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SummaryEndosymbiosis – where a microbe lives and replicates within a host – is an important contributor to organismal function that has accelerated evolutionary innovations and catalysed the evolution of complex life. The evolutionary processes associated with transitions to endosymbiosis, however, are poorly understood. Here, we use comparative genomics of the genusArsenophonusto reveal the complex processes that occur on evolution of an endosymbiotic lifestyle. We compared the genomes of 38 strains spanning diverse lifestyles from environmentally acquired infections to obligate inter-dependent endosymbionts. We observed recent endosymbionts had larger genome sizes than closely related environmentally acquired strains, consistent with evolutionary innovation and rapid gain of new function. Increased genome size was a consequence of prophage and plasmid acquisition including a cargo of type III effectors, and concomitant loss of CRISPR-Cas genome defence systems enabling mobile genetic element expansion. Persistent endosymbiosis was also associated with loss of type VI secretion, likely reflecting reduced microbe-microbe competition. Thereafter, the transition to stable endosymbiosis and vertical inheritance was associated with the expected relaxation of purifying selection, pseudogenisation of genes and reduction of metabolism, leading to genome reduction. However, reduced %GC that is typically considered a progressive linear process was observed only in obligate interdependent endosymbionts. We argue that a combination of the need for rapid horizontal gene transfer-mediated evolutionary innovation together with reduced phage predation in endosymbiotic niches drives loss of genome defence systems and rapid genome expansion upon adoption of endosymbiosis. These remodelling processes precede the reductive evolution traditionally associated with adaptation to endosymbiosis.

Virulence, the harm to hosts caused by parasite infection, can be selected for by several ecological factors acting synergistically or antagonistically. Here, we focus on the potential for interspecific host competition to shape virulence through such a network of effects. We first summarize how host natural mortality, body mass changes, population density and community diversity affect virulence evolution. We then introduce an initial conceptual framework highlighting how these host factors, which change during host competition, may drive virulence evolution via impacts on life-history trade-offs. We argue that the multi-faceted nature of both interspecific host competition and virulence evolution still requires consideration and experimentation to disentangle contrasting mechanisms. It also necessitates a differential treatment for parasites with various transmission strategies. However, such a comprehensive approach focusing on the role of interspecific host competition is essential to understand the processes driving the evolution of virulence in a tangled bank.

Defensive symbionts protect their hosts against imminent threats. A new study uncovers a symbiosis whereby a fungus safeguards its beetle host from predation, but also exploits the beetle as a vector to help it attack plants and cause disease.

Agricultural crops infected with vector-borne pathogens can suffer severe negative consequences, but the extent to which phytopathogens affect the fitness of their vector hosts remains unclear. Evolutionary theory predicts that selection on vector-borne pathogens will favour low virulence or mutualistic phenotypes in the vector, traits facilitating effective transmission between plant hosts. Here, we use a multivariate meta-analytic approach on 115 effect sizes across 34 unique plant–vector–pathogen systems to quantify the overall effect of phytopathogens on vector host fitness. In support of theoretical models, we report that phytopathogens overall have a neutral fitness effect on vector hosts. However, the range of fitness outcomes is diverse and span the parasitism–mutualism continuum. We found no evidence that various transmission strategies, or direct effects and indirect (plant-mediated) effects, of phytopathogens have divergent fitness outcomes for the vector. Our finding emphasizes diversity in tripartite interactions and the necessity for pathosystem-specific approaches to vector control.

Microbes that protect against infection inhabit hosts across the tree of life. It is unclear whether and how the host immune system may affect the formation of new protective symbioses. We investigated the transcriptomic response of Caenorhabditis elegans following novel interactions with a protective microbe (Enterococcus faecalis) able to defend against infection by pathogenic Staphylococcus aureus. We have previously shown that E. faecalis can directly limit pathogen growth within hosts. In this study, we show that colonisation by protective E. faecalis caused the differential expression of 1,557 genes in pathogen infected hosts, including the upregulation of immune genes such as lysozymes and C-type lectins. The most significantly upregulated host lysozyme gene, lys-7, impacted the competitive abilities of E. faecalis and S. aureus when knocked out. E. faecalis has an increased ability to resist lysozyme activity compared to S. aureus, suggesting that the protective microbe could gain a competitive advantage from this host response. Our finding that protective microbes can benefit from immune-mediated competition after introduction opens up new possibilities for biocontrol design and our understanding of symbiosis evolution. Crosstalk between the host immune response and microbe-mediated protection should favour the continued investment in host immunity and avoid the potentially risky evolution of host dependence.

