Arbuscular mycorrhizal fungi promote coexistence and niche divergence of sympatric palm species on a remote oceanic island

Abstract

Summary Microbes can have profound effects on their hosts, driving natural selection, promoting speciation and determining species distributions. However, soil‐dwelling microbes are rarely investigated as drivers of evolutionary change in plants.We used metabarcoding and experimental manipulation of soil microbiomes to investigate the impact of soil and root microbes in a well‐known case of sympatric speciation, the Howea palms of Lord Howe Island (Australia). Whereas H. forsteriana can grow on both calcareous and volcanic soils, H. belmoreana is restricted to, but more successful on, volcanic soil, indicating a trade‐off in adaptation to the two soil types.We suggest a novel explanation for this trade‐off. Arbuscular mycorrhizal fungi (AMF) are significantly depleted in H. forsteriana on volcanic soil, relative to both H. belmoreana on volcanic soil and H. forsteriana on calcareous soil. This is mirrored by the results of survival experiments, where the sterilization of natural soil reduces Howea fitness in every soil–species combination except H. forsteriana on volcanic soil. Furthermore, AMF‐associated genes exhibit evidence of divergent selection between Howea species.These results show a mechanism by which divergent adaptation can have knock‐on effects on host–microbe interactions, thereby reducing interspecific competition and promoting the coexistence of plant sister species.

Out of sight, but no longer out of mind – towards an increased recognition of the role of soil microbes in plant speciation

“…The study by Osborne et al . also illustrates the challenge of genotype‐by‐environment interactions for microbiome features, which complicate the evolutionary relationship between plants and microbes and appear to be both strong and common (Peiffer et al ., ; Wagner et al ., ). One possible cause of microbiome genotype‐by‐environment interactions is microbial biogeography: host genetic variation that affects recruitment of a particular symbiont may be undetectable in environments where that symbiont is absent.…”

“…Another common assumption is that the ‘core’ microbiome – the subset of microbes found in all or most individuals of a given plant species – is more important to host function than the microbes found only in some individuals. The study on Lord Howe Island palms by Osborne et al . illustrates how such assumptions may overestimate the importance of some micro‐organisms while overlooking non‐ubiquitous microbes that are actually critical. For instance, a simple sterilization experiment showed that H. forsteriana growing on volcanic soil derives no fitness benefit from its natural root microbiome.…”

“…In light of the accumulating evidence for specificity in several host plant species toward a restricted pool of fungal symbionts, the possible role of mycorrhizal fungi in plant speciation has long been hypothesized (Taylor et al ., ). In this issue of New Phytologist , Osborne et al . (pp. 1254–1266) present an elegant study on how specific arbuscular mycorrhizal fungi (AMF) can facilitate sympatric speciation by niche divergence in sister host‐plant species.…”

“…This is among the very first, and perhaps the most detailed study on the role of soil microbes in plant speciation. Osborne et al . not only report habitat‐driven differences in soil fungal community composition, which is in line with similar data from other biomes as well (Bonito et al ., ), but they also present a well‐documented example of the key innovation needed by the host to colonize a new habitat (calcareous soil) that is drastically different from the original habitat (volcanic soil). This innovation is the ability to associate with a new set of symbiotic fungi that are crucial for establishment and reproduction in the newly colonized habitat.…”

“…Both symbiotic mutualists and pathogens, two functional groups that have the most direct effects on plant and animal survival and reproduction, generally show strong compositional differences among habitats at a landscape scale (Geml et al ., ; Grau et al ., ). Because many of these exhibit substantial differences in interacting with various plants and animals, these soil microbes can enable the co‐existence of closely related species, either by niche divergence, as shown in Osborne et al ., or by density‐dependent interactions.…”