When native meets exotic: Uncovering hybridization between Cuban and introduced mahogany using chloroplast and nuclear microsatellites
Abstract
The introduction of closely related species can threaten the genetic integrity of endemic taxa through hybridization and introgression. In Cuba, Swietenia macrophylla was widely planted in the 1970s for its fast growth and high-value timber, raising concerns about its potential genetic impact on the native S. mahagoni and the emergence of hybrids. This study investigates the genetic consequences of introducing S. macrophylla to Cuba by analysing 357 individuals from five populations, including two naturally regenerated S. mahagoni populations, a pure S. macrophylla remnant, and two mixed stands containing both species and morphologically intermediate forms. The two predominant cpDNA haplotypes were shared across all five populations, whereas one mixed stand exhibited the highest diversity, with nine chloroplast DNA haplotypes—suggesting that its establishment involved seeds from multiple sources. cpDNA markers didn't reveal clear species-level differentiation. In contrast, nuclear microsatellites indicated moderate genetic differentiation (mean FST= 0.15±0.02) and substantial within-population variability, with expected heterozygosity (He) ranging from 0.46 to 0.85. At the same time, S. mahagoni showed a higher number of alleles (Na = 12.4–13.3) and expected heterozygosity (He = 0.73–0.78) than the remnant S. macrophylla population (Na = 5.75; He = 0.59), likely reflecting the smaller size of the existing S. macrophylla plantation in Cuba. Based on discriminant analysis of principal components and STRUCTURE results, the two parental species were clearly separated into distinct genetic clusters, while putative hybrid individuals were mainly concentrated in the two mixed stands. Leaf morphological and molecular classifications were highly concordant in parental populations (≈91%), confirming the phenotypic identifiability of S. mahagoni and S. macrophylla. The estimated proportion of hybrids varied: STRUCTURE (7.8–15.1%), whereas NewHybrids (36.1–39.2%). These findings provide a genetic framework for conservation-oriented management of native tree species, which is a tool for implementing long-term genetic monitoring and consolidating certified germplasm banks to safeguard the native Cuban mahogany.
References
Alves R.M., Chaves S.F. da S., Gama M.A.P., Pedroza Neto J.L., Santos T.G. dos, 2020. Simultaneous selection of cupuassu tree and Brazilian mahogany genotypes in an agroforestry system in Pará state, Brazil. Acta Amazonica, 50, 183–191. https://doi.org/10.1590/1809-4392202000711.
An M., Deng M., Zheng S.S., Jiang X.L., Song Y.G., 2017. Introgression Threatens the Genetic Diversity of Quercus austrocochinchinensis (Fagaceae), an Endangered Oak: A Case Inferred by Molecular Markers. Frontiers in Plant Science, 8. https://doi.org/10.3389/fpls.2017.00229.
Anderson E.C. & Thompson E.A., 2002. A Model-Based Method for Identifying Species Hybrids Using Multilocus Genetic Data. Genetics, 160(3), 1217–1229. https://doi.org/10.1093/genetics/160.3.1217.
Anderson J.L., 2004. Nature’s Currency: The Atlantic Mahogany Trade and the Commodification of Nature in the Eighteenth Century. Early American Studies, 2(1), 47–80.
André T., Lemes M.R., Grogan J., Gribel R., 2008. Post-logging loss of genetic diversity in a mahogany (Swietenia macrophylla King, Meliaceae) population in Brazilian Amazonia. Forest Ecology and Management, 255(2), 340–345. https://doi.org/10.1016/j.foreco.2007.09.055.
Andrianoelina O., Favreau B., Ramamonjisoa L., Bouvet, J.M., 2009. Small effect of fragmentation on the genetic diversity of Dalbergia monticola, an endangered tree species of the eastern forest of Madagascar, detected by chloroplast and nuclear microsatellites. Annals of Botany, 104(6), 1231–1242. https://doi.org/10.1093/aob/mcp231.
Bakewell-Stone P., 2023. Swietenia macrophylla (big leaved mahogany). CABI Compendium, CABI Compendium, 52155. https://doi.org/10.1079/cabicompendium.52155.
Bandelt H.J., Forster P., Röhl, A., 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036.
