Tree Genetics & Genomes

, 14:73 | Cite as

Population genetics of Cedrela fissilis (Meliaceae) from an ecotone in central Brazil

  • J. M. Diaz-Soto
  • A. Huamán-Mera
  • L. O. OliveiraEmail author
Original Article
Part of the following topical collections:
  1. Population structure


Cedrela fissilis is an endangered timber species associated with seasonal forests throughout South America. We investigated a population of C. fissilis (PAN) located toward central Brazil to uncover insights on how an ecotone may have shaped the evolutionary history of this species at the local scale. PAN consisted of 18 mother trees and their 283 offspring (18 families), which were genotyped with ten microsatellite loci. We supplemented our dataset with equivalent microsatellite data from 175 specimens representing the east and west lineages of C. fissilis. An array of complementary methods assessed PAN for genetic diversity, population structure, and mating system. In PAN, the gene pool of the east lineage combined with a third (previously unidentified) lineage to form an admixture population. PAN is under inbreeding (Ho = 0.80 and 0.74, uHe = 0.85 and 0.82, Ap = 1.1 and 7.1, F = 0.06 and 0.10, for mother trees and offspring, respectively). Mother trees were predominantly outcrossing (tm = 0.95), with some selfing (1 − tm = 0.05), and crossing between related individuals (tmts = 0.07); they received pollen from few donors (Nep = 9). Restricted gene flow within PAN gave rise to a strong population structure, which split the 18 families into six groups. Some mother trees were reproductively isolated. Conservation perspectives are discussed.


Microsatellites Phylogeography Population structure Seasonal forests South America 


Funding information

This work was supported by The Minas Gerais State Foundation of Research Aid – FAPEMIG (grant numbers PPM 00561-15 and APQ 03504-15) and by The National Council of Scientific and Technological Development – CNPq (fellowship number PQ 305827/2015-4) to LOO. JMDS received financial support from the Universidad de Sucre for his doctoral training. IBAMA and IEF-MG provided collecting permits.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Data archiving statement

Microsatellite genotype data are available in Supplementary Table S1.

Supplementary material

11295_2018_1287_MOESM1_ESM.xls (84 kb)
Table S1 Genotypic data (diploid individuals) for the population PAN (mother trees and offspring) of Cedrela fissilis obtained with ten microsatellite loci (XLS 84 kb)


