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Symbiotique (Termitomyces Spp.) ~ REPUBLIQUE DE CÔTE D'IVOIRE 6/,_6uo1b - &tMJâ11,0 - ~ Ministère de 1 'Enseignement Supérieur et de 1a Recherche Scientifique Université NANGUI ABROGOUA UFR des Sciences de la Nature Laboratoire de Biologie et Cytologie Animales THESE UNIQUE DE DOCTORAT DE L'UNIVERSITE NANGUI ABROGOUA en Gestion et Valorisation des Ressources Naturelles (GVRN) Spécialité: Biodiversité et Gestion Durable des Écosystèmes (BGDE) Présentée par M. KONE N'GOLO ABDOULA YE THÈME: SYMBIOSE TERMITE-CHAMPIGNON : origine, co-diversification et déterminisme de la fructification saisonnière du champignon symbiotique (Termitomyces spp.) ~ Mémoire soutenu publiquement le Jeudi 31 Janvier 2013 devant le Jury composé de: M. OTCHOUMOU Atcho Professeur Titulaire Président M. KONATE Souleymane Maître de Conférences Directeur de Thèse M. KOUASSI Kouassi Philippe Professeur Titulaire Rapporteur M. KONE Daouda Maître de Conférences Rapporteur M BAKAY OKO Adama Maître de Conférences Examinateur M. DOUMBIA Mamadou Maître de Conférences Examinateur ------- ----------------------------- • A notre regretté père Barra Be KONE ... • A notre mère Fatoumata OUATTARA ... • A notre oncle N'Golo KONE ... RESUME La symbiose est un facteur clé de l'évolution des espèces. L'évolution est orientée par des phénomènes de coopération, d'interaction et de dépendance mutuelle entre organismes vivants. Cette étude vise principalement à approfondir la compréhension de la symbiose entre les termites de la sous-famille des Macrotermitinae et les champignons du genre Termitomyces, en vue de la domestication du champignon symbiotique. Spécifiquement, elle a pour but de (i) déterminer les facteurs qui gouvernent et déterminent la fructification saisonnière du champignon, (ii) déterminer le centre d'origine de cette symbiose sur le continent africain et (iii) dater la co-diversification des organismes symbiotiques. La diversité et la distribution des fructifications saisonnières de Termitomyces de deux zones phytogéographiques (Centre et Sud) de la Côte d'Ivoire ont été examinées par des fouilles exhaustives et des méthodes standards, aussi bien pour les termites que pour les sporopbores de leurs symbiotes fongiques. Ces données ont ensuite été complétées avec quelques aspects biologiques des termites hôtes. En second lieu, des analyses moléculaires et phylogénétiques ont permis de tester l'hypothèse de la simultanéité des divergences adaptatives majeures au sein des populations de termites et de champignons, à travers une vérification de la théorie octroyant au centre d'origine d'une symbiose la possibilité d'en être le centre de plus grande diversité génétique des partenaires symbiotiques. Enfin, la co-diversification des organismes symbiotiques a été datée à partir d'une reconstruction phylogénétique. Quatre espèces de Termitomyces ont été collectées dont trois observées pour la première fois en Côte d'Ivoire. Seuls les sporophores des symbiotes fongiques des termites adoptant la transmission horizontale de leur Termitomyces ont été observés. La fructification du champignon survient durant les saisons pluvieuses, d'une manière synchronisée avec l'essaimage des imagos ailés des colonies matures et la production des ouvriers des colonies nouvellement établies du termite hôte respectif L'occurrence des sporophores de Termitomyces et l'abondance des termites champignonnistes dans les habitats se sont avérées significativement corrélées à leur richesse spécifique en plantes ligneuses. Il ressort également que les Termitomyces sont un groupe monophylétique reparti en quatre clades selon les genres de termites hôtes. Toutefois, aucune différenciation biogéographique de la diversité et de la distribution des Termitomyces symbiotiques n'a été observée entre termites hôtes et leurs régions de distribution en Afrique. Par contre, avec les termites, une faible diversité totale tmilaire a certes été observée entre les différentes régions, mais elle a été trouvée relativement plus grande en Afrique de l'Ouest. Enfin, la tentative de révision de l'origine de la co• diversification des partenaires symbiotiques a révélée que les termites champignonnistes proviennent effectivement des forêts humides d'Afrique, à partir desquelles ils ont ensuite colonisé les savanes, il y a environ 31 millions d'années. La radiation adaptative des Macrotermitinae s'étant produite en parallèle avec celle de leurs symbiotes fongiques pour les conduire à adopter cette symbiose particulière. Mots clés: Termites champignonnistes, Termitomyces, symbiose, fructification saisonnière, sporophores, essaimage, origine, datation, forêts tropicales afiicaines, cc-diversification, Côte d'Ivoire. ABSTRACT Mutualistic symbiosis has played a major rote in evolution. Througb synergy of combined abilities a