Barbosa Filho J., Carvalho M.A.D., Oliveira L.S.de, Konzen E.R., Campos W.F., Brondani G.E., 2016. Propagation of Khaya anthotheca: interspecific grafting with Swietenia macrophylla and air layering. CERNE, 22, 475–484. https://doi.org/10.1590/01047760201622042232.
Burge D.O., Parker V.T., Mulligan M., Sork V.L., 2019. Influence of a climatic gradient on genetic exchange between two oak species. American Journal of Botany, 106(6), 864–878. https://doi.org/10.1002/ajb2.1315.
Carlsson J., 2008. Effects of Microsatellite Null Alleles on Assignment Testing. Journal of Heredity, 99(6), 616–623. https://doi.org/10.1093/jhered/esn048.
Cavers S., Walker K., Boshier D., Rymer P., Harris S., Cordero J., Caron H., Scotti I., Scotti-Santaigne C., Petit R., Vendramin G., Buonamici A., Sebastiani F., Lemes M., Gribel R., Dick C., Navarro C., Finegan B., Cascante C., … Degen B., 2007. Developing best practice for seed sourcing of planted and natural regeneration in the neotropics. [Publication - Report]. NERC/Centre for Ecology & Hydrology. https://nora.nerc.ac.uk/id/eprint/4123/.
Céspedes M., Gutierrez M.V., Holbrook N.M., Rocha O., 2003. Restoration of genetic diversity in the dry forest tree Swietenia macrophylla (Meliaceae) after pasture abandonment in Costa Rica. Molecular Ecology, 12(12), 3201–3212. https://doi.org/10.1046/j.1365-294X.2003.01986.x.
Chinchilla O., Corea E., Meza V., Chinchilla O., Corea E., Meza V., 2020. Mejora genética y costos iniciales asociados al manejo de plantaciones clonales de Swietenia macrophylla en la región noreste de Costa Rica. Revista de Ciencias Ambientales, 54(2), 180–189. https://doi.org/10.15359/rca.54-2.10.
CITES., 2002. Convention on International Trade in Endangered Species of Wild Fauna and Flora, Appendix II. < www.cites. org/resources/species.html>.
Coca L.I.R., Ciocîrlan E., Boggiano A.G.T., Fernández L.A.D., Évora J.F.L., Codrean C., Curtu, A.L., 2024. Leaf-based characterization of intermediate forms between Cuban and Honduran mahogany. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(1), 13731–13731. https://doi.org/10.15835/nbha52113731.
Curtu A.L., Gailing O., Finkeldey R., 2007. Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evolutionary Biology, 7(1), Article 1. https://doi.org/10.1186/1471-2148-7-218.
Doyle J.J., Doyle J.L., 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. PHYTOCHEMICAL BULLETIN.
Eliades N.G.H., Papageorgiou A.C., Fady B., Gailing O., Leinemann L., Finkeldey R., 2019. An approach to genetic resources conservation of peripheral isolated plant populations: The case of an island narrow endemic species. Biodiversity and Conservation, 28(11), 3005–3035. https://doi.org/10.1007/s10531-019-01812-w.
Ennos R., 1994. Estimating the relative rates of pollen and seed migration among plant populations. Heredity, 72(3), 250-259, https://doi.org/10.1038/hdy.1994.35.
Evanno G., Regnaut S., Goudet, J. 2005. Detecting the number of clusters of individuals using the software structure: A simulation study. Molecular Ecology, 14(8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x.
FAO., 2000. Mahogany in the Amazon: Ecology and Management. FAO Forestry Paper No. 97. http://www.fao.org/4/XII/0553-B1.htm.
Frankham R., 2005. Genetics and extinction. Biological Conservation, 126(2), 131–140. https://doi.org/10.1016/j.biocon.2005.05.002.
Garza-López M., Ortega-Rodríguez J.M., Zamudio-Sánchez F.J., López-Toledo J. F., Domínguez-Álvarez F.A., Sáenz-Romero C., 2016. Calakmul como refugio de Swietenia macrophylla KING ante el cambio climático. Botanical Sciences, 94(1), 43–50. https://doi.org/10.17129/botsci.500.
Goldstein D.B., Ruiz Linares A., Cavalli-Sforza L.L., Feldman M.W., 1995. An evaluation of genetic distances for use with microsatellite loci. Genetics, 139(1), 463–471. https://doi.org/10.1093/genetics/139.1.463.
