Interações ecológicas interespecíficas que resultam em benefício para todos os organismos participantes são conhecidas como mutualismo. No entanto, a troca de benefícios apresenta custos para as espécies participantes. Este fato abre espaço para o surgimento de espécies que adotam estratégias oportunistas, denominadas parasitas de mutualismos. As plantas do gênero Ficus são adequadas para estudos dessas interações, pois apresentam relação mutualística com vespas polinizadoras da família Agaonidae e são exploradas por vespas não-polinizadoras (parasitas do mutualismo). O objetivo desse estudo foi elucidar a biologia larval de vespas não-polinizadoras do gênero Idarnes pertencentes aos grupos carme e flavicollis associadas a Ficus citrifolia no campus da USP em Ribeirão Preto. Foi possível elucidar que a espécie de Idarnes do grupo flavicollis é galhadora, ao passo que a espécie do grupo carme é incapaz de induzir galhas, sendo provavelmente inquilinas específicas da espécie polinizadora. Vespas flavicollis ovipositam nos sicônios antes da polinização e evitam a retaliação pela planta, adotando mecanismo de oviposição semelhante ao das vespas polinizadoras. Vespas carme, por sua vez, depositam seus ovos diretamente dentro do saco embrionário de flores já galhadas, onde se localiza a larva da polinizadora. Contrariando especulações prévias, os resultados mostram que mesmo em espécies próximas filogeneticamente, e.g. grupos flavicollis e carme do gênero Idarnes, podem ocorrer variações acentuadas na biologia e na estratégia de exploração de recursos. / Interspecific ecological interactions which benefit all participants are known as mutualisms. However, the benefit exchange implies in costs for the involved species. This fact enables the appearance of species adopting opportunist strategies, known as parasites of mutualism. Plants belonging to the genus Ficus are suitable for studying these ecological interactions since they show a mutualistic interaction with pollinating wasps belonging to Agaonidae family and are exploited by non-pollinating wasps (parasites of the mutualism). The aim of this study was to elucidate the larval biology of non-pollinating fig wasps, genus Idarnes, belonging to flavicollis and carme species groups, associated with Ficus citrifolia at USP campus in Ribeirão Preto. We showed that species of flavicollis group are gallers, while species of carme group were not able to induce galls, probably being specific inquilines of the pollinating species. flavicollis wasps oviposit in syconia before receptivity and avoid retaliation by the plant, adopting a similar mechanism of oviposition to the one of the pollinators. carme wasps, on the other hand, deposit their eggs directly inside the embrionary sac of already galled flowers, where the pollinator larva is located. In disagreement with previous speculations, the results show that even in phylogenetically close species, such as flavicollis and carme species groups, there may be considerable variation in biology and resource exploitation strategies.

La spéciation et la diversification sur les iles sont des processus évolutifs tirés par de nombreux facteurs tels qu’histoire géologique et complexité topographique. Réciproquement, l’histoire évolutive d’une espèce contribue à expliquer ses traits biologiques et écologiques actuels. J’ai cherché à analyser ces patrons et processus à travers un système modèle présent à travers toutes les régions tropicales du monde : les Ficus et leurs insectes pollinisateurs (Hymenoptera : Chacidoidea). Plus particulièrement je me suis focalisée sur les Ficus du sous genre Sycomorus et leurs pollinisateurs, les insectes du genre Ceratosolen. Les deux objectif principaux de ma thèse ont été de : (1) étudier l’histoire biogéographique des espèces de Ceratosolen des Philippines à partir des reconstructions phylogénétiques et (2) étudier quelques aspects de la biologie et de l’écologie de ces espèces et de les relier à leur histoire évolutive. Pour l’objectif 1, nous montrons que, comme la plupart des biota des Philippines, les Ceratosolen sont arrivés du sud par Palawan ou par l’archipel de Sulu, à de multiples reprises. Il semble que l’histoire géologique, les bras de mer profonds et les changements de niveau des mers du Pléistocène ont une valeur explicative faible pour comprendre la distribution et la diversification des groupes d’espèces. Les facteurs importants seraient plutôt la complexité topographique des iles, les distances entre iles, la capacité intrinsèque de dispersion des insectes et la spécialisation écologique. Pour l’objectif 2 nous avons étudié les traits suivants : la modification des pattes arrière, la durée de vie, l’activité journalière, la structuration génétique spatiale et la perception des odeurs de figues réceptives. Nous montrons que les pattes postérieures modifiées de C. corneri ont des propriétés hydrophobes plus fortes que celles, non modifiées, de son proche parent, C. jucundus. Le caractère hydrophobe de ces pattes permet aux males de C. corneri de respirer même submergé dans du liquide dans les figues. Cette adaptation est probablement le résultat de la sélection sexuelle car ces males peuvent émerger plus tôt de leurs galles pour féconder les femelles. Nous montrons ainsi comment un trait de la figue, la quantité de liquide, contraint la morphologie et le