Plants infected with vector-borne pathogens can suffer severe negative consequences, but the extent to which phytopathogens affect the fitness of their vector hosts remains unclear. Evolutionary theory predicts that selection on vector-borne pathogens should favour low virulence or mutualistic phenotypes in the vector, traits facilitating effective transmission between plant hosts. Here, we use a multivariate meta-analytic approach on 115 effect sizes across 34 unique plant-vector-pathogen systems to quantify the overall effect of phytopathogens on vector host fitness. In support of theoretical models, we report that phytopathogens overall have a neutral fitness effect on vector hosts. However, the range of possible fitness outcomes are diverse and span the parasitism-mutualism continuum. Contrary to previous predictions we found no evidence that transmission strategy, or the direct effects and indirect (plant-mediated) effects, of phytopathogens have divergent fitness outcomes for the vector. We discuss these findings in the context of plant – pathogen – vector ecology.

Many host organisms live in polymicrobial environments and must respond to a diversity of pathogens. The degree to which host defences towards one pathogen species affect susceptibility to others is unclear. We used a panel of Caenorhabditis elegans nematode isolates to test for natural genetic variation in fitness costs of immune upregulation and pathogen damage, as well as for trade-offs in defence against two pathogen species, Staphylococcus aureus and Pseudomonas aeruginosa. We examined the fitness impacts of transient pathogen exposure (pathogen damage and immune upregulation) or exposure to heat-killed culture (immune upregulation only) by measuring host population sizes, which allowed us to simultaneously capture changes in reproductive output, developmental time and survival. We found significant decreases in population sizes for hosts exposed to live versus heat-killed S. aureus and found increased reproductive output after live P. aeruginosa exposure, compared with the corresponding heat-killed challenge. Nematode isolates with relatively higher population sizes after live P. aeruginosa infection produced fewer offspring after live S. aureus challenge. These findings reveal that wild C. elegans genotypes display a trade-off in defences against two distinct pathogen species that are evident in subsequent generations.

Natural and anthropogenic stressors, including parasites and pesticides, may induce oxidative stress in animals. Measuring oxidative stress responses in sentinel species that are particularly responsive to environmental perturbations not only provides insight into host physiology but is also a useful readout of ecosystem health. Newly metamorphosed northern leopard frogs (Lithobates pipiens), a sentinel species, were collected from agricultural and non-agricultural wetlands exposed to varying concentrations of the herbicide atrazine. Significant effects of certain parasites' abundance and their interaction with atrazine exposure on frog oxidative stress were identified. Specifically, increased protein levels were detected in frogs infected with echinostome metacercariae. In addition, the nematode Oswaldocruzia sp. was significantly associated with increased thiol concentration and catalase activity. Significant parasite × atrazine interactions were observed for atrazine exposure and the abundance of Oswaldocruzia sp. on thiol, as thiol concentrations increased with parasite abundance at low atrazine localities and decreased in high atrazine wetlands. In addition, a significant interaction between the abundances of Oswaldocruzia sp. and gorgoderid trematodes on thiol concentrations was observed. These findings demonstrate that studies of oxidative stress on animals in natural ecosystems should account for the confounding effects of parasitism, particularly for amphibians in agricultural landscapes.

Resident microbes (microbiota) can shape host organismal function and adaptation in the face of environmental change. Invasion of new habitats exposes hosts to novel selection pressures, but little is known about the impact on microbiota and the host–microbiome relationship (e.g., how rapidly new microbial associations are formed, whether microbes influence invasion success). We used high‐throughput 16S rRNA sequencing of New Zealand (native) and European (invasive) populations of the freshwater snail Potamopyrgus antipodarum and found that while invaders do carry over some core microbial taxa from New Zealand, their microbial community is largely distinct. This finding highlights that invasions can result in the formation of novel host–microbiome relationships. We further show that the native microbiome is composed of fewer core microbes than the microbiome of invasive snails, suggesting that the microbiota is streamlined to a narrower set of core members. Furthermore, native snails exhibit relatively low alpha diversity but high inter‐individual variation, whereas invasive snails have higher alpha diversity but are relatively similar to each other. Together, our findings demonstrate that microbiota comparisons across native and invasive populations can reveal the impact of a long coevolutionary history and specialization of microbes in the native host range, as well as new associations occurring after invasion. We lay essential groundwork for understanding how microbial relationships affect invasion success and how microbes may be utilized in the control of invasive hosts.

