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Synergistic effect of multiple mutualists on plants: how bacteria, ants and bees contribute to the evolution of a hyper-diverse lineage of legumes

Abstract

In the last decades, we have experienced a large increase in the research interest in mutualistic interactions. Mutualism is now best viewed as reciprocal exploitation in which the benefits often outweigh the associated costs of interactions, with the net benefit varying as a function of biotic and abiotic factors that directly or indirectly modify costs and benefits. Although variable, the benefits arising from mutualistic partners have been recognized as one of the major drivers of species diversification and forces fueling the functioning and maintenance of several critical ecosystem services, including pollination, seed dispersal, nitrogen fixation, and carbon cycling. Despite such recent advances, much of our current knowledge has been built by studies focusing on only one type of mutualism. This view is incomplete, given that individuals of different species are commonly involved in more than one mutualism simultaneously. The joint effect of multiple mutualistic partners on a focal organism probably makes the outcome of such interactions much more variable than currently expected, as multiple partners may have synergistic, additive, neutral or diminished effects on the joint fitness benefits of the focal mutualist. Therefore, we propose a theoretical framework that will allow us to investigate the functioning of the three most common mutualism-involving plants (nitrogen fixation by rhizobial bacteria, protection by ants, and pollination), and that co-occurs in species of Chamaecrista (Fabaceae). Based on this information, we will be able to explore the interactive effect of such simultaneous mutualisms on the evolution of plants belonging to this hyper-diverse clade. As the nitrogen fixation symbiosis is established at an early age, we start focusing on this mutualism and on its the potential direct or indirect impact on the subsequent mutualisms in which the individuals will engage on. Our first aim is to investigate how different mutualisms can interfere with the outcome of each other when they are happening simultaneously in the same focal plant. As Chamaecrista plants offer carbohydrate-rich rewards for both ant guards (via extrafloral nectar) and rhizobial symbionts, we hypothesize the simultaneous occurrence of these mutualisms will impose a trade-off to the focal plants in which a higher investment in the bacteria partners implies a reduction in the investment in ant guards. On the other hand, the increase in the nitrogen availability due to the rhizobia association will favor the pollination via increasing plant investment on floral attributes. Our second aim is to investigate the adaptive signature of different mutualistic plant traits and the evolutionary trade-off or synergism between them. We hypothesized that there is a trade-off in the evolution of nodules and nectaries attributes and synergism in the evolution of nodules and flower traits. Finally, the third aim is to synthesize evidence for conflicting or synergistic effects of mutualisms on plants from published empirical studies, first evaluating the effect of ant protection on pollination efficiency and the effect of plant-rhizobia symbiosis on ant defense. This project can generate a large amount of data that may help us to understand factors driving the functioning of the ecological services resultant from the mutualisms approached here. In Brazil, Fabaceae is the most species-rich angiosperm family in several ecosystems, with some lineages being highly endemic. Therefore, understanding the role of mutualistic partners on the evolution of this clade and the role of those plants on the functioning of mutualisms may help us to understand part of the ecological services in our native ecosystems. (AU)