comportement du pollinisateur. Par ailleurs nous documentons plusieurs cas de coexistence locale de plusieurs espèces de pollinisateurs associées à F. septica. Dans un site nous montrons que les deux espèces de pollinisateurs diffèrent par leur durée de vie mais débutent leur activité en même temps. De plus, F. septica et ses clades de pollinisateurs noirs présentaient une structure géographique similaire. Ce patron a pu apparaitre dans le contexte de barrières géographiques fortes, menant à l’isolement, à l’adaptation locale et finalement, à la co-diversification. Nous montrons que la coexistence de pollinisateurs a probablement été rendue possible par un déplacement initial de caractère suivi d’une extension d’aire. Finalement, nous fournissons des éléments montrant que les variations géographiques d’odeurs de figues réceptives ne limitent pas l’expansion géographique des insectes pollinisateurs. Ceci est confirmé par nos résultats sur la gamme d’odeurs perçues par les insectes. Nous montrons que cette perception était fortement dépendante des stimuli rencontrés. Ainsi nous voyons une convergence des odeurs perçues entre insectes partageant un même hôte. Ceci est une démonstration de la plasticité évolutive du système de perception des odeurs des insectes. Ainsi notre travail explore des aspects historiques et biologiques de l’ensemble des Ceratosolen des Philippines, avec une focalisation sur la diversification en cours dans le système Ficus septica-insectes associés. La suite du travail abordera les moteurs biologiques et les processus biologiques tels que la co-spéciation ou le partage de pollinisateurs que nous avons documentés ici. / Speciation and diversification in islands are evolutionary processes that are driven by many factors such as geological history and topographic complexity. In turn, the evolutionary history of a species contributes to explaining its present biological and ecological traits. In wanting to investigate these patterns and processes, I chose a model system that is present throughout the tropical areas of the world: the figs (genus Ficus) and fig wasps (Hymenoptera: Chalcidoidea). Specifically, I focused on a subgroup of this model system: the subgenus Sycomorus figs and their associated pollinators, the Ceratosolen wasps. The two main objectives of this thesis were: (1) to investigate the biogeographic history of the Philippine Ceratosolen species using phylogenetic tree reconstructions and (2) to investigate certain biological and ecological traits of Philippine Ceratosolen species and to relate these traits to their evolutionary history. For Objective 1, we have shown that, like most Philippine biota, Ceratosolen wasps most likely arrived from the south of the Philippines via Palawan or the Sulu archipelago. It is likely that geological history, deep-water barriers and Pleistocene sea-level changes were not major factors explaining the distribution and diversification of these species groups. They are most likely affected by other factors such as island topographic complexity, distances between islands, intrinsic wasp dispersal ability and ecological specialization. For Objective 2, we specifically looked at the following wasp traits: hind leg modifications, life span and daily activity, spatial genetic structuring and odour perception. We have shown that male C. corneri modified hind legs were able to repel liquids more than its close relative, C. jucundus, that has unmodified hind legs. The hydrophobicity of these hind legs allows C. corneri male wasps to respire even when they are submerged in fig liquid. This adaptation is probably a response to sexual selection because these male wasps now have the ability to emerge earlier to search for mates. We have thus shown how fig functional traits, i.e. amount of fig liquid, can constrain fig wasp morphology and behaviour. Moreover, in the F. septica system, we documented several instances of multiple pollinator species associating with F. septica. In one site, these two pollinator species differed in life span, but are active the same time. Also, F. septica and its black pollinator clades exhibited similar geographic structuring. This could originally be due to strong geographic barriers leading to isolation, local adaptation, and finally co-diversification. We also show the co-existence of pollinating species in an area which probably had been brought about by initial character displacement and subsequent range expansion. Lastly, we provide evidence that receptive fig odours do not constrain the species specificity of the interactions. This was further supported by our results on the range of wasp odour perception. We saw that odour perception in fig wasps is highly dependent on the olfactory stimuli. Convergence in odour perception was seen when wasps shared hosts and divergence was demonstrated when wasp species were constrained to respond to different scent profiles. This is remarkable evidence of the evolutionary plasticity in the insect odour perception system. Thus, this work explored aspects of the history and biology of Philippine Ceratosolen, as a whole, with a focus on the current on-going diversification processes in the Ficus septica-wasp system. Future work should look at the biological drivers of evolutionary processes such as co-speciation and pollinator sharing that we have documented here.

