Abstract
Chaco is the largest remaining continuous tropical dry forest on the American continent and has one of the highest deforestation rates in the world. Copernicia alba Morong ex Morong & Britton is a typical species of Chaco forests and has been subjected to predatory extraction in its areas of occurrence. This study aims to assess the diversity and genetic structure of C. alba populations in the Brazilian Chaco region. By employing single-nucleotide polymorphism (SNP) markers, this research seeks to generate insights to guide effective management and conservation strategies for this palm tree. To obtain the SNPs, genomic libraries were developed using the genotyping-by-sequencing (GBS) approach. Populations showed considerable levels of genetic diversity (HE). The inbreeding coefficient (f) was negative for all populations, indicating an excess of heterozygotes. Additionally, clear signs of genetic flow were observed, indicating low to moderate genetic differentiation between populations. We detected 65 outlier SNPs associated mainly with general metabolic processes. Despite these results, conservation efforts should be adopted to avoid the loss of genetic variation. Conservation in situ or ex situ is pointed out as an important strategy for the preservation of C. alba populations, prioritizing sampling throughout the distribution area. The information obtained in this study will contribute to the conservation of genetic diversity, increasing the chances of the natural populations of C. alba persisting over time.
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Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Alves FM, Sartori ÂLB, Zucchi MI, Azevedo-Tozzi AMG, Tambarussi EV, Alves-Pereira A, de Souza AP (2018) Genetic structure of two Prosopis species in Chaco areas: A lack of allelic diversity diagnosis and insights into the allelic conservation of the affected species. Ecol Evol 8:6558–6574. https://doi.org/10.1002/ece3.4137
Alves-Pereira A, Novello M, Dequigiovanni G, Pinheiro JB, Brancalion PH, Veasey EA, Clement CR, Souza AP, Zucchi MI (2019) Genomic diversity of three Brazilian native food crops based on double-digest restriction site-associated DNA sequencing. Tropical Plant Biology 12(4):268–281. https://doi.org/10.1007/s12042-019-09229-z
Arrúa RD, Negrelle RRB (2014) Estructura poblacional, regeneración y producción potencial de cera de Copernicia alba Morong ex Morong & Britton en tres sitios de la región del Chaco, Paraguay. Iheringia, Série Botânica 69(2):277–284
Baldoni AB, Teodoro LPR, Teodoro PE, Tonini H, Tardin FD, Botin AA, Hoogerheide ESS, Botelho SDCC, Lulu J, Farias-Neto AL et al (2020) Genetic diversity of brazil nut tree (Bertholletia excelsa bonpl.) in southern Brazilian Amazon. For Ecol Manag 458:117795. https://doi.org/10.1016/j.foreco.2019.117795
Barbosa S, Mestre F, White TA, Paupério J, Alves PC, Searle JB (2018) Integrative approaches to guide conservation decisions: using genomics to define conservation units and functional corridors. Mol Ecol 27:3452–3465. https://doi.org/10.1111/mec.14806
Barrett RDH, Hoekstra HE (2011) Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12:767–780. https://doi.org/10.1038/nrg3015
Basualdo M, Huykman N, Volante JN, Paruelo JM, Piñeiro G (2018) Lost forever? Ecosystem functional changes occurring after agricultural abandonment and forest recovery in the semiarid Chaco forests. Sci Total Environ 650:1537–1546. https://doi.org/10.1016/j.scitotenv.2018.09.001
Baumann M, Israel C, Piquer-Rodríguez M, Gavier-Pizarro G, Volante JN, Kuemmerle T (2017) Deforestation and cattle expansion in the Paraguayan Chaco 1987–2012. Reg Environ Change 17:1179–1191. https://doi.org/10.1007/s10113-017-1109-5
Brito FA, Zucchi MI, Pinheiro JB, Arrigoni-Blank MF, Dequigiovanni G, Grando C, Batista CE, Alves-Pereira A, Blank AF (2021) Low diversity in the native populations of Croton tetradenius Baill. when using SNP markers: a future crop with an insecticidal activity. Resour Crop Evol 68:3145–3159. https://doi.org/10.1007/s10722-021-01176-7
Bullock JM, Bonte D, Pufal G, da Silva CC, Chapman DS, Garcı´a C, Garcı´a D, Matthysen E, Mar Delgado M (2018) Human-mediated dispersal and the rewiring of spatial networks. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2018.09.008
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140
Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. G3 (Bethesda) 1(3):171–182.
