Linking metacommunity theory and symbiont evolutionary ecology

Processes that occur both within and between hosts can influence the ecological and evolutionary dynamics of symbionts, a broad term that includes parasitic and disease-causing organisms. Metacommunity theory can integrate these local- and regional-scale dynamics to explore symbiont community composition patterns across space. In this article I emphasize that symbionts should be incorporated into the metacommunity concept. I highlight the utility of metacommunity theory by discussing practical and general benefits that emerge from considering symbionts in a metacommunity framework. Specifically, investigating the local and regional drivers of symbiont community and metacommunity structure will lead to a more holistic understanding of symbiont ecology and evolution and could reveal novel insights into the roles of symbiont communities in mediating host health.     

A specific mix of generalists: bacterial symbionts in Mediterranean Ircinia spp

Microbial symbionts form abundant and diverse components of marine sponge holobionts, yet the ecological and evolutionary factors that dictate their community structure are unresolved. Here, we characterized the bacterial symbiont communities of three sympatric host species in the genus Ircinia from the NW Mediterranean Sea, using electron microscopy and replicated 16S rRNA gene sequence clone libraries. All Ircinia host species harbored abundant and phylogenetically diverse symbiont consortia, comprised primarily of sequences related to other sponge-derived microorganisms. Community-level analyses of bacterial symbionts revealed host species-specific genetic differentiation and structuring of Ircinia-associated microbiota. Phylogenetic analyses of host sponges showed a close evolutionary relationship between Ircinia fasciculata and Ircinia variabilis, the two host species exhibiting more similar symbiont communities. In addition, several bacterial operational taxonomic units were shared between I.?variabilis and Ircinia oros, the two host species inhabiting semi-sciophilous communities in more cryptic benthic habitats, and absent in I.?fasciculata, which occurs in exposed, high-irradiance habitats. The generalist nature of individual symbionts and host-specific structure of entire communities suggest that: (1) a 'specific mix of generalists' framework applies to bacterial symbionts in Ircinia hosts and (2) factors specific to each host species contribute to the distinct symbiont mix observed in Ircinia hosts.     

Evolution in bacterial plasmids and levels of selection

Gene flow between different reproductive units such as bacterial plasmids and chromosomes presents unusual problems for evolutionary analysis. Far more than in eukaryotes, reproductive advantages at several levels of selection--genes, transposons, plasmids, cells, and clones--must be considered simultaneously to understand plasmid evolution. No level consistently prevails in conflict situations, and some reproductive units carry genes that restrain their own reproduction or survival, apparently to enhance the reproduction or survival of the higher-level reproductive units that carry them. Despite gene flow between plasmids and chromosomes, genes for certain functions show strong tendencies to occur on plasmids while others consistently occur on chromosomes. Functions generally associated with plasmids are diverse, but all are useful only in locally restricted contexts; it is argued that the selective consequences of the greater horizontal (within generation) transmission of plasmids are responsible for this pattern. The tendency for prokaryote transposons, which are also horizontally mobile, to carry genes similar to those commonly on plasmids supports this argument. The apparent trends in eukaryote plasmids and transposons to lack these same characters also accords with predictions of the local adaptation hypothesis, because genes on these genetic units are generally no more horizontally mobile than chromosomal genes. There are theoretical reasons to expect that plasmid genes tend to evolve more rapidly than chromosomal genes. "The selfish interests of genes have manifestly produced 'vehicles' in the forms of organelles, cells, individuals and yet higher units. If evolution is to predict as well as describe, then selfish interests must be understood in the framework of the constraints and opportunities generated by these 'vehicles'" (Buss, 1987, p. 182).     

Species differences in plasmid carriage in the Enterobacteriaceae

Modern concerns about the spread of antibiotic resistance raise questions about the effect of bacterial species on plasmid evolution and maintenance. We studied 223 Enterobacteriaceae isolated from wild mammals and determined the number of plasmids per isolate, the size of those plasmids, and the distribution of plasmid incompatibility groups N, P, W, FII, and A/C. All of these variables were non-randomly distributed with respect to bacterial species, suggesting that host-cell factors constrain the plasmids that a strain will carry. The implication for the evolution of multiple-resistance plasmids in a clinical setting is that although inter-generic plasmid transfer may introduce a novel resistance plasmid into a bacterial genus, it is likely to be modified to suit the requirements of the new host cell. This then further suggests that resistance plasmids will evolve independent lineages within bacterial species although the genes incorporated in them may have come from the same original source.     

