Genetic diversity and differentiation among the species of African mahogany (Khaya spp.) based on a large SNP array

Conservation Genetics volume 20, pages1035–1044(2019)Cite this article

Abstract

The genus Khaya includes some of the highest-value timber species in natural forests in Africa, which are under heavy exploitation pressure. Genetic identification of Khaya species is important to confirm the taxonomic classification for biodiversity conservation purposes and as a forensic tool aiding law enforcement in the fight against illegal logging. We collected samples from a total of 2222 trees belonging to five or six (depending on classification) different Khaya species (K. ivorensis, K. anthotheca/K. nyasica, K. grandifoliola, K. senegalensis, K. madagascariensis). Representative sampling was conducted over the natural ranges of all sampled Khaya species, in humid tropical forest and savanna zones. We genotyped individuals based on 101 molecular markers (67 nuclear, 11 chloroplast and 22 mitochondrial SNPs, 1 chloroplast indel). Bayesian clustering produced three main genetic groups assigning all K. ivorensis and all K. senegalensis trees, respectively, in two different clusters and all remaining individuals in a third cluster. Genetic self-assignment tests with all 101 SNPs had success rates of 97–100% for all species except for K. nyasica and K. madagascariensis, which could not be clearly distinguished from each other. A success rate for species identification nearly as high was observed using a subset of 15 highly differentiated SNPs. There was only very little evidence for hybridization among species and the vast majority (> 97%) of individuals were assigned to the same species group as identified based on morphological characters.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3

Data availability

Upon acceptance for publication of the manuscript all data (information on individuals, country of origin and SNP data) will be made available on OSF (Open Science Framework, https://osf.io, Accession number osf.io/v86jh). For SNP/indel marker sequence data (including primer sequences) see Pakull et al. (2016).

References

  1. Alamu LO, Agbeja BO (2011) Deforestation and endangered indigenous tree species in South-West Nigeria. Int J Biodivers Conserv 3:291–297

    Google Scholar 

  2. Aubréville A (1959) La flore forestière de la Côte d’Ivoire, 2nd edn. Centre Technique Forestier Tropical, Nogent-sur-Marne, Seine

    Google Scholar 

  3. Blanc-Jolivet C, Yanbaev Y, Kersten B, Degen B (2018) A set of SNP markers for timber tracking of Larix spp. in Europe and Russia. Forestry 91:614–628. https://doi.org/10.1093/forestry/cpy020

    Article  Google Scholar 

  4. Cornuet J-M, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Dainou K et al (2016) Revealing hidden species diversity in closely related species using nuclear SNPs, SSRs and DNA sequences—a case study in the tree genus Milicia. BMC Evol Biol 16:15. https://doi.org/10.1186/s12862-016-0831-9

    Article  Google Scholar 

  6. Dipelet UGB, Florence J, Doumenge C, Loumeto JJ, McKey D (2017) Khayae (Meliaceae) specierum nomenclator. Adansonia 39:15–30

    Article  Google Scholar 

  7. Duminil J, Caron H, Scotti I, Cazal SO, Petit RJ (2006) Blind population genetics survey of tropical rainforest trees. Mol Ecol 15:3505–3513. https://doi.org/10.1111/j.1365-294X.2006.03040.x

    Article  CAS  PubMed  Google Scholar 

  8. Duminil J, Kenfack D, Viscosi V, Grumiau L, Hardy OJ (2012) Testing species delimitation in sympatric species complexes: the case of an African tropical tree, Carapa spp. (Meliaceae). Mol Phylogenet Evolu 62:275–285. https://doi.org/10.1016/j.ympev.2011.09.020

    Article  Google Scholar 

  9. Dumolin S, Demesure B, Petit R (1995) Inheritance of chloroplast and mitochondrial genomes in pedunculate oak investigated with an efficient PCR method. Theor Appl Genet 91:1253–1256

    Article  CAS  PubMed  Google Scholar 

  10. Efron B (1983) Estimating the error rate of a prediction rule: improvement on cross-validation. J Am Stat Assoc 78:316–331

    Article  Google Scholar 

  11. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gonzalez MA et al (2009) Identification of Amazonian trees with DNA barcodes. PLoS ONE 4:e7483. https://doi.org/10.1371/journal.pone.0007483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gregorius HR (1984) A unique genetic distance. Biom J 26:13–18

    Article  Google Scholar 

  14. Gregorius H-R (1987) The relationship between the concepts of genetic diversity and differentiation. Theor Appl Genet 74:397–401

    Article  CAS  PubMed  Google Scholar 

  15. Gregorius H-R, Degen B, Konig A (2007) Problems in the analysis of genetic differentiation among populations—a case study in Quercus robur Silvae. Genetica 56:190–199

    Google Scholar 

  16. Hammer Ø, Harper D, Ryan P (2001) PAST: Paleontological Statistics Software Package for education and data analysis. Palaeontolia Electron 4:9

