Abstract
Eremanthus erythropappus (DC.) MacLeish, commonly known as candeia, is a threatened tree species that occurs in Seasonal Semideciduous Forests in Brazil. The tree is valued for the durability of its wood and essential oil production, from which the active agent (alpha-bisabolol) is used in pharmaceutical and cosmetic industries. Due to its high economic value, E. erythropappus has been exploited for several decades. Natural populations have been reduced, with the subsequent ecological and genetic negative impacts. We aimed to use a landscape genetics approach to identify if natural features influence the genetic diversity of E. erythropappus. In order to assess the genetic variability and provide information for the conservation of the species, genetics analyses were carried out for 200 individuals from ten natural populations of E. erythropappus. Nine ISSR primers produced 72 bands, of which 57 (79%) were polymorphic. Genetic diversity (\({H}_{E}\)) was 0.30 and gene flow was 1.4 migrants per population. The Bayesian clustering model indicated the occurrence of four genetically distinct populations (K = 4). Results of AMOVA showed high genetic differentiation between populations (30.8 %) and there was positive correlation between genetic and geographic distances (r = 0.632, P = 0.001). Based on a Mantel correlation and the genetic discontinuity among populations, we recommend the implementation of four operational units to support the conservation of this species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Almeida-Pereira CS, Muniz AVCDS, Alves RP, Feitosa-Alcantara RB, Arrigoni-Blank MDF, Carvalho SVÁ, Costa TS, White LAS, Pinto VDS, Sampaio TS, Blank AF (2017) Genetic diversity of native populations of Croton tetradenius Baill. using ISSR markers. Genet Mol Res 16(2):1–12. https://doi.org/10.4238/gmr16029602
Bhat KV (2002) Molecular data analysis. In: Proceedings of the short-term training course on molecular marker application in plant breeding. Molecular data Analysis, ICAR, New Delhi
Barreira S, Sebbenn AM, Scolforo JRS, Kageyama PY (2006) Diversidade genética em população natural de Eremanthus erythropappus (DC.) MacLeish como base para o manejo florestal. Sci For 71:119–130
Bezemer N, Krauss SL, Roberts DG, Hopper SD (2019) Conservation of old individual trees and small populations is integral to maintain species’ genetic diversity of a historically fragmented woody perennial. Mol Ecol 28(14):3339–3357. https://doi.org/10.1111/mec.15164
Bolliger J, Lander T, Balkenhol N (2014) Landscape genetics since 2003: status, challenges and future directions. Landsc Ecol 29:361–366. https://doi.org/10.1007/s10980-013-9982-x
Bowman J, Greenhorn JE, Marrotte RR, McKay MM, Morris KY, Prentice MB, Wehtje M (2016) On applications of landscape genetics. Conserv Genet 17:753–760. https://doi.org/10.1007/s10592-016-0834-5
Brandão MM, Vieira FA, Nazareno AG, Carvalho D (2015) Genetic diversity of neotropical tree Myrcia splendens (Myrtaceae) in a fragment-corridor system in the Atlantic rainforest. Flora (Jena) 216:35–41. https://doi.org/10.1016/j.flora.2015.07.006
Carvalho D, Barreira S, Moura MCO (2012) Genética, Manejo e Conservação. In: Scolforo JR, Oliveira AD, Davide AC (eds) O Manejo Sustentável da Candeia. O caminhar de uma nova experiência em Minas Gerais, 1rd edn. Editora UFLA, Lavras, pp 237–246
Carvalho MC, Gomide LR, Acerbi Júnior FW, Tng D (2019) Potential and future geographical distribution of Eremanthus erythropappus (DC.) MacLeish: a tree threatened by climate change. Floram 26(3):1–13. https://doi.org/10.1590/2179-8087.045518
Castilla AR, Pope N, Jaffé R, Jha S (2016) Elevation, not deforestation, promotes genetic differentiation in a pioneer tropical tree. PLoS ONE 11(6):1–22. https://doi.org/10.1371/journal.pone.0156694
Cavers S, Cottrell JE (2015) The basis of resilience in forest tree species and its use in adaptive forest management in Britain. Int J For Res 88(1):13–26. https://doi.org/10.1093/forestry/cpu027
Cordeiro EM, Macrini CM, Sujii PS, Schwarcz KD, Pinheiro JB, Rodrigues RR, Brancalion PHS, Zucchi MI (2019) Diversity, genetic structure, and population genomics of the tropical tree Centrolobium tomentosum in remnant and restored Atlantic forests. Conserv Genet 20(5):1073–1085. https://doi.org/10.1007/s10592-019-01195-z
Cruz CD (2001) Programa GENES versão Windows. Editora UFV, Viçosa
Diniz Filho JAF, Telles MPC (2002) Spatial autocorrelation analysis and the identification of operational units for conservation in continuous populations. Conserv Biol 16:924–935. https://doi.org/10.1046/j.1523-1739.2002.00295.x
