Article | Published:

A pantropically introduced tree is followed by specific ectomycorrhizal symbionts due to pseudo-vertical transmission

The ISME Journalvolume 12pages18061816 (2018) | Download Citation


Global trade increases plant introductions, but joint introduction of associated microbes is overlooked. We analyzed the ectomycorrhizal fungi of a Caribbean beach tree, seagrape (Coccoloba uvifera, Polygonacaeae), introduced pantropically to stabilize coastal soils and produce edible fruits. Seagrape displays a limited symbiont diversity in the Caribbean. In five regions of introduction (Brazil, Japan, Malaysia, Réunion and Senegal), molecular barcoding showed that seagrape mostly or exclusively associates with Scleroderma species (Basidiomycota) that were hitherto only known from Caribbean seagrape stands. An unknown Scleroderma species dominates in Brazil, Japan and Malaysia, while Scleroderma bermudense exclusively occurs in Réunion and Senegal. Population genetics analysis of S. bermudense did not detect any demographic bottleneck associated with a possible founder effect, but fungal populations from regions where seagrape is introduced are little differentiated from the Caribbean ones, separated by thousands of kilometers, consistently with relatively recent introduction. Moreover, dry seagrape fruits carry Scleroderma spores, probably because, when drying on beach sand, they aggregate spores from the spore bank accumulated by semi-hypogeous Scleroderma sporocarps. Aggregated spores inoculate seedlings, and their abundance may limit the founder effect after seagrape introduction. This rare pseudo-vertical transmission of mycorrhizal fungi likely contributed to efficient and repeated seagrape/Scleroderma co-introductions.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1.

    Boivin N, Petraglia M, Crassard R. Human dispersal and species movement. New York: Cambridge University Press; 2017.

  2. 2.

    Bradley BA, Blumenthal DM, Early R, Grosholz ED, Lawler JJ, Miller LP, et al. Global change, global trade, and the next wave of plant invasions. Front Ecol Env. 2012;10:20–28.

  3. 3.

    Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, et al. Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol. 2013;28:58–66.

  4. 4.

    Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett. 2011;14:702–8.

  5. 5.

    Dickie IA, Bufford JL, Cobb RC, Desprez-Loustau M-L, Grelet G, Hulme PE, et al. The emerging science of linked plant–fungal invasions. New Phytol. 2017;215:1314–32.

  6. 6.

    Mallon CA, van Elsas JD, Salles JF. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol. 2015;23:719–29.

  7. 7.

    Van der Putten WH, Klironomos JN, Wardle DA. Microbial ecology of biological invasions. ISME J. 2007;1:28.

  8. 8.

    Gladieux P, Feurtey A, Hood ME, Snirc A, Clavel J, Dutech C, et al. The population biology of fungal invasions. Mol Ecol. 2015;24:1969–86.

  9. 9.

    Dickie IA, Bolstridge N, Cooper JA, Peltzer DA. Co-invasion by Pinus and its mycorrhizal fungi. New Phytol. 2010;187:475–84.

  10. 10.

    Traveset A, Richardson DM. Mutualistic interactions and biological invasions. Ann Rev Ecol Evol Syst. 2014;45:89–113.

  11. 11.

    Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, et al. The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett. 2006;9:501–15.

  12. 12.

    Van der Heijden MGA, Martin F, Selosse M-A, Sanders I. Mycorrhizal ecology and evolution: the past, the present and the future. New Phytol. 2015;205:1406–23.

  13. 13.

    Rivera Y, Kretzer AM, Horton TR. New microsatellite markers for the ectomycorrhizal fungus Pisolithus tinctorius sensu stricto reveal the genetic structure of US and Puerto Rican populations. Fungal Ecol. 2015;13:1–9.

  14. 14.

    Selosse M-A, Jacquot D, Bouchard D, Martin F, Le Tacon F. Temporal persistence and spatial distribution of an American inoculant strain of the ectomycorrhizal basidiomycete Laccaria bicolor in a French forest plantation. Mol Ecol. 1998;7:561–73.

  15. 15.

    Vellinga EC, Wolfe BE, Pringle A. Global patterns of ectomycorrhizal introductions. New Phytol. 2009;181:960–73.

  16. 16.

