Parasitism within mutualist guilds explains the maintenance of diversity in multi-species mutualisms

Abstract

We consider here mutualisms where there are multiple species sharing a resource supplied by the same partner. If, as commonly assumed, there is competition between the species, then only the superior competitor should persist. Nevertheless, coexistence of multiple species sharing the same mutualistic partner is a widespread phenomenon. Regulation of nutrient exchange, where each species receives resources from the partner in proportion to the strength of the mutualism between the two, has been proposed as the main mechanism for coexistence in multi-species mutualisms involving the transfer of nutrients. Significant arguments, however, challenge the importance of partner selection processes. We present a mathematical model, applied to the arbuscular mycorrhizal symbiosis, to propose an alternative explanation for this coexistence. We show that asymmetric resource exchange between the plant and its fungal guild can lead to indirect parasitic interactions between guild members. In our model, the amount of carbon supplied by the plant to the fungi depends on both plant and fungal biomass, while the amount of phosphorus supplied by the fungi to the plant depends on both plant and fungal biomass when the plant is small, and effectively on fungal biomass only when the plant is large. As a consequence of these functional responses, more beneficial mutualists increase resource availability, and are indirectly exploited by less beneficial species that consume the resource and grow larger than they would in the absence of the better mutualists. As guild mutualists are not competing, competitive exclusion does not occur. Hence, the interaction structure can explain the maintenance of diversity within guilds in the absence of spatial structure and niche-related processes.

Diversity within mutualist guilds promotes coexistence and reduces the risk of invasion from an alien mutualist

“…In exchange, the plant provides fixed carbon to the fungi [42]. We use an existing model allowing for the coexistence of multiple mutualists [43] to model plant-fungi interactions, and consider the effect of adding direct competition between fungi. This new model therefore includes both mutualistic ( plant to fungi) and competitive (fungi to fungi) interactions.…”

“…Parameters α j and β j represent the ability of fungal species j to exchange phosphorus and carbon respectively. The choice of the functional forms of the f ( • , • ) functions, describing nutrients transfer, is tied to the biology and fully explained in [43]. Here we present a brief summary.…”

“…When only one fungal species is present, C(m j , m i ) is equal to 1 and equation (2.1) reduces to the original model of Martignoni et al [43]. When two or more species are present, competition between fungi reduces the carbon uptake capacity of each of the fungal species.…”

Co-inoculation with arbuscular mycorrhizal fungi differing in carbon sink strength induces a synergistic effect in plant growth

“…AM fungi can differ in their ability to provide phosphorus to the plant (Drew et al, 2003;Giovannini et al, 2020), or in their access to host carbon (Zhu and Miller, 2003), and these differences should by themselves result into differences in the plant growth dynamics (Afkhami et al, 2014). While some studies have investigated how plant productivity is affected by fungi to plant supply (i.e., phosphorus transfer), (Jansa et al, 2005;Mensah et al, 2015;Ibrahim, 2018;Martignoni et al, 2020a), changes in productivity due to carbon transfer (i.e., plant to fungi supply) have remained unexplored.…”

“…The need for a framework to study the mechanisms associated with the presence of multiple, functionally different mutualists has been recently highlighted also from the theoretical point of view (Afkhami et al, 2014). Theoretical work, however, has focused on explaining stable coexistence among mutualists (Bachelot and Lee, 2018;Johnson and Bronstein, 2019;Martignoni et al, 2020a), rather than on investigating the consequences of intraguild diversity on productivity. Multiple mutualists effects can potentially increase, reduce or have no repercussion on host performance, but it is unclear how interactions with the environment, direct and indirect interactions among mutualists, or nutrient exchange may contribute to the final outcome (Afkhami et al, 2014;Stanton, 2003).…”