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Reproductive isolation, gene flow and speciation in the former Coffea subgenus: a review

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The former Coffea subgenus is a species complex showing qualitative gene flow and reproductive barriers between species. Such qualitative gene flow allowed its evolution over time, particularly during the successive forest expansion-regression cycles in relation with glaciation periods.

Abstract

The present paper reviews the main botanical, geographical and genetic characteristics of the Coffea genus and then focuses on the former Coffea subgenus. Its broad distribution in Africa, Madagascar and Mascarene Islands is related to the high diversity of ecological situations. The importance of sympatry and parapatry cases and their role on gene flow possibilities between species is then underlined in the paper. Such gene flow is nevertheless partially limited by reproductive barriers: flowering date, frequency of hybrid F1 emergence, as well as the vigor and fertility of such hybrids. When hybridization occurs, distortion of segregation and disruptive selection would allow qualitative flow of non-adaptative genes, thus limiting the effect of genetic drift in small populations. The last part of the paper defines the notion of metaspecies in the case of the former Coffea by extension of the concept of metapopulation to species. The evolution over time of a metaspecies is finally discussed in relation with sympatry situations, gene flow possibilities and forest fragmentation.

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Notes

  1. Few 3-ovulated flowers occurs in some species as C. arabica and C. heterocalyx Stoff.

References

  • Anhuf D, Ledru MP, Behling H (2006) Paleo-environmental change in Amazonian and African rain forest during the LGM. Paleogeo Paleoclim Paleoecol 239:510–527

    Article  Google Scholar 

  • Anthony F (1992) Les ressources génétiques des caféiers : collecte, gestion d’un conservatoire et évaluation de la diversité génétique. TDM n°81, ORSTOM, Paris

  • Anthony F, Couturon E, De Namur C (1985) Les caféiers sauvages du Cameroun: résultats d’une mission de prospection effectuée par l’ORSTOM en 1983. Proc Int Congr ASIC 11:495–505

    Google Scholar 

  • Anthony F, Berthaud J, Guillaumet JL, Lourd M (1987) Collecting wild Coffea species in Kenya and Tanzania. Pl Genet Res Newslett 69:23–29

    Google Scholar 

  • Anthony F, Diniz LEC, Combes MC, Lashermes P (2010) Adaptive radiation in Coffea subgenus Coffea L. (Rubiaceae) in Africa and Madagascar. Pl Syst Evol 285:51–64

    Article  Google Scholar 

  • Anthony F, Bertrand B, Etienne H, Lashermes P (2011) Coffea and Psilanthus. In: Kole C (ed) Wild crop relatives: Genomic and breeding resources, vol 9., Plantation and ornemental cropsSpringer, Berlin, pp 41–61

    Chapter  Google Scholar 

  • Berthaud J (1983) Liste de matériel des prospections de Côte-d’Ivoire (mise à jour : juin 1983). ORSTOM, Adiopodoumé, Côte d’Ivoire

  • Berthaud J (1985) Gene flow and population structure in Coffea canephora coffee populations in Africa. In: Jacquard P, Heim G, Antonovics J (eds) Genetic differentiation and dispersal in plants. Springer-Verlag, Berlin Heidelberg, pp 355–366

    Chapter  Google Scholar 

  • Berthaud J, Guillaumet JL (1978) Les caféiers sauvages en Centrafrique. Résultats d’une mission de prospection (Janvier-février 1975). Café Cacao Thé 22:171–186

    Google Scholar 

  • Berthaud J, Anthony F, Lourd M (1983) Les caféiers sauvages de Tanzanie. Résultats d’une mission de prospection effectuée du 5 mars au 11 avril 1982. Café Cacao Thé 27:245–258

    Google Scholar 

  • Berthaud J, Anthony F, Charrier A, Couturon E, Le Pierres D, Louarn J (1989) Les caféiers en Afrique: diversité génétique et amélioration des plantes. Bull Soc Bot Fr 136:239–250