    Pringle A, Adams RI, Cross HB, Bruns TD. The ectomycorrhizal fungus Amanita phalloides was introduced and is expanding its range on the west coast of North America. Mol Ecol. 2009;18:817–33.

  17. 17.

    Hayward J, Horton TR, Pauchard A, Nunez MA. A single ectomycorrhizal fungal species can enable a Pinus invasion. Ecology. 2015;96:1438–44.

  18. 18.

    Nuñez MA, Horton TR, Simberloff D. Lack of belowground mutualisms hinders Pinaceae invasions. Ecology. 2009;90:2352–9.

  19. 19.

    Gazol A, Zobel M, Cantero JJ, Davison J, Esler KJ, Jairus T, et al. Impact of alien pines on local arbuscular mycorrhizal fungal communities—evidence from two continents. FEMS Microbiol Ecol. 2016;92:fiw073.

  20. 20.

    Remigi P, Faye A, Kane A, Deruaz M, Thioulouse J, Cissoko M, et al. The exotic legume tree species Acacia holosericea alters microbial soil functionalities and the structure of the arbuscular mycorrhizal community. Appl Env Microbiol. 2008;74:1485–93.

  21. 21.

    Nunez MA, Dickie IA. Invasive belowground mutualists of woody plants. Biol Invasions. 2014;16:645–61.

  22. 22.

    Bogar LM, Dickie IA, Kennedy PG. Testing the coinvasion hypothesis: ectomycorrhizal fungal communities on Alnus glutinosa and Salix fragilis in New Zealand. Divers Distrib. 2015;21:268–78.

  23. 23.

    Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H, et al. Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeo. 2011;38:1305-17.

  24. 24.

    Tedersoo L, Suvi T, Beaver K, Kõljalg U. Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytol. 2007;175:321-33.

  25. 25.

    Jairus T, Mpumba R, Chinoya S, Tedersoo L. Invasion potential and host shifts of Australian and African ectomycorrhizal fungi in mixed eucalypt plantations. New Phytol. 2011;192:179–87.

  26. 26.

    Bahram M, Koljalg U, Kohout P, Mirshahvaladi S, Tedersoo L. Ectomycorrhizal fungi of exotic pine plantations in relation to native host trees in Iran: evidence of host range expansion by local symbionts to distantly related host taxa. Mycorrhiza. 2013;23:11–19.

  27. 27.

    Moeller HV, Dickie IA, Peltzer DA, Fukami T. Mycorrhizal co-invasion and novel interactions depend on neighborhood context. Ecology. 2015;96:2336–47.

  28. 28.

    Diez J. Invasion biology of Australian ectomycorrhizal fungi introduced with eucalypt plantations into the Iberian Peninsula. Biol Invasions. 2005;7:3–15.

  29. 29.

    Ducousso M, Duponnois R, Thoen D, Prin Y. Diversity of ectomycorrhizal fungi associated with Eucalyptus in Africa and Madagascar. Int J Res. 2012;2012:450715.

  30. 30.

    Põlme S, Bahram M, Kõljalg U, Tedersoo L. Biogeography and specificity of ectomycorrhizal fungi of Coccoloba uvifera. In: Tedersoo L, editor. Biogeography of mycorrhizal symbiosis. Berlin: Springer; 2017. p. 345–59.

  31. 31.

    Tedersoo L, May TW, Smith ME. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza. 2010;20:217–63.

  32. 32.

    Séne S, Avril R, Chaintreuil C, Geoffroy A, Ndiaye C, Diédhiou AG, et al. Ectomycorrhizal fungal communities of Coccoloba uvifera (L.) L. mature trees and seedlings in the neotropical coastal forests of Guadeloupe (Lesser Antilles). Mycorrhiza. 2015;25:547–59.

  33. 33.

    Howard RA. Studies in the genus Coccoloba, X. New species and a summary distribution in South America. J Arn Arbor. 1961;42:87–95.

  34. 34.

    Bâ AM, McGuire KL, Diédhiou AG. Ectomycorrhizal symbioses in tropical and neotropical forests. Boca Raton: CRC Press; 2014.

  35. 35.