    Google Scholar 

  17. Hansen CP, Treue T (2008) Assessing illegal logging in Ghana. Int For Rev 10:573–590

    Google Scholar 

  18. Hawthorne W, Gyakari N (2006) Photoguide for the forest trees of Ghana: a tree-spotter’s field guide for identifying the largest trees. Oxford Forestry Institute, Department of Plant Sciences, Oxford

    Google Scholar 

  19. Höltken AM, 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. Holzforschung 66:97–104

    Google Scholar 

  20. Hyde MA, Wursten BT, Ballings P, Coates-Palgrave M (2018) Flora of Malawi: Genus page: Khaya. https://www.malawiflora.com/speciesdata/genus.php?genus_id=813. Accessed 18 Sept 2018

  21. Irvine FR (1961) Woody plants of Ghana with special reference to their uses. Oxford University Press, London

    Google Scholar 

  22. ITTO (2017) Biennial review and assessment of the world timber situation 2015–2016. International Tropical Timber Organization Publications. http://www.itto.int/annual_review/

  23. IUCN (2015) The IUCN red list of threatened species. http://www.iucnredlist.org

  24. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233

    Article  CAS  PubMed  Google Scholar 

  25. Karan M et al (2012) Rapid microsatellite marker development for African mahogany (Khaya senegalensis, Meliaceae) using next-generation sequencing and assessment of its intra-specific genetic diversity. Mol Ecol Resour 12:344–353

    Article  CAS  PubMed  Google Scholar 

  26. Kitpipit T, Thongjued K, Penchart K, Ouithavon K, Chotigeat W (2017) Mini-SNaPshot multiplex assays authenticate elephant ivory and simultaneously identify the species origin. Forensic Sci Int 27:106–115

    Article  CAS  Google Scholar 

  27. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lawal A, Adekunle VAJ, Onokpise OU (2016) Biosystematics, morphological variability and status of the genus Khaya in South West Nigeria. Appl Trop Agric 21:159–166

    Google Scholar 

  29. Lemes MR, Esashika T, Gaoue OG (2011) Microsatellites for mahoganies: twelve new loci for Swietenia macrophylla and its high transferability to Khaya senegalensis. Am J Bot 98:e207–e209

    Article  PubMed  Google Scholar 

  30. Li CH, Fong YK, Hong Y (2010) Isolation and characterization of 13 polymorphic microsatellite loci for Khaya senegalensis (Meliaceae). Mol Ecol Resour 10:1098–1105

    Article  PubMed  Google Scholar 

  31. Louppe D, Oteng-Amoako A, Brink M, Lemmens R, Oyen L, Cobbinah J (2008) Plant resources of tropical Africa 7(1). Timbers 1. PROTA Foundation, Wageningen

  32. Lowe AJ et al (2016) Opportunities for improved transparency in the timber trade through scientific verification. Bioscience 66:990–998

    Article  Google Scholar 

  33. Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231. https://doi.org/10.1111/mec.13243

    Article  PubMed  Google Scholar 

  34. Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA (2007) Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Research 17:240–248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Muellner AN, Samuel R, Johnson SA, Cheek M, Pennington TD, Chase MW (2003) Molecular phylogenetics of Meliaceae (Sapindales) based on nuclear and plastid DNA sequences. Am J Bot 90:471–480. https://doi.org/10.3732/ajb.90.3.471

    Article  CAS  PubMed  Google Scholar 

  36. Muellner AN, Schaefer H, Lahaye R (2011) Evaluation of candidate DNA barcoding loci for economically important timber species of the mahogany family (Meliaceae). Mol Ecol Resour 11:450–460. https://doi.org/10.1111/j.1755-0998.2011.02984.x

    Article  CAS  PubMed  Google Scholar 

  37. Opuni-Frimpong E (2008) Khaya grandifoliola C.DC. In: Louppe D, Oteng-Amoako AA, Brink M (eds) Plant reources of tropical Africa. Backhuys Publishers, Leiden, pp 329–333

    Google Scholar 

  38. Pakull B et al (2016) Development of nuclear, chloroplast and mitochondrial SNP markers for Khaya sp. Conserv Genet Resour 8:283–297. https://doi.org/10.1007/s12686-016-0557-4

    Article  Google Scholar 

  39. Parmentier I et al (2013) How effective are DNA barcodes in the identification of African rainforest trees? PLoS ONE 8:e54921. https://doi.org/10.1371/journal.pone.0054921

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pennington TD, Styles BT (1975) A generic monograph of the Meliaceae. Blumea 22:419–540

    Google Scholar 

  41. Petit RJ et al (2002) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manag 156:5–26. https://doi.org/10.1016/S0378-1127(01)00645-4

    Article  Google Scholar 

  42. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  CAS  PubMed  Google Scholar 

  43. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    Article  CAS  PubMed  Google Scholar 

  45. Ratnasingham S, Hebert PD (2007) BOLD: the Barcode of Life Data System (http://www.barcodinglife.org) Mol Ecol Notes 7:355–364

  46. Schroeder H, Cronn R, Yanbaev Y, Jennings T, Mader M, Degen B, Kersten B (2016) Development of molecular markers for determining continental origin of wood from white oaks (Quercus L. sect. Quercus). PLoS ONE 11:15. https://doi.org/10.1371/journal.pone.0158221