Pathogens continue to emerge from increased contact with novel host species. Whilst these hosts can represent distinct environments for pathogens, the impacts of host genetic background on how a pathogen evolves post-emergence are unclear. In a novel interaction, we experimentally evolved a pathogen (Staphylococcus aureus) in populations of wild nematodes (Caenorhabditis elegans) to test whether host genotype and genetic diversity affect pathogen evolution. After ten rounds of selection, we found that pathogen virulence evolved to vary across host genotypes, with differences in host metal ion acquisition detected as a possible driver of increased host exploitation. Diverse host populations selected for the highest levels of pathogen virulence, but infectivity was constrained, unlike in host monocultures. We hypothesise that population heterogeneity might pool together individuals that contribute disproportionately to the spread of infection or to enhanced virulence. The genomes of evolved populations were sequenced, and it was revealed that pathogens selected in distantly-related host genotypes diverged more than those in closely-related host genotypes. S. aureus nevertheless maintained a broad host range. Our study provides unique empirical insight into the evolutionary dynamics that could occur in other novel infections of wildlife and humans.

Coevolution between hosts and parasites is a major driver of rapid evolutionary change1 and diversification.2,3 However, direct antagonistic interactions between hosts and parasites could be disrupted4 when host microbiota form a line of defense, a phenomenon widespread across animal and plant species.5,6 By suppressing parasite infection, protective microbiota could reduce the need for host-based defenses and favor host support for microbiota colonization,6 raising the possibility that the microbiota can alter host-parasite coevolutionary patterns and processes.7 Here, using an experimental evolution approach, we co-passaged populations of nematode host (Caenorhabditis elegans) and parasites (Staphylococcus aureus) when hosts were colonized (or not) by protective bacteria (Enterococcus faecalis). We found that microbial protection during coevolution resulted in the evolution of host mortality tolerance—higher survival following parasite infection—and in parasites adapting to microbial defenses. Compared to unprotected host-parasite coevolution, the protected treatment was associated with reduced dominance of fluctuating selection dynamics in host populations. No differences in host recombination rate or genetic diversity were detected. Genomic divergence was observed between parasite populations coevolved in protected and unprotected hosts. These findings indicate that protective host microbiota can determine the evolution of host defense strategies and shape host-parasite coevolutionary dynamics.

Protective symbionts can defend hosts from parasites through several mechanisms, from direct interference to modulating host immunity, with subsequent effects on host and parasite fitness. While research on symbiont-mediated immune priming (SMIP) has focused on ecological impacts and agriculturally important organisms, the evolutionary implications of SMIP are less clear. Here, we review recent advances made in elucidating the ecological and molecular mechanisms by which SMIP occurs. We draw on current works to discuss the potential for this phenomenon to drive host, parasite, and symbiont evolution. We also suggest approaches that can be used to address questions regarding the impact of immune priming on host-microbe dynamics and population structures. Finally, due to the transient nature of some symbionts involved in SMIP, we discuss what it means to be a protective symbiont from ecological and evolutionary perspectives and how such interactions can affect long-term persistence of the symbiosis.

Microbiota can protect their hosts from infection. The short timescales in which microbes can evolve presents the possibility that “protective microbes” can take-over from the immune system of longer-lived hosts in the coevolutionary race against pathogens. Here, we found that coevolution between a protective bacterium (Enterococcus faecalis) and a virulent pathogen (Staphylococcus aureus) within an animal population (Caenorhabditis elegans) resulted in more disease suppression than when the protective bacterium adapted to uninfected hosts. At the same time, more protective E. faecalis populations became costlier to harbor and altered the expression of 134 host genes. Many of these genes appear to be related to the mechanism of protection, reactive oxygen species production. Crucially, more protective E. faecalis populations downregulated a key immune gene, , known to be effective against S. aureus infection. These results suggest that a microbial line of defense is favored by microbial coevolution and may cause hosts to plastically divest of their own immunity.

