Functional genomics and co-occurrence in a diverse tropical tree genus: The roles of drought and defense related genes

Tropical tree communities are among the most diverse in the world. A small number of genera often disproportionately contribute to this diversity. How so many species from a single genus can co-occur represents a major outstanding question in biology. Niche differences are likely to play a major role in promoting congeneric diversity, but the mechanisms of interest are often not well-characterized by the set of functional traits generally measured by ecologists. To address this knowledge gap, we used a functional genomic approach to investigate the mechanisms of co-occurrence in the hyper-diverse genus Ficus. Our study focused on over 800 genes related to drought and defense, providing detailed information on how these genes may contribute to the diversity of Ficus species. We find widespread and consistent evidence of the importance of defense gene dissimilarity in co-occurring species, providing genetic support for what would be expected under the Janzen-Connell mechanism. We also find that drought-related gene sequence similarity is related to Ficus co-occurrence, indicating that similar responses to drought promote co-occurrence. We provide the first detailed functional genomic evidence of how drought- and defense-related genes simultaneously contribute to the local co-occurrence in a hyper-diverse genus. Our results demonstrate the potential of community transcriptomics to identify the drivers of species co-occurrence in hyper-diverse tropical tree genera.

Methods
In this work, we utilized a community transcriptomics workflow to assess the functional similarity of co-occurring 13 Ficus species in 20-ha tropical forest dynamics plot in Xishuangbanna, Yunnan Province, China. We used a torus-translation test to quantify the habitat associations of focal Ficus tree species. Then we performed functional phylogenomic inference using the techniques and tools that recently published in the Yang et al. (2015), and then estimated the homologous functional gene trees of Ficus species in the community, in particular, the distance separating species in a gene tree represents the degree of their functional gene similarity. To investigate whether the degree of sequence similarity in drought and defense genes was related to the degree of pairwise species co-occurrence in the plot, we conducted a statistical approach that involved correlating the genetic distance between two species with their co-occurrence at the 20 m × 20 m scale in the forest dynamics plot. We used these gene trees to calculate the SES value for each 20 X 20 m subplot, and then compared these observed SES values to a null distribution to test for significant deviations from random co-occurrence patterns. We used a linear model to examine the association between the SES value and soil moisture gradient.