Understanding how horizontally transmitted mutualisms are maintained is a major focus of symbiosis research.1,2,3,4 Unlike vertical transmission, hosts that rely on horizontal transmission produce ...symbiont-free offspring that must find and acquire their beneficial microbes from the environment. This transmission strategy is inherently risky since hosts may not obtain the right symbiont every generation. Despite these potential costs, horizontal transmission underlies stable mutualisms involving a large diversity of both plants and animals.5,6,7,8,9 One largely unexplored way horizontal transmission is maintained is for hosts to evolve sophisticated mechanisms to consistently find and acquire specific symbionts from the environment. Here, we examine this possibility in the squash bug Anasa tristis, an insect pest that requires bacterial symbionts in the genus Caballeronia10 for survival and development.11 We conduct a series of behavioral and transmission experiments that track strain-level transmission in vivo among individuals in real-time. We demonstrate that nymphs can accurately find feces from adult bugs in both the presence and absence of those adults. Once nymphs locate the feces, they deploy feeding behavior that results in nearly perfect symbiont acquisition success. We further demonstrate that nymphs can locate and feed on isolated, cultured symbionts in the absence of feces. Finally, we show this acquisition behavior is highly host specific. Taken together, our data describe not only the evolution of a reliable horizontal transmission strategy, but also a potential mechanism that drives patterns of species-specific microbial communities among closely related, sympatric host species.
•Choice assays show A. tristis nymphs are highly attracted to symbiont-rich feces•A. tristis nymphs use flush feeding to acquire symbionts from fecal matter•Nymphs are only attracted to conspecific feces, reinforcing host-microbe associations
Villa et al. demonstrate how an agricultural pest reliably transmits their beneficial microbial symbionts despite having to acquire them from the environment every generation. Real-time tracking of fluorescently tagged symbionts shows that symbiont-free nymphs use species-specific homing and feeding behaviors to ingest symbionts from adult feces.
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.
Animal Behavior and the Microbiome Ezenwa, Vanessa O.; Gerardo, Nicole M.; Inouye, David W. ...
Science (American Association for the Advancement of Science),
10/2012, Letnik:
338, Številka:
6104
Journal Article
Recenzirano
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
).
Immune system processes serve as the backbone of animal defences against pathogens and thus have evolved under strong selection and coevolutionary dynamics. Most microorganisms that animals ...encounter, however, are not harmful, and many are actually beneficial. Selection should act on hosts to maintain these associations while preventing exploitation of within-host resources. Here, we consider how several key aspects of beneficial symbiotic associations may shape host immune system evolution. When host immunity is used to regulate symbiont populations, there should be selection to evolve and maintain targeted immune responses that recognize symbionts and suppress but not eliminate symbiont populations. Associating with protective symbionts could relax selection on the maintenance of redundant host-derived immune responses. Alternatively, symbionts could facilitate the evolution of host immune responses if symbiont-conferred protection allows for persistence of host populations that can then adapt. The trajectory of immune system evolution will likely differ based on the type of immunity involved, the symbiont transmission mode and the costs and benefits of immune system function. Overall, the expected influence of beneficial symbiosis on immunity evolution depends on how the host immune system interacts with symbionts, with some interactions leading to constraints while others possibly relax selection on immune system maintenance. This article is part of the theme issue 'The role of the microbiome in host evolution'.
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.
Numerous adaptations are gained in light of a symbiotic lifestyle. Here, we investigated the obligate partnership between tortoise leaf beetles (Chrysomelidae: Cassidinae) and their pectinolytic ...Stammera symbionts to detail how changes to the bacterium’s streamlined metabolic range can shape the digestive physiology and ecological opportunity of its herbivorous host. Comparative genomics of 13 Stammera strains revealed high functional conservation, highlighted by the universal presence of polygalacturonase, a primary pectinase targeting nature’s most abundant pectic class, homogalacturonan (HG). Despite this conservation, we unexpectedly discovered a disparate distribution for rhamnogalacturonan lyase, a secondary pectinase hydrolyzing the pectic heteropolymer, rhamnogalacturonan I (RG-I). Consistent with the annotation of rhamnogalacturonan lyase in Stammera, cassidines are able to depolymerize RG-I relative to beetles whose symbionts lack the gene. Given the omnipresence of HG and RG-I in foliage, Stammera that encode pectinases targeting both substrates allow their hosts to overcome a greater diversity of plant cell wall polysaccharides and maximize access to the nutritionally rich cytosol. Possibly facilitated by their symbionts’ expanded digestive range, cassidines additionally endowed with rhamnogalacturonan lyase appear to utilize a broader diversity of angiosperms than those beetles whose symbionts solely supplement polygalacturonase. Our findings highlight how symbiont metabolic diversity, in concert with host adaptations, may serve as a potential source of evolutionary innovations for herbivorous lineages.
