Testing the evolutionary drivers of nitrogen-fixing symbioses in challenging soil environments

Abstract

- While the importance of root nodular symbioses (RNS) in plants has long been recognized, the ecological and evolutionary factors maintaining RNS remain obscure. RNS is associated with environmental stressors such as aridity and nitrogen-poor soils; the ability to tolerate harsh environments may provide ecological opportunities for diversification, yet, nodulators are also diverse outside these environments. - We test several environmental determinants of increased survival and enhanced diversification of RNS species, using an explicitly phylogenetic approach for the first time. We assembled the largest phylogeny of the nitrogen-fixing clade to date and a comprehensive set of abiotic niche estimates and nodulation data. We used comparative phylogenetic tools to test environmental and diversification associations. - We found that RNS is associated with warm, arid, and nitrogen-poor habitats. However, RNS was gained long before lineages entered these habitats. RNS is associated with accelerated diversification, but diversification rates are heterogeneous among nodulators, and non-legume nodulators do not show elevated diversification. - Our findings undermine the interpretation that RNS directly drove the invasion of challenging habitats, and do not support a direct relationship between soil or climate and the diversity of nodulators. Still, RNS may have been an important exaptation allowing further niche evolution.

Spatial phylogenetics of Fagales: Investigating the history of temperate forests

“…1C) was unexpected. Previous studies have supported aridity as favoring RNS (Pellegrini et al, 2016;Siniscalchi et al, 2022) and especially the phylogenetic diversity of RNS (Doby et al, 2022).…”

“…The copyright holder for this preprint (which this version posted April 18, 2023. ; https://doi.org/10.1101/2023.04.17.537249 doi: bioRxiv preprint 2019), so we elected to use a recent approach combining genomic data with all Fagales sequences available on GenBank (Siniscalchi et al, 2022). This tree, based on 20 regions from the nucleus, chloroplast, and mitochondrion, comprises 707 species of Fagales (60.2% of species-level diversity; Stevens, 2001 onwards) with complete genus-level representation.…”

“…Briefly, the tree was reconstructed by aggregating all GenBank data available for these 20 markers, as well as extracting these same markers from a recent large-scale sequencing initiative (Kates et al, 2022). Tree inference, performed in RAxML-NG (Kozlov et al, 2019), was constrained by a high-quality backbone based on nuclear phylogenomic data derived from Kates et al (2022); analytical details are available in Siniscalchi et al (2022).…”

“…The copyright holder for this preprint (which this version posted April 18, 2023. ; https://doi.org/10.1101/2023.04.17.537249 doi: bioRxiv preprint Environmental associates of grid cell metrics-We fit a series of models under a model choice paradigm to assess the best environmental predictors of RPD, CANAPE endemism categories, and proportion of grid cell species engaging in nodulation. Environmental data were summarized by eight selected predictors chosen based on the biology of the plants following previous work in the clade (Doby et al, 2022;Siniscalchi et al, 2022): aridity (calculated as the UNEP aridity index following Folk et al, 2020), mean annual temperature (bio1), temperature annual range (bio7; included as a measure of temperature seasonality), annual precipitation (bio12), temperature of the driest quarter (bio17; included as a measure of precipitation seasonality), elevation, and three soil predictors: nitrogen content (chosen to study RNS distribution), soil pH, and soil carbon content (the latter two well-known as constraining plant distributions).…”

Phylogenetic diversity and regionalization of root nodule symbiosis

“…Root nodule symbiosis (RNS), a central adaptation in legumes, is intimately related to their predilection for arid open habitats (Sprent, 2007(Sprent, , 2009Sprent et al, 2017). A series of recent studies primarily focused on legumes (Adams et al, 2016;Doby et al, 2022;Pellegrini et al, 2016;Siniscalchi et al, 2022) has identified water stress as the preeminent driver of the geographic distribution of RNS, species richness, and phylogenetic diversity, reflecting the importance of nitrogen leaf economics for confronting drought challenge (Adams et al, 2016). This relationship suggests an important link between edaphic ecology and precipitation, with the former often seen as secondary in tropical forest ecology (Gentry, 1988).…”