    CAS  Article  Google Scholar 

  47. Scotti-Saintagne C et al (2013) Phylogeography of a species complex of lowland Neotropical rain forest trees (Carapa, Meliaceae). J Biogeogr 40:676–692. https://doi.org/10.1111/j.1365-2699.2011.02678.x

    Article  Google Scholar 

  48. Sexton G, Frere C, Dieters M, Godwin I, Prentis P (2010) Development and characterization of microsatellite loci for Khaya senegalensis (Meliaceae). Am J Bot 97:e111–e113

    Article  CAS  PubMed  Google Scholar 

  49. Sexton GJ et al (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 Genet Genomes 11:1–15

    Article  Google Scholar 

  50. Straub SC, Parks M, Weitemier K, Fishbein M, Cronn RC, Liston A (2012) Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Am J Bot 99:349–364

    Article  CAS  PubMed  Google Scholar 

  51. White G, Powell W (1997) Cross-species amplification of SSR loci in the Meliaceae family. Mol Ecol 6:1195–1197

    Article  CAS  Google Scholar 

  52. Wright S (1978) Evolution and the genetics of populations: a treatise in four volumes: Vol. 4: variability within and among natural populations. University of Chicago Press, Chicago

    Google Scholar 

Download references

Acknowledgments

This work was supported by the German Federal Ministry of Food and Agriculture (BMEL), the International Tropical Timber Organization (ITTO), the Prince Albert II of Monaco Foundation, the CGIAR Research Program on Forests, Trees and Agroforestry (FTA), the Service de Coopération et d’Action culturelle (SCAC) of the Embassy of France in Congo, the Fondation Internationale pour la Science (FIS), the Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD) and DoubleHelix Tracking Technologies. MassARRAY®MultiPLEX™ genotyping was performed at the Genome and Transcriptome Facility of Bordeaux and funded by grants from the Conseil Regional d’Aquitaine (n°20030304002FA and n°20040305003FA), from the European Union (FEDER n°2003227) and from Investissements d’Avenir (Convention attributive d’aide N°ANR-10-EQPX-16-01). We thank Maike Paulini, Vivian Kuhlenkamp, Susanne Bein and Adline Delcamp for their excellent technical assistance.

Author information

Affiliations

  1. Thünen Institute of Forest Genetics, Sieker Landstrasse 2, 22927, Grosshansdorf, Germany

    Birte Pakull & Bernd Degen

  2. Bioversity International, s/c IITA, BP 2008, Yaoundé, Cameroon

    Marius R. M. Ekué

  3. CIRAD, Forêts et Sociétés Unit, Université Montpellier, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France

    Ulrich G. Bouka Dipelet & Charles Doumenge

  4. Laboratoire de Botanique et Ecologie, Faculté des Sciences, Université Marien Ngouabi, BP 69, Brazzaville, Congo

    Ulrich G. Bouka Dipelet & Jean Joël Loumeto

  5. Unité Mixte de Recherche (UMR) 5175 Centre National de la Recherche Scientifique (CNRS), Université Montpellier et Centre d’Ecologie Fonctionnelle et Evolutive, 34293, Montpellier Cedex 5, France

    Doyle B. McKey

  6. University of Energy and Natural Resources, P.O. Box 214, Sunyani, Ghana

    Emmanuel Opuni-Frimpong

  7. Faculty of Agronomy, University of Parakou, BP 123, Parakou, Benin

    Soulemane N. Yorou

  8. Laboratory of Plant Biology and Ecology, Department of Plant Biology and Physiology, UFR-SVT, University of Ouagadougou, Ouagadougou, Burkina Faso

    Blandine M. Y. Nacoulma

  9. Département de Botanique, Faculté des Sciences, Université de Lomé, Lomé, Togo

    Kudzo A. Guelly

  10. Silo National des Graines Forestières, Antananarivo, Madagascar

    Lolona Ramamonjisoa

  11. Double Helix Tracking Technology, Singapore, Republic of Singapore

    Darren Thomas

  12. BIOGECO, INRA, University of Bordeaux, 33610, Cestas, France

    Erwan Guichoux

  13. Bioversity International, Rome, Italy

    Judy Loo

Authors
  1. Birte Pakull
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marius R. M. Ekué
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ulrich G. Bouka Dipelet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charles Doumenge
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Doyle B. McKey
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jean Joël Loumeto
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Emmanuel Opuni-Frimpong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Soulemane N. Yorou
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Blandine M. Y. Nacoulma
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Kudzo A. Guelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lolona Ramamonjisoa
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Darren Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Erwan Guichoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Judy Loo
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Bernd Degen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bernd Degen.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pakull, B., Ekué, M.R.M., Bouka Dipelet, U.G. et al. Genetic diversity and differentiation among the species of African mahogany (Khaya spp.) based on a large SNP array. Conserv Genet 20, 1035–1044 (2019). https://doi.org/10.1007/s10592-019-01191-3

Download citation

Keywords

  • Africa
  • Genetic assignment
  • Species identification
  • Timber
  • Tropical tree