Hammer O., Harper D.A.T., Ryan, P.D., 2001. PAST: Paleontological statistics software package for education and data analysis. Paleontologia Electronica, 4. https://cir.nii.ac.jp/crid/1573950401102233088.
Hamrick J.L., Godt M.J.W., Sherman-Broyles S.L., 1992. Factors influencing levels of genetic diversity in woody plant species. New Forests, 6(1), 95–124. https://doi.org/10.1007/BF001206s41.
Hardy O.J., 2003. Estimation of pairwise relatedness between individuals and characterization of isolation-by-distance processes using dominant genetic markers. Molecular Ecology, 12(6), 1577–1588. https://doi.org/10.1046/j.1365-294X.2003.01835.x.
Hensen I. & Oberprieler C., 2005. Effects of population size on genetic diversity and seed production in the rare Dictamnus albus (Rutaceae) in central Germany. Conservation Genetics, 6(1), 63–73. https://doi.org/10.1007/s10592-004-7745-6.
Höltken A.M., Schröder H., Wischnewski N., Degen B., Magel E., Fladung, M., 2012. Development of DNA-based methods to identify CITES-protected timber species: A case study in the Meliaceae family. 66(1), 97–104. https://doi.org/10.1515/HF.2011.142.
Jombart T., Devillard S., Balloux, F., 2010. Discriminant analysis of principal components: A new method for the analysis of genetically structured populations. BMC Genetics, 11(1), 94. https://doi.org/10.1186/1471-2156-11-94.
Jost L., 2008. GST and its relatives do not measure differentiation. Molecular Ecology, 17(18), 4015–4026. https://doi.org/10.1111/j.1365-294X.2008.03887.x
Kopelman N.M., Mayzel J., Jakobsson M., Rosenberg N.A., Mayrose, I., 2015. Clumpak: A program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources, 15(5), 1179–1191. https://doi.org/10.1111/1755-0998.12387.
Lamb D., 2011. Regreening the Bare Hills (Vol. 8). Springer Netherlands. https://doi.org/10.1007/978-90-481-9870-2.
Lemes M.R., Brondani R.P.V., Grattapaglia D., 2002. Multiplexed Systems of Microsatellite Markers for Genetic Analysis of Mahogany, Swietenia macrophylla King (Meliaceae), a Threatened Neotropical Timber Species. Journal of Heredity, 93(4), 287–290. https://doi.org/10.1093/jhered/93.4.287.
Lemes M.R., Dick C.W., Navarro C., Lowe A.J., Cavers S., Gribel R., 2010. Chloroplast DNA Microsatellites Reveal Contrasting Phylogeographic Structure in Mahogany (Swietenia macrophylla King, Meliaceae) from Amazonia and Central America. Tropical Plant Biology, 3(1), 40–49. https://doi.org/10.1007/s12042-010-9042-5.
Lemes M.R., Esashika T., Gaoue O.G., 2011. Microsatellites for mahoganies: Twelve new loci for Swietenia macrophylla and its high transferability to Khaya senegalensis. American Journal of Botany, 98(8), e207–e209. https://doi.org/10.3732/ajb.1100074
Lemes M.R., Gribel R., Proctor J., Grattapaglia D., 2003. Population genetic structure of mahogany (Swietenia macrophylla King, Meliaceae) across the Brazilian Amazon, based on variation at microsatellite loci: Implications for conservation. Molecular Ecology, 12(11), 2875–2883. https://doi.org/10.1046/j.1365-294X.2003.01950.x.
Li Y., Liu J., 2018. StructureSelector: A web‐based software to select and visualize the optimal number of clusters using multiple methods. Molecular Ecology Resources, 18(1), 176–177. https://doi.org/10.1111/1755-0998.12719.
Limongi Andrade R., Pico-Mendoza J., Morillo E., Buitrón J., Meneses S., Navarrete B., Pinoargote M., Carrasco B., 2022. Molecular characterization of mahogany tree (Swietenia macrophylla King, Meliaceae) in the remnant natural forest of Ecuador. Neotropical Biodiversity, 8(1), 222–228. https://doi.org/10.1080/23766808.2022.2080334.
López-Caamal A., Tovar-Sánchez E., 2014. Genetic, morphological, and chemical patterns of plant hybridization. Revista Chilena de Historia Natural, 87(1), 16. https://doi.org/10.1186/s40693-014-0016-0.