Interações ecológicas interespecíficas que resultam em benefício para todos os organismos participantes são conhecidas como mutualismo. No entanto, a troca de benefícios apresenta custos para as espécies participantes. Este fato abre espaço para o surgimento de espécies que adotam estratégias oportunistas, denominadas parasitas de mutualismos. As plantas do gênero Ficus são adequadas para estudos dessas interações, pois apresentam relação mutualística com vespas polinizadoras da família Agaonidae e são exploradas por vespas não-polinizadoras (parasitas do mutualismo). O objetivo desse estudo foi elucidar a biologia larval de vespas não-polinizadoras do gênero Idarnes pertencentes aos grupos carme e flavicollis associadas a Ficus citrifolia no campus da USP em Ribeirão Preto. Foi possível elucidar que a espécie de Idarnes do grupo flavicollis é galhadora, ao passo que a espécie do grupo carme é incapaz de induzir galhas, sendo provavelmente inquilinas específicas da espécie polinizadora. Vespas flavicollis ovipositam nos sicônios antes da polinização e evitam a retaliação pela planta, adotando mecanismo de oviposição semelhante ao das vespas polinizadoras. Vespas carme, por sua vez, depositam seus ovos diretamente dentro do saco embrionário de flores já galhadas, onde se localiza a larva da polinizadora. Contrariando especulações prévias, os resultados mostram que mesmo em espécies próximas filogeneticamente, e.g. grupos flavicollis e carme do gênero Idarnes, podem ocorrer variações acentuadas na biologia e na estratégia de exploração de recursos. / Interspecific ecological interactions which benefit all participants are known as mutualisms. However, the benefit exchange implies in costs for the involved species. This fact enables the appearance of species adopting opportunist strategies, known as parasites of mutualism. Plants belonging to the genus Ficus are suitable for studying these ecological interactions since they show a mutualistic interaction with pollinating wasps belonging to Agaonidae family and are exploited by non-pollinating wasps (parasites of the mutualism). The aim of this study was to elucidate the larval biology of non-pollinating fig wasps, genus Idarnes, belonging to flavicollis and carme species groups, associated with Ficus citrifolia at USP campus in Ribeirão Preto. We showed that species of flavicollis group are gallers, while species of carme group were not able to induce galls, probably being specific inquilines of the pollinating species. flavicollis wasps oviposit in syconia before receptivity and avoid retaliation by the plant, adopting a similar mechanism of oviposition to the one of the pollinators. carme wasps, on the other hand, deposit their eggs directly inside the embrionary sac of already galled flowers, where the pollinator larva is located. In disagreement with previous speculations, the results show that even in phylogenetically close species, such as flavicollis and carme species groups, there may be considerable variation in biology and resource exploitation strategies.

Thesis (MSc)--Stellenbosch University, 2015. / ENGLISH ABSTRACT: Cuticular hydrocarbon (CHC) profiles of insects play roles in behavioural interactions within and between species, encompassing species-, colony- and mate-recognition. CHCs are largely genetically determined and are thus unique to each species, making them useful in chemotaxonomy. However, species exhibit intra-species variation in their CHC profile which can be the result of both intra-species genetic variation as well as environmental influences such as habitat effects, colony effects, diet, host switching, as well as adsorption of CHCs from other insects. Studies have found that the CHC profiles of a specific insect species will often exhibit variations between regions as well as the species of host the insect is associated with. Therefore, an ideal system to investigate the effects of genetic population structure and environment on the CHC profiles of insects is within the fig – fig wasp mutualism. Fig species occur in a wide variety of habitats and host a diverse complement of fig wasp species. We were therefore offered the opportunity to investigate a wide range of potential influences on fig wasp CHC profiles ranging from environmental to genetic effects. Firstly, through GC-MS we found that the CHC profiles of the fig wasps investigated are both species-specific and species-group-specific, with the species Elisabethiella glumosae, Elisabethiella stuckenbergi and Ceratosolen capensis, and two Otitesella species-groups (the Uluzi and Sesqui species-groups) separating out significantly. Consensus phylogenies (based on COI, Cytb and EF-1α) showed that within the galling fig wasp genus Otitesella there were multiple genetic lineages within a species-group which corresponds to species-level genetic variation, and that each genetic lineage was confined to a single host fig species. The CHC profiles reflected the genetic relationships between the two species-groups, and the CHC profiles within a species group could be differentiated by genetic lineage/host species. This indicated that although genetic lineage was mostly responsible for the observed variation in CHC profiles, factors associated with different host species also had an effect. Strong regional variation overriding both the influence of genetic lineage and factors associated with host species were observed in the CHC profiles of the fig wasps