A highly diverse clade of melanized fungi associated with leaves and trichomes of the endemic tree Metrosideros polymorpha at high elevation sites in Hawai'i
The Hawaiian Islands are among the most isolated landmasses on earth, separated by thousands of miles of ocean from the nearest continent. The youngest island in the Hawaiian chain, the Island of Hawai'i, is home to multiple volcanoes reaching 4000m in elevation. One of these volcanoes, Mauna Loa, is still considered active; the alpine ecosystems on its upper slopes are therefore undergoing primary succession within a matrix of recent (< 1500 year old) lava flows. This combination of isolation, high elevation, and early successional stage creates a distinctive environment in which few plant species are able to establish and grow. Of the hundreds of endemic tree species in the archipelago, only one grows at these highest elevation sites: Metrosideros polymorpha (Myrtaceae). The ancestral Metrosideros sp. is thought to have colonized the Hawaiian Islands between 4 and 6 million years ago and has since diversified to occupy almost all of the Islands’ distinct habitats. At high elevations on Mauna Loa, the combination of harsh environmental context and a uniquely adapted endemic host provides a rare opportunity to better understand both the ecology and evolution of plant-fungal symbioses in environments at the edge of habitability.
Across these high elevation sites (1800m and 2400m elevation), we observed remarkably high genetic diversity in a single novel clade of foliar fungi, potentially indicative of recent and extensive diversification. Previous work in M. polymorpha across a broad elevation gradient (100m to 2400m) encompassing these high elevation sites suggested that fungal endophyte species richness was generally higher at lower elevations. However, the exception to this pattern was the portion of diversity represented by the novel clade: that lineage yields exceptionally high diversity at the highest sites. Well‐supported phylogenetic reconstructions using both Bayesian and Maximum Likelihood approaches place the clade in the Teratosphaeriaceae (Dothideomycetes). While the initial surveys were based on culture‐free pyrosequencing of the ITS1 region, subsequent culture‐based investigations revealed that members of this and closely related clades are highly melanized, live in close association with the leaves and trichomes of their hosts, and grow exceptionally slowly in culture. Genetic analyses at the population level provide insight into the origins and distribution of these fungi across the highest points on volcanoes of the Hawaiian Islands, and prompt hypotheses regarding ecological modes in these unusual and extreme environments.