Identifying different types of coevolutionary dynamics is important for understanding biodiversity and infectious disease. Past work has often focused on pairs of interacting species, but observations of extant communities suggest that coevolution in nature occurs in networks of antagonism and mutualism. We discuss challenges for measuring coevolutionary dynamics in species-rich communities, and we suggest ways that established approaches used for two-species interactions can be applied. We propose ways that such data can be complemented by genomic information and linked back to extant communities via network structure, and we suggest avenues for new theoretical work to strengthen these connections. Quantifying coevolution in species-rich communities has several potential benefits, such as identifying coevolutionary units within networks and uncovering coevolutionary interactions among pathogens of humans, livestock, and crops. ISSN:0169-5347 ISSN:1872-8383

Protective microbes have a major role in shaping host–pathogen interactions, but their relative importance in the structure of the host microbiota remains unclear. Here, we used a network approach to characterize the impact of a novel, experimentally evolved ‘protective microbial symbiont’ (Enterococcus faecalis) on the structure and predicted function of the natural microbiota of the model organism Caenorhabditis elegans. We used microbial network analysis to identify keystone taxa and describe the hierarchical placement of protective and non-protective symbionts in the microbiota. We found that early colonization with symbionts produce statistically significant changes in the structure of the community. Notably, only the protective E. faecalis became a keystone taxon in the nematode microbiota. Non-protective lineages of the same bacterial species remained comparatively unimportant to the community. Prediction of functional profiles in bacterial communities using PICRUSt2 showed that the presence of highly protective E. faecalis decreased the abundance of ergothioneine (EGT) biosynthesis pathway involved in the synthesis of the antioxidant molecule EGT, a potential public good. These data show that in addition to direct antagonism with virulent pathogens, keystone protective symbionts are linked to modified bacterial community structure and possible reductions in public goods, potentially driving decreased antioxidant defense. We suggest that this response could suppress infection via wholesale microbial community changes to further benefit the host. These findings extend the concept of protective symbionts beyond bodyguards to ecosystem engineers.

To maximize fitness upon pathogenic infection, host organisms might reallocate energy and resources among life-history traits, such as reproduction and defense. The fitness costs of infection can result from both immune upregulation and direct pathogen exploitation. The extent to which these costs, separately and together, vary by host genotype and across generations is unknown. We attempted to disentangle these costs by transiently exposing wild isolates and a lab-domesticated strain of Caenorhabditis elegans nematodes to the pathogen Staphylococcus aureus, using exposure to heat-killed pathogens to distinguish costs due to immune upregulation and pathogen exploitation. We found that host nematodes exhibit a short-term delay in offspring production when exposed to live and heat-killed pathogen, but their lifetime fecundity (total offspring produced) recovered to control levels. We also found genetic variation between host isolates for both cumulative offspring production and magnitude of fitness costs. We further investigated whether there were maternal pathogen exposure costs (or benefits) to offspring and revealed a positive correlation between the magnitude of the pathogen-induced delay in the parent's first day of reproduction and the cost to offspring population growth. Our findings highlight the capacity for hosts to recover fecundity after transient exposure to a pathogen.

Organisms harbour myriad microbes which can be parasitic or protective against harm. The costs and benefits resulting from these symbiotic relationships can be context-dependent, but the evolutionary consequences to hosts of these transitions remain unclear. Here, we mapped the Leucobacter genus across 13,715 microbiome samples (163 studies) to reveal a global distribution as a free-living microbe or a symbiont of animals and plants. We showed that across geographically distant locations (South Africa, France, Cape Verde), Leucobacter isolates vary substantially in their virulence to an associated animal host, Caenorhabditis nematodes. We further found that multiple Leucobacter sequence variants co-occur in wild Caenorhabditis spp. which combined with natural variation in virulence provides real-world potential for Leucobacter community composition to influence host fitness. We examined this by competing C. elegans genotypes that differed in susceptibility to different Leucobacter species in an evolution experiment. One Leucobacter species was found to be host-protective against another, virulent parasitic species. We tested the impact of host genetic background and Leucobacter community composition on patterns of host-based defence evolution. We found host genotypes conferring defence against the parasitic species were maintained during infection. However, when hosts were protected during coinfection, host-based defences were nearly lost from the population. Overall, our results provide insight into the role of community context in shaping host evolution during symbioses.

