Genotype specificity among hosts,pathogens, and beneficial microbes influences the strength of symbiont‐mediated protection

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.     

Coevolutionary dynamics in one-to-many mutualistic systems

“One-to-many” mutualisms are often observed in nature. In this type of mutualism, each host individual can interact with many symbionts, whereas each individual symbiont can interact with only one host individual. Partner choice by the host is a potentially critical mechanism for maintaining such systems; however, its long-term effects on the coevolution between the hosts and symbionts have not been completely explored. In this study, I developed a simple mathematical model to describe the coevolutionary dynamics between hosts and symbionts in a one-to-many mutualism. I assumed that each host chooses a constant number of symbionts from a potential symbiont population, a fraction of which are chosen through preferential choice on the basis of the cooperativeness of the symbionts and the rest are chosen randomly. Using numerical calculations, I found that mutualism is maintained when the preferential choice is not very costly and the mutation rate of symbionts is large. I also found that symbionts that receive benefits from hosts without a return (cheater symbionts) and hosts that do not engage in preferential partner choice (indiscriminator hosts) can coexist with mutualist symbionts and discriminator hosts, respectively. The parameter domain of pure mutualism, i.e., free from cheater symbionts and indiscriminator hosts, can be narrower than the whole domain where the mutualism persists.     

The evolutionary ecology of symbiont‐conferred resistance to parasitoids in aphids

Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal transmission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts have achieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont‐conferred resistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show that defensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of the host–parasitoid interaction, and by inducing environment‐dependent trade‐offs. These effects are conducive to very dynamic, symbiont‐mediated coevolution that is driven by frequency‐dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem by exploiting the parasitoids’ demonstrated ability to rapidly evolve counteradaptations to symbiont‐conferred resistance.     

Primary symbiont of the ancient scale insect family Coelostomidiidae exhibits strict cophylogenetic patterns

Bacterial symbionts play a critical role in the physiology, ecology and evolution of a diverse range of insects. Such symbionts with unknown roles in the ecology and evolution of their hosts have been reported from archaeococcoid scale insects of family Coelostomidiidae. We examine in detail the bacterial community associated with the remaining species of this family, and calculate the cophylogenetic relationship between the hosts and their symbionts. The 28S ribosomal RNA (rRNA) and mitochondrial cytochrome oxidase I genes were used to reconstruct the host phylogeny while the 16S rRNA gene was used for the bacterial phylogeny. Three well-supported clades were detected within the phylogeny of the monophyletic family Coelostomidiidae. Besides the known symbionts, a novel Sodalis-like symbiont was detected from three of the species. The primary bacteriome inhabiting B-symbiont (Bacteroidetes; ‘Candidatus Hoataupuhia coelostomidicola’) was widespread across the host family. Cophylogenetic comparison using Jungles-based reconciliation analysis and ParaFit statistical test revealed a strongly congruent phylogeny of this symbiont with the host family, with no host-switches and few losses and duplications. A similar pattern was observed across a relatively unrelated neococcoid family that exhibits a different physiology and symbiont community, besides a related Bacteroidetes symbiont. We reconfirm that the B-symbiont is a primary symbiont, owing to its strongly congruent evolution with the host and its bacteriome-inhabiting nature. Our analysis affirms recent suggestions that the Bacteroidetes-affiliated symbionts may have driven the hyper-diversification of scale insects worldwide.     

Weak sinks could cradle mutualistic symbioses – strong sources should harbour parasitic symbioses

Using a population model of selection on an obligate symbiont and its host, we evaluate how demographic differences across geographical landscapes can produce selection mosaics in interacting species. The model assumes that the host populations vary geographically from demographic sources to sinks in the absence of effects by the symbionts, and that a virulent and a relatively avirulent form of the symbiont compete with one another across all habitats. Our results indicate that productivity gradients can create selection mosaics across habitats, resulting in complex fitness landscapes over which evolution occurs. We find that relatively virulent symbionts only persist if they have an advantage over avirulent strains or species in terms of interference (i.e. competition, and/or cross‐transmission) interactions. When such a trade‐off exists, we predict that the more virulent symbiont is most likely to be found in habitats where host population growth is highest, whereas the more avirulent symbiont should tend to persist in more marginal habitats or even habitat sinks for symbiont‐free hosts. Demographic sinks may be the habitats most likely to favour the origin of new mutualisms. Very productive mutualisms can be exploited by hyperparasites or cheaters. We discuss our findings in terms of geographical scenarios for the emergence of mutualisms, and the long‐standing debate about geographical patterns in the maintenance of sex.     

