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[This corrects the article DOI: 10.1371/journal.pone.0180729.].

Bacterial symbionts are widespread in insects and other animals. Most of them are predominantly vertically transmitted, along with their hosts' genes, and thus extend the heritable genetic variation present in one species. These passengers have a variety of repercussions on the host's phenotypes: besides the cost imposed on the host for maintaining the symbiont population, they can provide fitness advantages to the host or manipulate the host's reproduction. We argue that insect symbioses are ideal model systems for community genetics. First, bacterial symbionts directly or indirectly affect the interactions with other species within a community. Examples include their involvement in modifying the use of host plants by phytophagous insects, in providing resistance to natural enemies, but also in reducing the global genetic diversity or gene flow between populations within some species. Second, one emerging picture in insect symbioses is that many species are simultaneously infected with more than one symbiont, which permits studying the factors that shape bacterial communities; for example, horizontal transmission, interactions between host genotype, symbiont genotype and the environment and interactions among symbionts. One conclusion is that insects' symbiotic complements are dynamic communities that affect and are affected by the communities in which they are embedded.

Symbiont specificity, both at the phylotype and strain level, can have profound consequences for host ecology and evolution. However, except for insights from a few model symbiosis systems, the degree of partner fidelity and the influence of host versus environmental factors on symbiont composition are still poorly understood. Nutritional symbioses between invertebrate animals and chemosynthetic bacteria at deep-sea hydrothermal vents are examples of relatively selective associations, where hosts affiliate only with particular, environmentally acquired phylotypes of gammaproteobacterial or campylobacterial symbionts. In hydrothermal vent snails of the sister genera Alviniconcha and Ifremeria, this phylotype specificity has been shown to play a role in habitat distribution and partitioning among different holobiont species. However, it is currently unknown if fidelity goes beyond species-level associations and influences genetic structuring, connectivity, and habitat adaptation of holobiont populations. We used metagenomic analyses to assess sequence variation in hosts and symbionts and identify correlations with geographic and environmental factors. Our analyses indicate that host populations are not differentiated across an ∼800-km gradient, while symbiont populations are clearly structured between vent locations due to a combination of neutral and selective processes. Overall, these results suggest that host individuals flexibly associate with locally adapted strains of their specific symbiont phylotypes, which supports a long-standing but untested paradigm of the benefits of horizontal transmission. Symbiont strain flexibility in these snails likely enables host populations to exploit a range of habitat conditions, which might favor widespread genetic connectivity and ecological resilience unless physical dispersal barriers are present.

Aim: Highly host-specific symbionts are very rarely found except with their typical host species. Although switches to new hosts are rare and difficult to detect, a switch to a host phylogenetically distant from the original one (a 'major host switch') could allow diversification of the symbionts onto the new host lineage. The consequences of such major host switches on the diversification of highly host-specific symbionts of animals have rarely been explored. Here, we examine the host specificity of vane-dwelling feather mites, a group that shows strong specificity, together with their host-switching dynamics and the consequences of major host switches for their diversification. Location: Global. Time period: From 1882 to 2015. Major taxa studied: Feather mites and birds. Methods: Using the largest published dataset of feather mite–bird associations, we analysed raw, phylogenetic and geographical host specificity of feather mites. We studied host-switching dynamics by describing the sharing by feather mites of bird species with different phylogenetic distances. For three of the most species-rich feather mite families, we quantified the consequences of major host switches for feather mite diversification. Results: Most feather mite species (84%) inhabit one to three very closely related host species. Assemblages of feather mites on birds do not show a geographical signature, but rather show strong host-driven structuring. The probability that a mite species occurs on two host species decays sharply with host phylogenetic distance, with only one instance of a feather mite species occupying distantly related hosts from different orders. However, results suggest that despite the strong host specificity, a few major host switches triggered the origin of 21% of the species and 38% of the genera of the mite families studied. Main conclusions: We show that feather mites are highly host-specific symbionts, whose assemblages do not show geographical structure, even at a continental scale. We conclude that major host switches are very rare events with strong macroevolutionary consequences for feather mite diversity.