    Google Scholar 

  • Bettencourt AJ (1973) Consideraçoes gerais sobre o ‘Hibrido de Timor’. Instituto Agronomico de Campinas, Campinas

    Google Scholar 

  • Bouharmont J (1963) Somatic chromosomes of some Coffea species. Euphytica 12:254–257

    Google Scholar 

  • Bremer B, Jansen RK (1991) Comparative restriction site mapping of chloroplast DNA implies new phylogenetic relationships within Rubiaceae. Am J Bot 78:198–213

    Article  CAS  Google Scholar 

  • Bridson DM (1982) Studies in Coffea and Psilanthus (Rubiaceae subfam. Cinchonoideae) for Part 2 of’ Flora of Tropical East Africa’: rubiaceae. Kew Bull 36:817–859

    Article  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Micoene/Pliocene boundary. Nature 389:153–158

    Article  CAS  Google Scholar 

  • Charrier A (1976) La structure génétique des caféiers spontanés de la région malgache (Mascarocoffea). Leurs relations avec les caféiers d’origine africaine (Eucoffea). Mémoires n°87, ORSTOM, Paris

  • Chevalier A (1947) Les caféiers du globe, fasc. 3. Systématique des caféiers et faux-caféiers. Maladies et insectes nuisibles. Lechevallier, Paris

  • Coulibaly I, Noirot M, Lorieux M, Charrier A, Hamon S, Louarn J (2002) Introgression of self-compatibility from Coffea heterocalyx to the cultivated species C. canephora. Theor Appl Genet 105:994–999

    Article  CAS  PubMed  Google Scholar 

  • Coulibaly I, Louarn J, Lorieux M, Charrier A, Hamon S, Noirot M (2003a) Pollen viability restoration in a Coffea canephora P. and C. heterocalyx Stoffelen backcross. QTL identification for marker-assisted selection. Theor Appl Genet 106:311–316

    CAS  PubMed  Google Scholar 

  • Coulibaly I, Revol B, Noirot M, Poncet V, Lorieux M, Carasco-Lacombe C, Minier J, Dufour M, Hamon P (2003b) AFLP and SSR polymorphism in a Coffea interspecific backcross progeny [(C. heterocalyx × C. canephora) × C. canephora]. Theor Appl Genet 107:1148–1155

    Article  CAS  PubMed  Google Scholar 

  • Couturon E, Lashermes P, Charrier A (1998) First intergeneric hybrids (Psilanthus ebracteolatus Hiern × Coffea arabica L.) in coffee trees. Can J Bot 76:542–546

    Google Scholar 

  • Cramer PJS (1957) Review of literature of coffee research in Indonesia. FL Wellman, Turrialba, Costa Rica

  • Cros J, Combes MC, Trouslot P, Anthony F, Hamon S, Charrier A, Lashermes P (1998) Phylogenetic analysis of chloroplast DNA variation in Coffea L. Mol Phylogenet Evol 9:109–117

    Article  CAS  PubMed  Google Scholar 

  • Crosby JL (1970) The evolution of genetic discontinuity: computer models of the selection of barriers to interbreeding between species. Heredity 25:253–297

    Article  Google Scholar 

  • Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Mol Ecol 10:1075–1086

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1859) The origin of species by means of natural selection. Murray, London

    Google Scholar 

  • Davis AP, Rakotonasolo F (2008) A taxonomic revision of the Baracoffea alliance: nine remarkable Coffea species from westerm Madagascar. Bot J Linn Soc 154:355–390

    Article  Google Scholar 

  • Davis AP, Bridson M, Rakotonasolo F (2005) A reexamination of Coffea subgenus Baracoffea and comments on the morphology and classification of Coffea and Psilanthus (Rubiaceae-Coffeeae). In: Keating RC, Hollowell V, Croat TB (eds) A Festschrift for William G. D’Arcy: the legacy of a taxonomist. (Monographs in systematic botany from the Missouri Botanical Garden 104, Missouri Botanical Garden, St. Louis, Missouri, pp 399–420