An ecological cost associated with protective symbionts of aphids

Beneficial symbioses are widespread and diverse in the functions they provide to the host ranging from nutrition to protection. However, these partnerships with symbionts can be costly for the host. Such costs, so called “direct costs”, arise from a trade‐off between allocating resources to symbiosis and other functions such as reproduction or growth. Ecological costs may also exist when symbiosis negatively affects the interactions between the host and other organisms in the environment. Although ecological costs can deeply impact the evolution of symbiosis, they have received little attention. The pea aphid Acyrthosiphon pisum benefits a strong protection against its main parasitoids from protective bacterial symbionts. The ecological cost of symbiont‐mediated resistance to parasitism in aphids was here investigated by analyzing aphid behavior in the presence of predatory ladybirds. We showed that aphids harboring protective symbionts expressed less defensive behaviors, thus suffering a higher predation than symbiont‐free aphids. Consequently, our study indicates that this underlined ecological cost may affect both the coevolutionary processes between symbiotic partners and the prevalence of such beneficial bacterial symbionts in host natural populations.     

Plasmid-mediated horizontal gene transfer is a coevolutionary process

Conjugative plasmids are key agents of horizontal gene transfer (HGT) that accelerate bacterial adaptation by vectoring ecologically important traits between strains and species. However, although many conjugative plasmids carry beneficial traits, all plasmids exert physiological costs-of-carriage on bacteria. The existence of conjugative plasmids, therefore, presents a paradox because non-beneficial plasmids should be lost to purifying selection, whereas beneficial genes carried on plasmids should be integrated into the bacterial chromosome. Several ecological solutions to the paradox have been proposed, but none account for co-adaptation of bacteria and conjugative plasmids. Drawing upon evidence from experimental evolution, we argue that HGT via conjugation can only be fully understood in a coevolutionary framework.     

Intraspecific phylogenetic congruence among multiple symbiont genomes

Eukaryotes often form intimate endosymbioses with prokaryotic organisms. Cases in which these symbionts are transmitted cytoplasmically to host progeny create the potential for co-speciation or congruent evolution among the distinct genomes of these partners. If symbionts do not move horizontally between different eukaryotic hosts, strict phylogenetic congruence of their genomes is predicted and should extend to relationships within a single host species. Conversely, even rare 'host shifts' among closely related lineages should yield conflicting tree topologies at the intraspecific level. Here, we investigate the historical associations among four symbiotic genomes residing within an aphid host: the mitochondrial DNA of Uroleucon ambrosiae aphids, the bacterial chromosome of their Buchnera bacterial endosymbionts, and two plasmids associated with Buchnera. DNA sequence polymorphisms provided a significant phylogenetic signal and no homoplasy for each data set, yielding completely and significantly congruent phylogenies for these four genomes and no evidence of horizontal transmission. This study thus provides the first evidence for strictly vertical transmission and 'co-speciation' of symbiotic organisms at the intraspecific level, and represents the lowest phylogenetic level at which such coevolution has been demonstrated. These results may reflect the obligate nature of this intimate mutualism and indicate opportunities for adaptive coevolution among linked symbiont genomes.     

Rule-based modelling of conjugative plasmid transfer and incompatibility

COSMIC-rules, an individual-based model for bacterial adaptation and evolution, has been used to study virtual transmission of plasmids within bacterial populations, in an environment varying between supportive and inhibitory. The simulations demonstrate spread of antibiotic resistance (R) plasmids, both compatible and incompatible, by the bacterial gene transfer process of conjugation. This paper describes the behaviour of virtual plasmids, their modes of exchange within bacterial populations and the impact of antibiotics, together with the rules governing plasmid transfer. Three case studies are examined: transfer of an R plasmid within an antibiotic-susceptible population, transfer of two incompatible R plasmids and transfer of two compatible R plasmids. R plasmid transfer confers antibiotic resistance on recipients. For incompatible plasmids, one or other plasmid could be maintained in bacterial cells and only that portion of the population acquiring the appropriate plasmid-encoded resistance survives exposure to the antibiotics. By contrast, the compatible plasmids transfer and mix freely within the bacterial population that survives in its entirety in the presence of the antibiotics. These studies are intended to inform models for examining adaptive evolution in bacteria. They provide proof of principle in simple systems as a platform for predicting the behaviour of bacterial populations in more complex situations, for example in response to changing environments or in multi-species bacterial assemblages.     