  1. Bawa KS (1977) The reproductive biology of Cupania guatemalensis Radlk. (Sapindaceae). Evolution 31:52–63CrossRefPubMedGoogle Scholar
  2. Bawa KS, Perry DR, Beach JH (1985) Reproductive biology of tropical lowland rain forest trees. I. Sexual systems and incompatibility mechanisms. Am J Bot 72:331–345CrossRefGoogle Scholar
  3. Bethonico MBM (2010) Rio Pandeiros: território e história de uma área de proteção ambiental no norte de Minas Gerais. Acta Geogr 3:23–38Google Scholar
  4. Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–789CrossRefPubMedGoogle Scholar
  5. Carneiro FS, Lacerda AEB, Lemes MR, Gribel R, Kanashiro M, Wadt LHO, Sebbenn AM (2011) Effects of selective logging on the mating system and pollen dispersal of Hymenaea courbaril L. (Leguminosae) in the eastern Brazilian Amazon as revealed by microsatellite analysis. Forest Ecol Manag 262:1758–1765CrossRefGoogle Scholar
  6. Carvalho PER (1994) Espécies florestais brasileiras: recomendações silviculturais, potencialidades e uso da madeira. EMBRAPA-CNPF/SPI, BrasiliaGoogle Scholar
  7. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570CrossRefPubMedGoogle Scholar
  8. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631CrossRefPubMedGoogle Scholar
  9. Chapuis MP, Lecoq M, Michalakis Y, Loiseau A, Sword GA, Piry S, Estoup A (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Mol Ecol 17:3640–3653CrossRefPubMedGoogle Scholar
  10. Charrad M, Ghazzali G, Boiteau V, Niknafs A (2014) NbClust: an R package for determining the relevant number of clusters in a data set. J Stat Softw 61:1–36CrossRefGoogle Scholar
  11. Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113CrossRefPubMedGoogle Scholar
  12. Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9:539CrossRefPubMedPubMedCentralGoogle Scholar
  13. Corander J, Waldmann P, Sillanpää MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedPubMedCentralGoogle Scholar
  14. Cota-Sánchez JH, Remarchuk K, Ubayasena K (2006) Ready-to-use DNA extracted with a CTAB method adapted for herbarium specimens and mucilaginous plant tissue. Plant Mol Biol Rep 24:161–167CrossRefGoogle Scholar
  15. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39:1–38Google Scholar
  16. Gandara FB (2009) Diversidade genética de populações de Cedro (Cedrela fissilis Vell. (Meliaceae) no Centro-Sul do Brasil. D. Phil. thesis, Universidade de São PauloGoogle Scholar
  17. Gandara FB, Tambarussi EV, Sebbenn AM, Ferraz EM, Moreno MA, Ciampi AY, Vianello RP, Grattapaglia D, Kageyama PY (2014) Development and characterization of microsatellite loci for Cedrela fissilis Vell (Meliaceae), an endangered tropical tree species. Silvae Genet 63:240–243CrossRefGoogle Scholar
  18. Garcia MG, Silva RS, Carniello MA, Veldman JW, Rossi AAB, Oliveira LO (2011) Molecular evidence of cryptic speciation, historical range expansion, and recent intraspecific hybridization in the Neotropical seasonal forest tree Cedrela fissilis (Meliaceae). Mol Phylogenet Evol 61:639–649CrossRefPubMedGoogle Scholar
  19. Goicoechea PG, Herrán A, Durand J, Bodénès C, Plomion C, Kremer A (2015) A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks. Heredity 114:373–386CrossRefPubMedGoogle Scholar
  20. Goodwillie C, Kalisz S, Eckert CG (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annu Rev Ecol Evol Syst 36:47–79CrossRefGoogle Scholar
  21. Gouvêa CF, Dornelas MC, Rodriguez APM (2008) Floral development in the tribe Cedreleae (Meliaceae, sub-family Swietenioideae): Cedrela and Toona. Ann Bot 101:39–48CrossRefPubMedGoogle Scholar
  22. Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates, SunderlandGoogle Scholar
  23. Hensen I, Oberprieler C (2005) Effects of population size on genetic diversity and seed production in the rare Dictamnus albus (Rutaceae) in central Germany. Conserv Genet 6:63–73CrossRefGoogle Scholar
  24. Hernández G, Buonamici A, Walker K, Vendramin GG, Navarro C, Cavers S (2008) Isolation and characterization of microsatellite markers for Cedrela odorata L. (Meliaceae), a high value neotropical tree. Conserv Genet 9:457–459CrossRefGoogle Scholar
  25. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  26. International Union for Conservation of Nature [IUCN] (2017) The IUCN red list of threatened species. Version 2017-3. Accessed 26 May 2018
  27. Islam MS, Lian C, Kameyama N, Hogetsu T (2015) Analysis of the mating system, reproductive characteristics, and spatial genetic structure in a natural mangrove tree (Bruguiera gymnorrhiza) population at its northern biogeographic limit in the southern Japanese archipelago. J For Res 20:293–300CrossRefGoogle Scholar
  28. Jamovi Project (2018) Jamovi (Version v0.8.1.17). Accessed 26 May 2018
  29. Langella O (1999) POPULATIONS. Version 1.2.28. A population genetic software. CNRS, UPR9034.;tryphon/populations. Accessed 26 May 2018
  30. Lopes LE, Neto SD, Leite LO, Moraes LL, Capurucho JMG (2010) Birds from Rio Pandeiros, southeastern Brazil: a wetland in an arid ecotone. Rev Bras Ornitol 18:267–282Google Scholar
  31. Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95CrossRefGoogle Scholar
  32. Mangaravite E, Vinson CC, Rody HVS, Garcia MG, Carniello MA, Silva RS, Oliveira LO (2016) Contemporary patterns of genetic diversity of Cedrela fissilis offer insight into the shaping of seasonal forests in eastern South America. Am J Bot 103:307–316CrossRefPubMedGoogle Scholar
  33. Mayle FE (2004) Assessment of the Neotropical dry forest refugia hypothesis in the light of palaeoecological data and vegetation model simulations. J Quat Sci 19:713–720CrossRefGoogle Scholar
  34. Ministério do Meio Ambiente [MMA] (2014) Lista Nacional Oficial de Espécies da Flora Ameaçadas de Extinção. Portaria 443, December 17th, 2014. Accessed 26 May 2018
