Abstract
Adaptive genetic and neutral variations are essential for maintaining population viability in changing environmental conditions. Habitat loss and fragmentation can be reflected in the patterns of genetic variation in the populations. White-lipped peccaries (WLPs, Tayassu pecari) are wide-ranging Neotropical ungulates with important ecological roles in the ecosystem suffering local extinctions worldwide. Here, we used a RAD-seq protocol to genotype 192 individuals. After filtering, we identified sets of SNP markers (ranging from 147 to 151,792 SNPs) to assess the genetic diversity and population structure of WLPs from Pantanal, Cerrado, and Atlantic Forest in Brazil. We found signals of loss (θw < θπ) and lower genetic diversity (allelic richness, nucleotide diversity, and observed and expected heterozygosities) in the Central Cerrado and Atlantic Forest populations. Principal Component Analysis (PCA) and admixture analyses (NGSAdmix) using genome-wide and neutral SNP data sets showed three major genetic clusters according to the biomes. Multiple matrix regression with randomization (MMRR) analysis found an isolation-by-distance pattern explaining the neutral genetic differentiation. We used Latent Factor Mixed Models (LFMM) and Redundancy Analysis (RDA) to identify candidate SNPs involved in different biological processes, such as metabolism and immune and neuronal responses, mainly associated with temperature and precipitation variables. We found an adaptive population genetic structure, suggesting three adaptive units with significant patterns of isolation-by-distance and isolation-by-environment. Our results highlighted the importance of conservation strategies for maintaining the genetic diversity of WLP populations. Furthermore, conservation plans and translocation programs should preserve and consider the adaptive variation.
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(Source: http://mapbiomas.org, Mapbiomas collection 4.1, 2016). Non-forest natural formations: wetland, grassland, and other non-forest natural formations
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Data availability
Raw sequence data are available at NCBI (SRA accession: Bioproject PRJNA1062824). Other data, such as genotypes and environmental data, are available at Figshare (https://doi.org/10.6084/m9.figshare.25438330).
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Acknowledgements
We want to thank Tatiana P. Freitas, Ezidio Arruda, Celso Vicente, Maria do Carmo A. Santos, Paulino A. O. Santos, Renata R. Rocha, Cícero Sebastião, Cyntia K. Kashivakura, Maria Luisa S. P. Jorge, Donald P. Eaton, and Julia Oshima for their assistance capturing, collaring, collecting biological samples and monitoring white-lipped peccaries. We thank the support from Earthwatch Institute and Global Ecotours volunteers, Biofaces, WCS Brazil, and the landowners from the Upper Paraguay Basin in the southern Pantanal that allowed us to study on their property. We want to thank Anna Carolina R. C. Martin, Nataly F. Vieira, and Danilo A. Rufo for their help with the DNA extraction from the samples and members of Miller’s Lab – UC Davis for their assistance with the bioinformatic analyses. We thank Instituto Florestal de São Paulo (IF) and Instituto de Pesquisas Ecológicas (IPE) for the logistical support. We are also grateful to two anonymous reviewers for their comments on earlier versions of this manuscript.
Funding
This work was funded by FAPESP (Grant number 2015/20133-0), CNPq (Grant number 479760/2012-8), Fundação Manoel Barros, Pantanal and Cerrado ranchers, and Earthwatch Institute volunteers. Author F.G.M. has received support from CAPES (Grant numbers PhD – Funding code 001 and PDSE – 88881.134372/2016-01).
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F.G.M. and C.B. designed the study. M.R.M. contributed to study design, advised, and assisted with bioinformatics. A.K., A.F.D.N., M.S.N., A.T.A.J., L.S., M.M.F., and N.M.T. performed the sample collection. F.G.M. and S.O’R. performed the laboratory work. M.J. and W.H. assisted with bioinformatic analyses. G.S., L.R.T., and M.S.P.B. helped to obtain the environmental data. F.G.M. performed the data analyses and wrote the manuscript. C.B. helped write the manuscript and advised and assisted with the laboratory work and genetic analyses. M.J., W.H., G.S., L.R.T., M.S.P.B., A.K., A.F.D.N., M.M.F., and C.B. revised and edited the manuscript.
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de Góes Maciel, F., O’Rourke, S., Jones, M. et al. Loss of genetic diversity and isolation by distance and by environment in populations of a keystone ungulate species. Conserv Genet (2024). https://doi.org/10.1007/s10592-024-01614-w
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DOI: https://doi.org/10.1007/s10592-024-01614-w