Skip to main content
SpringerLink
Log in

The African timber tree Entandrophragma congoense (Pierre ex De Wild.) A.Chev. is morphologically and genetically distinct from Entandrophragma angolense (Welw.) C.DC

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Interpreting morphological variability in terms of species delimitation can be challenging. However, correcting species delineation can have strong implications for the sustainable management of exploited species. Up to now, species delimitation between two putative timber species from African forests, Entandrophragma congoense and E. angolense, remained unclear. To investigate their differences, we applied an integrated approach which combines morphological traits and genetic markers. We defined 13 morphological characters from 81 herbarium specimens and developed 15 new polymorphic microsatellite markers to genotype 305 samples (herbarium samples and specimens collected in the field across the species distribution ranges). Principal component analysis (PCA) of morphological data and the Bayesian clustering analyses of genetic data were used to assess differentiation between putative species. These analyses support two well-differentiated groups (FST = 0.30) occurring locally in sympatry. Moreover, these two groups present distinct morphological characters at the level of the trunk, leaflets, and seeds. Our genetic markers identified few individuals (4%) that seem to be hybrids, though there is no evidence of genetic introgression from geographic patterns of genetic variation. Hence, our results provide clear support to recognize E. congoense as a species distinct from E. angolense, with a much lower genetic diversity than the latter, and that should be managed accordingly. This work highlights the power of microsatellite markers in resolving species boundaries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • African Plant Database - version 3.4.0 (2018). Conservatoire et Jardin botaniques de la Ville de Genève and South African National Biodiversity Institute, Pretoria. Retrieved June 2018, from <http://www.ville-ge.ch/musinfo/bd/cjb/africa/>

  • Anderson EC, Thompson EA (2002) A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160:1217–1229 http://www.ville-ge.ch/musinfo/bd/cjb/africa

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chessel D, Dufour AB, Thioulouse J et al (2004) The ade4 package-I-One-table methods. R news 4:5–10

    Google Scholar 

  • Chevalier A (1909) Les végétaux utiles de l’Afrique tropicale française: études scientifiques et agronomiques. Dépot des publications

  • Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113. https://doi.org/10.1093/jhered/esn088

    Article  CAS  PubMed  Google Scholar 

  • Culley TM, Weller SG, Sakai AK, Putnam KA (2008) Characterization of microsatellite loci in the Hawaiian endemic shrub Schiedea adamantis (Caryophyllaceae) and amplification in related species and genera. Mol Ecol Resour 8:1081–1084

    Article  CAS  PubMed  Google Scholar 

  • Dainou K, Blanc-Jolivet C, Degen B, Kimani P, Ndiade-Bourobou D, Donkpegan AS, Tosso F, Kaymak E, Bourland N, Doucet JL, Hardy OJ (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 16:259. https://doi.org/10.1186/s12862-016-0831-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Daïnou K, Flot J-F, Degen B, Blanc-Jolivet C, Doucet J-L, Lassois L, Hardy OJ (2017) DNA taxonomy in the timber genus Milicia: evidence of unidirectional introgression in the West African contact zone. Tree Genet Genomes 13:90. https://doi.org/10.1007/s11295-017-1174-4

    Article  Google Scholar 

  • Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415

    Article  Google Scholar 

  • de Candolle C (1894) Meliaceae novae. 2. Asiaticae et Africanae. Bull Herb Boissier 2:577–584

    Google Scholar 

  • De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886

    Article  PubMed  Google Scholar 

  • de Wilde JJFE (2015) Meliaceae. In: Sosef MSM, Florence J, Ngok BL, Bourobou BHP (eds) Flore du Gabon, vol 47. Margraf Publishers, Wekersheim, pp 5–74

    Google Scholar 

  • Doyle JJ, Doyle JL (1987) CTAB DNA extraction in plants. Phytochem Bull 19:11–15

    Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

  • Duminil J, Di Michele M (2009) Plant species delimitation: a comparison of morphological and molecular markers. Plant Biosyst 143:528–542

    Article  Google Scholar 

  • 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 Evol 62:275–285

    Article  PubMed  Google Scholar 

  • Earl DA, VonHoldt BM, von Reumont B (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

    Article  Google Scholar 

  • Edwards DL, Knowles LL (2014) Species detection and individual assignment in species delimitation: can integrative data increase efficacy? Proceedings Biol Sci 281:20132765. https://doi.org/10.1098/rspb.2013.2765

    Article  Google Scholar 

  • 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  Google Scholar 

  • Hardy OJ, Vekemans X (2001) Patterns of allozyme variation in diploid and tetraploid Centaurea jacea at different spatial scales. Evolution 55:943–954

    Article  CAS  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haselhorst M, Buerkle C (2011) Detection of hybrids in natural populations of Picea glauca and Picea englemannii. Univ Wyoming Natl Park Serv Res Cent Annu Rep 33