mutualistic alliance between two or more species can adapt faster tban individual organism. The mutuaListic symbiosis between fungus-growing termites and the fungi of the genus Termitomyces originated in Africa and shows moderate degree of interaction specificity. The most common and presumably primitive mode of reproduction for the symbiont fungus is to produce basidiocarps on the mounds of the host termite colony. These basidiocarps appear genus-specifically each year at the sarne periods, however only in specific vegetation types while the respective fungus-growing termites are by far wider distributed. ln addition, the exclusive regional biogeographic origin of the symbiosis remind unknown. It is then questionable if: the determination of this exclusive regional center of origin of the syrnbiosis on the African continent could lead to an estimation of the age of the co-evolution of the symbiotic partners? Here we first examined Termitomyces diversity and distribution in two phytogeographic zones (Central and Southern) in Côte d'Ivoire. Data were collected in different habitats in exhaustive searches with standardized methods for termites and basidiocarps as well. The respective findings were complemeoted witb bebavioural and Life cycle data of the associated termite species. Secondly, using molecular and phylogenetic techniques, we test the hypotbesis that the major splits have occurred simultaneously in the host and in the symbiont, through the theory proposing the center of origin of a symbiosis as the center of high diversity of its symbiotic organisms. These results were finally used to update the estimate of the age of the origin of the co-evolution in the mutualistic relationship between termite and Termitomyces. Basidiocarps of four species of Termitomyces were recorded. Three of these species are new records for Côte d'Ivoire. Only those Termitomyces species produced basidiocarps which are associated with termite species that are dependent on horizontal transmission of their fungal symbiont were collected. Termitomyces were observed bearing fruit bodies during rainy seasons. Fructification in the recorded Termitomyces species was found to occur species-specifically after the respective host alates' first swa.rm.ing of mature colonies and the production of first workers in newly established ones. The distribution of the collected fungus-growing termites and their associated fungi were significantly correlated with plant species richness of visited habitats. Monophyletic groups of termites are associated with monophyletic groups of Termitomyces into four main clades. However, there is a lack of geographical differentiation of fungal symbionts diversity and distribution between regions and across host species. In contrast, on the termite side, the low overall mean diversity is also quite similar between regions, although suggesting a slightly higher diversity in western Africa. Finally, fungus-growing termites originated indeed in the African rain forest, just before the expansion of savanna, about 31 mya. The credibility intervals of the split into the four main clades for both symbiotic partners are always overlapping, suggesting tbat these splits occurred simultaneously. Key words: Fungus-growing termites, Termitomyces, basidiocarps, symbiosis, seasonal fructification, alates nuptial tlight, Origin, Age estimate, African rainforest, co-evolution, Côte d'Ivoire. -- TABLE DES MATIERES A V ANT PROPOS i LISTE DES ABBREVJA TIONS ou SIGLES ··············································································· V LISTE DES FIGURES, Il,LUSTRATIONS ET PLANCHES vi LISTE DES TABLEAUX ix INTRODUCTION GENERALE 1 PREMIERE PARTIE· GENERALITES 6 CHAPITRE 1 : PRESENTATION DU MJLŒU D'ETUDE 6 1.1/ Situation géographique 6 1.2/ Climat. 6 1.2.1/Pluviométrie 6 1.2.2/ Température 7 1.3/ Hydrographie et relief 7 1.4/ Sols 10 1.5/ Végétation 10 CHAPITRE 2 : GENERALITES SUR LA SYMBIOSE ENTRE LES MACROTERMJTlNAE ET LES TERMITOMYCES 12 2.1/ Introduction 12 2.2/ Classes d'interactions entre les organismes vivants 12 2.3/ Classification des termites 13 2.4/ Régime alimentaire des termites 15 2.5/ Diversité et distribution géographique des termites 15 2.6/ Sous-famille des Macrotermitinae ou termites champignonnistes 15 2.6.1/ Symbiose Macrotermitinae-Termitomyces 16 2.6.2/ Association Xy/aria-Macroterrnitinae 16 2.6.3/ Meule à champignon : support exclusif du Termitomyces 17 2.6.3.1/ Origine de la meule à champignon 17 2.6.3.2/ Structure et dynamique de la meule à champignon 18 2.6.3.3/ Classification des meules à champignon 21 2.6.4/ Rôle des organismes partenaires dans la relation symbiotique 22 2.6.5/ Transmission du champignon symbiotique d'une génération de termite à une autre 24 2.6.6/ Co-spéciation des organismes symbiotiques 26 2.6.7/
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