  • Davis AP, Govaerts R, Bridson D, Stoffelen P (2006) An annotated conspectus of the genus Coffea (Rubiaceae). Bot J Linn Soc 152:465–512

    Article  Google Scholar 

  • Davis AL, Tosh J, Rush N, Fay MF (2011) Growing coffee: Psilanthus (Rubiaceae) subsumed on the basis of molecular and morphological data; implications for the size, morphology, distribution and evolutionary history of Coffea. Bot J Linn Soc 167:357–377

    Article  Google Scholar 

  • De Namur C, Couturon E, Sita P, Anthony F (1987) Résultats d’une mission de prospection des caféiers sauvages du Congo. Proc Int Congr ASIC 12:397–404

    Google Scholar 

  • Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature 400:354–357

    Article  CAS  PubMed  Google Scholar 

  • Dulloo ME, Maxted N, Guarino L, Florens D, Newbury HJ, Ford Lloyd BV (1999) Ecogeographic survey of the genus Coffea in the Mascarene islands. Bot J Linn Soc 131:263–284

    Article  Google Scholar 

  • Elenga H, Peyron O, Bonnefille R, Jolly D, Cheddadi R, Guiot J et al (2000) Pollen-based biome reconstruction for southern Europe and Africa 18,000 yr BP. J Biogeogr 27:621–634

    Article  Google Scholar 

  • Faria R, Navarro A (2010) Chromosomal speciation revisited: rearranging theory with species of evidence. Trends Ecol Evol 25:660–669

    Article  PubMed  Google Scholar 

  • Gavrilets S, Vose A, Barluenga M, Salzburger W, Meyer A (2007) Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake. Mol Ecol 16:2893–2909

    Article  PubMed  Google Scholar 

  • Gomez C, Batti H, Le Pierres D, Campa C, Hamon S, De Kochko A et al (2010) Favourable habitats for Coffea inter-specific hybridization in central New Caledonia: combined genetic and spatial analyses. J Appl Ecol 47:85–95

    Article  CAS  Google Scholar 

  • Grant V (1977) Organismic evolution. WH Freeman & Co, San Francisco

    Google Scholar 

  • Hamilton AC (1975) The dispersal of forest species in Uganda during the Upper Pleistocene. Boissiera 24:29–32

    Google Scholar 

  • Hiern WP (1877) Psilanthus. In: Oliver D (ed) Flora of tropical Africa, vol 3. Reeve L & Co, Ashford, pp 185–187

    Google Scholar 

  • King M (1993) Species evolution. The role of chromosome change. Cambridge University Press, United Kingdom

    Google Scholar 

  • Kirkpatrick M, Barton N (2006) Chromosome inversion, local adaptation and speciation. Genetics 173:419–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kondrashov AS, Kondrashov FA (1999) Interactions among quantitative traits in the course of sympatric speciation. Nature 400:351–354

    Article  CAS  PubMed  Google Scholar 

  • Krug CA, Carvalho A (1951) The genetics of Coffea. Adv Genet 4:127–158

    Article  CAS  PubMed  Google Scholar 

  • Krug CA, Mendes AJT (1940) Cytological observations in Coffea. J Genet 39:189–203

    Article  Google Scholar 

  • Ky CL, Barre P, Lorieux M, Trouslot P, Akaffou S, Louarn J et al (2000) Interspecific genetic linkage map, segregation distortion and genetic conversion in coffee (Coffea sp.). Theor Appl Genet 101:669–676

    Article  CAS  Google Scholar 

  • Lashermes P, Combes MC, Trouslot P, Charrier A (1997) Phylogenetic relationships of coffee-tree species (Coffea L.) as inferred from ITS sequences of nuclear ribosomal DNA. Theor Appl Genet 95:947–955