The role of defensive symbionts in host–parasite coevolution

Understanding the coevolution of hosts and parasites is a long‐standing goal of evolutionary biology. There is a well‐developed theoretical framework to describe the evolution of host–parasite interactions under the assumption of direct, two‐species interactions, which can result in arms race dynamics or sustained genotype fluctuations driven by negative frequency dependence (Red Queen dynamics). However, many hosts rely on symbionts for defence against parasites. Whilst the ubiquity of defensive symbionts and their potential importance for disease control are increasingly recognized, there is still a gap in our understanding of how symbionts mediate or possibly take part in host–parasite coevolution. Herein we address this question by synthesizing information already available from theoretical and empirical studies. First, we briefly introduce current hypotheses on how defensive mutualisms evolved from more parasitic relationships and highlight exciting new experimental evidence showing that this can occur very rapidly. We go on to show that defensive symbionts influence virtually all important determinants of coevolutionary dynamics, namely the variation in host resistance available to selection by parasites, the specificity of host resistance, and the trade‐off structure between host resistance and other components of fitness. In light of these findings, we turn to the limited theory and experiments available for such three‐species interactions to assess the role of defensive symbionts in host–parasite coevolution. Specifically, we discuss under which conditions the defensive symbiont may take over from the host the reciprocal adaptation with parasites and undergo its own selection dynamics, thereby altering or relaxing selection on the hosts' own immune defences. Finally, we address potential effects of defensive symbionts on the evolution of parasite virulence. This is an important problem for which there is no single, clear‐cut prediction. The selection on parasite virulence resulting from the presence of defensive symbionts in their hosts will depend on the underlying mechanism of defence. We identify the evolutionary predictions for different functional categories of symbiont‐conferred resistance and we evaluate the empirical literature for supporting evidence. We end this review with outstanding questions and promising avenues for future research to improve our understanding of symbiont‐mediated coevolution between hosts and parasites.     

The natural occurrence of secondary bacterial symbionts in aphids

1. Many insects host secondary bacterial symbionts that are known to have wide‐ranging effects on their hosts, from host‐plant use to resistance against natural enemies. This has been most widely studied in aphids, which have become a model system to study insect–bacteria interactions. 2. While there is an increasing understanding of the role of symbionts in aphids from controlled laboratory studies, we are only beginning to explore the impact of hosting these symbionts on eco‐evolutionary dynamics in natural systems. To date, many research groups have identified bacterial symbionts from various aphid species, providing us with a bank of literature on aphid–symbiont associations in natural populations. 3. The role of secondary symbionts in aphids is discussed, and the taxonomic and geographical distribution of symbionts among aphids are summarised, and the potential reasons for the patterns observed. The need to test for multiple symbiont species (and co‐infections) across many individuals and the whole distribution range of an aphid is highlighted, including sampling on all known host‐plant species. 4. It is further important also to consider variation within the symbiont, the aphid‐host and the surrounding community, e.g. host‐plants or the natural enemies, to understand how these have the potential to mediate aphid–symbiont interactions. 5. Finally, the knowledge gained from experimental work should now be used to understand the role of aphid secondary symbionts in field systems, to fully understand the potentially far‐reaching consequences of aphid endosymbionts on community and ecosystem processes.     

Muller’s ratchet in symbiont populations

Muller’s ratchet, the inevitable accumulation of deleterious mutations in asexual populations, has been proposed as a major factor in genome degradation of obligate symbiont organisms. Essentially, if left unchecked the ratchet will with certainty cause extinction due to the ever increasing mutational load. This paper examines the evolutionary fate of insect symbionts, using mathematical modelling to simulate the accumulation of deleterious mutations. We investigate the effects of a hierarchical two level population structure. Since each host contains its own subpopulation of symbionts, there will be a large number of small symbiont populations linked indirectly via selection on the host level. We show that although the separate subpopulations will accumulate deleterious mutations quickly, the symbiont population as a whole will be protected from extinction by selection acting on the hosts. As a consequence, the extent of genome degradation observed in present day symbionts is more likely to represent loss of functions that were (near-) neutral to the host, rather than a snap shot of a decline towards complete genetic collapse.     