within a species-group. This regional variation in CHC profiles was also observed within two pollinating fig wasp species, Elisabethiella stuckenbergi and Ceratosolen capensis, which was not supported by population genetic data (COI and Cytb). In fact, very little genetic population structure was found within the pollinating species, even though the pollinators were collected across South Africa. The lack of genetic structure in pollinating fig wasps can be the result of high gene flow caused by the large dispersal capability of pollinating fig wasps. Our results indicated that fig wasp CHC profiles have the potential to be used in chemotaxonomy and are possibly used as species and mate-recognition cues by the fig wasps. Furthermore, we found both a regional and associated host species effect on the CHC profile. We suggest that the observed regional effect in this study could be attributed to habitat differences and differences in fig wasp community between regions. Moreover, the effect host species had on the CHC profiles may be as a result of dietary differences between galls in different host species. A possible consequence of the observed regional/host speciesassociated effect on fig wasp CHC profiles is that it could lead to pre-mating isolation within fig wasp species, which could ultimately result in speciation. In addition, our results indicated that the interpretation of the variation in the fig wasp CHC profile was dependent on the scale of the analysis: on a broad, inter-species-level scale, fig wasp CHC profiles were species-specific; on a finer intra-species scale, variation in CHC profiles occurred between fig wasps collected from different regions; and on a within-region scale, variation in CHC profiles within species-groups occurred between genetic lineages/host species. Future studies should look at the application of CHCs in chemotaxonomic studies on the fig wasp phylogeny, as well as the effect of fig wasp community composition on fig wasp CHCs. / AFRIKAANSE OPSOMMING: Kutikulêre koolwaterstof (KK) profiele van insekte speel rolle in die gedragsinteraksies binne sowel as tussen spesies, en behels die herkenning van spesieof kolonielidmaatskap asook potensiële maats. Kutikulêre koolwaterstowwe word meestal deur gene bepaal en is dus uniek vir elke spesie, wat dit handig maak vir chemotaksonomie. Spesies vertoon egter soms intraspesie variasie in hul KK profiele wat die gevolg kan wees van beide intraspesie genetiese variasie sowel as omgewingsinvloede soos habitat effekte, kolonie effekte, dieet, tussen-gasheer skuiwings, asook die adsorpsie van ander insekte se kutikulêre koolwaterstowwe. Studies het gevind dat die kutikulêre koolwaterstof profiele van ʼn spesifieke insek spesie op ʼn gereelde basis verskille vertoon tussen streke asook tussen die verskillende gasheer spesies waarmee die insek geassosieer is. Om hierdie redes is die vy – vy-wesp mutualisme ʼn ideale sisteem om die uitwerking van genetiese populasie struktuur en omgewing op die KK profiele van insekte te ondersoek. Vy spesies kom in ʼn wye verskeidenheid van habitatte voor en ondersteun ʼn diverse groep vy-wesp spesies. Dit het ons die geleentheid gebied om ʼn wye reeks moontlike invloede van vy-wesp KK profiele te ondersoek, van omgewings- tot genetiese invloede. Eerstens, deur die gebruik van GC-MS het ons gevind dat die KK profiele van die vy-wespe wat ondersoek was beide spesie-spesifiek en spesie-groep-spesifiek is, met die spesies Elisabethiella glumosae, Elisabethiella stuckenbergi en Ceratosolen capensis, asook twee Otitesella spesie-groepe (die Uluzi en Sesqui spesie-groepe) wat betekenisvol onderskei kon word. Konsensus filogenieë (gegrond op COI, Cytb en EF1-1α) het getoon dat daar in die gal-induserende vy-wesp genus Otitesella veelvuldige genetiese lyne binne die spesie-groepe voorgekom het ooreenstemmend met tussen-spesie genetiese variasie, en dat elke genetiese lyn beperk was tot ʼn enkele gasheer vy spesie. Die KK profiele het die genetiese verhoudings tussen die twee spesie-groepe weerspieël, en die KK profiele binne ʼn spesie-groep kon onderskei word op grond van hul genetiese lyn/gasheer spesie. Hierdie het getoon dat, alhoewel genetiese lyn meestal verantwoordelik was vir die waargeneemde variasie in KK profiele, faktore wat met verskille in gasheer spesies gepaard gaan ook ʼn effek gehad het. Sterk streeks-verbonde variasie wat beide die invloed van genetiese lyn, én faktore wat met verskille in gasheer spesie gepaard gaan, oortref het, was waargeneem in die KK profiele van die vy-wespe binne ʼn spesie-groep. Hierdie streeks-verbonde variasie in KK profiele was ook waargeneem in twee bestuiwende vy-wespe, Elisabethiella stuckenbergi en Ceratosolen capensis, ʼn resultaat wat nie ondersteun was deur die genetiese bevolkingsdata nie (COI en Cytb). In werklikheid was baie min genetiese bevolkings-struktuur opgespoor binne die bestuiwer spesies, selfs as was die bestuiwer spesies regoor Suid-Afrika ingesamel. Die tekort aan genetiese struktuur in die vy-wesp bestuiwers kan die gevolg wees van hoë geenvloei wat veroorsaak word deur die hoë verspreidingskapasiteit van bestuiwende vy-wespe. Die resultate toon aan dat vy-wesp KK profiele die potensiaal besit om in chemotaksonomie gebruik te word, en word moontlik deur vy-wespe gebruik as kenmerke vir die herkenning van spesie en potensiële maats. Verder was daar gevind dat daar beide ʼn streekseffek en ʼn effek geassosieer met gasheer