Environmental drivers for cheaters of arbuscular mycorrhizal symbiosis in tropical rainforests

Abstract

Summary Hundreds of nonphotosynthetic mycoheterotrophic plant species cheat the arbuscular mycorrhizal symbiosis. Their patchy local occurrence suggests constraints by biotic and abiotic factors, among which the role of soil chemistry and nutrient status has not been investigated. Here, we examine the edaphic drivers predicting the local‐scale distribution of mycoheterotrophic plants in two lowland rainforests in South America. We compared soil chemistry and nutrient status in plots where mycoheterotrophic plants were present with those without these plants. Soil pH, soil nitrate, and the interaction between soil potassium and nitrate concentrations were the best predictors for the occurrence of mycoheterotrophic plants in these tropical rainforests. Mycoheterotrophic plant occurrences decreased with a rise in each of these predictors. This indicates that these plants are associated with low‐fertility patches. Such low‐fertility conditions coincide with conditions that potentially favour a weak mutualism between plants and arbuscular mycorrhizal fungi according to the trade balance model. Our study points out which soil properties favour the cheating of arbuscular mycorrhizal networks in tropical forests. The patchy occurrence of mycoheterotrophic plants suggests that local soil heterogeneity causes the stability of arbuscular mycorrhizal networks to vary at a very small scale.

Cheating in arbuscular mycorrhizal mutualism: a network and phylogenetic analysis of mycoheterotrophy

“…Third, such a pattern of reciprocal specializations could also come from ecological constraints limiting the niches and habitats of mycoheterotrophic plants. Indeed, mycoheterotrophic plants often tend to occur specifically in patches of low soil fertility (Gomes et al , 2019). It is important to acknowledge that although the global pattern of reciprocal specialization observed in the present work is likely to be linked to cheating, it also might be influenced by the specific local environmental conditions where cheating is promoted.…”

Plant cheaters preferentially target arbuscular mycorrhizal fungi that are highly connected to mutualistic plants

“…Since mycoheterotrophic plants are relatively rare and often have patchy distributions (Gomes et al , 2019b), we sampled two proximate 4 × 4 m plots (plot 1 and plot 2) in a coastal rainforest in French Guiana (5°28’25”N 53°34’51”W) on 28 July 2014, with overlapping mycoheterotrophs as replicates. In both plots, root tips of mycoheterotrophic plants (cheaters) and surrounding autotrophic plants (mutualists) were sampled, cleaned with water, and stored on CTAB buffer at −20°C until further processing.…”

The Evolution of Mutualistic Dependence

“…Or is it because stabilizing mechanisms have likewise evolved that prevent cheating from spreading, for instance, partner choice or sanctions (e.g., Kiers et al 2003) that diminish cheater success and occurrence? Local factors can change the frequency of cheaters in a system, as shown in mycoheterotrophic plant species that cheat the arbuscular mycorrhizal symbiosis, depending on soil heterogeneity (Gomes et al 2019). Work on the legume-rhizobia symbiosis suggests the existence Arms-race dynamic: evolutionary mechanism that typically occurs in host-parasite interactions involving adaptations and counteradaptations occurring as positive feedbacks By-product mutualism: a mutualism in which the benefit to one partner has no cost for the other, and thus there is no benefit to cheating or exploitation of an arms-race dynamic between rhizobium genotypes that provide negligible mutualist services to hosts and hosts with mechanisms that defend against these rhizobia (Gano-Cohen et al 2019).…”