Lowe A.J., Jourde B., Breyne P., Colpaert N., Navarro C., Wilson J., Cavers S., 2003. Fine-scale genetic structure and gene flow within Costa Rican populations of mahogany (Swietenia macrophylla). Heredity, 90(3), Article 3. https://doi.org/10.1038/sj.hdy.6800247.
Mantel N., 1967. The Detection of Disease Clustering and a Generalized Regression Approach. Cancer Research, 27(2_Part_1), 209–220.
Navarro-Martínez A., Ellis E.A., Hernández-Gómez I., Romero-Montero J.A., Sánchez-Sánchez O., 2018. Distribution and Abundance of Big-Leaf Mahogany (Swietenia macrophylla) on the Yucatan Peninsula, Mexico. Tropical Conservation Science, 11, 1940082918766875. https://doi.org/10.1177/1940082918766875.
Nei M., 1987. Molecular evolutionary genetics. Columbia Univ.
Novick R.R., Dick C.w., Lemes M.R., Navarro C., Caccone A., Bermingham E., 2003. Genetic structure of Mesoamerican populations of Big-leaf mahogany (Swietenia macrophylla) inferred from microsatellite analysis. Molecular Ecology, 12(11), 2885–2893. https://doi.org/10.1046/j.1365-294X.2003.01951.x
Pajuelo Romero A.H., 2021. Caracterización molecular de seis poblaciones de Caoba (Swietenia macrophylla King) en el Perú. http://repositorio.lamolina.edu.pe/handle/20.500.12996/4772.
Peakall R. & Smouse P.E., 2006. Genalex 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x.
Petit J.R., Duminil J., Fineschi S., Hampe A., Salvini D., Ven-dramin G.G., 2005. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology 14(3), 689-701.
Pfeilsticker T.R., Jones R.C., Steane D.A., Harrison P.A., Vaillancourt R.E., Potts B.M., 2022. Expansion of the rare Eucalyptus risdonii under climate change through hybridization with a closely related species despite hybrid inferiority. Annals of Botany, 129(1), 1–14. https://doi.org/10.1093/aob/mcab103.
Pons O. & Petit R.J., 1996. Measuring and testing genetic differentiation with ordered Versus unordered alleles. Genetics, 144(3), 1237–1245.
Pritchard J.K., Stephens M., Donnelly P., 2000. Inference of Population Structure Using Multilocus Genotype Data. Genetics, 155(2), 945–959. https://doi.org/10.1093/genetics/155.2.945.
Quiala E., Barbón R., Mestanza S., La O M., Merlan G., Nuñez-Ramos J., Pérez N., Leiva M., Jiménez E., Daniels D., Noceda, C., 2022. Somatic embryogenesis and plant regeneration from leaf of the interspecific hybrid of mahogany (Swietenia macrophylla King × S. mahagoni (L.) Jacq.). Trees, 36(1), 167–178. https://doi.org/10.1007/s00468-021-02192-x.
Rajora O.P., Zinck, J.W.R., 2021. Genetic Diversity, Structure and Effective Population Size of Old-Growth vs. Second-Growth Populations of Keystone and Long-Lived Conifer, Eastern White Pine (Pinus strobus): Conservation Value and Climate Adaptation Potential. Frontiers in Genetics, 12, 650299. https://doi.org/10.3389/fgene.2021.650299.
Ramos-Ortiz S., Oyama K., Rodríguez-Correa H., González-Rodríguez A., 2015. Geographic structure of genetic and phenotypic variation in the hybrid zone between Quercus affinis and Q. laurina in Mexico. Plant Species Biology. https://doi.org/10.1111/1442-1984.12109.
Raymond M. & Rousset F., 1995. GENEPOP (Version 1.2): Population Genetics Software for Exact Tests and Ecumenicism. Journal of Heredity, 86(3), 248.
Rousset F., 2008. Genepop’007: A complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x.
RStudio., 2025. RStudio: Integrated Development Environment for R (Version 2025.05.0) [Computer software]. Posit Software, PBC. https://posit.co.