    Article  Google Scholar 

  • Lashermes P, Combes MC, Robert J, Trouslot P, D’Hont A, Anthony F, Charrier A (1999) Molecular characterisation and origin of the Coffea arabica L. genome. Mol Gen Genet 261:259–266

    Article  CAS  PubMed  Google Scholar 

  • Lashermes P, Combes MC, Prakash NS, Trouslot P, Lorieux M, Charrier A (2001) Genetic linkage map of Coffea canephora: effect of segregation distortion and analysis of recombination rate and female meiosis. Genome 44:589–596

    Article  CAS  PubMed  Google Scholar 

  • Leroy JF (1961) Sur deux caféiers remarquables de la forêt sèche du Sud-Ouest de Madagascar (C. Humbertii JF Ler. et C. Capuronii JF Ler.). Coffea. C R Acad Sci Paris 252:2285–2287

    Google Scholar 

  • Leroy JF (1967) Recherches sur les caféiers. Sur la classification biologique des caféiers et sur l’origine et l’aire du genre Coffea. C R Acad Sci Paris 265:1043–1045

    Google Scholar 

  • Leroy JF, Plu A (1966) Sur les nombres chromosomiques des caféiers malgaches. Café Cacao Thé 10:216–218

    Google Scholar 

  • Levins R (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull Entom Soc Amer 71:237–240

    Article  Google Scholar 

  • Louarn J (1972) Introduction à l’étude génétique des Mascarocoffea: nouvelles déterminations de leurs nombres chromosomiques. Café Cacao Thé 16:312–316

    Google Scholar 

  • Louarn J (1975) Hybrides interspécifiques entre Coffea canephora Pierre et C. eugenioides Moore. Café Cacao Thé 20:33–52

    Google Scholar 

  • Louarn J (1992) La fertilité des hybrides interspécifiques et les relations génomiques entre caféiers diploïdes d’origine africaine (Genre Coffea L. sous-genre Coffea). Thesis, Paris-Sud University

  • Mahé L, Le Pierrès D, Combes MC, Lashermes P (2007) Introgressive hybridization between the allotetraploid Coffea arabica and one of its diploid ancestors, C. coffea canephora, in an exceptional sympatric zone in New Caledonia. Genome 50:316–324

    Article  PubMed  Google Scholar 

  • Maley J (1987) Fragmentation de la forêt dense humide africaine et extension des biotopes montagnards au quaternaire récent: nouvelles données polliniques et chronologiques. Implications paléoclimatiques et biogéographiques. Palaeoecol Afr Surround Isl 18:307–334

    Google Scholar 

  • Maley J (1991) The African rain forest vegetation and paleoenvironments during late quaternary. Clim Change 19:79–98

    Article  Google Scholar 

  • Mather K (1955) Polymorphism as an outcome of disruptive selection. Evolution 9:52–61

    Article  Google Scholar 

  • Maurin O, Davis AP, Chester M, Mvungi EF, Jaufeerally-Fakim Y, Fay MF (2007) Towards a phylogeny for Coffea (Rubiaceae): identifying well-supported lineages based on nuclear and plastid DNA sequences. Ann Bot 100:1565–1583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maynard Smith J (1966) Sympatric speciation. Am Nat 100:637–650

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347:550–553

    Article  CAS  PubMed  Google Scholar 

  • Meyer A, Knowles LL, Verheyen E (1996) Widespread geographical distribution of haplotypes in rock-dwelling cichlid fishes from Lake Tanganyika. Mol Ecol 5:341–350

    Article  CAS  PubMed  Google Scholar 

  • N’Diaye A, Poncet V, Louarn J, Hamon S, Noirot M (2005) Genetic differentiation between Coffea liberica var liberica and C. liberica var Dewevrei. Comparison with C. canephora. Pl Syst Evol 253:95–104

    Article  Google Scholar 

  • N’Diaye A, Noirot M, Hamon S, Poncet V (2007) Genetic basis of species differentiation between Coffea liberica Hiern and C. canephora Pierre: analysis of an interspecific cross. Genet Res Crop Evol 54:1011–1021