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•Stammera genomes are structurally conserved across Cassidinae species•Symbiont pectinases complement the host’s endogenous cellulases and xylanases•Stammera differentially encode pectinases in their reduced genomes•Symbiont pectinolytic range reflects host plant breadth
Tortoise leaf beetles rely on the symbiotic bacterium, Stammera, to digest foliage rich in pectin. Salem et al. reveal that Stammera varies in the pectinases it encodes and supplements. Stammera encoding a more dynamic digestive range allows its host to overcome a greater diversity of plant polysaccharides, corresponding to a wider ecological distribution.
In recent years, the formalization of artisanal and small-scale gold mining (ASGM) activities has become a key strategy for governments to better govern and regulate the sector. While scholars have ...focused on examining the viability of formalization itself, little is known about the outcomes once ASGM operations become formal, or whether formalization efforts are sustainable. Peru has made great strides on simplifying the formalization process and has formalized over 9600 artisanal miners. Drawing on a case study from one of these formalized operations, this research examines postformalization outcomes. Findings from interviews with government officials and members of the ASGM community in one of the most important ASGM regions of Peru, Puno, demonstrate that formalization has yielded mixed results. Formal ASGM operations have improved health and safety practices and labor conditions, and miners believe their environmental awareness has increased. Despite these changes, miners who have become formalized feel even more pursued and scrutinized than they did when they operated informally, and they continue to face challenges obtaining technical support and accessing capital. We argue that although some progress has been made in formalization efforts, the problems and weaknesses within the approach may inadvertently push miners back into informality.We conclude that in order for formalization to be more fruitful for governments and miners, governments working on formalizing ASGM activities would greatly benefit from the creation of a solid postformalization strategy focused on educating and supporting formal ASGM operations.
•Analyzes the benefits and challenges of formalization from the perspectives of government officials and miners.•Formal ASGM operations have made changes in health and safety protocols, labor organization, and environmental protection.•Post-formalization requirements can lead miners to revert to informality if support is not provided.•Provides insights for governments and international organizations as they tailor policies, regulations, and donor projects.•Concludes that governments would benefit from the creation of a post-formalization strategy to support formal miners.
Microbial associations are integral to all eukaryotes. Mutualism, the interaction of two species for the benefit of both, is an important aspect of microbial associations, with evidence that ...multicellular organisms in particular benefit from microbes. However, the microbe's perspective has largely been ignored, and it is unknown whether most microbial symbionts benefit from their associations with hosts. It has been presumed that microbial symbionts receive host-derived nutrients or a competition-free environment with reduced predation, but there have been few empirical tests, or even critical assessments, of these assumptions. We evaluate these hypotheses based on available evidence, which indicate reduced competition and predation are not universal benefits for symbionts. Some symbionts do receive nutrients from their host, but this has not always been linked to a corresponding increase in symbiont fitness. We recommend experiments to test symbiont fitness using current experimental systems of symbiosis and detail considerations for other systems. Incorporating symbiont fitness into symbiosis research will provide insight into the evolution of mutualistic interactions and cooperation in general.
Several insect groups have obligate, vertically transmitted bacterial symbionts that provision hosts with nutrients that are limiting in the diet. Some of these bacteria have been shown to descend ...from ancient infections. Here we show that the large group of related insects including cicadas, leafhoppers, treehoppers, spittlebugs, and planthoppers host a distinct clade of bacterial symbionts. This newly described symbiont lineage belongs to the phylum BACTEROIDETES: Analyses of 16S rRNA genes indicate that the symbiont phylogeny is completely congruent with the phylogeny of insect hosts as currently known. These results support the ancient acquisition of a symbiont by a shared ancestor of these insects, dating the original infection to at least 260 million years ago. As visualized in a species of spittlebug (Cercopoidea) and in a species of sharpshooter (Cicadellinae), the symbionts have extraordinarily large cells with an elongate shape, often more than 30 microm in length; in situ hybridizations verify that these correspond to the phylum BACTEROIDETES: "Candidatus Sulcia muelleri" is proposed as the name of the new symbiont.
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