Abstract
Spondias tuberosa occurs in the Caatinga domain (seasonally dry tropical forest biome) of north-eastern Brazil, a large biome with ecogeographic regions that may have modelled the population structure of the species. Here we studied the phylogeographic pattern of S. tuberosa using sequences of the accD-psaI plastid region and six SSR markers in individuals distributed across 20 localities. The results for accD-psaI demonstrated nine haplotypes: some of which were exclusive to Caatinga ecoregions, whereas others were found in all localities. Spatial analysis of molecular variance revealed two groups (Fct = 0.34, P < 0.0039) with 33.91% variation between them. The SSR analyses displayed 2–5 alleles at each locus, some of which were unique to certain localities. As in the accD-psaI region, the population structure obtained using SSR markers fell into two groups: (1) a large group containing the majority of the geographic region of Caatinga and (2) a small group near the Atlantic forest. We demonstrate the population structure of S. tuberosa, identifying the Caatinga as large, continuous refuge and the region near the interface between the Caatinga and the Atlantic forest as second refuge.
Similar content being viewed by others
References
Bruvo R, Michiels NK, D’souza TG, Schulenburg H (2004) A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Mol Ecol 13:2101–2106
Costa GC, Hampe A, Ledru MP, Martinez PA, Mazzochini GG, Shepard BD, Werneck FP, Moritz C, Carnaval AC (2017) Biome stability in South America over the last 30 kyr: inferences from long-term vegetation dynamics and habitat modelling. Glob Ecol Biogeogr 27:285–297
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:419
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581
Espíndola ACM, Almeida CCS, Carvalho NSG, Roza MLA (2004) Diâmetro do caule e método de enxertia na formação de mudas de umbuzeiro (Spondias tuberosa Arr. Cam.). Rev Bras Agrociência 10:371–372
Estoup A, Guillot G, Santos F (2007) Geneland: simulation and MCMC inference in landscape genetics. R package version 2.0.5. URL: http://cran.r-project.org/
Ferreira ME, Grattapaglia D (1998) Introdução ao uso de marcadores moleculares em análise genética. Embrapa, Brasília
Gonçalves-Oliveira RC, Wöhrmann T, Benko-Iseppon AM, Krapp F, Alves M, Wanderley MGL, Weising K (2017) Population genetic structure of the rock outcrop species Encholirium spectabile (Bromeliaceae): the role of pollination vs. seed dispersal and evolutionary implications. Am J Bot 104:868–878
Gruber B, Adamack A (2017) PopGenReport v3.0.0 https://github.com/green-striped-gecko/PopGenReport. A simple framework to analyse population and landscape genetic data
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Kamvar ZN, Tabima JF, Grünwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281. https://doi.org/10.7717/peerj.281
Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066
Leite YL, Costa LP, Loss AC, Rocha RG, Batalha-Filho H, Bastos AC, Quaresma VS, Fagundes V, Paresque R, Passamani M, Pardini R (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. PNAS 113:1008–1013
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lorenzi H (2008) Árvores Brasileiras: Manual de identificação e cultivo de plantas arbóreas do Brasil. Nova Odessa, São Paulo
Machado MC, Carvalho PCL, Berg CVD (2015) Domestication, hybridization, speciation, and the origins of an economically import ant tree crop of Spondias (anacardiaceae) from the Brazilian caatinga dry forest. Neodiversity 8:8–49
Manolopoulou I, Legarreta L, Emerson BC, Brooks S, Tavare S (2011) A Bayesian approach to phylogeographic clustering. Interface Focus 1(6):909–921
Mitchell JD, Daly DC (2015) A revision of Spondias L. (Anacardiaceae) in the Neotropics. PhytoKeys 55:1–92
Moro MF, Silva IA, Araújo FS, Lughadha EN, Meagher TC, Martins FR (2015) The role of edaphic environment and climate in structuring phylogenetic pattern in seasonally dry tropical plant communities. Journal Plos one 13:083–970
Paradis E, Jombart T, Schliep K, Potts A, Winter D (2017) Pegas v0.10 population and evolutionary genetics analysis system
Rambaut A, Drummond AJ (2009) Tracer version 1.5 [computer program] http://beast.bio.ed.ac.uk
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–269
Santos CAF (1997) Dispersão da variabilidade fenotípica do umbuzeiro no semi-árido brasileiro. Pesq Agrop Brasileira 32:923–930
Santos CAF, Oliveira VR (2008) Inter-relações genéticas entre espécies do gênero Spondias com base em marcadores AFLP. Rev Bras Frutic 30:731–735
Scarcelli N, Barnaud A, Eiserhardt W, Treier UA, Seveno M, d'Anfray A, Vigouroux Y, Pintaud J-C (2011) A set of 100 chloroplast DNA primer pairs to study population genetics and phylogeny in monocotyledons. PLoS One 6:e19954
Team RC (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III Cladogram estimation. Genetics 132:619–633
Vieira FDA, Lage Novaes RM, Fajardo CG, Dos Santos RM, Almeida HDS, De Carvalho D, Lovato MB (2015) Holocene southward expansion in seasonally dry tropical forests in South America: phylogeography of Ficus bonijesulapensis (Moraceae). Bot J Linn Soc 177:189–201
Acknowledgments
The authors acknowledge the Federal University of Alagoas for the laboratory and scientific support.
Funding
The authors thank the Fundação de Apoio à Pesquisa de Alagoas (FAPEAL) for funding this Project.
Author information
Authors and Affiliations
Contributions
E.B. and B.C. collected tissue and molecular data. C.A. analysed the data and led the writing. All authors conceived the ideas and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by A. Brunner
Data archiving statement
Haplotype sequence data for intergenic region have been submitted to GenBank: accession numbers MH370296-MH370344
Electronic supplementary material
Fig. S1
(A) position sites for SNPs and indels for the accD-psaI intergenic spacer. (B) Phylogenetic analysis using Bayesian analysis, with support inferred by posterior probability (here, represented in percentage). (PNG 175 kb)
Fig. S2
(A) Minimum-spanning network depicting the distribution of Spondias tuberosa multilocus microsatellites. (B) Principal component analysis (PCA) revealing a two-dimensional distribution of Spondias tuberosa genotypes. (PNG 2549 kb)
Fig. S3
The observed (red) and expected (blue) pairwise mismatch distribution of accD-psaI haplotypes evidencing past population expansion. (PNG 51 kb)
Table S1
(DOCX 14 kb)
Table S2
(DOCX 14 kb)
Rights and permissions
About this article
Cite this article
Balbino, E., Caetano, B. & Almeida, C. Phylogeographic structure of Spondias tuberosa Arruda Câmara (Anacardiaceae): seasonally dry tropical forest as a large and continuous refuge. Tree Genetics & Genomes 14, 67 (2018). https://doi.org/10.1007/s11295-018-1279-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11295-018-1279-4