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
Eukaryotic hosts must exhibit control mechanisms to select against ineffective bacterial symbionts. Hosts can minimize infection by less-effective symbionts ( partner choice) and can divest of uncooperative bacteria after infection (sanctions). Yet, such host-control traits are predicted to be context dependent, especially if they are costly for hosts to express or maintain. Legumes form symbiosis with rhizobia that vary in symbiotic effectiveness (nitrogen fixation) and can enforce partner choice as well as sanctions. In nature, legumes acquire fixed nitrogen from both rhizobia and soils, and nitrogen deposition is rapidly enriching soils globally. If soil nitrogen is abundant, we predict host control to be downregulated, potentially allowing invasion of ineffective symbionts. We experimentally manipulated soil nitrogen to examine context dependence in host control. We co-inoculated Lotus strigosus from nitrogen depauperate soils with pairs of Bradyrhizobium strains that vary in symbiotic effectiveness and fertilized plants with either zero nitrogen or growth maximizing nitrogen. We found efficient partner choice and sanctions regardless of nitrogen fertilization, symbiotic partner combination or growth season. Strikingly, host control was efficient even when L. strigosus gained no significant benefit from rhizobial infection, suggesting that these traits are resilient to short-term changes in extrinsic nitrogen, whether natural or anthropogenic.
Our data suggest an elegant cell autonomous mechanism by which legumes can detect and defend against ineffective rhizobia even when nodules harbor a mix of effective and ineffective rhizobial genotypes.
Symbioses are modelled as evolutionarily and ecologically variable with fitness outcomes for hosts shifting on a continuum from mutualism to parasitism. In a classic example, rhizobia fix atmospheric nitrogen for legume hosts in exchange for photosynthetic carbon. Rhizobial infection often enhances legume growth, but hosts also incur interaction costs because of root tissues and or metabolites needed to support symbionts in planta. Rhizobia exhibit genetic variation in symbiotic effectiveness, and ecological changes in light or mineral nitrogen availability can also alter the benefits of rhizobial infection for hosts. The net effects of symbiosis thus can range from mutualistic to parasitic in a context-dependent manner. We tested the extent of the mutualism-parasitism continuum in the legume-rhizobium symbiosis and the degree to which host investment can shape its limits. We infected Lotus strigosus with sympatric Bradyrhizobium genotypes that vary in symbiotic effectiveness. Inoculations occurred under different mineral nitrogen and light regimes spanning ecologically relevant ranges. Net growth benefits of Bradyrhizobium infection varied for Lotus and were reduced or eliminated dependent on Bradyrhizobium genotype, mineral nitrogen and light availability. But we did not detect parasitism. Lotus proportionally reduced investment in Bradyrhizobium as net benefit from infection decreased. Lotus control occurred primarily after infection, via fine-scale modulation of nodule growth, as opposed to control over initial nodulation. Our results show how divestment of symbiosis by Lotus can prevent shifts to parasitism.
The patterns and drivers of bacterial strain dominance remain poorly understood in natural populations. Here, we cultured 1292 Bradyrhizobium isolates from symbiotic root nodules and the soil root interface of the host plant Acmispon strigosus across a >840-km transect in California. To investigate epidemiology and the potential role of accessory loci as epidemic drivers, isolates were genotyped at two chromosomal loci and were assayed for presence or absence of accessory Bsymbiosis island^loci that encode capacity to form nodules on hosts. We found that Bradyrhizobium populations were very diverse but dominated by few haplotypeswith a single Bepidemic^haplotype constituting nearly 30 % of collected isolates and spreading nearly statewide. In many Bradyrhizobium lineages, we inferred presence and absence of the symbiosis island suggesting recurrent evolutionary gain and or loss of symbiotic capacity. We did not find statistical phylogenetic evidence that the symbiosis island acquisition promotes strain dominance and both symbiotic and nonsymbiotic strains exhibited population dominance and spatial spread. Our dataset reveals that a strikingly few Bradyrhizobium genotypes can rapidly spread to dominate a landscape and suggests that these epidemics are not driven by the acquisition of accessory loci as occurs in key human pathogens.
Summary1. The Northern Clade of the fish genus Poeciliopsis includes six closely related species, three of which lack placentas and three that have placentas but vary in the extent of post-fertilization provisioning. 2. We used this diversity to evaluate a series of hypotheses proposed in earlier publications concerning why the placenta has evolved. All hypotheses share the attribute of arguing that the placenta evolved to enhance the evolution of some other life-history trait, such as to reduce the age at maturation or to increase offspring size. We refer to these hypotheses collectively as 'life-history facilitation hypotheses'. 3. A general way to evaluate the plausibility of such proposals is to ask whether the evolution of the placenta is predictably associated with the evolution of other components of the life history. 4. We evaluated such associations in two ways. First, we performed a multivariate analysis of life-history data for fish collected and preserved in nature. This analysis included 16 populations across all six species. Secondly, we performed a more complete quantification of the life histories of the laboratory descendents from five populations representing four species, then performed a similar multivariate analysis. The laboratory study added information about the timing of reproduction (age at maturity, frequency of reproduction). 5. Both analyses yielded similar results, which were that the evolution of increased placentation is correlated with the evolution of a smaller size at first reproduction, the production of fewer and smaller offspring per litter, but an increase in the number of litters that were developing simultaneously in the ovary (superfetation). Increased placentation is associated with progressively earlier ages at maturation and shorter intervals between the birth of successive litters of offspring. Overall, increased placentation was associated with an increase in the rate of production of offspring early in life. A peculiar attribute of placentation is that this increase in the rate of offspring production can be attained despite a simultaneous reduction in the proportional quantity of resources devoted to reproduction. 6. These trends support one of the life history facilitation hypotheses, which is that placentation facilitates earlier maturity and a higher rate of reproduction early in life. They also suggest a possible connection between the evolution of the placenta and the well-established theory of life-history evolution, since these same life history attributes are predicted to evolve in response to exposure to high extrinsic rates of adult mortality.
Efficient host control predicts the extirpation of ineffective symbionts, but they are nonetheless widespread in nature. We tested three hypotheses for the maintenance of symbiotic variation in rhizobia that associate with a native legume: partner mismatch between host and symbiont, such that symbiont effectiveness varies with host genotype; resource satiation, whereby extrinsic sources of nutrients relax host control; and variation in host control among host genotypes. We inoculated Acmispon strigosus from six populations with three Bradyrhizobium strains that vary in symbiotic effectiveness on sympatric hosts. We measured proxies of host and symbiont fitness in single- and co-inoculations under fertilization treatments of zero added nitrogen (N) and near-growth-saturating N. We examined two components of host control: 'host investment' into nodule size during single- and co-inoculations, and 'host sanctions' against less effective strains during co-inoculations. The Bradyrhizobium strains displayed conserved growth effects on hosts, and host control did not decline under experimental fertilization. Host sanctions were robust in all hosts, but host lines from different populations varied significantly in measures of host investment in both single- and co-inoculation experiments. Variation in host investment could promote variation in symbiotic effectiveness and prevent the extinction of ineffective Bradyrhizobium from natural populations.
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