Predation success by a plant-ant indirectly favours the growth and fitness of its host myrmecophyte

Mutualisms, or interactions between species that lead to net fitness benefits for each species involved, are stable and ubiquitous in nature mostly due to "byproduct benefits" stemming from the intrinsic traits of one partner that generate an indirect and positive outcome for the other. Here we verify if myrmecotrophy (where plants obtain nutrients from the refuse of their associated ants) can explain the stability of the tripartite association between the myrmecophyte Hirtella physophora, the ant Allomerus decemarticulatus and an Ascomycota fungus. The plant shelters and provides the ants with extrafloral nectar. The ants protect the plant from herbivores and integrate the fungus into the construction of a trap that they use to capture prey; they also provide the fungus and their host plant with nutrients. During a 9-month field study, we over-provisioned experimental ant colonies with insects, enhancing colony fitness (i.e., more winged females were produced). The rate of partial castration of the host plant, previously demonstrated, was not influenced by the experiment. Experimental plants showed higher δ¹⁵N values (confirming myrmecotrophy), plus enhanced vegetative growth (e.g., more leaves produced increased the possibility of lodging ants in leaf pouches) and fitness (i.e., more fruits produced and more flowers that matured into fruit). This study highlights the importance of myrmecotrophy on host plant fitness and the stability of ant-myrmecophyte mutualisms

Conflicts and evolutionary stability of a tripartite mutualism between plants, ants and fungi

Les mutualismes, interactions interspécifiques où chaque partenaire retire un bénéfice net de leur association, sont centraux dans l’origine et l’organisation de la biodiversité. Bien que globalement bénéfiques pour chacun des partenaires, ces interactions n’enlèvent rien à l’égoïsme inhérent de chaque espèce pour sa survie et sa reproduction, générant des conflits d’intérêts entre les espèces. Ainsi, comprendre les processus écologiques et évolutifs qui maintiennent le caractère mutualiste d’interactions entre plusieurs espèces est primordial dans la compréhension du maintien de la biodiversité. Néanmoins, le corpus scientifique s’est jusqu'à présent surtout concentré sur des paires d’espèces en interaction. Or, ces avancées scientifiques restent partielles car la plupart de ces interactions s’englobent dans un contexte communautaire. C’est dans ce cadre conceptuel que se place mon travail de thèse. Alors que la diversité structurelle des mutualismes de protection entre plantes et fourmis en ont fait un modèle d’étude clé dans la compréhension des mutualismes, j’ai concentré mes recherches sur l’intégration d’un troisième partenaire fongique pour comprendre ses conséquences sur les résultantes écologiques et évolutives de ces mutualismes tripartites. Je me suis tout d’abord intéressé à définir la relation qui lie de façon mutualiste le champignon aux deux autres partenaires et à établir les conflits d’intérêts émanant de ces différentes interactions pour comprendre quels facteurs permettaient de les réguler. Ainsi, la relation qui lie le champignon aux fourmis peut être qualifiée d’agriculture. Les fourmis protègent, nourrissent et disséminent le champignon et celui-ci, via ses propriétés structurales, permet l’élaboration de galeries servant de piège pour capturer des proies. Ce phénomène crée cependant un conflit d’allocation de la force ouvrière des fourmis et nuit directement aux bénéfices de la plante par une diminution de l’intensité des patrouilles sur ses feuilles, diminuant consécutivement sa protection et sa fitness. Néanmoins, le rôle du champignon dans les transferts de nutriments entre les fourmis et la plante, ainsi que certaines réponses évolutives de la plante permettent de réguler ces conflits, stabilisant les bénéfices nets de chaque partenaire dans ce mutualisme tripartite. Puis, je me suis concentré à comprendre comment certains facteurs évolutifs pouvaient moduler cette résultante écologique. La prise en compte du caractère multipartite d’un mutualisme change radicalement la vision de l’évolution des mutualismes jusqu’alors étudiée entre paires d’espèces. Alors que le corpus scientifique s’accorde à dire que la spécialisation entre espèce par coévolution renforce la stabilité et les bénéfices perçus par chaque partenaire, le contexte multipartite semble altérer ces prédictions. Au contraire la spécialisation multipartite peut être dans certains cas un moteur d’instabilité et de baisse des bénéfices. Enfin cette thèse permet de faire le lien entre deux concepts qui s’opposent : la coévolution diffuse et la coévolution par paire. Je montre ainsi que la coévolution peut intervenir sur plus de deux espèces à la fois, mais qu’elle peut quand même entrainer une spécialisation multispécifique. Finalement, au contraire des prédictions de la coévolution diffuse, cette thèse montre que plusieurs pressions de sélection contrastées émanant de différentes espèces envers un seul trait d’une troisième espèce peuvent promouvoir la spécialisation multi-spécifique.Mutualisms, defined as interspecific interactions where each partner receives net benefices from their interactions, are central to the organization of earth biodiversity. Although globally beneficial for each partner, such interactions do not modify the inherent selfishness of species for their survival and reproduction, generating conflicts of interests between species. Thus understanding the ecological and the evolutionary processes maintaining positive outcomes in mutualisms is fundamental to understand how mutualisms shape earth biodiversity. However, scientific research on mutualisms has most of the time focused on interaction between pairs of species. Such knowledge is thus partial as mutualisms are embraced in a community context. My doctoral thesis takes place in this conceptual framework. I focused my research on the integration of a third fungal partner in protective interactions between ants and plants to evaluate its consequences on the ecological and evolutionary outcomes of such mutualisms, taken as multispecies interactions. I first focused my researches in defining the mutualistic interaction linking the fungal partner with its two other associates and in revealing any conflict of interests and their regulation that may emerge from such tripartite interactions. The interactions between the ants and the fungi can be qualified as a case of non-food fungiculture. The ants protect, provide food and disseminate the fungus, and the latter, thanks to its structural properties, allows the elaboration of galleries used that are then used as trap to capture preys. This phenomenon creates a conflict of interest in the allocation of the worker force, altering host plant benefits through a decrease of worker patrolling activity and consequently leaves protection and thus fitness. However, the role of the fungus in the nutrient transfers between ants and plants added to evolutionary responses from the plant allows regulating this conflict, stabilizing the net benefits towards the plant. Then I have concentrated my researches in understanding how evolutionary factors would modulate the ecological outcomes of such interactions. Taking into account the multispecific character of mutualisms changes radically the vision on the evolution of mutualisms when pair of species are considered. While it is widely accepted that specialization of mutualist species through coevolution reinforce the stability of the interaction and the net benefit of each partner, the multispecific context seems to deviate these predictions. Conversely, I show that specialization between three mutualistic partners can drive instability and decrease of benefits. Finally, the results of this thesis join the gap between two previously opposed concepts: diffuse coevolution and pairwise coevolution. I show that coevolution can happen between more than two species simultaneously and that it can drive mutlispecific specialization. Opposed to the diffuse coevolution, I show that contrasting selective pressures on a same trait from different partner can promote specialization of species

