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Disentangling the contemporary and historical effects of landscape on the population genomic variation of two bird species restricted to the highland forest enclaves of northeastern Brazil


Investigating the impact of landscape features on patterns of genetic variation is crucial to understand spatially dependent evolutionary processes. Here, we assess the population genomic variation of two bird species (Conopophaga cearae and Sclerurus cearensis) through the Caatinga moist forest enclaves in northeastern Brazil. To infer the evolutionary dynamics of bird populations through the Late Quaternary, we used genome-wide polymorphism data obtained from double-digestion restriction-site-associated DNA sequencing (ddRADseq), and integrated population structure analyses, historical demography models, paleodistribution modeling, and landscape genetics analyses. We found the population differentiation among enclaves to be significantly related to the geographic distance and historical resistance across the rugged landscape. The climate changes at the end of the Pleistocene to the Holocene likely triggered synchronic population decline in all enclaves for both species. Our findings revealed that both geographic distance and historical connectivity through highlands are important factors that can explain the current patterns of genetic variation. Our results further suggest that levels of population differentiation and connectivity cannot be explained purely on the basis of contemporary environmental conditions. By combining historical demographic analyses and niche modeling predictions in a historical framework, we provide strong evidence that climate fluctuations of the Quaternary promoted population differentiation and a high degree of temporal synchrony among population size changes in both species.

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Fig. 1: Distribution of the genetic variation of Conopophaga cearae and Sclerurus cearensis from island-like forest enclaves of the Brazilian Atlantic Forest domain (green in the inset map of South America) within the Caatinga domain (beige in the inset map).
Fig. 2: Estimated effective migration surface (EEMS).
Fig. 3: Generalized dissimilarity fitted model for population differentiation (Dxy genomic distance) and significant landscape predictors.
Fig. 4: Historical demography model testing.
Fig. 5: Ecological niche models (ENMs) for Conopophaga cearae and Sclerurus cearensis across the Caatinga moist forest enclaves.

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The authors thank Caio Graco (UEFS) and Helder Araújo (UFPB) for providing some of the tissues used in this study, and Sidnei Santos, Rilquer Mascarenhas, and Lucas Passos for their help during the fieldwork. The authors are grateful to Pedro Andrade for helping with the demultiplexing of Illumina runs. The authors also thank Rilquer Mascarenhas for help with ecological niche modeling scripts; the editor and two anonymous reviewers for immensely improving this manuscript; and the National Laboratory for Scientific Computing (LNCC/MCTI, Brazil) for providing HPC resources for the SDumont supercomputer. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio license number 52235-1) and Secretaria do Meio Ambiente of the state of Bahia (SEMA/INEMA license number 11553) provided permits to collect the samples. This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 443249/2014-8, 303713/2015-1, 406968/2021-7), Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB JCB0026/2016), and the joint National Science Foundation, Fundação de Amparo à Pesquisa do Estado de São Paulo and NASA grant (Dimensions US-Biota-SP, FAPESP 2013/50297-0/NSF DOB 1343578). FS was supported by National Funds through FCT-Fundação para a Ciência e a Tecnologia under the project UIDB/50027/2020. HB-F and CYM also acknowledge the CNPq Research Productivity Fellowships (310673/2021-6 and 306204/2019-3, respectively). MC was supported by a research contract from the Fundação para a Ciência e Tecnologia (FCT; CEECINST/00014/2018/CP1512/CT0002).

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HB-F conceived the original idea. HB-F, MC, and FS designed the research. HB-F and MHBS conducted the fieldwork. SA performed the laboratory work. HB-F and SBB performed the analyses. HB-F wrote the manuscript with significant contributions from SBB and FS. All other authors contributed to the revision of the final version of the manuscript.

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Correspondence to Henrique Batalha-Filho.

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Associate editor: Lounès Chikhi.

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Batalha-Filho, H., Barreto, S.B., Silveira, M.H.B. et al. Disentangling the contemporary and historical effects of landscape on the population genomic variation of two bird species restricted to the highland forest enclaves of northeastern Brazil. Heredity 132, 77–88 (2024).

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