How does an ecological cost of a protective mutualism affect the evolution of flower phenotype?

Abstract

Individuals interact simultaneously during their life cycle with multiple mutualistic partners that provides different resources or services. Although we have information about the effect of multiple mutualisms on the same individual on local ecological scale, the evolutionary consequences of the co-occurrence of different mutualisms on one lineage has been mostly neglected. This study aims to fill this gap, investigating the macroevolutionary trajectories of plant traits mediating two types of mutualisms simultaneously occurring on plants: protective and pollination mutualism. Plant species bearing extrafloral nectaries (EFN) attract ant partners that reduce plant herbivory damage by repelling or preying on herbivores. However, these ants can also negatively interact with pollinators by repelling or preying on them, decreasing pollination success. The indirect negative interaction between ant bodyguards and pollinators of EFN-bearing plants represents an ecological cost that may lead to marked evolutionary implications for the plant traits mediating both interactions. In a meta-analysis that is part of my thesis, I observed that ants have an overall negative effect on the patterns of flower visitation by bees, but not by other floral visitors. Translating it into an evolutionary perspective, it is reasonable to expect that plants with EFNs that are also pollinated by animals, specially by bees, are selected to develop strategies to reduce this conflict over the evolutionary time (e.g. spatial or temporal segregation between EFNs and flowers). To evaluate these strategies, I will investigate the macroevolutionary trajectory of plant phenotypic traits mediating plant interactions with ant bodyguards and pollinators. For that, I will adopt two different sampling strategies: a broader scale perspective exploring the evolution of EFN and poricidal anthers, a common trait of plants exclusively pollinated by bees, across Angiosperms species, and a narrower scale perspective, exploring the evolution of EFN and floral traits in the bee-pollinated legume genus Chamaecrista (Fabaceae). In the first sampling strategy, I will combine the EFN database compiled by Dr. Marjorie Weber and the poricidal anther dataset compiled by Dr. Mario Vallejo-Marin. I hypothesize that the evolutionary arising and maintenance of extrafloral nectaries on plants is negatively associated with the evolution of poricidal anthers. In the second approach, I will conduct a literature search on floral and EFN traits of Chamaecrista. I hypothesize that the spatial or temporal separation between the protective mutualism and the pollination mutualism will increase across evolutionary time. I will develop this project in collaboration with Dr. Marjorie Weber who is an expert in EFN biology and mutualisms using comparative phylogenetic methods. Additionally, this study is co-advised by Dr. Anselmo Nogueira, PI of a FAPESP JP research grant (process number: 19/19544-7) which this proposal is linked to. Thus, the execution of this project will enable not only the improvement of my theoretical skills as an evolutionary ecologist, but also allow the establishment of a new international partnership that will improve the quality of the products resulting from a FAPESP grant and contribute to the internationalization of Brazilian science. (AU)