Convergent structure and function of mycelial galleries in two unrelated Neotropical plant-ants

International audienceThe construction process and use of galleries by Azteca brevis (Myrmicinae: Dolichoderinae) inhabiting Tetrathylacium macrophyllum (Salicaceae) were compared with Allomerus decemarticulatus (Myrmicinae: Solenopsidini) galleries on Hirtella physophora (Chrysobalanaceae). Though the two ant species are phylogenetically distant, the gallery structure seems to be surprisingly similar and structurally convergent: both are pierced with numerous holes and both ant species use Chaetothyrialean fungi to strengthen the gallery walls. Al. decemarticulatus is known to use the galleries for prey capture and whether this is also the case for Az. brevis was tested in field experiments. We placed Atta workers as potential prey/threat on the galleries and recorded the behaviour of both ant species. We found considerable behavioural differences between them: Al. decemarticulatus was quicker and more efficient at capture than was Az. brevis. While most Atta workers were captured after the first 5 min by Al. decemarticulatus, significantly fewer were captured by Az. brevis even after 20 min. Moreover, the captured Atta were sometimes simply discarded and not taken to the nest by Az. brevis. As a consequence, the major function of the galleries built by Az. brevis may, therefore, be defense against intruders in contrast to Al. decemarticulatus which uses them mainly for prey capture. This may be due to a higher need for protein in Al. decemarticulatus compared to coccid-raising Az. brevis