    Séne S. Analyse de la diversité ectomycorhizienne du Coccoloba uvifera en zone d’origine et en zone d’introduction. PhD thesis, Université Antilles-Guyane, Pointe-à-Pitre, France; 2015.

  36. 36.

    Wilson AW, Binder M, Hibbett DS. Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytol. 2012;194:1079–95.

  37. 37.

    Richard F, Millot S, Gardes M, Selosse M-A. Diversity and structuration by hosts of the below-ground mycorrhizal community in an old-growth Mediterranean forest dominated by Quercus ilex L. New Phytol. 2005;166:1011–23.

  38. 38.

    Rousset F. Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol Ecol Res. 2008;8:103–6.

  39. 39.

    Garza JC, Williamson EG. Detection of reduction in population size using data from microsatellite loci. Mol Ecol. 2001;10:305–18.

  40. 40.

    Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–59.

  41. 41.

    Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res. 2010;10:564–7.

  42. 42.

    Koljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, et al. UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol. 2005;166:1063–8.

  43. 43.

    Ebenye HCM, Taudière A, Niang N, Ndiaye C, Sauve M, Awana ON, et al. Ectomycorrhizal fungi are shared between seedlings and adults in a monodominant Gilbertiodendron dewevrei rain forest in Cameroon. Biotropica. 2017;49:256–67.

  44. 44.

    Bandou E, Lebailly F, Muller F, Dulormne M, Toribio A, Chabrol J, et al. The ectomycorrhizal fungus Scleroderma bermudense alleviates salt stress in seagrape (Coccoloba uvifera L.) seedlings. Mycorrhiza. 2006;16:559–65.

  45. 45.

    Bechem EET, Alexander IJ. Mycorrhiza status of Gnetum spp. in Cameroon: evaluating diversity with a view to ameliorating domestication efforts. Mycorrhiza. 2012;22:99–108.

  46. 46.

    Tedersoo L, Põlme S. Infrageneric variation in partner specificity: multiple ectomycorrhizal symbionts associate with Gnetum gnemon (Gnetophyta) in Papua New Guinea. Mycorrhiza. 2012;22:663–8.

  47. 47.

    Douglas AE, Werren JH. Holes in the hologenome: why host-microbe symbioses are not holobionts. MBio. 2016;7:e02099–15.

  48. 48.

    Selosse M-A, Richard F, He X, Simard SW. Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol. 2006;21:621–8.

  49. 49.

    Wilkinson DM. The role of seed dispersal in the evolution of mycorrhizae. Oikos. 1997;78:394–6.

  50. 50.

    Taschen E, Rousset F, Sauve M, Benoît L, Dubois M-P, Richard F, et al. How the truffle got its mate: insights from genetic structure in spontaneous and managed Mediterranean populations of Tuber melanosporum. Molr Ecol. 2016;25:5611–27.

  51. 51.

    Vincenot L, Selosse M-A. Population biology and ecology of ectomycorrhizal fungi. In: Tedersoo L, editor. Biogeography of mycorrhizal symbiosis. Berlin: Springer; 2017. p. 39–59.

  52. 52.

    Douglas AE. Conflict, cheats and the persistence of symbioses. New Phytol. 2008;177:849–58.

  53. 53.

    Sachs JL, Wilcox TP. A shift to parasitism in the jellyfish symbiont Symbiodinium microadriaticum. Proc R Soc Lond B. 2006;273:425–9.

  54. 54.

    Ramadhani I, Sukarno N, Listiyowati S. Basidiospores attach to the seed of Shorea leprosula in lowland tropical dipterocarp forest and form functional ectomycorrhiza on seed germination. Mycorrhiza. 2017.

  55. 55.

    Rousset F. Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics. 1997;145:1219–28.

  56. 56.

    Slatkin M. Isolation by distance in equilibrium and non‐equilibrium populations. Evolution. 1993;47:264–79.

  57. 57.

    McGuire KL. Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology. 2007;88:567–74.

  58. 58.

    Bever JD, Mangan SA, Alexander HM. Maintenance of plant species diversity by pathogens. Ann Rev Ecol Evol Syst. 2015;46:305–25.

  59. 59.

    Nei M. Molecular evolutionary genetics. New York: Columbia University Press; 1987.

  60. 60.