Sebbenn A.M., Degen B., Azevedo V.C.R., Silva M.B., de Lacerda A.E.B., Ciampi A.Y., Kanashiro M., Carneiro F.daS., Thompson I., Loveless M.D., 2008. Modelling the long-term impacts of selective logging on genetic diversity and demographic structure of four tropical tree species in the Amazon forest. Forest Ecology and Management, 254(2), 335–349. https://doi.org/10.1016/j.foreco.2007.08.009.
Sebbenn A.M., Licona J.C., Mostacedo B., Degen B., 2012. Gene flow in an overexploited population of Swietenia macrophylla King (Meliaceae) in the Bolivian Amazon. Silvae Genetica, 61(1–6), 212–220. https://doi.org/10.1515/sg-2012-0027.
Sexton G.J., Frere C.H., Kalinganire A., Uwamariya A., Lowe A.J., Godwin I.D., Prentis P.J., Dieters, M.J., 2015. Influence of putative forest refugia and biogeographic barriers on the level and distribution of genetic variation in an African savannah tree, Khaya senegalensis (Desr.) A. Juss. Tree Genetics & Genomes, 11(5), 103. https://doi.org/10.1007/s11295-015-0933-3.
Sheng Y., Zheng W., Pei K., 2005. Genetic Variation Within and Among Populations of a Dominant Desert Tree Haloxylon ammodendron (Amaranthaceae) in China. Annals of Botany, 96(2), 245–252. https://doi.org/10.1093/aob/mci171.
Slatkin M., 1995. A measure of population subdivision based on microsatellite allele frequencies. Genetics, 139(1), 457–462. https://doi.org/10.1093/genetics/139.1.457.
Smouse R.P.P., Peakall P., 2012. GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—An update. Bioinformatics, 28(19), 2537–2539.
Sobreiro M.B., Vieira L.D., Nunes R., Novaes E., Coissac E., Silva-Junior O.B., Grattapaglia D., Collevatti R.G., 2020. Chloroplast genome assembly of Handroanthus impetiginosus: Comparative analysis and molecular evolution in Bignoniaceae. Planta, 252(5), 91. https://doi.org/10.1007/s00425-020-03498-9
Thompson K.M., Culley T.M., Zumberger A.M., Lentz D.L. 2015. Genetic variation and structure in the neotropical tree, Manilkara zapota (L) P. Royen (Sapotaceae) used by the ancient Maya. Tree Genetics & Genomes, 11(3), 40. https://doi.org/10.1007/s11295-015-0867-9.
Trujillo-Sierra J.E., Delgado-Valerio P., Ramírez-Morillo I., Rebolledo-Camacho V., Pérez-Nasser N., 2013. Variación genética en poblaciones mexicanas de Swietenia macrophylla KING, una especie tropical en expansión geográfica reciente. Botanical Sciences, 91(3), 307–317. http://www.scielo.org.mx/scielo.php?script=sci_abstract&pid=S2007-42982013000300006&lng=es&nrm=iso&tlng=es.
Vähä J.P. & Primmer C.R., 2006. Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Molecular Ecology, 15(1), 63–72. https://doi.org/10.1111/j.1365-294X.2005.02773.x.
Van Oosterhout C., Hutchinson W.F., Wills D.P.M., Shipley P., 2004. micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4(3), 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x.
Weir B.S. & Cockerham C.C., 1984. Estimating F-Statistics for the Analysis of Population Structure. Evolution, 38(6), 1358–1370. https://doi.org/10.2307/2408641.
Weising K. & Gardner R.C., 1999. A set of conserved PCR primers for the analysis of simple sequence repeat polymorphisms in chloroplast genomes of dicotyledonous angiosperms. Genome, 42(1), 9–19.
Downloads
Published
Issue
Section
License
All the papers published in Annals of Forest Research are available under an open access policy (Gratis Gold Open Access Licence), which guaranty the free (of taxes) and unlimited access, for anyone, to entire content of the all published articles. The users are free to "read, copy, distribute, print, search or refers to the full text of these articles", as long they mention the source.
The other materials (texts, images, graphical elements presented on the Website) are protected by copyright.
The journal exerts a permanent quality check, based on an established protocol for publishing the manuscripts. The potential article to be published are evaluated (peer-review) by members of the Editorial Board or other collaborators with competences on the paper topics. The publishing of manuscript is free of charge, all the costs being supported by Forest Research and Management Institute.
More details about Open Access:
Wikipedia: http://en.wikipedia.org/wiki/Open_access