spesie op KK profiele was. Ons stel voor dat die waargeneemde streekseffek in hierdie studie toegeskryf kan word aan verskille tussen habitatte asook streeksverbonde verskille tussen vy-wesp gemeenskappe. Boonop kan die effek wat gasheer spesie op die KK profiele gehad het ʼn gevolg wees van dieetverskille tussen die galle in verskillende gasheer spesies. ʼn Moontlike gevolg van die waargeneemde streeks/gasheer-spesie-geassosieerde effek op vy-wesp KK profiele is dat dit moontlik kon lei tot voor-paring-isolasie binne vy-wesp spesies, wat uiteindelik spesiasie kon veroorsaak het. Daarbenewens wys ons resultate dat die interpretasie van die variasie in die vy-wesp KK profiel was afhanklik van die skaal van die analise: op ʼn breë interspesie vlak was die vy-wesp KK profiele spesiespesifiek; op ʼn fyner intra-spesie vlak het variasie in KK profiele voorgekom tussen vy-wespe wat in verskillende streke ingesamel was; en op streeksvlak het variasie in die KK profiele binne spesie-groepe voorgekom tussen genetiese lyne/gasheer spesies. Toekomstige studies behoort te kyk na die toepassing van kutikulêre koolwaterstowwe in chemotaksonomiese studies van die vy-wesp filogenie, asook die effek wat vy-wesp gemeenskap samestelling het op vy-wesp kutikulêre koolwaterstowwe.

The Sycoecinae are a distinct and well-defined subfamily of old world fig wasps (Agaonidae, Chalcidoidea 1 Hymenoptera) , exclusively associated with the figs of Ficus species (Moraceae). The most likely sister group of the Sycoecinae was determined to be the Sycoryctini (Sycoryctinae) based largely on synapomorphies of the underside of the head. 67 sycoecine species and 3 subspecies were recognised and included in a phylogenetic analysis of the subfamily. This analysis clearly delimited six genera (four African and two extra-African), although the phylogenetic relationships between the genera were not strongly supported and remain flexible. Comparisons of the phylogeny of the Sycoecinae with the classifications of the Agaoninae and their host fig trees (Ficus, Moraceae) suggest a degree of cospeciation sensu lato. Numerous homoplasies were detected within the Sycoecinae, some of which were shared with another group of fig wasps that also enter the fig to oviposit, the Agaoninae. The anatomy of the figs apparently provides strong selection pressures that have resulted in both parallelisms and convergences within and between the two subfamilies. Among the 67 species and 3 subspecies that were recognised, 43 species and 2 subspecies are described as new. The males of three previously recognised species are also described for the first time. One generic and two specific synonyms are established together with five new combinations. Keys are provided to the genera and species, for both sexes.

Pour l'ensemble des organismes vivants, la communication (intra ou interspécifique) est le véhicule de l'information, un élément central dans l'interaction entre individus. Elle a ainsi des impacts primordiaux sur les traits d'histoire de vie des espèces, et est donc façonnée par la sélection naturelle. Au cours de cette thèse, nous nous sommes intéressés à l'évolution de la médiation chimique, c'est-à-dire à la transmission d'informations par voie chimique entredeux individus, dans les interactions plantes/animaux. Nous avons choisi le modèle figuier et ses partenaires mutualistes, de la guêpe pollinisatrice aux vertébrés disperseurs de graines. La médiation chimique (ici émission de bouquets volatils constitués de terpènes et de dérivés benzéniques et d'acides gras) permet aux figuiers d'assurer leur reproduction, par attraction des pollinisateurs et des disperseurs de graines. Il existe environ 800 espèces de figuiers à travers le monde, à distribution principalement tropicale. Les figuiers, fructifiant toute l'année,sont souvent qualifiés d'espèce clef de voute des écosystèmes tropicaux, car ils assurent ainsi le maintien des populations de frugivores dans les forêts tropicales dans les périodes où très peu d'espèces d'arbres fructifient. L'interaction figuier/disperseur est plutôt généraliste, alors que le mutualisme figuier/pollinisateur, un exemple de nursery pollination, est hautement spécifique et obligatoire. Au cours de cette thèse, nous avons mis en évidence que les contraintes phylogénétiques et géographiques exercées sur la médiation chimique étaient négligeables, alors que les pressions de sélection que représentent les mutualistes sont nettement plus importantes dans l'évolution de cette médiation. Ainsi, sexe et stade phénologique du figuier et identité du partenaire mutualiste sont des informations qui peuvent être portées par la médiation chimique. Notre approche, globale et multidisciplinaire, des interactions entre les figuiers et leurs partenaires mutualistes aux deux phases de dispersions des gènes de la plante, permet une meilleure compréhension de l'évolution de la communication, et montre que les pressions façonnant ce message façonnent l'interaction elle-même. / For all living organisms, communication (intra-or interspecific) is the vehicle of information, anelement central to interactions among individuals. It thus has fundamental impacts on lifehistory traits of species, and is shaped by natural selection. This thesis is concerned with thechemical mediation of communication, i.e., the transmission of information by chemical signals,in the context of animal-plant interactions. We chose as a model system the