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus Rockv 12:13–15
Duarte JF, Carvalho D, Vieira FA (2015) Genetic conservation of Ficus bonijesulapensis R.M. Castro in a dry forest on limestone outcrops. Biochem Syst Ecol 59:54–62. https://doi.org/10.1016/j.bse.2015.01.008
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Estopa RA, Sousa AM, Moura MCO, Botrel MCG, Mendonça EG, Carvalho D (2006) Diversidade genética em populações naturais de candeia (Eremanthus erythropappus (DC.) MacLeish). Sci For 70:97–106
Excoffier L, Laval G, Schneider S (2007) Arlequin: a software for population data analysis. Version 3.1. University of Geneva, Geneva. Accessed 10 Sept 2019
Finkeldey R, Ziehe M (2004) Genetic implications of silvicultural regimes. For Ecol Manag 197:231–244. https://doi.org/10.1016/j.foreco.2004.05.036
Freitas VLO, Lemos Filho JP, Lovato MB (2008) Contrasting genetic diversity and defferentiations of populations of two sucessional stages Iná a Neotropical pionner tree (Eremanthus erythropappus, Asteraceae). Genet Mol Res 7:388–398. https://doi.org/10.4238/vol7-2gmr429
Gamba D, Muchhala N (2020) Global patterns of population genetic differentiation in seed plants. Mol Ecol 29(18):3413–3428. https://doi.org/10.1111/mec.15575
Hamrick JL, Godt MJW, Sherman-Broyles SL (1992) Factors influencing levels of genetic diversity in woody plant species. In: Adams WT, Strauss SH, Copes DL, Griffin AR (eds) Population genetics of forest trees, vol 42. Springer, Dordrecht
Hanson T, Brunsfeld S, Finegan B, Waits L (2007) Conventional and genetic measures of seed dispersal for Dipteryx panamensis (Fabaceae) in continuous and fragmented Costa Rican rain forest. J Trop Ecol 23:635–642. https://doi.org/10.1017/S0266467407004488
Holderegger R, Buehler D, Gugerli F, Manel S (2010) Landscape genetics of plants. Trends Plant Sci 15:675–683. https://doi.org/10.1016/j.tplants.2010.09.002
Holsinger KE, Lewis PO (2007) Hickory: a package for analysis of population genetic data V1.1. Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs
Keller D, Holderegger R, van Strien MJ, Bolliger J (2015) How to make landscape genetics beneficial for conservation management? Conserv Genet 16:503–512. https://doi.org/10.1007/s10592-014-0684-y
Kidd DM, Ritchie MG (2006) Phylogeographic information systems: putting the geography into phylogeography. J Biogeogr 33:1851–1865. https://doi.org/10.1111/j.1365-2699.2006.01574.x
Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The paradox of forest fragmentation genetics. Conserv Biol 22:878–885. https://doi.org/10.1111/j.1523-1739.2008.00944.x
Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam
Loeuille B (2015) Eremanthus in lista de especies da flora do Brasil. Jardim Botânico do Rio de Janeiro. Accessed 19 Sept 2019
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Evol Syst 15:65–95. https://doi.org/10.1146/annurev.es.15.110184.000433
Loveless MD, Hamrick JL (1987) Distribuicion de la variacion em espécies de arboles tropicales. Rev Biol Trop 35:165–175
Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 28:614–621. https://doi.org/10.1016/j.tree.2013.05.012
Manel S, Schwartz MK, Luikart, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18(4):189–197. https://doi.org/10.1016/S0169-5347(03)00008-9
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190. https://doi.org/10.1353/hub.2004.0034
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Miller MP (1997) Tools for population genetic analyses (TFPGA): a Windows program for the analysis of allozyme and molecular population genetic data, version 1.3. Department of Biological Sciences, Northern Arizona University, Flagstaff
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:586–590
Nybom H, Bartish I (2000) Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect Plant Ecol 3:93–114. https://doi.org/10.1078/1433-8319-00006
Palkar RS, Sellappan K (2019) Genetic diversity between and within the natural populations of Garcinia indica (Thouars) Choisy: a high value medicinal plant from Northern Western Ghats of India using ISSR markers. J Appl Res Med Aroma 15:1–8. https://doi.org/10.1016/j.jarmap.2019.100219
Pearse DE, Crandall KA (2004) Beyond FST: analysis of population genetic data for conservation. Conserv Genet 5:585–602. https://doi.org/10.1007/s10592-003-1863-4
