Long-term nitrogen addition causes the evolution of less-cooperative mutualists

Abstract

Human activities have altered the global nitrogen (N) cycle, and as a result, elevated N inputs are causing profound ecological changes in diverse ecosystems. The evolutionary consequences of this global change have been largely ignored even though elevated N inputs are predicted to cause mutualism breakdown and the evolution of decreased cooperation between resource mutualists. Using a long-term (22 years) N-addition experiment, we find that elevated N inputs have altered the legume-rhizobium mutualism (where rhizobial bacteria trade N in exchange for photosynthates from legumes), causing the evolution of less-mutualistic rhizobia. Plants inoculated with rhizobium strains isolated from N-fertilized treatments produced 17-30% less biomass and had reduced chlorophyll content compared to plants inoculated with strains from unfertilized control plots. Because the legume-rhizobium mutualism is the major contributor of naturally fixed N to terrestrial ecosystems, the evolution of less-cooperative rhizobia may have important environmental consequences.

Ecological genomics of mutualism decline in nitrogen-fixing bacteria

“…Thus R. leguminosarum in nature appear to form dynamic, diverse populations that are unified by gene flow despite selection acting at one or more loci. In our case, where genomic islands of differentiation (this study) and large phenotypic differences [5] were detected, selection due to N addition must be exceptionally strong.…”

“…On the one hand, new mutations could have arisen and increased in frequency atop a diverse phylogeny of rhizobium strains (selection on new mutations); on the other hand, pre-existing alleles could have increased in frequency (selection on standing genetic variation). Given the levels of nucleotide diversity found throughout the genome, in addition to our observations of substantial standing variation in partner quality variation within the control plots [5], we suspect that the alleles at the key outlier region on the pSym pre-dated the establishment of the N plots-i.e. that selection has acted on standing genetic variation.…”

Nitrogen deposition decreases the benefits of symbiosis in a native legume

“…We find it fascinating that both in our experiment and in the field sites we nonetheless observe that A. strigosus plants are always highly nodulated. If hosts are gaining little or no benefit from rhizobia but continue to allow nodulation, this could lead to the evolutionary degradation of host traits that differentiate beneficial from ineffective rhizobia (Sachs and Simms 2006;Kiers et al 2010), as has been suggested by research on soybean (Kiers et al 2007) and experimental populations of clover (Weese et al 2015). An important caveat for our work is that we did not assess benefits that UCR lines gain from sympatric Bradyrhizobium strains.…”

“…Over longer time scales, exposure to N r deposition and enrichment could favor plants that adapt to better utilize mineral N r for growth or tolerate high soil N r concentrations, as can occur in agricultural systems (Herridge and Danso 1995). Moreover, increased N r concentrations in soil is predicted to lead to plants that depend less on BNF and thus evolve relaxed control over rhizobia (Kiers et al 2007;Akcay and Simms 2011;Regus et al 2014;Weese et al 2015).…”

Application of herb chronology: Annual fertilization and climate reveal annual ring signatures within the roots of US tallgrass prairie plants

“…In fact, increased nitrogen inputs may even negatively affect the legume-rhizobium mutualism and result in decreased foliar biomass in some legumes (Weese et al 2015). The extent to which this negative reaction may exist may highly differ from plant to plant, possibly explaining the weakness of intra-treatment pairwise correlation we found with D. purpurea.…”