Chase MW, Hills HG (1991) Silica gel: an ideal material for field preservation of samples for DNA studies. Taxon 40:215–220
Chung MY, Son S, Herrando-Moraira S, Tang CQ, Maki M, Kim YD, Lo´pez-Pujol J, Hamrick JL, Chung MG (2020) Incorporating differences between genetic diversity of trees and herbaceous plants in conservation strategies. Conserv Biol 34:1142–1151. https://doi.org/10.1111/cobi.13467
Cisz ME (2011) The spatial distribution of Copernicia alba (Morong) in the district of Bahía Negra, Paraguay. M.S. thesis, Michigan Technological University, Houghton
Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing with the species-population continuum in the age of genomics. Front Ecol Evol 6:65. https://doi.org/10.3389/fevo.2018.00165
Díaz BG, Zucchi MI, Alves-Pereira A, Almeida CP, Moraes ACL, Vianna AS, Azevedo-Filho J, Colombo CA (2021) Genome-wide SNP analysis to assess the genetic population structure and diversity of Acrocomia species. PLoS ONE 16(7):e0241025. https://doi.org/10.1371/journal.pone.0241025
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bull 12:11–15
Fava WS, Gomes VGN, Lorenz AP, Paggi GM (2020) Cross-amplification of microsatellite loci in the cacti species from Brazilian Chaco. Mol Biol Rep 47:1535–1542. https://doi.org/10.1007/s11033-019-05064-3
Flanagan SP, Jones AG (2017) Constraints on the FST-heterozygosity outlier approach. J Hered 108(5):561–573. https://doi.org/10.1093/jhered/esx048
Garcia-Jacas N, Requena J, Massó S, Vilatersana R, Blanche C, López-Pujol J (2021) Genetic diversity and structure of the narrow endemic Seseli farrenyi (Apiaceae): implications for translocation. PeerJ 9:e10521. https://doi.org/10.7717/peerj.10521
Gene Ontology Consortium (2019) The gene ontology resource: 20 years and still GOing strong. Nucleic Acids Res 47:D330–D338. https://doi.org/10.1093/nar/gky1055
Gladfelter HJ, Yadav LK, Merkle SA, Wilde HD (2020) Genetic diversity and population structure analysis of Franklinia alatamaha, a tree species existing only in cultivation. Tree Genet Genomes 16(4):1–9. https://doi.org/10.1007/s11295-020-01455-x
González AV, Gómez-Silva V, Ramírez MJ, Fontúrbel FE (2020) Meta-analysis of the differential effects of habitat fragmentation and degradation on plant genetic diversity. Conserv Biol 34(3):711–720. https://doi.org/10.1111/cobi.13422
Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High- through-put functional annotation and data mining with the Blsat2Go suite. Nucleic Acids Res 36(10):3420–3435. https://doi.org/10.1093/nar/gkn176
Hartvig I, So T, Changtragoon S, Tran HT, Bouamanivong S, Ogden R, Seen H, Vieira FG, Turner F, Talbot R, Theilade I, Nielsen LR, Kjær ED (2020) Conservation genetics of the critically endangered Siamese rosewood (Dalbergia cochinchinensis): recommendations for management and sustainable use. Conserv Genet 21(4):677–692. https://doi.org/10.1007/s10592-020-01279-1
Hoban S, Kelley JL, Lotterhos KE, Antolin MF, Bradburd G, Lowry DB, Poss ML, Reed LK, Storfer A, Whitlock MC (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188(4):379–397. https://doi.org/10.1086/688018
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071
Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94
Kamvar ZN, Tabima JF, Grunwald NJ (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2:e281
Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation of population genetics parameters and their associated errors. Methods Ecol Evol 4(8):782–878
Kireta D, Christmas MJ, Lowe AJ, Breed MF (2019) Disentangling the evolutionary history of three related shrub species using genome-wide molecular markers. Conserv Genet 20:1101–1112. https://doi.org/10.1007/s10592-019-01197-x
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Lanes ECM, Motoike SY, Kuki KN, Resende MDV, Caixeta ET (2016) Mating system and genetic composition of the macaw palm (Acrocomia aculeata): implications for breeding and genetic conservation programs. J Hered 107:527–536. https://doi.org/10.1093/jhered/esw038
Laviola BG, Santos A, Rodrigues EV, Teodoro LPR, Teodoro PE, Rosado TB, Guimarães CG, Conceição LDHCS (2021) Structure and genetic diversity of macauba [Acrocomia aculeata (Jacq.) Lodd. ex Mart.] approached by SNP markers to assist breeding strategies. Genet Resour Crop Evol 1–13. https://doi.org/10.1007/s10722-021-01295-1
LeBlanc NM, Gahagan BI, Andrews SN, Avery TS, Puncher GN, Reading BJ, Buhariwalla CF, Curry RA, Whiteley AR, Pavey SA (2020) Genomic population structure of striped bass (Morone saxatilis) from the Gulf of St. Lawrence to Cape Fear River. Evol Appl 13:1468–1486. https://doi.org/10.1111/eva.12990
