Stabilité évolutive des mutualismes et mécanismes de contrôle : le cas d'une relation plante-fourmis

La lutte pour le plus grand bénéfice à moindre coût est supposée transformer tout organisme mutualiste en tricheur. Or l'ubiquité et la diversité des mutualismes contredisent ces prédictions théoriques, suggérant l'existence de mécanismes favorisant la stabilité de ces relations. Nous avons étudié l'association spécifique et obligatoire entre la plante Hirtella physophora et les fourmis Allomerus decemarticulatus. Par des approches mêlant écologie de terrain et biologie moléculaire, nous avons mis en évidence un conflit qui se manifeste via le comportement de castration parasitaire des fourmis. Ce conflit est maintenu sous contrôle par des mécanismes de sanctions et de fidélité au partenaire. Le résultat de leur mise en œuvre est modulé par des interactions avec d'autres organismes, eux aussi impliqués dans l'association. Notre étude met en lumière l'importance de l'appréhension des différentes dimensions écologiques, spatiales et temporelles dans la compréhension de la trajectoire évolutive d'un système d'interactions.The struggle to attain more for less is supposed to transform every mutualist into a cheater. However, mutualisms are ubiquitous and of major importance in ecosystems, suggesting the existence of mechanisms enhancing the maintenance of such relationships. We focused on the obligatory specific association between the plant Hirtella physophora (Chrysobalanaceae) and the ants Allomerus decemarticulatus (Myrmicineae). By combining field ecology and molecular biology, we highlighted a conflict that results in the parasitic castration behaviour of ants. This conflict is controlled thanks to sanctions and partner fidelity feedback. The outcome of these mechanism is affected by interactions with other organisms that are involved in the relationship. This study highlights the importance of investigating the ecological, spatial and temporal dimensions in order to understand the evolutionary fate of a mutualistic relationship

Dynamics of the association between a long-lived understory myrmecophyte and its specific associated ants

Myrmecophytic symbioses are widespread in tropical ecosystems and their diversity makes them useful tools for understanding the origin and evolution of mutualisms. Obligate ant–plants, or myrmecophytes, provide a nesting place, and, often, food to a limited number of plant–ant species. In exchange, plant–ants protect their host plants from herbivores, competitors and pathogens, and can provide them with nutrients

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

Data from: Limited gene dispersal and spatial genetic structure as stabilizing factors in an ant-plant mutualism

Comparative studies of the population genetics of closely associated species are necessary to properly understand the evolution of these relationships because gene flow between populations affects the partners' evolutionary potential at the local scale. As a consequence (at least for antagonistic interactions), asymmetries in the strength of the genetic structures of the partner populations can result in one partner having a co-evolutionary advantage. Here, we assess the population genetic structure of partners engaged in a species-specific and obligatory mutualism: the Neotropical ant-plant, Hirtella physophora, and its ant associate, Allomerus decemarticulatus. Although the ant cannot complete its life cycle elsewhere than on H. physophora and the plant cannot live for long without the protection provided by A. decemarticulatus, these species also have antagonistic interactions: the ants have been shown to benefit from castrating their host plant and the plant is able to retaliate against too virulent ant colonies. We found similar short dispersal distances for both partners, resulting in the local transmission of the association and, thus, inbred populations in which too virulent castrating ants face the risk of local extinction due to the absence of H. physophora offspring. On the other hand, we show that the plant populations probably experienced greater gene flow than did the ant populations, thus enhancing the evolutionary potential of the plants. We conclude that such levels of spatial structure in the partners' populations can increase the stability of the mutualistic relationship. Indeed, the local transmission of the association enables partial alignments of the partners' interests, and population connectivity allows the plant retaliation mechanisms to be locally adapted to the castration behaviour of their symbionts

Characterization of polymorphic microsatellite loci in the neotropical plant ant allomerus decemarticulatus (Formicidae: Myrmicinae) and multiplexing with other microsatellites from the ant subfamily Myrmicinae