Background Dinoflagellates in the family Symbiodiniaceae are important photosynthetic symbionts in cnidarians (such as corals) and other coral reef organisms. Breakdown of the coral-dinoflagellate symbiosis due to environmental stress (i.e. coral bleaching) can lead to coral death and the potential collapse of reef ecosystems. However, evolution of Symbiodiniaceae genomes, and its implications for the coral, is little understood. Genome sequences of Symbiodiniaceae remain scarce due in part to their large genome sizes (1–5 Gbp) and idiosyncratic genome features. Results Here, we present de novo genome assemblies of seven members of the genus Symbiodinium , of which two are free-living, one is an opportunistic symbiont, and the remainder are mutualistic symbionts. Integrating other available data, we compare 15 dinoflagellate genomes revealing high sequence and structural divergence. Divergence among some Symbiodinium isolates is comparable to that among distinct genera of Symbiodiniaceae. We also recovered hundreds of gene families specific to each lineage, many of which encode unknown functions. An in-depth comparison between the genomes of the symbiotic Symbiodinium tridacnidorum (isolated from a coral) and the free-living Symbiodinium natans reveals a greater prevalence of transposable elements, genetic duplication, structural rearrangements, and pseudogenisation in the symbiotic species. Conclusions Our results underscore the potential impact of lifestyle on lineage-specific gene-function innovation, genome divergence, and the diversification of Symbiodinium and Symbiodiniaceae. The divergent features we report, and their putative causes, may also apply to other microbial eukaryotes that have undergone symbiotic phases in their evolutionary history.

Ambrosia beetles and their microbial communities, housed in specialized structures termed mycangia, represent one of the oldest and most diverse systems of mutualism and parasitism described thus far. Comprised of core filamentous fungal members, but also including bacteria and yeasts, the mycangia represent a unique adaptation that allows beetles to store and transport their source of nutrition. Although perhaps the most ancient of “farmers,” the nature of these interactions remains largely understudied, with the exception of a handful of emerging pathosystems, where the fungal partner acts as a potentially devastating tree pathogen. Such virulence is often seen during “invasions,” where (invasive) beetles carrying the fungal symbiont/plant pathogen expand into new territories and presumably “naïve” trees. Here, we summarize recent findings on the phylogenetic relationships between beetles and their symbionts and advances in the developmental and genetic characterization of the mechanisms that underlie insect-fungal-plant interactions. Results on genomic, transcriptomic, and metabolomic aspects of these relationships are described. Although many members of the fungal Raffaelea-beetle symbiont genera are relatively harmless to host trees, specialized pathosystems including wilt diseases of laurel and oak, caused by specific subspecies (R. lauricola and R. quercus, in the USA and East Asia, respectively), have emerged as potent plant pathogens capable of killing healthy trees. With the development of genetic tools, coupled to biochemical and microscopic techniques, the ambrosia beetle-fungal symbiont is establishing itself as a unique model system to study the molecular determinants and mechanisms that underlie the convergences of symbioses, mutualism, parasitism, and virulence.Key points• Fungal-beetle symbioses are diverse and ancient examples of microbial farming.• The mycangium is a specialized structure on insects that houses microbial symbionts.• Some beetle symbiotic fungi are potent plant pathogens vectored by the insect.

The microbial symbionts of eukaryotes influence disease resistance in many host-parasite systems. Symbionts show substantial variation in both genotype and phenotype, but it is unclear how natural selection maintains this variation. It is also unknown whether variable symbiont genotypes show specificity with the genotypes of hosts or parasites in natural populations. Genotype by genotype interactions are a necessary condition for coevolution between interacting species. Uncovering the patterns of genetic specificity among hosts, symbionts, and parasites is therefore critical for determining the role that symbionts play in host-parasite coevolution. Here, we show that the strength of protection conferred against a fungal pathogen by a vertically transmitted symbiont of an aphid is influenced by both host-symbiont and symbiont-pathogen genotype by genotype interactions. Further, we show that certain symbiont phylogenetic clades have evolved to provide stronger protection against particular pathogen genotypes. However, we found no evidence of reciprocal adaptation of co-occurring host and symbiont lineages. Our results suggest that genetic variation among symbiont strains may be maintained by antagonistic coevolution with their host and/or their host’s parasites.

