The role of indirect effects in coevolution as mutualism transitions into antagonism

Abstract

Species interactions have evolved from antagonistic to mutualistic and back several times throughout life’s history. Yet, it is unclear how changes in the type of interaction between species alter the coevolutionary dynamics of entire communities. This is a pressing matter, as transitions from mutualisms to antagonisms may be becoming more common with human-induced global change. Here, we combine network and evolutionary theory to simulate how shifts in interaction types alter the coevolution of empirical communities. We show that as mutualistic networks shift to antagonistic, selection imposed by direct partners begins to outweigh that imposed by indirect partners. This weakening of indirect effects is associated with communities losing their tight integration of traits and increasing their rate of adaptation. The above changes are more pronounced when specialist consumers are the first species to switch to antagonism. A shift in the outcome of species’ interactions may therefore reverberate across communities and alter the direction and speed of coevolution.

Effects of habitat destruction on coevolving metacommunities

“…While mutualistic networks become more connected and nested with habitat loss (positive PC1 values), antagonistic networks become more modular (negative PC1 values). As nested networks achieve greater trait similarity across all species (Pedraza et al, 2021), we find smaller changes in spatial trait variability in mutualistic communities. Conversely, while antagonistic species in some modules coevolve, others may lack partners altogether and evolve toward their environmental optima, thus reducing their spatial trait variability.…”

“…Firstly, as expected, habitat loss reduces species' regional abundance (Figure S5), making the local networks smaller (Figure 3 and Figure S6, bottom panels). Smaller networks achieve higher trait similarity (Figure 5 and Pedraza et al, 2021). Secondly, habitat loss makes the local species composition more varied across the landscape (Figure S7 and Urban & Skelly, 2006), leading to different coevolutionary trajectories.…”

“…As predicted by theory (Fortuna et al, 2013), and confirmed empirically (Chase et al, 2020; Haddad et al, 2015), habitat destruction reduces species' regional abundance resulting in the remaining pristine habitats harbouring smaller networks (Figure 6, top left panel). Since smaller networks achieve higher trait similarity (see also Pedraza et al, 2021), and local species composition becomes more varied with habitat loss (see also Urban & Skelly, 2006), differences between the local coevolutionary outcomes develop, thus altering the geographic mosaic of coevolution (Figure 6, top right panel). We found that this leads to increased spatial trait variability of mutualists.…”

When cheating turns into a stabilizing mechanism of mutualistic networks

“…Innovative cheating could also emerge because of divergent optimal trait matching between plant and pollinators (37), leading to an arm race between them, than is likely to evolve towards antagonistic interactions (38), and thus innovative cheating in this context. Given the importance of innovative cheating for community stability, our results stress the need to revisit eco-evolutionary theory of cheating in a network context (11,39). This future direction would provide new insights on the astonishing faculty of evolutionary processes to sometimes create structures that promote ecological stability at the community level (40).…”

“…However, it is hard to substantiate this idea because studies focusing on cheating and evolution of mutualism considered conservative cheating only (8-10, 24, 30). Given the importance of innovative cheating for community stability, our results stress the need to revisit eco-evolutionary theory of cheating in a network context (11,31). This future direction would provide new insights on the astonishing faculty of evolutionary processes to sometimes create structures that promote ecological stability at the community level.…”