interactionsbetween figs and their mutualist partners, including both pollinating fig wasps and vertebrateseed dispersers. Chemical mediation (in this case the emission of bouquets of volatilecompounds comprising terpenes, benzenoids and fatty acid derivatives) enables figs to ensuretheir reproduction by attracting pollinators and seed dispersers. There exist about 800 species ofFicus worldwide, principally in tropical regions. Figs, which fruit throughout the year, are oftenconsidered keystone species of tropical ecosystems, because their year-round fruiting maintainspopulations of seed-dispersing frugivores during fruit-poor lean seasons'. Interactions betweenfig species and seed-dispersing animals are generalist' (i.e., broad food species ranges), whilefig/pollinator mutualisms, examples of nursery pollination' systems, are highly species-specificand obligatory. In this thesis, we showed that phylogenetic and geographic constraints actingon chemical mediation are negligible, whereas selection pressures grounded in pollination andseed-dispersal mutualisms play a strong role in shaping the evolution of chemical mediation.Thus, chemical mediation carries information such as the sex and developmental stage of thefig tree, as well as the identity of the mutualistic partner. Our comprehensive, multidisciplinaryapproach to interactions between figs and their mutualist partners in the two phases ofdispersal of the plant's genes leads to an improved understanding of the evolution ofcommunication, and showed that the selective pressures shaping the message are also thoseshaping the interaction itself.

A interação mutualística, espécie-especifica, vespas de figo-figueiras envolve dois processos antagonísticos, predação de sementes e polinização, realizadas por vespas da família Agaonidae. Sabe-se que a larva da vespa se alimenta de tecido da semente durante seu desenvolvimento, mas o processo pelo qual isto ocorre é pouco conhecido, não se sabendo até que ponto a larva depende do desenvolvimento da semente. Neste trabalho foi estudada a biologia larval de Pegoscapus tonduzi, polinizadora de Ficus citrifolia (Moraceae). O estudo foi realizado em plantas de F. citrifolia presentes no campus da Universidade de São Paulo em Ribeirão Preto/SP, durante o período de julho de 2007 a agosto de 2008. Para tal, quatro coortes de vespas foram estudas, nas quais cerca de cinco figos foram coletados em intervalos de dois dias, ao longo do ciclo de desenvolvimento larval. Os figos foram dissecados para observação das larvas e para a obtenção de ovários/galhas da planta para o preparo de lâminas histológicas. Os resultados mostraram que o processo de predação de sementes realizado pelas larvas de P. tonduzi é elaborado, com o desenvolvimento larval intimamente relacionado aos processos embriogênicos da planta. O desenvolvimento larval apresenta quatro instares, detectados pela mudança de tamanho e formadas larvas. A duração do ciclo de vida de P. tonduzi foi de 40 a 70 dias, aproximadamente, correlacionando-se negativamente com a temperatura ambiente no período. O ovo é depositado na região próxima à base do estilete, entre o nucelo e o tegumento interno do ovário da planta. Nessa fase, observase o surgimento do embrião vegetal, indicando que o ovário em que larva se desenvolve foi fertilizado. No segundo estádio larval, o inseto migra para a região micropilar e passa a se alimentar oralmente do endosperma da planta. Nesta fase, ainda, nota-se o desaparecimento do embrião vegetal, sugerindo que este é consumido pela larva da vespa. Os resultados sugerem a existência de um ajuste evolutivo fino entre inseto-planta, uma vez que o desenvolvimento da larva da vespa de figo parece depender da fertilização e conseqüente formação do endosperma. / The species-specific mutualistic interaction between fig trees and fig wasps engages two antagonist processes: seed predation and pollination, both achieved by wasps of the Agaonidae family. It is well known that fig wasp larvae feed on seed tissues for their development but the process itself is poorly known. Here is a study on the larval biology of Pegoscapus tonduzi, pollinator of Ficus citrifolia (Moraceae). The study was carried out between July 2007 and August 2008 at the Sao Paulo University campus in Ribeirao Preto, Sao Paulo State. Four cohorts of fig wasps were studied; for each cohort, about five figs were sampled each two days until complete larval cycle. Sampled figs were dissected for larvae observation and measurement, and flower ovaries/galls subsamples destined to histological study. Results showed that seed predation by fig wasps is a complex process, with larval development closely related to plant embryogenesis. Four larval instars were determined by changes on larva size and shape. Larval cycle extended from 40 to 70 days, showing a negative relation with environmental temperature. The egg is laid near the style insertion, between nucleus and inner integument of the flower ovary. Vegetal embryo was observed along with first larval instar, indicating that fertilization took place inside the ovary where larva develops. At second instar, the larva migrates to the micropilar region and begins to feed orally from endosperm. In this phase, the embryo disappears, suggesting that it is consumed by the larva. Our results suggest a fine tune evolutionary insect-plant adjustment, as fig wasp larvae seems to depend on ovary fertilization and endosperm development.

