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 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

Microsatellite data

This MSExcel file contains the microsatellite data used to run the clustering analyses

From museums to genomics: old herbarium specimens shed light on a C-3 to C-4 transition

International audienceCollections of specimens held by natural history museums are invaluable material for biodiversity inventory and evolutionary studies, with specimens accumulated over 300 years readily available for sampling. Unfortunately, most museum specimens yield low-quality DNA. Recent advances in sequencing technologies, so called next-generation sequencing, are revolutionizing phylogenetic investigations at a deep level. Here, the Illumina technology (HiSeq) was used on herbarium specimens of Sartidia (subfamily Aristidoideae, Poaceae), a small African-Malagasy grass lineage (six species) characteristic of wooded savannas, which is the C-3 sister group of Stipagrostis, an important C-4 genus from Africa and SW Asia. Complete chloroplast and nuclear ribosomal sequences were assembled for two Sartidia species, one of which (S. perrieri) is only known from a single specimen collected in Madagascar 100 years ago. Partial sequences of a few single-copy genes encoding phosphoenolpyruvate carboxylases (ppc) and malic enzymes (nadpme) were also assembled. Based on these data, the phylogenetic position of Malagasy Sartidia in the subfamily Aristidoideae was investigated and the biogeographical history of this genus was analysed with full species sampling. The evolutionary history of two genes for C-4 photosynthesis (ppc-aL1b and nadpme-IV) in the group was also investigated. The gene encoding the C-4 phosphoenolpyruvate caroxylase of Stipagrostis is absent from S. dewinteri suggesting that it is not essential in C-3 members of the group, which might have favoured its recruitment into a new metabolic pathway. Altogether, the inclusion of historical museum specimens in phylogenomic analyses of biodiversity opens new avenues for evolutionary studies

Data from: An ant–plant mutualism through the lens of cGMP-dependent kinase genes

In plant–animal mutualisms, how an animal forages often determines how much benefit its plant partner receives. In many animals, foraging behaviour changes in response to foraging gene expression or activation of the cGMP-dependent protein kinase (PKG) that foraging encodes. Here, we show that this highly conserved molecular mechanism affects the outcome of a plant–animal mutualism. We studied the two PKG genes of Allomerus octoarticulatus, an Amazonian ant that defends the ant–plant Cordia nodosa against herbivores. Some ant colonies are better ‘bodyguards’ than others. Working in the field in Peru, we found that colonies fed with a PKG activator recruited more workers to attack herbivores than control colonies. This resulted in less herbivore damage. PKG gene expression in ant workers correlated with whether an ant colony discovered an herbivore and how much damage herbivores inflicted on leaves in a complex way; natural variation in expression levels of the two genes had significant interaction effects on ant behaviour and herbivory. Our results suggest a molecular basis for ant protection of plants in this mutualism