    Article  Google Scholar 

  • Navarro A, Barton NH (2003a) Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447–459

    Article  PubMed  Google Scholar 

  • Navarro A, Barton NH (2003b) Chromosomal speciation and molecular divergence-accelerated evolution in rearranged chromosomes. Science 300:321–324

    Article  CAS  PubMed  Google Scholar 

  • Ornduff R (1969) Reproductive biology in relation to systematics. Taxon 18:121–244

    Article  Google Scholar 

  • Pernès J (1984) Gestion des ressources génétiques. Tome 2: Manuel. Lavoisier, Paris

  • Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer K (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164

    Article  CAS  Google Scholar 

  • Portères R (1946) Action de l’eau après une période sèche sur le déclenchement de la floraison chez Coffea arabica L. Agron Trop 3:148–158

    Google Scholar 

  • Savolainen V, Anstett MC, Lexer C, Hutton I, Clarkson JJ, Norup MV et al (2006) Sympatric speciation in palms on an oceanic island. Nature 441:210–213

    Article  CAS  PubMed  Google Scholar 

  • Seehausen O, Butlin RK, Keller I, Wagner CE, Boughman JW, Hohenlohe PA et al (2014) Genomics and the origin of species. Nature Rev Genet 15:176–192

    Article  CAS  PubMed  Google Scholar 

  • Stam P (1983) The evolution of reproductive isolation in closely adjacent plant populations through differential flowering time. Heredity 50:105–118

    Article  Google Scholar 

  • Stebbins GL (1967) Variation and evolution in plants. Columbia University Press, New York

    Google Scholar 

  • Stoffelen P (1998) Coffea and Psilanthus in tropical Africa: a systematic and palynological study, including a revision of the West and Central African species. Thesis, Katholieke Universiteit, Leuven

  • Stoffelen P, Noirot M, Couturon E, Bontems S, De Block P, Anthony F (2009) Coffea anthonyi, a self-compatible Central African coffee species, closely related to an ancestor of C. arabica L. Taxon 58:133–140

    Google Scholar 

  • Thoday JM, Boam TB (1959) Effects of disruptive selection. II. Polymorphism and divergence without isolation. Heredity 13:205–218

    Google Scholar 

  • Thoday JM, Gibson JB (1962) Isolation by disruptive selection. Nature 193:1164–1166

    Article  CAS  PubMed  Google Scholar 

  • Thomas AS (1944) The wild coffees of Uganda. Emp J Exp Agri 12:1–12

    Google Scholar 

  • Tregenza T, Butlin RK (1999) Speciation without isolation. Nature 400:311–312

    Article  CAS  PubMed  Google Scholar 

  • White MJD (1978) Modes of speciation. WH Freeman & Co, San Francisco

    Google Scholar 

  • White F (1983) The vegetation of Africa. Unesco, Paris

    Google Scholar 

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Acknowledgments

We thank M. Georges Rizet, Professor of Genetics at the Paris XI University (dead in 2005), without which most of Coffea genetic resources would not exist today. We also thank referees for their relevant remarks.

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Authors and Affiliations

  1. UMR RPB, IRD-Centre de Montpellier, 34000, Montpellier, France

    Michel Noirot & François Anthony

  2. Montpellier-SUPAGRO, 2 place Pierre Viala, 34060, Montpellier Cedex 2, France

    André Charrier

  3. National Botanic Garden of Belgium, Domein van Bouchout, B-1860, Meise, Belgium

    Piet Stoffelen

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  1. Michel Noirot
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  2. André Charrier
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  4. François Anthony
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Correspondence to Michel Noirot.

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Noirot, M., Charrier, A., Stoffelen, P. et al. Reproductive isolation, gene flow and speciation in the former Coffea subgenus: a review. Trees 30, 597–608 (2016). https://doi.org/10.1007/s00468-015-1335-8

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