    Dickie IA, Bennett BM, Burrows LE, Nuñez MA, Peltzer DA, Porté A, et al. Conflicting values: ecosystem services and invasive tree management. Biol Invasions. 2014;16:705–19.

  61. 61.

    Hulme PE. Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol. 2009;46:10–18.

Download references


We thank three referees for revisions, David Marsh for English corrections, and the Service de Systématique Moléculaire (UMS2700 MNHN/CNRS) for its facilities. Seynabou Séne received grants from the Guadeloupe Region, Institut de Recherche pour le Développement, Ministry of Education and Research of Senegal, World Federation of Scientists, and the Laboratoire Mixte International-Adaptation des Plantes et microorganismes associés aux Stress Environnementaux (Dakar).

Author information

Author notes

  1. These authors contributed equally: Seynabou Séne, Marc-André Selosse, Amadou Bâ.


  1. LMI-LAPSE/Laboratoire Commun de Microbiologie, IRD/UCAD/ISRA, BP 1386, Dakar, Senegal

    • Seynabou Séne
    • , Khoudia Cissé
    • , Abdala Gamby Diédhiou
    •  & Samba Ndao Sylla
  2. Institut de Systématique, Évolution, Biodiversité (UMR 7205 – CNRS, MNHN, UPMC, EPHE), Muséum National d’Histoire Naturelle, Sorbonne Universités, 57 rue Cuvier, 75005, Paris, France

    • Seynabou Séne
    • , Marc-André Selosse
    • , Mathieu Forget
    •  & Josie Lambourdière
  3. Faculty of Biology, Department of Plant Taxonomy and Nature Conservation, University of Gdańsk, Wita Stwosza 59, 80-308, Gdansk, Poland

    • Marc-André Selosse
  4. Departamento de Biología, Universidad de Puerto Rico, Parque Industrial Minillas Carr 174, Bayamón, PR, 00959-1911, USA

    • Elsie Rivera-Ocasio
  5. Université de La Réunion, 15 Av. R. Cassin CS 92003, 97744, Saint-Denis, Réunion, France

    • Hippolyte Kodja
  6. Faculty of Agriculture, University of the Ryukyus, 1 Senbaru, Nishihara, Okinawa, 903-0213, Japan

    • Norikazu Kameyama
  7. Graduate School of Frontier Science, University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8563, Japan

    • Kazuhide Nara
  8. Normandie Univ, UNIROUEN, IRSTEA, ECODIV, 76000, Rouen, France

    • Lucie Vincenot
  9. Laboratoire C3MAG, Université des Antilles, BP 592, 97159, Pointe-à-Pitre, Guadeloupe, France

    • Jean-Louis Mansot
  10. Pusat Asasi Sains Pertanian, Universiti Putra Malaysia, 43400 UPM, Serdang, Malaysia

    • Jean Weber
  11. Laboratoire Evolution et Diversité Biologique, Université Paul Sabatier – CNRS, 118 route de Narbonne, 31062, Toulouse Cedex, France

    • Mélanie Roy
  12. Laboratoire de Biologie et Physiologie Végétales, Université des Antilles, BP 592, 97159, Pointe-à-Pitre, France

    • Amadou Bâ
  13. Laboratoire des Symbioses Tropicales et Méditerranéennes, UMR113 INRA/AGRO-M/CIRAD/IRD/UM2-TA10/J, Campus International de Baillarguet, 34398, Montpellier Cedex 5, France

    • Amadou Bâ


  1. Search for Seynabou Séne in:

  2. Search for Marc-André Selosse in:

  3. Search for Mathieu Forget in:

  4. Search for Josie Lambourdière in:

  5. Search for Khoudia Cissé in:

  6. Search for Abdala Gamby Diédhiou in:

  7. Search for Elsie Rivera-Ocasio in:

  8. Search for Hippolyte Kodja in:

  9. Search for Norikazu Kameyama in:

  10. Search for Kazuhide Nara in:

  11. Search for Lucie Vincenot in:

  12. Search for Jean-Louis Mansot in:

  13. Search for Jean Weber in:

  14. Search for Mélanie Roy in:

  15. Search for Samba Ndao Sylla in:

  16. Search for Amadou Bâ in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Marc-André Selosse.

Electronic supplementary material

About this article

Publication history