  35. Muona O, Moran GF, Bell JC (1991) Hierarchical patterns of correlated mating in Acacia melanoxylon. Genetics 127:619–626PubMedPubMedCentralGoogle Scholar
  36. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497CrossRefGoogle Scholar
  37. Murawski DA, Hamrick JL (1991) The effect of the density of flowering individuals on the mating systems of nine tropical tree species. Heredity 67:167–174CrossRefGoogle Scholar
  38. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci U S A 70:3321–3323CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nunes YRF, Azevedo IFP, WV VMDM, Souza RA, Fernandes GW (2009) Pandeiros: o Pantanal Mineiro. MGBiota 2:4–17Google Scholar
  40. Oliveira-Filho AT, Jarenkow JA, Rodal MJN (2006) Floristic relationships of seasonally dry forests of eastern South America based on tree species distribution patterns. In: Pennington RT, Ratter JA, Lewis GP (eds) Neotropical savannas and seasonally dry forests: plant diversity, biogeography and conservation. CRC, Boca Raton, pp 159–192Google Scholar
  41. Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on earth. BioScience 51:933–938CrossRefGoogle Scholar
  42. Patino-Valera F (1997) Recursos geneticos de Swietenia y Cedrela en los Neotropicos: propuestas para acciones coordinadas. FAO, RomeGoogle Scholar
  43. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefPubMedPubMedCentralGoogle Scholar
  44. Pennington RT, Lavin M, Prado DE, Pendry CA, Pell SK, Butterworth CA (2004) Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philos Trans R Soc B 359:515–538CrossRefGoogle Scholar
  45. Pennington TD, Muellner AN (2010) A monograph of Cedrela (Meliaceae). DH Books, SherborneGoogle Scholar
  46. Prado DE, Gibbs PE (1993) Patterns of species distributions in the dry seasonal forests of South America. Ann Mo Bot Gard 80:902–927CrossRefGoogle Scholar
  47. Queiroz LP (2006) The Brazilian caatinga: phytogeographical patterns inferred from distribution data of the Leguminosae. In: Pennington RT, Ratter JA, Lewis GP (eds) Neotropical savannas and seasonally dry forests: plant diversity, biogeography and conservation. CRC, Boca Raton, pp 113–149Google Scholar
  48. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283CrossRefPubMedGoogle Scholar
  50. Riahi M, Zarre S, Maassoumi AA, Attar F, Kazempour Osaloo S (2009) An inexpensive and rapid method for extracting papilionoid genomic DNA from herbarium specimens. Genet Mol Res 9:1334–1342CrossRefGoogle Scholar
  51. Ritland K (1989) Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848–859CrossRefPubMedGoogle Scholar
  52. Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228CrossRefPubMedGoogle Scholar
  53. Ritland K, Jain S (1981) A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity 47:35–52CrossRefGoogle Scholar
  54. Rodrigues PMS, Azevedo IFP, Veloso MDM, Santos RM, Menino GCO, Nunes YRF, Fernandes W (2009) Riqueza florística da vegetação ciliar do rio Pandeiros, norte de Minas Gerais. MGBiota 2:18–37Google Scholar
  55. Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  56. Rymer PD, Sandiford M, Harris SA, Billingham MR, Boshier DH (2013) Remnant Pachira quinata pasture trees have greater opportunities to self and suffer reduced reproductive success due to inbreeding depression. Heredity 115:115–124CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sales RH, Souza SCA, Luz GR, Costa FM, Amaral VB, Santos RM, Veloso RM, Nunes YRF (2009) Flora arbórea de uma floresta estacional decidual na APA Estadual do Rio Pandeiros, Januária/MG. MGBiota 2:31–41Google Scholar
  58. Sebbenn AM (2002) Número de árvores matrizes e conceitos genéticos na coleta de sementes para reflorestamentos com espécies nativas. Rev Inst Florestal 14:115–132Google Scholar
  59. Sebbenn AM (2006) Sistemas de reprodução em espécies tropicais e suas implicações para a seleção de árvores matrizes para reflorestamentos ambientais. In: Higa AR, Duque SL (eds) Pomares de sementes de espécies florestais nativas. FUPEF, Curitiba, pp 93–138Google Scholar
  60. Silva MB, Kanashiro M, Ciampi AY, Thompsom I, Sebbenn AM (2008) Genetic effects of selective logging and pollen gene flow in a low-density population of the dioecious tropical tree Bagassa guianensis in the Brazilian Amazon. For Ecol Manag 255:1548–1558CrossRefGoogle Scholar
  61. Styles BT (1972) The flower biology of the Meliaceae and its bearing on tree breeding. Silvae Genet 5:175–182Google Scholar
  62. Styles BT (1981) Swietenioideae. In: Pennington TD, Styles BT, Taylor DAH (eds) Flora Neotropica monograph: Meliaceae. New York Botanical Gardens, BronxGoogle Scholar
  63. Surles SE, Arnold J, Schnabel A, Hamrick JL, Bongarten BC (1990) Genetic relatedness in open-pollinated families of two leguminous tree species, Robinia pseudoacacia L. and Gleditsia triacanthos L. Theor Appl Genet 80:49–56CrossRefPubMedGoogle Scholar
  64. Tang J, Hanage WP, Fraser C, Corander J (2009) Identifying currents in the gene pool for bacterial populations using an integrative approach. PLoS Comput Biol 5:e1000455CrossRefPubMedPubMedCentralGoogle Scholar
  65. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  66. Vinson CC, Dal’Sasso TCS, Sudré CP, Mangaravite E, Oliveira LO (2015) Population genetics of the naturally rare tree Dimorphandra wilsonii (Caesalpinioideae) of the Brazilian Cerrado. Tree Genet Genomes 11:46CrossRefGoogle Scholar
  67. Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associates, SunderlandGoogle Scholar
  68. Whitmore TC, Prance GT (1987) Biogeography and Quaternary history in tropical America. Clarendon, OxfordGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departamento de Bioquímica e Biologia MolecularUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento de Biología y QuímicaUniversidad de SucreSincelejoColombia

Personalised recommendations