Trade-offs in an ant–plant–fungus mutualism

Species engaged in multiple, simultaneous mutualisms are subject to trade-offs in their mutualistic investment if the traits involved in each interaction are overlapping, which can lead to conflicts and affect the longevity of these associations. We investigate this issue via a tripartite mutualism involving an ant plant, two competing ant species and a fungus the ants cultivate to build galleries under the stems of their host plant to capture insect prey. The use of the galleries represents an innovative prey capture strategy compared with the more typical strategy of foraging on leaves. However, because of a limited worker force in their colonies, the prey capture behaviour of the ants results in a trade-off between plant protection (i.e. the ants patrol the foliage and attack intruders including herbivores) and ambushing prey in the galleries, which has a cascading effect on the fitness of all of the partners. The quantification of partners' traits and effects showed that the two ant species differed in their mutualistic investment. Less investment in the galleries (i.e. in fungal cultivation) translated into more benefits for the plant in terms of less herbivory and higher growth rates and vice versa. However, the greater vegetative growth of the plants did not produce a positive fitness effect for the better mutualistic ant species in terms of colony size and production of sexuals nor was the mutualist compensated by the wider dispersal of its queens. As a consequence, although the better ant mutualist is the one that provides more benefits to its host plant, its lower host–plant exploitation does not give this ant species a competitive advantage. The local coexistence of the ant species is thus fleeting and should eventually lead to the exclusion of the less competitive species

Data from: Trade-offs in an ant–plant–fungus mutualism

Species engaged in multiple, simultaneous mutualisms are subject to trade-offs in their mutualistic investment if the traits involved in each interaction are overlapping, which can lead to conflicts and affect the longevity of these associations. We investigate this issue via a tripartite mutualism involving an ant plant, two competing ant species and a fungus the ants cultivate to build galleries under the stems of their host plant to capture insect prey. The use of the galleries represents an innovative prey capture strategy compared with the more typical strategy of foraging on leaves. However, because of a limited worker force in their colonies, the prey capture behaviour of the ants results in a trade-off between plant protection (i.e. the ants patrol the foliage and attack intruders including herbivores) and ambushing prey in the galleries, which has a cascading effect on the fitness of all of the partners. The quantification of partners' traits and effects showed that the two ant species differed in their mutualistic investment. Less investment in the galleries (i.e. in fungal cultivation) translated into more benefits for the plant in terms of less herbivory and higher growth rates and vice versa. However, the greater vegetative growth of the plants did not produce a positive fitness effect for the better mutualistic ant species in terms of colony size and production of sexuals nor was the mutualist compensated by the wider dispersal of its queens. As a consequence, although the better ant mutualist is the one that provides more benefits to its host plant, its lower host–plant exploitation does not give this ant species a competitive advantage. The local coexistence of the ant species is thus fleeting and should eventually lead to the exclusion of the less competitive species

New findings in insect fungiculture: Have ants developed non-food, agricultural products?

The interaction between Allomerus plant-ants and an ascomycete fungus growing on and strengthening their galleries is not opportunistic. We previously demonstrated that this association is highly specific as only one fungal species represented by a few haplotypes was found associated with the ants. We also discovered that the ants' behavior revealed a major investment in manipulating and enhancing the growth of their associated fungus. We have growing evidence that this specificity is consistent with selection by the ants. Here, we discuss this selection within the framework of insect agriculture, as we believe these ants fulfill all of the prerequisites to be considered as farmers. Allomerus ants promote their symbiont's growth, protect it from potential pathogens and select specific cultivars. Taken together, we think that the interaction between Allomerus ants and their cultivar might represent the first case of insect fungiculture used as a means of obtaining building material

Hirtella datasets

Hirtella dataset

Trade-offs in mutualistic investment ESM from Trade-offs in mutualistic investment in a tripartite symbiosis

Detailed methodology and supplementary dat

<i>Hirtella physophora</i> leaves, flowers and fruits.

<p>(a) Leaves bear leaf pouches (left arrow) at the base of their laminas. <i>Allomerus decemarticulatus</i> workers capture a green locust thanks to their trap: a gallery made using severed host plant trichomes and the mycelium of an Astomycota fungus that the ants manipulate to create a composite material pierced by numerous holes (from under which the workers ambush prey). A wasp is seen robbing a piece of the locust abdomen; the wasp was also captured in turn as was the red Reduviid (right arrow). (b) At the distal position of the branch, flowers are segregated on racemous inflorescences at different stages of maturation from flower buds to fully open flowers. (c) Development of young, green (i.e. unripe) drupes. (d) A dark purple (i.e. ripe) drupe. Scale bars represent 1 cm.</p

Four developmental stages of <i>Hirtella physphora</i> leaves.

<p>(a) Juvenile leaves: less than 5 cm long, positioned vertically; the domatia are not fully developed. (b) Expanding leaves: have fully developed domatia, but the blade is still immature. (c) Young leaves: from 15 to 25 cm long; positioned horizontally, mature but still relatively tender, and light green in color. (d) Old leaves: older, non-senescent, mature leaves of up to 30 cm in length, positioned horizontally, stiff, and dark green in color. Scale bars represent 5 cm.</p