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Abiotic and biotic factors can affect host resistance to parasites. Host diet and host gut microbiomes are two increasingly recognized factors influencing disease resistance. In particular, recent studies demonstrate that (1) particular diets can reduce parasitism; (2) diets can alter the gut microbiome; and (3) the gut microbiome can decrease parasitism. These three separate relationships suggest the existence of indirect links through which diets reduce parasitism through an alteration of the gut microbiome. However, such links are rarely considered and even more rarely experimentally validated. This is surprising because there is increasing discussion of the therapeutic potential of diets and gut microbiomes to control infectious disease. To elucidate these potential indirect links, we review and examine studies on a wide range of animal systems commonly used in diet, microbiome, and disease research. We also examine the relative benefits and disadvantages of particular systems for the study of these indirect links and conclude that mice and insects are currently the best animal systems to test for the effect of diet-altered protective gut microbiomes on infectious disease. Focusing on these systems, we provide experimental guidelines and highlight challenges that must be overcome. Although previous studies have recommended these systems for microbiome research, here we specifically recommend these systems because of their proven relationships between diet and parasitism, between diet and the microbiome, and between the microbiome and parasite resistance. Thus, they provide a sound foundation to explore the three-way interaction between diet, the microbiome, and infectious disease.

Specialized host–microbe symbioses canonically show greater diversity than expected from simple models, both at the population level and within individual hosts. To understand how this heterogeneity arises, we utilize the squash bug, Anasa tristis , and its bacterial symbionts in the genus Caballeronia . We modulate symbiont bottleneck size and inoculum composition during colonization to demonstrate the significance of ecological drift, the noisy fluctuations in community composition due to demographic stochasticity. Consistent with predictions from the neutral theory of biodiversity, we found that ecological drift alone can account for heterogeneity in symbiont community composition between hosts, even when 2 strains are nearly genetically identical. When acting on competing strains, ecological drift can maintain symbiont genetic diversity among different hosts by stochastically determining the dominant strain within each host. Finally, ecological drift mediates heterogeneity in isogenic symbiont populations even within a single host, along a consistent gradient running the anterior-posterior axis of the symbiotic organ. Our results demonstrate that symbiont population structure across scales does not necessarily require host-mediated selection, as it can emerge as a result of ecological drift acting on both isogenic and unrelated competitors. Our findings illuminate the processes that might affect symbiont transmission, coinfection, and population structure in nature, which can drive the evolution of host–microbe symbioses and microbe–microbe interactions within host-associated microbiomes.

Feedbacks between microbiomes and their hosts affect a range of animal behaviors. Human bodies house trillions of symbiotic microorganisms. The genes in this human microbiome outnumber human genes by 100 to 1, and their study is providing profound insights into human health. But humans are not the only animals with microbiomes, and microbiomes do not just impact health. Recent research is revealing surprising roles for microbiomes in shaping behaviors across many animal taxa—shedding light on how behaviors from diet to social interactions affect the composition of host-associated microbial communities ( 1 , 2 ), and how microbes in turn influence host behavior in dramatic ways ( 2 – 6 ).

Agriculture has evolved independently in three insect orders: once in ants, once in termites, and seven times in ambrosia beetles. Although these insect farmers are in some ways quite different from each other, in many more ways they are remarkably similar, suggesting convergent evolution. All propagate their cultivars as clonal monocultures within their nests and, in most cases, clonally across many farmer generations as well. Long-term clonal monoculture presents special problems for disease control, but insect farmers have evolved a combination of strategies to manage crop diseases: They (a) sequester their gardens from the environment; (b) monitor gardens intensively, controlling pathogens early in disease outbreaks; (c) occasionally access population-level reservoirs of genetically variable cultivars, even while propagating clonal monocultures across many farmer generations; and (d) manage, in addition to the primary cultivars, an array of \"auxiliary\" microbes providing disease suppression and other services. Rather than growing a single cultivar solely for nutrition, insect farmers appear to cultivate, and possibly \"artificially select\" for, integrated crop-microbe consortia. Indeed, crop domestication in the context of coevolving and codomesticated microbial consortia may explain the 50-million year old agricultural success of insect farmers.

Environmental stressors can be key drivers of phenotypes, including reproductive strategies and morphological traits. The response to stress may be altered by the presence of microbial associates. For example, in aphids, facultative (secondary) bacterial symbionts can provide protection against natural enemies and stress induced by elevated temperatures. Furthermore, aphids exhibit phenotypic plasticity, producing winged (rather than wingless) progeny that may be better able to escape danger, and the combination of these factors improves the response to stress. How symbionts and phenotypic plasticity, both of which shape aphids’ stress response, influence one another, and together influence host fitness, remains unclear. In this study, we investigate how environmental stressors drive shifts in fecundity and winged/wingless offspring production, and how secondary symbionts influence the process. We induced production of winged offspring through distinct environmental stressors, including exposure to aphid alarm pheromone and crowding, and, in one experiment, we assessed whether the aphid response is influenced by host plant. In the winged morph, energy needed for wing maintenance may lead to trade‐offs with other traits, such as reproduction or symbiont maintenance. Potential trade‐offs between symbiont maintenance and fitness have been proposed but have not been tested. Thus, beyond studying the production of offspring of alternative morphs, we also explore the influence of symbionts across wing/wingless polyphenism as well as symbiont interaction with cross‐generational impacts of environmental stress on reproductive output. All environmental stressors resulted in increased production of winged offspring and shifts in fecundity rates. Additionally, in some cases, aphid host‐by‐symbiont interactions influenced fecundity. Stress on first‐generation aphids had cross‐generational impacts on second‐generation adults, and the impact on fecundity was further influenced by the presence of secondary symbionts and presence/absence of wings. Our study suggests a complex interaction between beneficial symbionts and environmental stressors. Winged aphids have the advantage of being able to migrate out of danger with more ease, but energy needed for wing production and maintenance may come with reproductive costs for their mothers and for themselves, where in certain cases, these costs are altered by secondary symbionts. The authors’ work sheds new light on the interaction between environmental stressors and beneficial symbionts, and how these factors act as drivers in pea aphid life‐history characteristics. Organisms need to adapt to ever‐changing environments, and this study shows how beneficial symbionts influence shifts in response to distinct types of environmental stress.