Pena DN, Moura EF, Rodrigues SM, Oliveira MSP, Sanches JP, Moura MF (2020) Molecular characterization of a germplasm bank of Platonia insignis Mart.: a fruit tree. Genet Resour Crop Evol 67(2):411–420. https://doi.org/10.1007/s10722-019-00855-w
Portela RM, Tambarussi EV, de Aguiar AV, Gandara FB, Peres FSB, Rosa JRBF (2020) Using a coalescent approach to assess gene flow and effective population size of Acrocomia aculeata (Jacq.) Lodd. Ex Mart. in the Brazilian Atlantic Forest. Tree Genet Genom 16(2):1–9. https://doi.org/10.1007/s11295-020-1426-6
Pritchard JK, Wen W (2012) Structure software version 2.3.4. Stanford University. Accessed 23 May 2019
Rao VR, Hodgkin T (2002) Genetic diversity and conservation and utilization of plant genetic resources. Plant Cell Tiss Org 68(1):1–19. https://doi.org/10.1023/A:1013359015812
Rico Y (2019) Landscape genetics of Mexican biodiversity: a review. Landscape 29:1–23. https://doi.org/10.15174/au.2019.1894
Rocha LF, do Carmo IEP, Póvoa JSR, Carvalho D (2020) Effects of climate changes on distribution of Eremanthus erythropappus and E. incanus (Asteraceae) in Brazil. J For Res 31(2):353–364. https://doi.org/10.1007/s11676-019-00968-z
Rohlf FJ (2000) Numerical taxonomy and multivariate analysis system version 2.11. Applied Biostatistic, New York
Roldan-Ruiz I, Dendauw JE, Van bockstaele E, Depicker A, Loose M (2000) AFLP markers reveal high polymorphic rates in ryegrasses (Lolium spp.). Mol Breed 6:125–126. https://doi.org/10.1023/A:1009680614564
Santos BA, Peres CA, Oliveira MA, Grillo A, Alves-Costa CP, Tabarelli M (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol Conserv 141:249–260. https://doi.org/10.1016/j.biocon.2007.09.018
Santos JC, Leal IR, Almeida-Cortez JS, Fernandes GW, Tabarelli M (2011) Caatinga: the scientific negligence experienced by a dry tropical forest. Trop Conserv Sci 4:276–286. https://doi.org/10.1177/194008291100400306
Silva-Junior V, Souza DG, Queiroz RT, Souza LG, Ribeiro EM, Santos BA (2018) Landscape urbanization threatens plant phylogenetic diversity in the Brazilian Atlantic Forest. Urban Ecosyst 21(4):625–634. https://doi.org/10.1007/s11252-018-0745-y
Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc 64:583–639. https://doi.org/10.1111/1467-9868.00353
Tian XY, Ye JW, Wang TM, Bao L, Wang HF (2020) Different processes shape the patterns of divergence in the nuclear and chloroplast genomes of a relict tree species in East Asia. Ecol Evol 10(10):4331–4342. https://doi.org/10.1002/ece3.6200
Vieira FA, Fajardo CG, Souza AM, Carvalho D (2010) Landscape e level and fine-scale genetic structure of the neotropical tree Protium spruceanum (Burceraceae). Int J For Res. https://doi.org/10.1155/2010/1209792010/120979
Vieira FA, Fajardo CG, Souza AM, Reis CAF, Carvalho D (2012) Fine-scale genetic dynamics of a dominant neotropical tree in the threatened Brazilian Atlantic Rainforest. Tree Genet Genom 8:1191–1201. https://doi.org/10.1007/s11295-012-0506-7
Wright S (1943) Isolation by distance. Genetics 28:114–138
Yeh FC, Yang RC, Boyle TBJ, Ye ZH, Mao JX (1997) POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Center University of Alberta, Edmonton
Zanella L, Folkard AM, Blackburn GA, Carvalho LM (2017) How well does random forest analysis model deforestation and forest fragmentation in the Brazilian Atlantic forest? Environ Ecol Stat 24(4):529–549. https://doi.org/10.1007/s10651-017-0389-8
Acknowledgements
We thank Dr. Evelyn R. Nimmo for the English proofreading of this manuscript. We would like to thank the Department of Forest Science (Departamento de Ciências Florestais), the Federal University of Lavras (Universidade Federal de Lavras). We are also thankful to the reviewers for their thoughtful efforts towards improving the manuscript.
Funding
Funding for this project and a Master’s scholarship were provided by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnologico-CNPq) and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for the Visiting Researcher Grant to Murilo Malveira Brandão (BPV). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES)-Finance Code 001.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by JARdP, LFR, MMB, FdAV, DdC. The first draft of the manuscript was written by JAR and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
de Pádua, J.A.R., Rocha, L.F., Brandão, M.M. et al. Title: priority areas for genetic conservation of Eremanthus erythropappus (DC.) MacLeish in Brazil. Genet Resour Crop Evol 68, 2483–2494 (2021). https://doi.org/10.1007/s10722-021-01144-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10722-021-01144-1