Li YL, Xue DX, Zhang BD, Liu JX (2019) Population genomic signatures of genetic structure and environmental selection in the catadromous roughskin sculpin Trachidermus fasciatus. Genome Biol Evol 11:1751–1764. https://doi.org/10.1093/gbe/evz118
Luu K, Bazin E, Blum MG (2017) Pcadapt: an R package to perform genome scans for selection based on principal component analysis. Mol Ecol Res 17:67–77. https://doi.org/10.1111/1755-0998.12592
Miller JM, Cullingham CI, Peery RM (2020) The infuence of a priori grouping on inference of genetic clusters: simulation study and literature review of the DAPC method. Heredity. https://doi.org/10.1038/s41437-020-0348-2
Negrelle RRB, Degen-Naumannn RL (2012) Copernicia alba Morong ex Morong & Britton: aspectos botânicos, ecológicos, etnobotânicos e agronômicos. Visão Acadêmica 13(2):60–71
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89(3):583–590. https://doi.org/10.1093/genetics/89.3.583
Nielsen ES, Beger M, Henriques R, von der Heyden S (2020) A comparison of genetic and genomic approaches to represent evolutionary potential in conservation planning. Biol Conserv 251:108770. https://doi.org/10.1016/j.biocon.2020.108770
Novello M, Viana JPG, Alves-Pereira A, Silvestre EA, Nunes HF, Pinheiro JB, Brancalion PHS, Zucchi MI (2018) Genetic conservation of a threatened Neotropical palm through community management of fruits in agroforest and second-growth forests. Forest Ecol Manag 407:200–209. https://doi.org/10.1016/j.foreco.2017.06.059
Ottewell KM, Bickerton DC, Byrne M, Lowe AJ (2016) Bridging the gap: a genetic assessment framework for population-level threatened plant conservation prioritization and decision-making. Divers Distrib 22:174–188. https://doi.org/10.1111/ddi.12387
Oyundelger K, Herklotz V, Harpke D, Oyuntsetseg B, Wesche K, Ritz CM (2021) Contrasting effects of local environment and grazing pressure on the genetic diversity and structure of Artemisia frigida. Conserv Gene 1–16. https://doi.org/10.1007/s10592-021-01375-w
Paquette SR (2012) Useful functions for (batch) file conversion and data resampling in microsatellite datasets. https://cran.r-project.org/package=PopGenKit
Poland JA, Brown PJ, Sorrells ME, Jannink J-L (2012) Development of high-density genetic maps for barley and wheat using a novel two-enzyme genotyping-by-sequencing approach. PloS one 7(2):e32253. pmid:22389690. https://doi.org/10.1371/journal.pone.0032253
Porth I, El-Kassaby YA (2014) Assessment of the genetic diversity in forest tree populations using molecular markers. Diversity 6:283–295. https://doi.org/10.3390/d6020283
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical computing. R Foundation for Statistical Computing, Vienna.
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Sammartino LEK, Aranguren MI, Reboredo MM (2010) Chemical and mechanical characterization of two south-American plant fibers for polymer reinforcement: caranday palm and phormium. J Appl Polym Sci 115(4):2236–2245
Silva AR, Resende-Moreira LC, Carvalho CS, Lanes ECM, Ortiz-Vera MP et al (2020) Range-wide neutral and adaptive genetic structure of an endemic herb from Amazonian Savannas. AoB Plants 12:plaa003. https://doi.org/10.1093/aobpla/plaa003
Teixeira JC, Huber CD (2021) The inflated significance of neutral genetic diversity in conservation genetics. PNAS 118:e2015096118. https://doi.org/10.1073/pnas.2015096118
Vallejos M, Volante JN, Mosciaro MJ, Vale LM, Bustamante ML, Paruelo JM (2015) Transformation dynamics of the natural cover in the Dry Chaco ecoregion: a plot level geo-database from 1976 to 2012. J Arid Environ 123:3–11. https://doi.org/10.1016/j.jaridenv.2014.11.009
Wadt LHO, Faustino CL, Staudhammer CL, Kainer KA, Evangelista JS (2018) Primary and secondary dispersal of Bertholletia excelsa: implications for sustainable harvests. For Ecol Manag 415:98–105. https://doi.org/10.1016/j.foreco.2018.02.014
Wright S (1943) Isolation by distance. Genetics 28:114–138
Funding
This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), process 431226/2018–0 and 311811/2019–1.
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M.F.C., F.A.V. and M.I.Z. conceived the study design. J.A.M.M., C.E.A.B. and M.F.C. performed the laboratory work of the research. A.A.P. and M.F.C. carried out the data analysis. M.F.C. wrote the first version of the manuscript. A.A.P., F.A.V. and M.I.Z. edited and revised the manuscript. All authors read and approved the final manuscript.
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Costa, M.F., Marroquín, J.A.M., de Araújo Batista, C.E. et al. Population Genomics and Conservation of Copernicia alba: a Non-Timber Palm of Economic Importance in the Brazilian Chaco. Plant Mol Biol Rep (2023). https://doi.org/10.1007/s11105-023-01419-0
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DOI: https://doi.org/10.1007/s11105-023-01419-0