  • Ikabanga DUDU, Stévart T, Koffi KGG, Monthé FK, Doubindou ECN, Dauby G, Souza A, M’BATCHI B, Hardy O (2017) Combining morphology and population genetic analysis uncover species delimitation in the widespread African tree genus Santiria (Burseraceae). Phytotaxa 321:166–180. https://doi.org/10.11646/phytotaxa.321.2.2

    Article  Google Scholar 

  • Janzen DH, Burns JM, Cong Q, Hallwachs W, Dapkey T, Manjunath R, Hajibabaei M, Hebert PDN, Grishin NV (2017) Nuclear genomes distinguish cryptic species suggested by their DNA barcodes and ecology. Proc Natl Acad Sci U S A 114:8313–8318. https://doi.org/10.1073/pnas.1621504114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasongo-Yakusu E, Monthe FK, Nils B, Hardy OJ, Louppe D, Lokanda FBM, Hubau W, Kahindo J-MM, Van Den Bulcke J, Van Acker J, Beeckman H (2018) Le genre Entandrophragma (Meliaceae): taxonomie et écologie d’arbres africains d’intérêt économique (synthèse bibliographique). Biotechnol Agron société Environ 22:1–15

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  • Klopper RR, Chatelain C, Habashi C, Gautier L, Spichiger R-E (2006) Checklist of the flowering plants of sub-Saharan Africa: an index of accepted names and synonyms. Sabonet

  • Le Guyader H (2002) Doit-on abandonner le concept d’espèce? Le Courr l’environnement l’INRA 51–64

  • Ley A, Hardy O (2010) Species delimitation in the Central African herbs Haumania (Marantaceae) using georeferenced nuclear and chloroplastic DNA sequences. Mol Phylogenet Evol. https://doi.org/10.1016/j.ympev.2010.08.027

    Article  CAS  PubMed  Google Scholar 

  • Ley AC, Hardy OJ (2017) Hybridization and asymmetric introgression after secondary contact in two tropical African climber species, Haumania danckelmaniana and Haumania liebrechtsiana (Marantaceae). Int J Plant Sci 178:421–430. https://doi.org/10.1086/691628

    Article  Google Scholar 

  • Liben L (1970) La répartition géographique d’Entandrophragma congoënse (De Wild.) A. Chev.(Meliaceae). Bull du Jard Bot Natl Belgique/Bulletin van Natl Plantentuin van Belgie 299–300

  • Liben L, Dechamps R (1966) Entandrophragma congoense (De Wild.) A. Chev. espèce méconnue du Congo. Bull du Jard Bot l’Etat, Bruxelles/Bulletin van den Rijksplantentuin, Brussel 415–424

  • Mayr E (1992) Species concepts and their application. Units Evol MIT 15–25

  • Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press

  • Meunier Q, Moumbogou C, Doucet J-L (2015) Les arbres utiles du Gabon. Presses Agronomiques de Gembloux

  • Micheneau C, Dauby G, Bourland N, Doucet JL, Hardy OJ (2011) Development and characterization of microsatellite loci in Pericopsis elata (Fabaceae) using a cost-efficient approach. Am J Bot 98:e268–e270. https://doi.org/10.3732/ajb.1100070

    Article  CAS  PubMed  Google Scholar 

  • Monthe F, Duminil J, Tosso F, Migliore J, Hardy OJ (2017) Characterization of microsatellite markers in two exploited African trees, Entandrophragma candollei and E. utile (Meliaceae). Appl Plant Sci 5:1600130. https://doi.org/10.3732/apps.1600130

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenALEx 6.5: genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410. https://doi.org/10.1046/j.1365-2435.1999.00332.x

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55:421–438

    Article  CAS  PubMed  Google Scholar 

  • Slik JWF, Arroyo-Rodríguez V, Aiba S-I, Alvarez-Loayza P, Alves LF, Ashton P, Balvanera P, Bastian ML, Bellingham PJ, van den Berg E, Bernacci L, da Conceição BP, Blanc L, Böhning-Gaese K, Boeckx P, Bongers F, Boyle B, Bradford M, Brearley FQ et al (2015) An estimate of the number of tropical tree species. Proc Natl Acad Sci U S A 112:7472–7477. https://doi.org/10.1073/pnas.1423147112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sosef MSM, Dauby G, Blach-Overgaard A, van der Burgt X, Catarino L, Damen T, Deblauwe V, Dessein S, Dransfield J, Droissart V, Duarte MC, Engledow H, Fadeur G, Figueira R, Gereau RE, Hardy OJ, Harris DJ, de Heij J, Janssens S, Klomberg Y, Ley AC, Mackinder BA, Meerts P, van de Poel JL, Sonké B, Stévart T, Stoffelen P, Svenning J-C, Sepulchre P, Zaiss R, Wieringa JJ, Couvreur TLP (2017) Exploring the floristic diversity of tropical Africa. BMC Biol 15:15. https://doi.org/10.1186/s12915-017-0356-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Sprague TA (1910) Entandrophragma, Leioptyx and Pseudocedrela. Bull Misc Inf (Royal Gard Kew) 1910:177–182

