Macroevolution of multiple mutualisms in the genus Chamaecrista: synergisms and conflicts in Cerrado and rocky outcrops lineage

Abstract

Mutualism is now best viewed as reciprocal exploitation. The benefits often outweigh the associated costs of interactions, with the outcome varying as a function of biotic and abiotic factors that directly or indirectly modify costs and benefits. Although variable, the benefits of 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. In plants, three mutualist associations are well known: (i) mutualism of pollen transport with bee species; (ii) protection mutualism with ant species protecting plants against herbivores and (iii) mutualism of nutrition with bacteria that can fix atmospheric nitrogen. Despite such recent advances, much of our current knowledge has been built by studies focusing on the evolution of 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 mutualisms on a focal organism probably makes the outcome of such interactions much more variable than currently expected. Multiple partners may have synergistic, additive, neutral, or diminished effects on the focal mutualist's joint fitness benefits. On the macroevolutionary scale, the emergence and modification of specialized structures in making plant resources available to mutualists may have been optimized by selection and constrained by other evolutionary forces. Given this context, our first aim is to investigate the adaptive signature in phenotypic divergence pattern between Chamaecrista species, considering different functional traits directly linked to mutualistic interactions with nitrogen-fixing bacteria, protective ants and pollinating bees. We will also investigate the evolutionary trade-off or synergism between these mutualistic traits. We hypothesized a trade-off in the evolution of nodules and extrafloral nectaries and synergism in the evolution of nodules and floral traits. We also hypothesize that the phenotypic divergence between species will have an adaptive signature with different optimal phenotypes between contrasting habitats, so we expect that species that grow under low levels of resources have had a reduction in the traits associated with mutualisms throughout the evolution of this plant lineage. 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 those plants' role in mutualisms' functioning may help us understand part of the ecological services in our native ecosystems. (AU)