Virtually all plants and animals, including humans, are home to symbiotic microorganisms. Symbiotic interactions can be neutral, harmful or have beneficial effects on the host organism. However, growing evidence suggests that microbial symbionts can evolve rapidly, resulting in drastic transitions along the parasite–mutualist continuum. In this Review, we integrate theoretical and empirical findings to discuss the mechanisms underpinning these evolutionary shifts, as well as the ecological drivers and why some host–microorganism interactions may be stuck at the end of the continuum. In addition to having biomedical consequences, understanding the dynamic life of microorganisms reveals how symbioses can shape an organism’s biology and the entire community, particularly in a changing world., Symbiotic interactions can be neutral, harmful or have beneficial effects for host organisms. In this Review, Drew, Stevens and King discuss the evolutionary transitions of host–microorganism symbioses along the parasite–mutualist continuum, the mechanisms underlying evolutionary changes, the selective pressures involved and common empirical approaches for studying them.

Ecological interactions can generate strong selection. Two new studies reveal that the tempo and patterns of evolutionary change in a mammalian gut commensal can be altered dramatically during interactions with both the host and its microbiome.

Interactions in nature vary from competitive to neutral to symbiotic. An interesting case of symbiosis is seen when one organism provides protection to the other-a relationship termed 'defensive symbiosis'. Kayla King highlights this interesting type of relationship, which can be found throughout the tree of life.

Microbes that protect against infection inhabit hosts across the tree of life. It is unclear whether many protective microbes use or reduce the need for a host immune response, or how the immune system reacts when these microbes newly encounter a host species naturally and as part of a biocontrol strategy. We sequenced the transcriptome of a host (Caenorhabditis elegans) following its interaction with a non-native bacterium (Enterococcus faecalis) that has protective traits against the pathogen, Staphylococcus aureus. We show that microbe-mediated protection caused the differential expression of 1,557 genes, including the upregulation of many immune gene families conserved across the animal kingdom (e.g. lysozymes and c-type lectins). We found that this modulation of the host’s immune response was beneficial for both the protective microbe and the host. Given E. faecalis’ increased ability to resist lysozyme activity compared to S. aureus, our results indicate that the protective microbe could more easily invade and protect infected hosts by upregulating lysozyme genes. These results suggest that a protective microbe can exploit the host immune system even when introduced into a novel species. Microbes that protect via the host immune response in this way should favour continued investment into host immunity and avoid the evolution of host dependence.Author summaryOrganisms can be protected from infectious disease by the microbes they house. It is unclear, however, whether protective microbes affect the host immune response to infection, particularly in the early stages of symbiosis. In this study, we investigated the role of the host immune system in a novel protective interaction. We examined gene expression in a nematode after colonisation by a non-native microbe capable of suppressing the pathogen Staphylococcus aureus. The protective microbe altered the host immune response to infection in a way that it could exploit. By causing the host to increase the production of antimicrobials to which it itself is relatively resistant, the protective microbe was better able to colonise and defend infected hosts. These results indicate that protective microbes introduced into new host species can take advantage of the host immune system. Such a mechanism at the beginning of a protective symbiosis, formed either naturally or as part of a biocontrol strategy, could ensure continued investment in host-based defences over evolutionary time.

Background Bacteria adapted to live within animals can protect their hosts against harmful infections. Beyond antagonism with parasites, a ‘defensive’ bacterial symbiont could engage in additional interactions with other colonizing micro-organisms. A single bacterium might thus have cascading ecological impacts on the whole microbiome that are rarely investigated. Here, we assess the role of a symbiont as a driver of host-associated microbiota composition by using an experimentally-adapted bacterium with protective properties ( Enterococcus faecalis ) inside a nematode host model ( Caenorhabditis elegans ).Results An analysis of 16S rRNA data from C. elegans exposed to E. faecalis and subsequently reared in soil, reveal that E. faecalis presence and adaptation to host environment had minimal impact on microbiota diversity. In addition, the protective effects of E. faecalis against opportunistic Staphylococcus aureus pathogens were still maintained despite multi-species interactions within the microbiota.Conclusions Our results reveal the degree to which a novel, evolving symbiont can colonise and maintain its conferred phenotype (i.e., parasite-resistance) with minimal change to the host microbiome.

