Recurrent mutualism breakdown events in a legume rhizobia metapopulation

Bacterial mutualists generate major fitness benefits for eukaryotes, reshaping the host phenotype and its interactions with the environment. Yet, microbial mutualist populations are predicted to generate mutants that defect from providing costly services to hosts while maintaining the capacity to exploit host resources. Here, we examined the mutualist service of symbiotic nitrogen fixation in a metapopulation of root-nodulating Bradyrhizobium spp . that associate with the native legume Acmispon strigosus . We quantified mutualism traits of 85 Bradyrhizobium isolates gathered from a 700 km transect in California spanning 10 sampled A. strigosus populations. We clonally inoculated each Bradyrhizobium isolate onto A. strigosus hosts and quantified nodulation capacity and net effects of infection, including host growth and isotopic nitrogen concentration. Six Bradyrhizobium isolates from five populations were categorized as ineffective because they formed nodules but did not enhance host growth via nitrogen fixation. Six additional isolates from three populations failed to form root nodules. Phylogenetic reconstruction inferred two types of mutualism breakdown, including three to four independent losses of effectiveness and five losses of nodulation capacity on A. strigosus . The evolutionary and genomic drivers of these mutualism breakdown events remain poorly understood.

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases in which two species cease to cooperate and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways toward breakdowns of the mutualism between plants and arbuscular mycorrhizal fungi. By using a comparative approach, we identify ∼25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.

Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases where two species cease to cooperate, and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways towards breakdowns of the mutualism between plants and arbuscular mycorrhizal (AM) fungi. Using a comparative approach, we identify ~25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants either: (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.Significance StatementCooperative interactions among species – mutualisms – are major sources of evolutionary innovation. However, despite their importance, two species that formerly cooperated sometimes cease their partnership. Why do mutualisms breakdown? We asked this question in the partnership between arbuscular mycorrhizal (AM) fungi and their plant hosts, one of the most ancient mutualisms. We analyse two potential trajectories towards evolutionary breakdown of their cooperation, symbiont switching and mutualism abandonment. We find evidence that plants stop interacting with AM fungi when they switch to other microbial mutualists or when they evolve alternative strategies to extract nutrients from the environment. Our results show vital cooperative interactions can be lost - but only if successful alternatives evolve.

Partner abundance controls mutualism stability and the pace of morphological change over geologic time

Mutualisms that involve symbioses among specialized partners may be more stable than mutualisms among generalists, and theoretical models predict that in many mutualisms, partners exert reciprocal stabilizing selection on traits directly involved in the interaction. A corollary is that mutualism breakdown should increase morphological rates of evolution. We here use the largest ant-plant clade (Hydnophytinae), with different levels of specialization for mutualistic ant symbionts, to study the ecological context of mutualism breakdown and the response of a key symbiosis-related trait, domatium entrance hole size, which filters symbionts by size. Our analyses support three predictions from mutualism theory. First, all 12 losses apparently only occur from a generalist symbiotic state. Second, mutualism losses occurred where symbionts are scarce, in our system at high altitudes. Third, domatium entrance hole size barely changes in specialized symbiotic species, but evolves rapidly once symbiosis with ants has broken down, with a “morphorate map” revealing that hotspots of entrance hole evolution are clustered in high-altitude areas. Our study reveals that mutualistic strategy profoundly affects the pace of morphological change in traits involved in the interaction and suggests that shifts in partners’ relative abundances may frequently drive reversions of generalist mutualisms to autonomy.