Many organisms harbor microbial associates that have profound impacts on host traits. The phenotypic effect of symbionts on their hosts may include changes in development, reproduction, longevity, and defense against natural enemies. Determining the consequences of associating with a microbial symbiont requires experimental comparison of hosts with and without symbionts. Then, determining the mechanism by which symbionts alter these phenotypes can involve genomic, genetic, and evolutionary approaches; however, many host-associated symbionts are not amenable to genetic approaches that require cultivation of the microbe outside the host. In the current issue of PLOS Biology, Chrostek and Teixeira highlight an elegant approach to studying functional mechanisms of symbiont-conferred traits. They used directed experimental evolution to select for strains of Wolbachia wMelPop (a bacterial symbiont of fruit flies) that differed in copy number of a region of the genome suspected to underlie virulence. Copy number evolved rapidly when under selection, and wMelPop strains with more copies of the region shortened the lives of their Drosophila hosts more than symbionts with fewer copies. Interestingly, the wMelPop strains with more copies also increase host resistance to viruses compared to symbionts with fewer copies. Their study highlights the power of exploiting alternative approaches when elucidating the functional impacts of symbiotic associations.

Aphids, like most animals, mount a diverse set of defenses against pathogens. For aphids, two of the best studied defenses are symbiont-conferred protection and transgenerational wing induction. Aphids can harbor bacterial symbionts that provide protection against pathogens, parasitoids and predators, as well as against other environmental stressors. In response to signals of danger, aphids also protect not themselves but their offspring by producing more winged than unwinged offspring as a way to ensure that their progeny may be able to escape deteriorating conditions. Such transgenerational wing induction has been studied most commonly as a response to overcrowding of host plants and presence of predators, but recent evidence suggests that pea aphids (Acyrthosiphon pisum) may also begin to produce a greater proportion of winged offspring when infected with fungal pathogens. Here, we explore this phenomenon further by asking how protective symbionts, pathogen dosage and environmental conditions influence this response. Overall, while we find some evidence that protective symbionts can modulate transgenerational wing induction in response to fungal pathogens, we observe that transgenerational wing induction in response to fungal infection is highly variable. That variability cannot be explained entirely by symbiont association, by pathogen load or by environmental stress, leaving the possibility that a complex interplay of genotypic and environmental factors may together influence this trait.

Protective symbionts can allow hosts to occupy otherwise uninhabitable niches. Despite the importance of symbionts in host evolution, we know little about how these associations arise. Encountering a microbe that can improve host fitness in a stressful environment may favor persistent interactions with that microbe, potentially facilitating a long‐term association. The bacterium Bacillus subtilis protects Caenorhabditis elegans nematodes from heat shock by increasing host fecundity compared to the nonprotective Escherichia coli. In this study, we ask how the protection provided by the bacterium affects the host's evolutionary trajectory. Because of the stark fitness contrast between hosts heat shocked on B. subtilis versus E. coli, we tested whether the protection conferred by the bacteria could increase the rate of host adaptation to a stressful environment. We passaged nematodes on B. subtilis or E. coli, under heat stress or standard conditions for 20 host generations of selection. When assayed under heat stress, we found that hosts exhibited the greatest fitness increase when evolved with B. subtilis under stress compared to when evolved with E. coli or under standard (nonstressful) conditions. Furthermore, despite not directly selecting for increased B. subtilis fitness, we found that hosts evolved to harbor more B. subtilis as they adapted to heat stress. Our findings demonstrate that the context under which hosts evolve is important for the evolution of beneficial associations and that protective microbes can facilitate host adaptation to stress. In turn, such host adaptation can benefit the microbe.

Microbes can provide their hosts with protection from biotic and abiotic factors. While many studies have examined how certain bacteria can increase host lifespan, fewer studies have examined how host reproduction can be altered. The nematode Caenorhabditis elegans has been a particularly useful model system to examine how bacteria affect the fitness of their hosts under different contexts. Here, we examine how the bacterium Bacillus subtilis, compared to the standard C. elegans lab diet, Escherichia coli, affects C. elegans survival and reproduction after experiencing a period of intense heat stress. We find that under standard conditions, nematodes reared on B. subtilis produce fewer offspring than when reared on E. coli.However, despite greater mortality rates on B. subtilis after heat shock, young adult nematodes produced more offspring after heat shock when fed B. subtilis compared to E. coli. Because offspring production is necessary for host population growth and evolution, the reproductive advantage conferred by B. subtilis supersedes the survival advantage of E. coli. Furthermore, we found that nematodes must be reared on B. subtilis (particularly at the early stages of development) and not merely be exposed to the bacterium during heat shock, to obtain the reproductive benefits provided by B. subtilis. Taken together, our findings lend insight into the importance of environmental context and interaction timing in shaping the protective benefits conferred by a microbe toward its host. We examine the importance of timing and environmental context in a bacterium–nematode interaction. We find that while the bacterium is costly under standard conditions, it benefits the nematode host when heat stressed, particularly when the interaction occurs at an early stage in the development of the host.