Climate change and anthropogenic activity are currently driving large changes in nutritional availability across ecosystems, with consequences for infectious disease. An increase in host nutrition could lead to more resources for hosts to expend on the immune system or for pathogens to exploit. In this paper, we report a meta-analysis of studies on host–pathogen systems across the tree of life, to examine the impact of host nutritional quality and quantity on pathogen virulence. We did not find broad support across studies for a one-way effect of nutrient availability on pathogen virulence. We thus discuss a hypothesis that there is a balance between the effect of host nutrition on the immune system and on pathogen resources, with the pivot point of the balance differing for vertebrate and invertebrate hosts. Our results suggest that variation in nutrition, caused by natural or anthropogenic factors, can have diverse effects on infectious disease outcomes across species.

Human activities are greatly reducing the genetic diversity of species worldwide. Given the prediction that parasites better exploit less diverse host populations, many species could be vulnerable to disease outbreaks. However, the widespread nature of the ‘monoculture effect’ remains unclear outside agricultural systems. We conducted a meta-analysis of 22 studies, obtaining a total of 66 effect sizes, to directly test the biological conditions under which host genetic diversity limits infectious disease in populations. Overall, we found broad support for the monoculture effect across host and parasite species. The effect was independent of host range, host reproduction, parasite diversity, and the method by which the monoculture effect was recorded. Conversely, we found that parasite functional group, virulence, and empirical environment matters. Together, these results highlight the general susceptibility of genetically homogenous populations to infection. Consequently, this phenomenon could become increasingly common and alarming for at-risk populations due to human-driven declines in genetic diversity and shifts in parasite distributions.

In an ideal world, funding agencies could identify the best scientists and projects and provide them with the resources to undertake these projects. Most scientists would agree that in practice, how funding for scientific research is allocated is far from ideal and likely compromises research quality. We, nine evolutionary biologists from different countries and career stages, provide a comparative summary of our impressions on funding strategies for evolutionary biology across eleven different funding agencies. We also assess whether and how funding effectiveness might be improved. We focused this assessment on 14 elements within four broad categories: (a) topical shaping of science, (b) distribution of funds, (c) application and review procedures, and (d) incentives for mobility and diversity. These comparisons revealed striking among‐country variation in those elements, including wide variation in funding rates, the effort and burden required for grant applications, and the extent of emphasis on societal relevance and individual mobility. We use these observations to provide constructive suggestions for the future and urge the need to further gather informed considerations from scientists on the effects of funding policies on science across countries and research fields.

Host-parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host-parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host-parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.

At the beginning of the pandemic, as universities were shutting, a meme did the rounds on social media. Some academics suggested that they were looking forward to increased productivity in grant and paper writing under lockdown. They cited the fact that Isaac Newton came up with his theory of gravity whilst quarantined during the bubonic plague. Globally, the reaction from many was to inwardly - or publicly - scream.

Species interactions can shift along the parasitism-mutualism continuum. However, the consequences of these transitions for coevolutionary interactions remain unclear. We experimentally coevolved a novel species interaction between Caenorhabditis elegans hosts and a mildly parasitic bacterium, Enterococcus faecalis, with host-protective properties against virulent Staphylococcus aureus. Coinfections drove the evolutionary transition of the C. elegans–E. faecalis relationship toward a reciprocally beneficial interaction. As E. faecalis evolved to protect nematodes against S. aureus infection, hosts adapted by accommodating greater numbers of protective bacteria. The mutualism was strongest in pairings of contemporary coevolved populations. To generally assess the conditions under which these defensive mutualisms can arise and coevolve, we analyzed a model that showed that they are favored when mild parasites confer an intermediate level of protection. Our results reveal that coevolution can shape the transition of animal-parasite interactions toward defensive symbioses in response to coinfections.

Host-parasite species pairs are known to coevolve, but how multiple parasites coevolve with their host is unclear. By using experimental coevolution of a host bacterium and its viral parasites, we revealed that diverse parasite communities accelerated host evolution and altered coevolutionary dynamics to enhance host resistance and decrease parasite infectivity. Increases in parasite diversity drove shifts in the mode of selection from fluctuating (Red Queen) dynamics to predominately directional (arms race) dynamics. Arms race dynamics were characterized by selective sweeps of generalist resistance mutations in the genes for the host bacterium’s cell surface lipopolysaccharide (a bacteriophage receptor), which caused faster molecular evolution within host populations and greater genetic divergence among populations. These results indicate that exposure to multiple parasites influences the rate and type of host-parasite coevolution.