Coexistence of novel gammaproteobacterial and Arsenophonus symbionts in the scale insect Greenisca brachypodii (Hemiptera,Coccomorpha: Eriococcidae)

Scale insects are commonly associated with obligate, intracellular microorganisms which play important roles in complementing their hosts with essential nutrients. Here we characterized the symbiotic system of Greenisca brachypodii, a member of the family Eriococcidae. Histological and ultrastructural analyses have indicated that G. brachypodii is stably associated with coccoid and rod‐shaped bacteria. Phylogenetic analyses have revealed that the coccoid bacteria represent a sister group to the secondary symbiont of the mealybug Melanococcus albizziae, whereas the rod‐shaped symbionts are close relatives of Arsenophonus symbionts in insects – to our knowledge, this is the first report of the presence of Arsenophonus bacterium in scale insects. As a comparison of 16S and 23S rRNA genes sequences of the G. brachypodii coccoid symbiont with other gammaprotebacterial sequences showed only low similarity (～90%), we propose the name ‘Candidatus Kotejella greeniscae’ for its tentative classification. Both symbionts are transovarially transmitted from one generation to the next. The infection takes place in the neck region of the ovariole. The bacteria migrate between follicular cells, as well as through the cytoplasm of those cells to the perivitelline space, where they form a characteristic ‘symbiont ball’. Our findings provide evidence for a polyphyletic origin of symbionts of Eriococcidae.     

The more,the merrier? Obligate symbiont density changes over time under controlled environmental conditions,yet holds no clear fitness consequences

Symbiotic bacteria are highly diverse, play an important role in ecology and evolution, and are also of applied relevance because many pest insects rely on them for their success. However, the dynamics and regulation of symbiotic bacteria within hosts is complex and still poorly understood outside of a few model systems. One of the most intriguing symbiotic relationships is the obligate, tripartite nutritional mutualism in sap‐feeding, economically‐destructive mealybugs (Hemiptera: Sternorrhyncha: Pseudococcidae), which involves γ‐proteobacteria hosted within β‐proteobacteria hosted within the mealybugs. The present study examines whether there is population variation in symbiont density (i.e. infection intensity, or titre) in the citrus mealybug Planococcus citri (Risso) and how this impacts host life‐history. Symbiont density is found to differ significantly between populations when reared under controlled environmental conditions, indicating that the density of symbiont infections is influenced by host or symbiont genotype. However, symbiont density changes in populations over multiple generations, indicating that symbiont densities are dynamic. Surprisingly, given that the symbionts are essential nutritional mutualists, the density of the symbionts does not correlate significantly with either host fecundity or development. Higher levels of symbionts have no clear benefit to hosts and therefore appear to be superfluous, at least under constant, optimized environmental conditions. Excessive symbiont density may be an evolutionary artefact from a period of inefficient vertical transmission when the balance of conflict between host and symbiont was still being established.     

Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts

The Adelgidae (Insecta: Hemiptera), a small group of insects, are known as severe pests on various conifers of the northern hemisphere. Despite of this, little is known about their bacteriocyte‐associated endosymbionts, which are generally important for the biology and ecology of plant sap‐sucking insects. Here, we investigated the adelgid species complexes Adelges laricis/tardus, Adelges abietis/viridis and Adelges cooleyi/coweni, identified based on their coI and ef1alpha genes. Each of these insect groups harboured two phylogenetically different bacteriocyte‐associated symbionts belonging to the Betaproteobacteria and the Gammaproteobacteria, respectively, as inferred from phylogenetic analyses of 16S rRNA gene sequences and demonstrated by fluorescence in situ hybridization. The betaproteobacterial symbionts of all three adelgid complexes (‘Candidatus Vallotia tarda’, ‘Candidatus Vallotia virida’ and ‘Candidatus Vallotia cooleyia’) share a common ancestor and show a phylogeny congruent with that of their respective hosts. Similarly, there is evidence for co‐evolution between the gammaproteobacterial symbionts (‘Candidatus Profftia tarda’, ‘Candidatus Profftia virida’) and A. laricis/tardus and A. abietis/viridis. In contrast, the gammaproteobacterial symbiont of A. cooleyi/coweni (‘Candidatus Gillettellia cooleyia’) is different from that of the other two adelgids but shows a moderate relationship to the symbiont ‘Candidatus Ecksteinia adelgidicola’ of A. nordmannianae/piceae. All symbionts were present in all adelgid populations and life stages analysed, suggesting vertical transmission from mother to offspring. In sharp contrast to their sister group, the aphids, adelgids do not consistently contain a single obligate (primary) symbiont but have acquired phylogenetically different bacterial symbionts during their evolution, which included multiple infections and symbiont replacement.     

