Neighbourhood defence gene similarity effects on tree performance: a community transcriptomic approach

Abstract

1. The structure and dynamics of ecological communities are ultimately the outcome of the differential demographic rates of individuals. Individual growth and mortality rates largely result from the interaction between an organism's phenotype and the abiotic and biotic environment. Functional traits have been used extensively over the past decade to elucidate links among phenotypes, demography and community dynamics. 2. A fundamental weakness of most functional trait approaches is the use of 'soft' traits associated with resource acquisition to examine how neighbourhood similarity affects tree survival and growth. However, these 'soft' traits are unlikely to be good predictors of similarities among co-occurring species. Less easily measured aspects of organismal functionsuch as those related to defencehave frequently gone unmeasured. This is particularly problematic for testing important hypotheses in forest ecology, such as the Janzen-Connell hypothesis where focal trees are expected to be at a disadvantage if their neighbours share the same natural enemies. 3. A potential alternative to functional trait approaches is to quantify the transcriptomic or functional genomic similarity of species. Such analyses are now possible in natural systems where de novo transciptome assemblies can be used to conduct functional phylogenomic analyses where homologous gene trees are produced. Using demographic plot data for 21 species from a North American forest dynamic plot, we conduct a community functional phylogenomic analysis of a plant community to elucidate the similarity in defence response genes across species. This similarity was then used to ask whether the similarity in defence genes of heterospecific species in the local neighbourhood of a focal individual tree influences its growth and mortality rates. 4. The results show that individual growth rates are higher when surrounded by dissimilar heterospecific species for 16 of 27 defence genes analysed. Additionally, survival rates are increased when an individual is in a neighbourhood with dissimilar species for 4 of the 27 defence genes studied. Lastly, strong conspecific effects were found in all analyses, underscoring that future analyses investigating the genetic variation and differential expression of defence-related genes in neighbourhoods may prove important. 5. Synthesis. In summary, this research leverages recent advances in RNA sequencing and bioinformatics to conduct community-wide transcriptomic analyses and analyses of defence-related gene similarity across a tree community. The results demonstrate that defence gene similarity in neighbourhoods often does have negative effects on individual demographic performance as predicted by the Janzen-Connell hypothesis.

Dos and don'ts when inferring assembly rules from diversity patterns

“…The diversity of expressed functions could help to provide insights into assembly processes that are much more tightly linked to physiological responses than the standard trait diversity measures, which are often based on “soft” traits (i.e., few easily measurable features). For example, a recent community‐wide transcriptomic analysis has supported the Janzen–Connell hypothesis by demonstrating that growth rates and survival of individual trees were higher when the neighbourhood consisted of trees with dissimilar (rather than similar) defense genes (Zambrano et al, 2017). However, even more than with metabarcoding, this approach adds uncertainty with respect to traditional surveys that are linked to sampling, laboratory work and interpretation of results (Wang et al, 2016).…”

Functional perspectives on tropical tree demography and forest dynamics

“…However, recent work has been accomplished that compares many species simultaneously and successfully translates the results to ecological questions of general interest. For example, multiple studies have now investigated homologous gene similarities as it relates to drought effects (Kobayashi et al 2013;, light responses , and even defense (Zambrano et al 2017). Specifically, Zambrano et al (2017) annotated homologous gene trees for plant defense responses across 21 temperate species to test the Janzen-Connell hypothesis on species coexistence.…”

“…For example, multiple studies have now investigated homologous gene similarities as it relates to drought effects (Kobayashi et al 2013;, light responses , and even defense (Zambrano et al 2017). Specifically, Zambrano et al (2017) annotated homologous gene trees for plant defense responses across 21 temperate species to test the Janzen-Connell hypothesis on species coexistence. Bowsher et al (2017) determined differential gene expression in competition experiments for co-occurring Trifolium species to highlight potential niche axes differentiation that allow species to coexist and Kobayashi et al (2013) investigated the environmental influence on mass flowering of the tropical tree Shorea beccariana [Dipterocarpaceae].…”

Progress Towards Plant Community Transcriptomics: Pilot RNA-Seq Data from 24 Species of Vascular Plants at Harvard Forest

“…Genomic analyses of single species, although important, do not capture the larger patterns occurring within an interacting community of plants. Trancriptome profiling or genome sequencing of multiple species and individuals within a community will open new, integrative avenues of analyses and allow us to address existing questions that require sampling of floras and communities (Bragg et al, 2015;Fitzpatrick and Keller, 2015;Bowsher et al, 2017;Han et al, 2017;Swenson and Jones, 2017;Zambrano et al, 2017;Matthews et al, 2018;Subrahmaniam et al, 2018;Breed et al, 2019) . This is especially true for understanding responses to climate change where community level analyses are needed to capture the interacting dynamics of different species responses (Liu et al, 2018;Komatsu et al, 2019;Snell et al, 2019) .…”