Darwin recognized that natural selection could not favor a trait in one species solely for the benefit of another species. The modern, selfish-gene view of the world suggests that cooperation between individuals, whether of the same species or different species, should be especially vulnerable to the evolution of noncooperators. Yet, cooperation is prevalent in nature both within and between species. What special circumstances or mechanisms thus favor cooperation? Currently, evolutionary biology offers a set of disparate explanations, and a general framework for this breadth of models has not emerged. Here, we offer a tripartite structure that links previously disconnected views of cooperation. We distinguish three general models by which cooperation can evolve and be maintained: (i) directed reciprocation--cooperation with individuals who give in return; (ii) shared genes--cooperation with relatives (e.g., kin selection); and (iii) byproduct benefits--cooperation as an incidental consequence of selfish action. Each general model is further subdivided. Several renowned examples of cooperation that have lacked explanation until recently--plant-rhizobium symbioses and bacteria-squid light organs--fit squarely within this framework. Natural systems of cooperation often involve more than one model, and a fruitful direction for future research is to understand how these models interact to maintain cooperation in the long term.
Diverse bacterial lineages form beneficial infections with eukaryotic hosts. The origins, evolution, and breakdown of these mutualisms represent important evolutionary transitions. To examine these key events, we synthesize data from diverse interactions between bacteria and eukaryote hosts. Five evolutionary transitions are investigated, including the origins of bacterial associations with eukaryotes, the origins and subsequent stable maintenance of bacterial mutualism with hosts, the capture of beneficial symbionts via the evolution of strict vertical transmission within host lineages, and the evolutionary breakdown of bacterial mutualism. Each of these transitions has occurred many times in the history of bacterial-eukaryote symbiosis. We investigate these evolutionary events across the bacterial domain and also among a focal set of well studied bacterial mutualist lineages. Subsequently, we generate a framework for examining evolutionary transitions in bacterial symbiosis and test hypotheses about the selective, ecological, and genomic forces that shape these events.conflict | cooperation | endosymbiont | major transition | phylogeny
Rhizobial bacteria nodulate legume roots and fix nitrogen in exchange for photosynthates. These symbionts are infectiously acquired from the environment and in such cases selection models predict evolutionary spread of uncooperative mutants. Uncooperative rhizobia – including nonfixing and non‐nodulating strains – appear common in agriculture, yet their population biology and origins remain unknown in natural soils. Here, a phylogenetically broad sample of 62 wild‐collected rhizobial isolates was experimentally inoculated onto Lotus strigosus to assess their nodulation ability and effects on host growth. A cheater strain was discovered that proliferated in host tissue while offering no benefit; its fitness was superior to that of beneficial strains. Phylogenetic reconstruction of Bradyrhizobium rDNA and transmissible symbiosis‐island loci suggest that the cheater evolved via symbiotic gene transfer. Many strains were also identified that failed to nodulate L. strigosus, and it appears that nodulation ability on this host has been recurrently lost in the symbiont population. This is the first study to reveal the adaptive nature of rhizobial cheating and to trace the evolutionary origins of uncooperative rhizobial mutants.
Mutualisms can be viewed as biological markets in which partners of different species exchange goods and services to their mutual benefit. Trade between partners with conflicting interests requires mechanisms to prevent exploitation. Partner choice theory proposes that individuals might foil exploiters by preferentially directing benefits to cooperative partners. Here, we test this theory in a wild legumerhizobium symbiosis.Rhizobial bacteria inhabit legume root nodules and convert atmospheric dinitrogen (N 2 ) to a plant available form in exchange for photosynthates. Biological market theory suits this interaction because individual plants exchange resources with multiple rhizobia. Several authors have argued that microbial cooperation could be maintained if plants preferentially allocated resources to nodules harbouring cooperative rhizobial strains. It is well known that crop legumes nodulate non-fixing rhizobia, but allocate few resources to those nodules. However, this hypothesis has not been tested in wild legumes which encounter partners exhibiting natural, continuous variation in symbiotic benefit.Our greenhouse experiment with a wild legume, Lupinus arboreus, showed that although plants frequently hosted less cooperative strains, the nodules occupied by these strains were smaller. Our survey of wild-grown plants showed that larger nodules house more Bradyrhizobia, indicating that plants may prevent the spread of exploitation by favouring better cooperators.
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Bacteria often infect their hosts from environmental sources, but little is known about how environmental and host-infecting populations are related. Here, phylogenetic clustering and diversity were investigated in a natural community of rhizobial bacteria from the genus Bradyrhizobium. These bacteria live in the soil and also form beneficial root nodule symbioses with legumes, including those in the genus Lotus. Two hundred eighty pure cultures of Bradyrhizobium bacteria were isolated and genotyped from wild hosts, including Lotus angustissimus, Lotus heermannii, Lotus micranthus, and Lotus strigosus. Bacteria were cultured directly from symbiotic nodules and from two microenvironments on the soil-root interface: root tips and mature (old) root surfaces. Bayesian phylogenies of Bradyrhizobium isolates were reconstructed using the internal transcribed spacer (ITS), and the structure of phylogenetic relatedness among bacteria was examined by host species and microenvironment. Inoculation assays were performed to confirm the nodulation status of a subset of isolates. Most recovered rhizobial genotypes were unique and found only in root surface communities, where little bacterial population genetic structure was detected among hosts. Conversely, most nodule isolates could be classified into several related, hyper-abundant genotypes that were phylogenetically clustered within host species. This pattern suggests that host infection provides ample rewards to symbiotic bacteria but that host specificity can strongly structure only a small subset of the rhizobial community.
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