Lineage‐specific plasmid acquisition and the evolution of specialized pathogens in Bacillus thuringiensis and the Bacillus cereus group

Bacterial plasmids can vary from small selfish genetic elements to large autonomous replicons that constitute a significant proportion of total cellular DNA. By conferring novel function to the cell, plasmids may facilitate evolution but their mobility may be opposed by co‐evolutionary relationships with chromosomes or encouraged via the infectious sharing of genes encoding public goods. Here, we explore these hypotheses through large‐scale examination of the association between plasmids and chromosomal DNA in the phenotypically diverse Bacillus cereus group. This complex group is rich in plasmids, many of which encode essential virulence factors (Cry toxins) that are known public goods. We characterized population genomic structure, gene content and plasmid distribution to investigate the role of mobile elements in diversification. We analysed coding sequence within the core and accessory genome of 190 B. cereus group isolates, including 23 novel sequences and genes from 410 reference plasmid genomes. While cry genes were widely distributed, those with invertebrate toxicity were predominantly associated with one sequence cluster (clade 2) and phenotypically defined Bacillus thuringiensis. Cry toxin plasmids in clade 2 showed evidence of recent horizontal transfer and variable gene content, a pattern of plasmid segregation consistent with transfer during infectious cooperation. Nevertheless, comparison between clades suggests that co‐evolutionary interactions may drive association between plasmids and chromosomes and limit wider transfer of key virulence traits. Proliferation of successful plasmid and chromosome combinations is a feature of specialized pathogens with characteristic niches (Bacillus anthracis, B. thuringiensis) and has occurred multiple times in the B. cereus group.     

Bacterial genospecies that are not ecologically coherent: population genomics of Rhizobium leguminosarum

Biological species may remain distinct because of genetic isolation or ecological adaptation, but these two aspects do not always coincide. To establish the nature of the species boundary within a local bacterial population, we characterized a sympatric population of the bacterium Rhizobium leguminosarum by genomic sequencing of 72 isolates. Although all strains have 16S rRNA typical of R. leguminosarum, they fall into five genospecies by the criterion of average nucleotide identity (ANI). Many genes, on plasmids as well as the chromosome, support this division: recombination of core genes has been largely within genospecies. Nevertheless, variation in ecological properties, including symbiotic host range and carbon-source utilization, cuts across these genospecies, so that none of these phenotypes is diagnostic of genospecies. This phenotypic variation is conferred by mobile genes. The genospecies meet the Mayr criteria for biological species in respect of their core genes, but do not correspond to coherent ecological groups, so periodic selection may not be effective in purging variation within them. The population structure is incompatible with traditional ‘polyphasic taxonomy′ that requires bacterial species to have both phylogenetic coherence and distinctive phenotypes. More generally, genomics has revealed that many bacterial species share adaptive modules by horizontal gene transfer, and we envisage a more consistent taxonomic framework that explicitly recognizes this. Significant phenotypes should be recognized as ‘biovars'' within species that are defined by core gene phylogeny.     

A complete genome sequence for Pseudomonas syringae pv. pisi PP1 highlights the importance of multiple modes of horizontal gene transfer during phytopathogen evolution

Hybrid assembly strategies that combine long-read sequencing reads from Oxford Nanopore's MinION device combined with high-depth Illumina paired-end reads have enabled completion and circularization of both plasmids and chromosomes from multiple bacterial strains. Here we demonstrate the utility of supplementing Illumina paired-end reads from a previously published draft genome of P. syringae pv. pisi PP1 with long reads to generate a complete genome sequence for this strain. The phylogenetic placement and genomic repertoire of virulence factors within this strain provides a unique perspective on virulence evolution within P. syringae phylogroup 2, and highlights that strains can rapidly acquire virulence factors through horizontal gene transfer by acquisition of plasmids as well as through chromosomal recombination.     

Why do bacterial plasmids carry some genes and not others?

Previous explanations of why bacterial genes for certain "optional" traits tend to occur on plasmids rather than chromosomes are based on an outdated misunderstanding of natural selection. They also fail to explain why certain characters that are ubiquitous in some bacterial species tend to occur on plasmids. This paper shows that all major classes of traits usually associated with plasmids rather than chromosomes confer adaptations to locally restricted conditions. A new "local adaptation" model of plasmid evolution, based on simultaneous application of modern selection theory at the levels of gene, plasmid, cell, and clone reproduction, shows that genes coding local adaptations will reproduce more successfully when on plasmids than when on chromosomes, due to plasmids' greater horizontal mobility.     

The genome of alpha-proteobacteria : complexity, reduction, diversity and fluidity

The alpha-proteobacteria displayed diverse and often unconventional life-styles. In particular, they keep close relationships with the eucaryotic cell. Their genomic organization is often atypical. Indeed, complex genomes, with two or more chromosomes that could be linear and sometimes associated with plasmids larger than one megabase, have been described. Moreover, polymorphism in genome size and topology as well as in replicon number was observed among very related bacteria, even in a same species. Alpha-proteobacteria provide a good model to study the reductive evolution, the role and origin of multiple chromosomes, and the genomic fluidity. The amount of new data harvested in the last decade should lead us to better understand emergence of bacterial life-styles and to build the conceptual basis to improve the definition of the bacterial species.     