EXPERIMENTAL EVOLUTION OF PARASITOID INFECTIVITY ON SYMBIONT‐PROTECTED HOSTS LEADS TO THE EMERGENCE OF GENOTYPE SPECIFICITY

Host‐parasitoid interactions may lead to strong reciprocal selection for traits involved in host defense and parasitoid counterdefense. In aphids, individuals harboring the facultative bacterial endosymbiont, Hamiltonella defensa, exhibit enhanced resistance to parasitoid wasps. We used an experimental evolution approach to investigate the ability of the parasitoid wasp, Lysiphlebus fabarum, to adapt to the presence of H. defensa in its aphid host Aphis fabae. Sexual populations of the parasitoid were exposed for 11 generations to a single clone of A. fabae, either free of H. defensa or harboring artificial infections with three different isolates of H. defensa. Parasitoids adapted rapidly to the presence of H. defensa in their hosts, but this adaptation was in part specific to the symbiont isolate they were evolving against and did not result in an improved infectivity on all symbiont‐protected hosts. Comparisons of life‐history traits among the evolved lines of parasitoids did not reveal any evidence for costs of adaptation to H. defensa in terms of correlated responses that could constrain such adaptation. These results show that parasitoids readily evolve counter‐adaptations to heritable defensive symbionts of their hosts, but that different symbiont strains impose different evolutionary challenges. The symbionts thus mediate the host‐parasite interaction by inducing line‐by‐line genetic specificity.     

Symbiont‐mediated phenotypic variation without co‐evolution in an insect–fungus association

Recent studies have shown that symbionts can be a source of adaptive phenotypic variation for their hosts. It is assumed that co‐evolution between hosts and symbionts underlies these ecologically significant phenotypic traits. We tested this assumption in the ectosymbiotic fungal associate of the gall midge Asteromyia carbonifera. Phylogenetic analysis placed the fungal symbiont within a monophyletic clade formed by Botryosphaeria dothidea, a typically free‐living (i.e. not associated with an insect host) plant pathogen. Symbiont isolates from four divergent midge lineages demonstrated none of the patterns common to heritable microbial symbioses, including parallel diversification with their hosts, substitution rate acceleration, or A+T nucleotide bias. Amplified fragment length polymorphism genotyping of the symbiont revealed that within‐lineage genetic diversity was not clustered along host population lines. Culture‐based experiments demonstrated that the symbiont‐mediated variation in gall phenotype is not borne out in the absence of the midge. This study shows that symbionts can be important players in phenotypic variation for their hosts, even in the absence of a co‐evolutionary association.     

The impact of transmission mode on the evolution of benefits provided by microbial symbionts

While past work has often examined the effects of transmission mode on virulence evolution in parasites, few studies have explored the impact of horizontal transmission on the evolution of benefits conferred by a symbiont to its host. Here, we identify three mechanisms that create a positive covariance between horizontal transmission and symbiont‐provided benefits: pleiotropy within the symbiont genome, partner choice by the host, and consumption of host waste by‐products by symbionts. We modify a susceptible‐infected model to incorporate the details of each mechanism and examine the evolution of symbiont benefits given variation in either the immigration rate of susceptible hosts or the rate of successful vertical transmission. We find conditions for each case under which greater opportunity for horizontal transmission (higher migration rate) favors the evolution of mutualism. Further, we find the surprising result that vertical transmission can inhibit the evolution of benefits provided by symbionts to hosts when horizontal transmission and symbiont‐provided benefits are positively correlated. These predictions may apply to a number of natural systems, and the results may explain why many mutualisms that rely on partner choice often lack a mechanism for vertical transmission.     