    Article  Google Scholar 

  • Staner P (1941) Les Méliacées du Congo Belge. Bull du Jard Bot l’Etat, Bruxelles/Bulletin van den Rijksplantentuin, Brussel 16:109–251

    Article  Google Scholar 

  • Tarasjev A, Barisić Klisarić N, Stojković B, Avramov S (2009) Phenotypic plasticity and between population differentiation in Iris pumila transplants between native open and anthropogenic shade habitats. Genetika 45:1078–1086

    CAS  PubMed  Google Scholar 

  • The Plant List (2013) Version 1.1. Retrieved June 2018, from http://www.theplantlist.org/

  • Tosso F, Dainou K, Hardy OJ, Sinsin B, Doucet J-L (2015) Le genre Guibourtia Benn., un taxon à haute valeur commerciale et sociétale (synthèse bibliographique). Biotechnol Agron société Environ 19:71–88

    Google Scholar 

  • Weber AA-T, Stöhr S, Chenuil A (2017) Species delimitation in the presence of strong incomplete lineage sorting and hybridization. bioRxiv. https://doi.org/10.1101/240218

Download references

Acknowledgments

We are grateful to Meise Botanic Garden (Belgium), the Herbarium and African Botanical Library (BRLU) of Université Libre de Bruxelles (ULB), and Naturalis Biodiversity Center (Leiden, the Netherlands), for making the herbarium specimens available. We thank the forest company PALLISCO, especially Bienvenue Ango for its support to field sampling. We are also grateful to the DynAfFor and P3FAC projects, funded by the Fonds Français pour l’Environnement Mondial, which facilitated access to the field, and to two anonymous referees for their comments.

Data archiving statement

The microsatellite markers are submitted to GenBank (Table 3).

Funding

We thank the Fonds pour la Formation à la Recherche dans l’Industrie et l’Agriculture (FRIA-FNRS, Belgium) through a PhD grant to the first author, the Fonds de la Recherche Scientifique (FRS-FNRS) through grant X.3040.17, and the Belgian Science Policy (Belspo) for funding the project AFRIFORD.

Author information

Authors and Affiliations

  1. Faculté des Sciences, Service Evolution Biologique et Ecologie, Université Libre de Bruxelles, CP 160/12, 50 Av. F. Roosevelt, 1050, Brussels, Belgium

    Franck K. Monthe, Jérôme Duminil & Olivier J. Hardy

  2. DIADE, IRD, Univ Montpellier, 911 Avenue Agropolis, BP 64501, 34394, Montpellier, France

    Jérôme Duminil

  3. Forest Genetic Resources and Restoration Programme, Sub-Regional Office for Central Africa, Bioversity International, Messa, P.O. Box 2008, Yaoundé, Cameroon

    Jérôme Duminil

  4. Wood Biology Service, Royal Museum for Central Africa, Leuvensesteenweg 13, 3080, Tervuren, Belgium

    Emmanuel Kasongo Yakusu, Hans Beeckman & Nils Bourland

  5. Laboratory of Wood Technology, Ghent University, Coupure Links 653, 9000, Ghent, Belgium

    Emmanuel Kasongo Yakusu

  6. Faculté de Gestion des Ressources Naturelles Renouvelables, Université de Kisangani, B.P.: 2012, Avenue Kitima, 3, Kisangani, Democratic Republic of the Congo

    Emmanuel Kasongo Yakusu

  7. Center For International Forestry Research, Situ Gede, Bogor Barat, 16115, Indonesia

    Nils Bourland

  8. Resources and Synergies Development Pte Ltd, Raffles Quay 33-03, Singapore, 048581, Singapore

    Nils Bourland

  9. TERRA Teaching and Research Centre, Central African Forests, BIOSE Department, Gembloux Agro-Bio Tech, Université de Liège, 2 Passage des Déportés, 5030, Gembloux, Belgium

    Jean-Louis Doucet

  10. Botanic Garden Meise, Nieuwelaan 38, 1860, Meise, Belgium

    Marc S. M. Sosef

Authors
  1. Franck K. Monthe
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jérôme Duminil
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emmanuel Kasongo Yakusu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hans Beeckman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Nils Bourland
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jean-Louis Doucet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marc S. M. Sosef
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olivier J. Hardy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Franck K. Monthe.

Additional information

Communicated by Y. Tsumura

Compliance with ethical standards

ESM 1

(DOCX 852 kb)

Appendix

Appendix

Table 5 Morphological characters differentiating Entandrophragma species as reported by Liben and Dechamps (1966) and by de Wilde (2015)
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Monthe, F.K., Duminil, J., Kasongo Yakusu, E. et al. The African timber tree Entandrophragma congoense (Pierre ex De Wild.) A.Chev. is morphologically and genetically distinct from Entandrophragma angolense (Welw.) C.DC. Tree Genetics & Genomes 14, 66 (2018). https://doi.org/10.1007/s11295-018-1277-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-018-1277-6

Keywords

Search

Navigation