Patchy distribution of flexible genetic elements in bacterial populations mediates robustness to environmental uncertainty

The generation and maintenance of genetic variation seems to be a general ecological strategy of bacterial populations. Thereby they gain robustness to irregular environmental change, which is primarily the result of the dynamic evolution of biotic interactions. A benefit of maintaining population heterogeneity is that only a fraction of the population has to bear the cost of not (yet) beneficial deviation. On evolutionary time frames, an added value of the underlying mechanisms is evolvability, i.e. the heritable ability of an evolutionary lineage to generate and maintain genetic variants that are potentially adaptive in the course of evolution. Horizontal gene transfer is an important mechanism that can lead to differences between individuals within bacterial populations. Broad host-range plasmids foster this heterogeneity because they are typically present in only a fraction of the population and provide individual cells with genetic modules newly acquired from other populations or species. We postulate that the benefit of robustness on population level could balance the cost of transfer and replication functions that plasmids impose on their hosts. Consequently, mechanisms that make a subpopulation conducive to specific conjugative plasmids may have evolved, which could explain the persistence of even cryptic plasmids that do not encode any traits.     

Sex, ecology and the brain: evolutionary correlates of brain structure volumes in Tanganyikan cichlids

Analyses of the macroevolutionary correlates of brain structure volumes allow pinpointing of selective pressures influencing specific structures. Here we use a multiple regression framework, including phylogenetic information, to analyze brain structure evolution in 43 Tanganyikan cichlid species. We analyzed the effect of ecological and sexually selected traits for species averages, the effect of ecological traits for each sex separately and the influence of sexual selection on structure dimorphism. Our results indicate that both ecological and sexually selected traits have influenced brain structure evolution. The patterns observed in males and females generally followed those observed at the species level. Interestingly, our results suggest that strong sexual selection is associated with reduced structure volumes, since all correlations between sexually selected traits and structure volumes were negative and the only statistically significant association between sexual selection and structure dimorphism was also negative. Finally, we previously found that monoparental female care was associated with increased brain size. However, here cerebellum and hypothalamus volumes, after controlling for brain size, associated negatively with female-only care. Thus, in accord with the mosaic model of brain evolution, brain structure volumes may not respond proportionately to changes in brain size. Indeed selection favoring larger brains can simultaneously lead to a reduction in relative structure volumes.     

Environmental factors influence both abundance and genetic diversity in a widespread bird species

Genetic diversity is one of the key evolutionary variables that correlate with population size, being of critical importance for population viability and the persistence of species. Genetic diversity can also have important ecological consequences within populations, and in turn, ecological factors may drive patterns of genetic diversity. However, the relationship between the genetic diversity of a population and how this interacts with ecological processes has so far only been investigated in a few studies. Here, we investigate the link between ecological factors, local population size, and allelic diversity, using a field study of a common bird species, the house sparrow (Passer domesticus). We studied sparrows outside the breeding season in a confined small valley dominated by dispersed farms and small‐scale agriculture in southern France. Population surveys at 36 locations revealed that sparrows were more abundant in locations with high food availability. We then captured and genotyped 891 house sparrows at 10 microsatellite loci from a subset of these locations (N = 12). Population genetic analyses revealed weak genetic structure, where each locality represented a distinct substructure within the study area. We found that food availability was the main factor among others tested to influence the genetic structure between locations. These results suggest that ecological factors can have strong impacts on both population size per se and intrapopulation genetic variation even at a small scale. On a more general level, our data indicate that a patchy environment and low dispersal rate can result in fine‐scale patterns of genetic diversity. Given the importance of genetic diversity for population viability, combining ecological and genetic data can help to identify factors limiting population size and determine the conservation potential of populations.     

Hosts do not simply outsource pathogen resistance to protective symbionts

Microbial symbionts commonly protect their hosts from natural enemies, but it is unclear how protective symbionts influence the evolution of host immunity to pathogens. One possibility is that ‘extrinsic’ protection provided by symbionts allows hosts to reduce investment in ‘intrinsic’ immunological resistance mechanisms. We tested this idea using pea aphids (Acyrthosiphon pisum) and their facultative bacterial symbionts that increase host resistance to the fungal pathogen Pandora neoaphidis. The pea aphid taxon is composed of multiple host plant associated populations called biotypes, which harbor characteristic communities of symbionts. We found that biotypes that more frequently carry protective symbionts have higher, rather than lower, levels of intrinsic resistance. Within a biotype there was no difference in intrinsic resistance between clones that did and did not carry a protective symbiont. The host plant on which an aphid feeds did not strongly influence intrinsic resistance. We describe a simple conceptual model of the interaction between intrinsic and extrinsic resistance and suggest that our results may be explained by selection favoring both the acquisition of protective symbionts and enhanced intrinsic resistance in habitats with high pathogen pressure. Such combined protection is potentially more robust than intrinsic resistance alone.