A interação mutualística, espécie-especifica, vespas de figo-figueiras envolve dois processos antagonísticos, predação de sementes e polinização, realizadas por vespas da família Agaonidae. Sabe-se que a larva da vespa se alimenta de tecido da semente durante seu desenvolvimento, mas o processo pelo qual isto ocorre é pouco conhecido, não se sabendo até que ponto a larva depende do desenvolvimento da semente. Neste trabalho foi estudada a biologia larval de Pegoscapus tonduzi, polinizadora de Ficus citrifolia (Moraceae). O estudo foi realizado em plantas de F. citrifolia presentes no campus da Universidade de São Paulo em Ribeirão Preto/SP, durante o período de julho de 2007 a agosto de 2008. Para tal, quatro coortes de vespas foram estudas, nas quais cerca de cinco figos foram coletados em intervalos de dois dias, ao longo do ciclo de desenvolvimento larval. Os figos foram dissecados para observação das larvas e para a obtenção de ovários/galhas da planta para o preparo de lâminas histológicas. Os resultados mostraram que o processo de predação de sementes realizado pelas larvas de P. tonduzi é elaborado, com o desenvolvimento larval intimamente relacionado aos processos embriogênicos da planta. O desenvolvimento larval apresenta quatro instares, detectados pela mudança de tamanho e formadas larvas. A duração do ciclo de vida de P. tonduzi foi de 40 a 70 dias, aproximadamente, correlacionando-se negativamente com a temperatura ambiente no período. O ovo é depositado na região próxima à base do estilete, entre o nucelo e o tegumento interno do ovário da planta. Nessa fase, observase o surgimento do embrião vegetal, indicando que o ovário em que larva se desenvolve foi fertilizado. No segundo estádio larval, o inseto migra para a região micropilar e passa a se alimentar oralmente do endosperma da planta. Nesta fase, ainda, nota-se o desaparecimento do embrião vegetal, sugerindo que este é consumido pela larva da vespa. Os resultados sugerem a existência de um ajuste evolutivo fino entre inseto-planta, uma vez que o desenvolvimento da larva da vespa de figo parece depender da fertilização e conseqüente formação do endosperma. / The species-specific mutualistic interaction between fig trees and fig wasps engages two antagonist processes: seed predation and pollination, both achieved by wasps of the Agaonidae family. It is well known that fig wasp larvae feed on seed tissues for their development but the process itself is poorly known. Here is a study on the larval biology of Pegoscapus tonduzi, pollinator of Ficus citrifolia (Moraceae). The study was carried out between July 2007 and August 2008 at the Sao Paulo University campus in Ribeirao Preto, Sao Paulo State. Four cohorts of fig wasps were studied; for each cohort, about five figs were sampled each two days until complete larval cycle. Sampled figs were dissected for larvae observation and measurement, and flower ovaries/galls subsamples destined to histological study. Results showed that seed predation by fig wasps is a complex process, with larval development closely related to plant embryogenesis. Four larval instars were determined by changes on larva size and shape. Larval cycle extended from 40 to 70 days, showing a negative relation with environmental temperature. The egg is laid near the style insertion, between nucleus and inner integument of the flower ovary. Vegetal embryo was observed along with first larval instar, indicating that fertilization took place inside the ovary where larva develops. At second instar, the larva migrates to the micropilar region and begins to feed orally from endosperm. In this phase, the embryo disappears, suggesting that it is consumed by the larva. Our results suggest a fine tune evolutionary insect-plant adjustment, as fig wasp larvae seems to depend on ovary fertilization and endosperm development.