Intracellular symbionts and the evolution of uniparental cytoplasmic inheritance.

Uniparental inheritance of cytoplasmic elements is widespread among eukaryotic organisms and is achieved by a diverse range of mechanisms. This paper shows that the cytoplasmic genetic system would be expected to evolve towards uniparental inheritance, given the existence of deleterious symbionts capable of invading the host cytoplasm together with nuclear genes that lead to the elimination of cytoplasmic elements from one of the gamete types. The reason for this is that, under biparental inheritance, foreign symbionts with strong deleterious effects are able to spread through host populations. A nuclear modifier gene which leads to the loss of cytoplasmic elements from one gamete type gains a net advantage as a symbiont spreads, because the modifier sometimes gives rise to a symbiont-free zygote. Insofar as small gametes reduce the rate of symbiont transmission to the zygote, modifier genes causing small gamete size would tend to accumulate, so that cytoplasmic inheritance would become associated with maternal rather than paternal gametes. Once uniparental inheritance predominates in the host population, the population is protected from invasions by a large class of harmful symbionts, but at the same time those symbionts that benefit their hosts are still able to increase in frequency.     

A niche perspective on the range expansion of symbionts

Range expansion results from complex eco‐evolutionary processes where range dynamics and niche shifts interact in a novel physical space and/or environment, with scale playing a major role. Obligate symbionts (i.e. organisms permanently living on hosts) differ from free‐living organisms in that they depend on strong biotic interactions with their hosts which alter their niche and spatial dynamics. A symbiotic lifestyle modifies organism–environment relationships across levels of organisation, from individuals to geographical ranges. These changes influence how symbionts experience colonisation and, by extension, range expansion. Here, we investigate the potential implications of a symbiotic lifestyle on range expansion capacity. We present a unified conceptual overview on range expansion of symbionts that integrates concepts grounded in niche and metapopulation theories. Overall, we explain how niche‐driven and dispersal‐driven processes govern symbiont range dynamics through their interaction across scales, from host switching to geographical range shifts. First, we describe a background framework for range dynamics based on metapopulation concepts applied to symbiont organisation levels. Then, we integrate metapopulation processes operating in the physical space with niche dynamics grounded in the environmental arena. For this purpose, we provide a definition of the biotope (i.e. living place) specific to symbionts as a hinge concept to link the physical and environmental spaces, wherein the biotope unit is a metapopulation patch (either a host individual or a land fragment). Further, we highlight the dual nature of the symbionts' niche, which is characterised by both host traits and the external environment, and define proper conceptual variants to provide a meaningful unification of niche, biotope and symbiont organisation levels. We also explore variation across systems in the relative relevance of both external environment and host traits to the symbiont's niche and their potential implications on range expansion. We describe in detail the potential mechanisms by which hosts, through their function as biotopes, could influence how some symbionts expand their range – depending on the life history and traits of both associates. From the spatial point of view, hosts can extend symbiont dispersal range via host‐mediated dispersal, although the requirement for among‐host dispersal can challenge symbiont range expansion. From the niche point of view, homeostatic properties of host bodies may allow symbiont populations to become insensitive to off‐host environmental gradients during host‐mediated dispersal. These two potential benefits of the symbiont–host interaction can enhance symbiont range expansion capacity. On the other hand, the central role of hosts governing the symbiont niche makes symbionts strongly dependent on the availability of suitable hosts. Thus, environmental, dispersal and biotic barriers faced by suitable hosts apply also to the symbiont, unless eventual opportunities for host switching allow the symbiont to expand its repertoire of suitable hosts (thus expanding its fundamental niche). Finally, symbionts can also improve their range expansion capacity through their impacts on hosts, via protecting their affiliated hosts from environmental harshness through biotic facilitation.     

