The effects of above- and belowground mutualisms on orchid speciation and coexistence.

Both pollination by animals and mycorrhizal symbioses with fungi are believed to have been important for the diversification of flowering plants. However, the mechanisms by which these above- and belowground mutualisms affect plant speciation and coexistence remain obscure. We provide evidence that shifts in pollination traits are important for both speciation and coexistence in a diverse group of orchids, whereas shifts in fungal partner are important for coexistence but not for speciation. Phylogenetic analyses show that recently diverged orchid species tend either to use different pollinator species or to place pollen on different body parts of the same species, consistent with the role of pollination-mode shifts in speciation. Field experiments provide support for the hypothesis that colonization of new geographical areas requires adaptation to new pollinator species, whereas co-occurring orchid species share pollinator species by placing pollen on different body parts. In contrast to pollinators, fungal partners are conserved between closely related orchid species, and orchids recruit the same fungal species even when transplanted to different areas. However, co-occurring orchid species tend to use different fungal partners, consistent with their expected role in reducing competition for nutrients. Our results demonstrate that the two dominant mutualisms in terrestrial ecosystems can play major but contrasting roles in plant community assembly and speciation.

Flies and flowers in Darwin's race.

The idea of coevolution originated with Darwin's proposal that long-proboscid pollinators and long-tubed flowers might be engaged in reciprocal selection, but this has not been demonstrated. Here we test key aspects of Darwin's hypothesis of reciprocal selection in an experiment with naturally interacting populations of extremely long-proboscid flies (Moegistorhynchus longirostris: Nemestinidae) and long-tubed irises (Lapeirousia anceps: Iridaceae). We show that the benefit derived by both the fly (volume of nectar consumed) and the plant (number pollen grains received) depends on the relative length of their interacting organs. Each trait is shown to act both as agent and target in directional reciprocal selection, potentially leading to a race. This understanding of how fitness in both species varies in relation to the balance of their armament allows us to make tentative predictions about the nature of selection across multiple communities. We find that in each community a core group of long-tubed plant species might together be involved in diffuse coevolution with the fly. In poorly matched populations, the imbalance in armament is too great to allow reciprocal selection to act, and these species might instead experience one-sided selection that leads to convergence with the core species. Reciprocal selection drives the evolution of the community, then, additional species become attached to the network of interacting mutualists by convergence.