O sucesso reprodutivo das figueiras, e a consequente manutenção do mutualismo Ficus vespas de figo, depende do sucesso na polinização das flores pistiladas (produção de frutos) e do desenvolvimento de vespas polinizadoras em alguns ovários galhados (produção de vespas vetoras de pólen). No entanto, o período de receptividade das flores pistiladas para a polinização e oviposição pelas vespas polinizadoras de Ficus é curta, em relação à duração total do desenvolvimento do figo. A pequena janela temporal de receptividade pode ser um fator limitante na estabilidade do mutualismo, uma vez que o sucesso reprodutivo da planta será nulo se os figos não forem visitados por vespas polinizadoras durante o período de receptividade. O presente trabalho avaliou o papel das vespas não-polinizadoras galhadoras (Idarnes grupo flavicollis) durante o período de polinização Ficus citrifolia. Especificamente avaliou-se se as vespas galhadoras interferem (1) na atratividade do figo às vespas polinizadoras, (2) na receptividade do estigma e (3) no sucesso das vespas polinizadoras (produção de frutos e prole de vespas polinizadoras). O estudo experimental foi realizado no campus da USP Ribeirão Preto (21°10S; 47°48W), durante os meses de 02/2008 e 07/2009. Foi observado que os períodos de receptividade do estigma e de atratividade do figo duraram cerca de uma semana e não sofreram efeito da presença das vespas galhadoras. No entanto, o sucesso reprodutivo da planta foi afetado em situações de alta infestação das vespas não-polinizadoras, devido ao fechamento precoce do ostíolo causado pelo crescimento das galhas dessas vespas / The breeding success of Ficus trees and the maintenance of their mutualistic fig wasps depend on the successful pollination of pistilate flowers (seed production) and on the development of pollinating wasps in some galled ovaries (production of pollen vectors). The period during which pistilate flowers are receptive for pollination and oviposition is short compared to the total length of fig development. This narrow temporal window may be limiting to the stability of the mutualism, since the reproductive success of the plant will be null if wasps fail to find receptive trees. We investigated the role of the non-pollinating galler wasps (Idarnes group flavicollis) on the pollination period of Ficus citrifolia figs. Specifically, we tested if galler wasps interfere on (1) fig attraction for pollinating fig wasps, (2) length of stigma receptivity and (3) pollinating success (seed and pollinator offspring production). The study was carried out at the campus of University of São Paulo in Ribeirão Preto (21° 10\' S, 47° 48\' W) between february/2008 and march/2009. The periods of stigma receptivity and fig attractiveness lasted about one week and were not affected by the presence of galling non-pollinating fig wasps. However, the early ostiole closure caused by the growth of non-pollinating wasps galls may affect the plant reproductive success in high levels of infestation by these wasps

L'ile de Taiwan est apparue, il y a deux millions d'années. Nous avons étudié les figuiers de Taiwan afin de comprendre comment l'ile fut colonisée et comment l'insularité a pu affecter les espèces colonisatrices. Le genre Ficus est caractérisé par son association mutualiste avec des insectes pollinisateurs extrêmement dispersifs. De plus les figues, inflorescences fermées des Ficus, sont consommés par un grand nombre d'espèces qui elles aussi dispersent efficacement les graines. Nous avons développé une série de marqueurs génétiques afin de pouvoir étudier plusieurs espèces avec les mêmes outils. Ensuite nous avons analysé la structure génétique dans Taiwan d'un groupe de quatre espèces. Une espèce présenta une différenciation génétique claire dans le Sud de Taiwan au climat plus chaud, suggérant la possibilité un début de spéciation écologique chez une espèce hautement dispersive. Une seconde espèce a montré des indices de processus de sélection en cours dans le Sud de Taiwan. A une échelle plus étendue, nous avons montre que les données microsatellites et spécifiquement les R statistiques donnent un premier aperçu de la phylogéographie des figuiers. Pour plusieurs espèces, l'Asie continentale semble être la trame de fond génétique de ces espèces malgré une forte différenciation parmi les populations. Pour Ficus variegata, nous avons montré que la colonisation de Taiwan a pour origine les Philippines et nous n'avons pas détecté de trace de flux génétique venant du continent. L'étude de la phénologie reproductive des Ficus suggère que seulement des espèces produisant de fréquentes récoltes ont colonisé l'ile. Ces travaux ouvrent de nombreuses perspectives sur la réponse des figuiers à l'insularité. / The Island of Taiwan appeared some two million years ago. We investigated the Ficus species of Taiwan in order to understand how the island was colonized and how insular conditions affected the colonizing species. Genus Ficus is characterized by its mutualistic association with highly dispersive pollinating wasps. Further figs, the closed inflorescences of Ficus, are consumed by a large number of highly efficient seed dispersers. We developed a set of portable genetic markers in order to analyze several species using a single set of markers. We then analyzed genetic structuring within Taiwan in a set of four species. One species presented clear genetic differentiation in the warm south Taiwan, suggesting the possibility of incipient ecological speciation in a highly dispersive species. Another species presented indications of ongoing selective processes also in south Taiwan. On a broader scale we show that microsatellite data and notably R statistics provide useful insights into Ficus phylogeography. In several species, continental Asia seems to correspond to a single genetic background despite strong genetic differentiation among populations. For Ficus variegata, we show that it colonized Taiwan from the Philippines and we detect no trace of gene flow from the continent. An investigation of Ficus reproductive phenology suggests that only species producing frequent fig crops have established on the island. This work opens up a series of perspectives on the response of Ficus to insular conditions.