Why mutualist partners vary in quality: mutation–selection balance and incentives to cheat in the fig tree–fig wasp mutualism

Mutualisms between species are ecologically ubiquitous but evolutionarily puzzling. Host discrimination mechanisms that reduce the fitness of uncooperative symbionts can stabilise mutualism against collapse, but also present a paradox – if discrimination is effective, why do uncooperative symbionts persist? Here, we test whether mutations or fitness benefits of cheating best explain the prevalence of uncooperative wasps in the fig tree–fig wasp mutualism. By combining theory with field‐collected data we demonstrate that the proportions of pollen‐free wasps of strongly discriminating hosts are reached with reasonable mutation rates. In contrast, in weakly discriminating hosts, the required mutation rates, assuming a single locus, are untenably high, but the required cheater advantages fall within expected ranges. We propose that when discrimination is weak, uncooperative symbionts proliferate until they reach the equilibrium proportion that balances costs and benefits of cheating. Our results suggest that mechanisms that resolve the paradox of uncooperative symbionts differ among host species.     

Band‐aids for Buchnera and B vitamins for all

Evolution lacks foresight, and hence, key adaptations may produce major challenges over the long run. The natural world is rife with examples of long‐term ‘side effects’ associated with quick‐fix tinkering, including blind spots in vertebrate eyes. An important question is how nature compensates for imperfections once evolution has set a course. The symbioses associated with sap‐feeding insects present a fascinating opportunity to address this issue. On one hand, the substantial diversity and biomass of sap‐feeding insects are largely due to ancient acquisitions of nutrient‐provisioning bacterial symbionts. Yet, the insularity and small population sizes enforced by intracellular life and strict maternal transfer inevitably result in the degradation of symbiont genomes and, often, the beneficial services that symbionts provide. Stabilization through lateral transfer of bacterial genes into the host nucleus (often from exogenous sources) or replacement of the long‐standing symbiont with a new partner are potential solutions to this evolutionary dilemma (Bennett & Moran 2015 ). A third solution is adoption of a cosymbiont that compensates for specific losses in the original resident. Ancient ‘co‐obligate’ symbiont pairs in mealybugs, leafhoppers, cicadas and spittlebugs show colocalization, codiversification, metabolite exchange and generally nonredundant nutrient biosynthesis (Bennett & Moran 2015 ). But in this issue, Meseguer et al. ( 2017 ) report on a different flavour of cosymbiosis among conifer‐feeding Cinara aphids.     

Genomic signatures of obligate host dependence in the luminous bacterial symbiont of a vertebrate

The majority of bacteria engaged in bioluminescent symbiosis are environmentally acquired and facultatively symbiotic. A few enigmatic bioluminescent symbionts have not been successfully cultured, which has led to speculation that they may be obligately dependent on their hosts. Here, we report the draft genome of the uncultured luminous symbiont of an anomalopid flashlight fish, ‘Candidatus Photodesmus katoptron’. The genome of the anomalopid symbiont is reduced by 80% compared with close relatives and lacks almost all genes necessary for amino acid synthesis and for metabolism of energy sources other than glucose, supporting obligate dependence on the host for growth. ‘Candidatus Photodesmus katoptron’ is the first described obligate mutualistic symbiont of a vertebrate. Unlike most other obligate mutualists, the anomalopid symbiont genome has retained complete pathways for chemotaxis and motility as well as most genes involved in cell wall production, consistent with the hypothesis that these bacteria may be transmitted environmentally during an extra‐host phase.     

Evolution of transmission mode in conditional mutualisms with spatial variation in symbiont quality

Many symbioses have costs and benefits to their hosts that vary with the environmental context, which itself may vary in space. The same symbiont may be a mutualist in one location and a parasite in another. Such spatially conditional mutualisms pose a dilemma for hosts, who might evolve (higher or lower) horizontal or vertical transmission to increase their chances of being infected only where the symbiont is beneficial. To determine how transmission in hosts might evolve, we modeled transmission evolution where the symbiont had a spatially conditional effect on either host lifespan or fecundity. We found that over ecological time, symbionts that affected lifespan but not fecundity led to high frequencies of infected hosts in areas where the symbiont was beneficial and low frequencies elsewhere. In response, hosts evolved increased horizontal transmission only when the symbiont affected lifespan. We also modeled transmission evolution in symbionts, which evolved high horizontal and vertical transmission, indicating a possible host–symbiont conflict over transmission mode. Our results suggest an eco‐evolutionary feedback where the component of host fitness affected by a conditionally mutualistic symbiont in turn determines its distribution in the population, and, through this, the transmission mode that evolves.