The Effects of Above- and Belowground Mutualisms on Orchid Speciation and Coexistence

Abstract

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 aboveand 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.

The epiphytic orchids Ionopsis utricularioides and Psygmorchis pusilla associate with different Ceratobasidium lineages at Valle del Cauca, Colombia

“…Co-occurring orchid species tend to use different fungal partners, consistent with their expected role in reducing competition for nutrients (Waterman et al 2011). Although without a broader sampling approach it is difficult to verify, we hypothesize that these two orchid species use different fungal partners as a strategy to succeed in the same environment.…”

Forest tree neighborhoods are structured more by negative conspecific density dependence than by interactions among closely related species

“…and Levine 2010) and positive interactions among individuals (Waterman et al 2011) should all act to increase the relatedness of neighboring individuals over time (Fig. 1b).…”

The intimacy between sexual traits and Grime’s CSR strategies for orchids coexisting in semi-natural calcareous grassland at the Olive Lawn

“…Can these explain coexistence? Co-occurring orchid species are known to exhibit floral/pollinator differences that are especially important for the separation and coexistence of recently diverged species (Waterman et al 2011; see also Waser 1983). In general, pollinators are considered a resource for which plants compete (Rathcke 1983;Pierce et al 2007) and the differential exploitation of resources (resource partitioning) is essential for niche segregation and thus coexistence (Martin 1996).…”

“…Pollinator resource partitioning is hypothesized to play a key role in the assembly of flowering plant communities (e.g. Armbruster et al 1994), and specifically the divergence of floral traits has been implicated in the speciation and subsequent coexistence of South African oil-secreting orchids (subtribe Coryciinae; Waterman et al 2011).…”

“…However, although floral/pollination differences are important during speciation less closely related orchid species tend to form pollination guilds in which pollinators are shared, and pollinator resource partitioning is evidently less important to coexistence (Waterman et al 2011). Even species that are extremely specialized, such as the European bee orchids (Ophrys spp.…”