Diverse insects are associated with ancient bacterial symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here,we report an insect group wherein an ancient symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeast-like fungal symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal symbionts. Most fungal symbionts of cicadas were uncultivable, but the fungal symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal symbiont replacement. Genome sequencing of the fungal symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.

Ticks are among the most important vectors of pathogens affecting humans and other animals worldwide. They do not only carry pathogens however, as a diverse group of commensal and symbiotic microorganisms are also present in ticks. Unlike pathogens, their biology and their effect on ticks remain largely unexplored, and are in fact often neglected. Nonetheless, they can confer multiple detrimental, neutral, or beneficial effects to their tick hosts, and can play various roles in fitness, nutritional adaptation, development, reproduction, defense against environmental stress, and immunity. Non-pathogenic microorganisms may also play a role in driving transmission of tick-borne pathogens (TBP), with many potential implications for both human and animal health. In addition, the genetic proximity of some pathogens to mutualistic symbionts hosted by ticks is evident when studying phylogenies of several bacterial genera. The best examples are found within members of the , and genera: while in medical and veterinary research these bacteria are traditionally recognized as highly virulent vertebrate pathogens, it is now clear to evolutionary ecologists that many (if not most) , and bacteria are actually non-pathogenic microorganisms exhibiting alternative lifestyles as mutualistic ticks symbionts. Consequently, ticks represent a compelling yet challenging system in which to study microbiomes and microbial interactions, and to investigate the composition, functional, and ecological implications of bacterial communities. Ultimately, deciphering the relationships between tick microorganisms as well as tick symbiont interactions will garner invaluable information, which may aid in the future development of arthropod pest and vector-borne pathogen transmission control strategies.

Phyllosphere bacterial diversity is shaped through interactions between hosts and microbes. Most studies having focused on pairwise associations between host taxa and their symbionts, little is yet understood about the influence of the host community as a whole in shaping these interactions. Envisioning phyllosphere bacterial communities as a spatially structured network of communities linked by dispersal (i.e., metacommunities) can help us better understand the relative importance of species sorting among host populations and species versus dispersal from the neighboring host community for bacterial community assembly in forest ecosystems. Here we investigate drivers of metacommunity structure of epiphytic bacteria of the phyllosphere among 33 tree host species distributed across a large-scale transition from deciduous to boreal forest. We expect the identity and traits of hosts to play an important role in determining phyllosphere bacterial composition. We further hypothesize that bacterial dispersal from neighboring host species will modulate the match between a focal host species and its microbiota, and shape opportunities for host specialization of phyllosphere bacteria at local and regional scales. We defined specialization as the level of phylogenetic similarity among hosts that a bacterial symbiont associates with. We found that host taxonomic identity and traits were important drivers of bacterial community turnover and variation in host specialization across the landscape. Dispersal from neighboring communities further played a role in homogenizing bacterial communities. The microbiota of focal hosts such as sugar maple was thus increasingly similar to that of neighboring host species along the transition from deciduous to boreal forest. Specialization of bacterial taxa on sugar maple was further positively correlated with the relative abundance of this host in the landscape, revealing a role for the host community context in shaping evolutionary relationships between phyllosphere bacteria and their tree hosts. These results overall suggest that the dispersal of phyllosphere bacteria from the dominant tree community members may be constraining the match between tree species and their symbionts, particularly at their range limits. We also demonstrate that considering host-associated microbial communities as part of metacommunities within the host landscape is a promising tool for improving our understanding of host-symbiont matching.