Hosts are often infected by multiple parasite species, yet the ecological and evolutionary implications of the interactions between hosts and coinfecting parasites are largely unknown. Most theoretical models of evolution among coinfecting parasites focus on the evolution of virulence, but parasites may also evolve to protect their hosts by reducing susceptibility (i.e., conferring resistance) to other parasites or reducing the virulence of coinfecting parasites (i.e., conferring tolerance). Here, we analyze the eco-evolutionary dynamics of parasite-conferred resistance and tolerance using coinfection models. We show that both parasite-conferred resistance and tolerance can evolve for a wide range of underlying trade-offs. The shape and strength of the trade-off qualitatively affects the outcome causing shifts between the minimisation or maximization of protection, intermediate stable strategies, evolutionary branching, and bistability. Furthermore, we find that a protected dimorphism can readily evolve for parasite-conferred resistance, but find no evidence of evolutionary branching for parasite-conferred tolerance, in general agreement with previous work on host evolution. These results provide novel insights into the evolution of parasite-conferred resistance and tolerance, and suggest clues to the underlying trade-offs in recent experimental work on microbe-mediated protection. More generally, our results highlight the context dependence of host-parasite relationships in complex communities.

Artificial selection for antibiotic resistance in microorganisms reveals why and how expected evolutionary trade-offs between population growth rate and population carrying capacity are not observed in resource-limited environments, with ‘trade-ups’ occurring instead.

Understanding how sexual and asexual forms of the same species coexist is a challenge for evolutionary biology. The Red Queen hypothesis predicts that sex is favored by parasite-mediated selection against common asexual genotypes, leading to the coexistence of sexual and asexual hosts. In a geographic mosaic, where the risk of infection varies in space, the theory also predicts that sexual reproduction would be positively correlated with disease prevalence. We tested this hypothesis in lake populations of a New Zealand freshwater snail, Potamopyrgus antipodarum, by comparing pairwise difference matrices for infection frequency and male frequency using partial Mantel tests. We conducted the test at three spatial scales: among lakes on the South Island, among depths within an intensively sampled lake (Lake Alexandrina), and within depths at Lake Alexandrina. We found that the difference in infection risk and the difference in the proportion of sexual snails were significantly and positively correlated at all spatial scales. Our results thus suggest that parasite-mediated selection contributes to the long-term coexistence of sexual and asexual individuals in coevolutionary hotspots, and that the "warmth" of hotspots can vary on small spatial scales.

Characteristics of hosts and parasites have a genetic basis, and thus can be shaped by coevolution. Infections measured under laboratory conditions have shown that the environment in which hosts and parasites interact might substantially affect the strength and specificity of selection. In addition, various components of host-parasite fitness are differentially altered by the environment. Despite this, environmental fluctuations are often excluded from experimental coevolutionary studies and theoretical models as 'noise'. Because most host-parasite interactions exist in heterogeneous environments, we argue that there is a need to incorporate fluctuating environments into future empirical and theoretical work on host-parasite coevolution.

It is a commonly held view that genetically homogenous host populations are more vulnerable to infection than genetically diverse populations. The underlying idea, known as the ‘monoculture effect,' is well documented in agricultural studies. Low genetic diversity in the wild can result from bottlenecks (that is, founder effects), biparental inbreeding or self-fertilization, any of which might increase the risk of epidemics. Host genetic diversity could buffer populations against epidemics in nature, but it is not clear how much diversity is required to prevent disease spread. Recent theoretical and empirical studies, particularly in Daphnia populations, have helped to establish that genetic diversity can reduce parasite transmission. Here, we review the present theoretical work and empirical evidence, and we suggest a new focus on finding ‘diversity thresholds.'