International audienceFive polymorphic microsatellite loci of the arboreal ant Allomerus decemarticulatus (Myrmicinae) were isolated and characterized. The amplification and polymorphism of seven additional microsatellite loci, previously developed for the ant species A. octoarticulatus and Wasmannia auropunctata, were also tested and the amplification conditions necessary for genotyping the complete set of 12 multiplexed markers in A. decemarticulatus determined. The number of alleles per locus ranged from three to 15 and observed heterozygosity varied front 0.09 to 0.95. Cross-species amplification of these loci was also successfully achieved in additional species of the same ant subfamily, Myrmicinae. This set of microsatellite markers will be used in studies on the mating system and population genetic structure of Myrmicinae in general and A. decemarticulatus in particular

The potential effects of global warming on changes in canine leishmaniasis in a focus outside the classical area of the disease in Southern France

In 1994, an ecoepidemiologic study was carried out in the mid-Ariège valley (French Pyrenees) where autochthonous cases of canine leishmaniasis had been previously reported. Serologic samples were collected from 336 dogs in two groups of villages. The seroprevalences were 11.67% in the valley villages and only 1.43% in the foothill villages. Five lymph node biopsies were taken from serologically positive dogs, and resultant isolates were identified as Leishmania infantum zymodeme MON-1. Phlebotomine sandflies were collected in five locations by CDC light traps. Both of the known French vectors, Phlebotomus ariasi and P. perniciosus, were identified. Bioclimatic and floristic studies showed that this area is an enclave of the supra-Mediterranean climatic zone, containing a typically xerothermophilic Mediterranean flora. The Pyrenees Mountains are usually considered to be outside of the endemic range of leishmaniasis in southern France, and so our demonstration of a microfocus of canine leishmaniasis in the northern foothills is noteworthy. A second serologic survey carried out in 2007 (216 dogs) showed an inversion of the seropositive rates between the two groups of villages compared with those of 1994: only 2.72% in the valley villages and 11.32% in the foothills villages. The decrease of seroprevalence in the first area (valley villages) can be related to a considerable use of deltamethrin collars during the transmission season. The increase of seroprevalence of the foothill villages could be related to climatic conditions, since there was an increase of about 1°C in the mean annual temperatur

The reproductive biology of the myrmecophyte, Hirtella physophora, and the limitation of negative interactions between pollinators and ants

International audienceMyrmecophytism occurs in plants that offer ants a nesting space and, often, food rewards in exchange for protection from predators and competitors. Such biotic protection by ants can, however, interfere with the activity of pollinators leading to potential negative consequences for the plant’s reproduction. In this study, we focused on the association between the understory myrmecophyte, Hirtella physophora (Chrysobalanaceae), and its obligate ant partner, Allomerus decemarticulatus (Myrmicinae). We investigated the reproductive biology of H. physophora and the putative mechanisms that may limit ant–pollinator conflict. Our results show that H. physophora is an obligate outcrosser, self-incompatible, and potentially insect-pollinated species. The reproduction of H. physophora relies entirely on pollen transfer by pollinators that are likely quite specific. Potential interference between flower-visiting insects during pollination may also be lessened by a spatial and temporal segregation of ant and pollinator activities, thus enabling pollen transfer and fruit production

Using text-mined trait data to test for cooperate-and-radiate co-evolution between ants and plants.

Mutualisms may be "key innovations" that spur lineage diversification by augmenting niche breadth, geographic range, or population size, thereby increasing speciation rates or decreasing extinction rates. Whether mutualism accelerates diversification in both interacting lineages is an open question. Research suggests that plants that attract ant mutualists have higher diversification rates than non-ant associated lineages. We ask whether the reciprocal is true: does the interaction between ants and plants also accelerate diversification in ants, i.e. do ants and plants cooperate-and-radiate? We used a novel text-mining approach to determine which ant species associate with plants in defensive or seed dispersal mutualisms. We investigated patterns of lineage diversification across a recent ant phylogeny using BiSSE, BAMM, and HiSSE models. Ants that associate mutualistically with plants had elevated diversification rates compared to non-mutualistic ants in the BiSSE model, with a similar trend in BAMM, suggesting ants and plants cooperate-and-radiate. However, the best-fitting model was a HiSSE model with a hidden state, meaning that diversification models that do not account for unmeasured traits are inappropriate to assess the relationship between mutualism and ant diversification. Against a backdrop of diversification rate heterogeneity, the best-fitting HiSSE model found that mutualism actually decreases diversification: mutualism evolved much more frequently in rapidly diversifying ant lineages, but then subsequently slowed diversification. Thus, it appears that ant lineages first radiated, then cooperated with plants

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