River, and less structure but secondary contact in southern Amazonia and dry forests. The Northern Amazonian lineage diverged from the other lineages through dispersal followed by vicariance due to the Amazon River about 1.35 Mya, while the Southern Amazonian and Cerrado lineages diverged through dispersal about 0.78 Mya. Paleodistribution models revealed expansions of dry forest lineages consistent with the Refugia Hypothesis, but not retraction for the humid forest lineage, which were not congruent with historical demography data. Niche divergence was not supported for the Northern Amazonian lineage, whereas habitat corridors linking current lineages suggest environmental continuity to their distributions that is concordant with a riverine barrier. In contrast, niche divergence was supported between the Southern Amazonian and Cerrado lineages, indicating that isolation followed by ecological divergence likely acted on this diversification. The recent Amazon River barrier and ecological differentiation observed here will surely provide insight for future studies and hypotheses of biodiversity diversification in the Neotropics. Studies that integrate evolution and ecology promise to disentangle alternative hypotheses and shed light on the biogeography of this megadiverse region.

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Acknowledgements

We thank A. Townsend Peterson, Fernanda P. Werneck, Rafael N. Leite and Igor L. Kaeffer for help in delineating the project; Rafael N. Leite and Rogério Rossi for providing tissue samples; Cleuton L. Miranda for reviewing the manuscript and William T. Peçanha for help with phylogenetic analyses. We also thank the team from LEGAL for helping with molecular sampling and analyses, and Camila D. Ritter, Cristiane F. Marks and Tomas Hrbek for help with phylogenetic analyses and for reviewing this manuscript. Thanks got to Glenn H. Shepard and Erik Wild for helping with the English language. This research was supported by CNPq/FAPEAM/SISBIOTA (Rede BioPHAM) 563348/2010 to IPF and MNFS. This study is part of AFM’s Master’s thesis in the ecology graduate program of INPA, and was supported by a fellowship from CNPq. The authors declare no conflicts of interest.

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Authors and Affiliations

  1. Programa de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia – INPA, Manaus, AM, Brazil

    Arielli Fabrício Machado & Marcelo Augusto dos Santos Jr.

  2. Laboratório de Evolução e Genética Animal - LEGAL, Universidade Federal do Amazonas – UFAM, Manaus, AM, Brazil

    Mário Silva Nunes & Izeni Pires Farias

  3. Coordenação de Pesquisas em Biodiversidade/COBIO e Coleções Zoológicas, Instituto Nacional de Pesquisas da Amazônia – INPA, Manaus, AM, Brazil

    Maria Nazareth Ferreira da Silva & Marina Anciães

  4. Programa de Pós-Graduação em Genética, Conservação e Biologia Evolutiva, Instituto Nacional de Pesquisas da Amazônia – INPA, Manaus, AM, Brazil

    Cláudia Regina Silva

  5. Laboratório de Mamíferos, Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá - IEPA, Macapá, AP, Brazil

    Cláudia Regina Silva

  6. Phylogenetic and Functional Ecology Lab (LEFF), Av. Bento Gonçalves, 9500 – Building 43.113, Porto Alegre, RS, 91501-970, Brazil

    Arielli Fabrício Machado

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  1. Arielli Fabrício Machado
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  2. Mário Silva Nunes
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  3. Cláudia Regina Silva
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  4. Marcelo Augusto dos Santos Jr.
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  5. Izeni Pires Farias
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  6. Maria Nazareth Ferreira da Silva
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  7. Marina Anciães
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Correspondence to Arielli Fabrício Machado.

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S1.

Laboratory techniques used for amplification of mitochondrial cytochrome b gene sequence fragments. (DOCX 15 kb)

Table S2.

Occurrence records for Hylaeamys megacephalus used for producing the ecological niche model (ENM) for the entire species. ID = identification number. The records with identification number 66, 68, 69, 90, 92 102, 104, 113 and 114 were added for the ENM of the Southern Amazonian lineage (black dots in Fig. 1). (XLSX 16 kb)

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Machado, A.F., Nunes, M.S., Silva, C.R. et al. Integrating phylogeography and ecological niche modelling to test diversification hypotheses using a Neotropical rodent. Evol Ecol 33, 111–148 (2019). https://doi.org/10.1007/s10682-019-09968-1

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