Agricultural contaminants can have devastating impacts on amphibian survival and development, particularly considering their sensitivity to environmental perturbation. However, it is commonly overlooked that amphibians are infected with various parasites that can influence the overall health of the animal when exposed to a stressful environment. We investigated the interaction of agriculture and parasitism on the health of bullfrogs (Rana catesbeiana) in the field. Nine physiological and immunological biomarkers were related to naturally acquired parasite infections, along a gradient of agricultural activity. Most health biomarkers were affected by agriculture, parasitism, or both. Although bullfrogs residing in agricultural areas were infected with fewer parasite species, reflecting environmentally compromised ecosystems, certain persistent parasites interacted with agricultural disturbance to alter the physiology and immune competence of bullfrogs. The consequences of the combination for animal health highlight the importance of parasitism in ecotoxicological studies. Consideration of parasitism is warranted when evaluating the influence of anthropogenic disturbance on amphibian declines and environmental health.

Ploidy-level variation is common and can drastically affect organismal fitness. We focus on the potential consequences of this variation for parasite resistance. First, we elucidate connections between ploidy variation and key factors determining resistance, including allelic diversity, gene expression and physiological condition. We then argue that systems featuring both natural and artificially manipulated ploidy variation should be used to evaluate whether ploidy level influences host–parasite interactions.

Heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. Whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. For instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. Despite this, horizontal transmission, and the host contact structures that facilitates it, have not been considered in heritable symbiont epidemiology. Here, we tested for the importance of host contact, and resulting horizontal transmission, for the epidemiology of a male-killing heritable symbiont (Arsenophonus nasoniae) in parasitoid wasp hosts. We observed that host contact through superparasitism is necessary for this symbiont’s spread in populations of its primary host Nasonia vitripennis, such that when superparasitism rates are high, A. nasoniae almost reaches fixation, causes highly female biased population sex ratios and consequently causes local host extinction. We further tested if natural interspecific variation in superparasitism behaviours predicted symbiont dynamics among parasitoid species. We found that A. nasoniae was maintained in laboratory populations of a closely related set of Nasonia species, but declined in other, more distantly related pteromalid hosts. The natural proclivity of a species to superparasitise was the primary factor determining symbiont persistence. Our results thus indicate that host contact behaviour is a key factor for heritable microbe dynamics when horizontal transmission is possible, and that ‘reproductive parasite’ phenotypes, such as male-killing, may be of secondary importance in the dynamics of such symbiont infections., Author Summary Most insects house heritable symbionts and these represent an important component of their biology, both as partners conveying beneficial traits such as defence against natural enemies, or as antagonists manipulating their hosts’ reproduction. Work on these bacteria mostly assumes that such phenotypes have evolved primarily to facilitate the symbiont’s vertical transmission from parent to offspring. However, several such bacteria also move horizontally between unrelated individuals. Here, we show that a male-killing symbiont actually depends upon horizontal transmission for its spread and maintenance. We observed Arsenophonus nasoniae was only maintained in parasitoid wasp populations when the route enabling horizontal transmission, superparasitism of fly pupae, was allowed. When superparasitism was common enough to cause epidemic spread of A. nasoniae, host population extinction occurred due to lack of males. Our study indicates that superparasitism behaviour is likely to be the key element determining which wasp species maintain this symbiont in nature. This provides new insights into the factors determining heritable symbiont frequency within and amongst species, and highlights the extreme effects such symbionts can have on their host populations. The data also indicate that male-killing may evolve and be maintained as an additional, rather than primary, driver of heritable symbiont fitness.

Different reproductive strategies and the transition to asexuality can be associated with microbial symbionts. Whether such a link exists within mollusks has never been evaluated. We took the first steps towards addressing this possibility by performing pyrosequencing of bacterial 16S rRNA genes associated with Potamopyrgus antipodarum, a New Zealand freshwater snail. A diverse set of 60 tissue collections from P. antipodarum that were genetically and geographically distinct and either obligately sexual or asexual were included, which allowed us to evaluate whether reproductive mode was associated with a particular bacterial community. 2624 unique operational taxonomic units (OTU, 97% DNA similarity) were detected, which were distributed across ~30 phyla. While alpha diversity metrics varied little among individual samples, significant differences in bacterial community composition and structure were detected between sexual and asexual snails, as well as among snails from different lakes and genetic backgrounds. The mean dissimilarity of the bacterial communities between the sexual and asexual P. antipodarum was 90%, largely driven by the presence of Rickettsiales in sexual snails and Rhodobacter in asexual snails. Our study suggests that there might be a link between reproductive mode and the bacterial microbiome of P. antipodarum, though a causal connection requires additional study.