Uncovering the hidden complexity of multicellular magnetotactic bacteria.

Multicellular magnetotactic bacteria (MMB) have a surprisingly complex multicellular lifestyle. A new study in PLOS Biology combines genomics, microscopy, and isotopic labeling to show that MMB form obligately multicellular consortia of genetically diverse cells with rudimentary division of labor.

Host-associated transmission favors transition of a commensal toward antagonism.

The impacts of host-associated microbes on their hosts vary along a continuum of antagonistic, neutral, and beneficial interactions. Transmission mode is predicted to contribute to transitions along the continuum by altering opportunities for the alignment of host and microbe fitness interests. Under vertical transmission, microbial evolution is tightly coupled to the host environment, which may facilitate fitness alignment. In contrast, environmentally transmitted microbes spend time in the external environment, outside of hosts, partially decoupling their evolution from the host. This decoupling may misalign host and microbe fitness interests, potentially favoring antagonistic microbial traits. Here, we tested whether transmission environment alters microbial evolution by manipulating the interaction between a commensal Serratia marcescens bacteria and their insect host Anasa tristis, which is the primary vector of these bacteria into plants, where they cause disease. We experimentally evolved S. marcescens through several selection environments. The bacteria were passaged between A. tristis hosts, between A. tristis hosts and soil, through soil, or through standard culture media. We observed rapid evolution of virulence toward hosts across treatments when bacterial evolution occurred within the host environment, indicating that direct host-to-host transmission can increase opportunities for microbes to adapt to hosts and evolve antagonistic traits.

Evaluating coevolution in a horizontally transmitted mutualism.

Many interspecific interactions are shaped by coevolution. Transmission mode is thought to influence opportunities for coevolution within symbiotic interactions. Vertical transmission maintains partner fidelity, increasing opportunities for coevolution, but horizontal transmission may disrupt partner fidelity, potentially reducing opportunities for coevolution. Despite these predictions, the role of coevolution in the maintenance of horizontally transmitted symbioses is unclear. Leveraging a tractable insect-bacteria symbiosis, we tested for signatures of pairwise coevolution by assessing patterns of host-symbiont specialization. If pairwise coevolution defines the interaction, we expected to observe evidence of reciprocal specialization between hosts and their local symbionts. We found no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts. We predict that selection from multiple host species may favor generalist symbiont traits through diffuse coevolution. Alternatively, selection for generalist traits may be a consequence of selection by hosts for fixed cooperative symbiont traits without coevolution.

Competitive Exclusion of Phytopathogenic Serratia marcescens from Squash Bug Vectors by the Gut Endosymbiont Caballeronia.

Many insects harbor microbial symbiotic partners that offer protection against pathogens, parasitoids, and other natural enemies. Mounting evidence suggests that these symbiotic microbes can play key roles in determining infection outcomes in insect vectors, making them important players in the quest to develop novel vector control strategies. Using the squash bug Anasa tristis, we investigated how the presence of Caballeronia symbionts affected the persistence and intensity of phytopathogenic Serratia marcescens within the insect vector. We reared insects aposymbiotically and with different Caballeronia isolates, infected them with S. marcescens, and then sampled the insects periodically to assess the intensity and persistence of pathogen infection. Squash bugs harboring Caballeronia consistently had much lower-intensity infections and cleared S. marcescens significantly faster than their aposymbiotic counterparts. These patterns held even when we reversed the timing of exposure to symbiont and pathogen. Taken together, these results indicate that Caballeronia symbionts play an essential role in S. marcescens infection outcomes in squash bugs and could be used to alter vector competence to enhance agricultural productivity in the future. IMPORTANCE Insect-microbe symbioses have repeatedly been shown to profoundly impact an insect's ability to vector pathogens to other hosts. The use of symbiotic microbes to control insect vector populations is of growing interest in agricultural settings. Our study examines how symbiotic microbes affect the dynamics of a plant pathogen infection within the squash bug vector Anasa tristis, a well-documented pest of squash and other cucurbit plants and a vector of Serratia marcescens, the causative agent of cucurbit yellow vine disease. We provide evidence that the symbiont Caballeronia prevents successful, long-term establishment of S. marcescens in the squash bug. These findings give us insight into symbiont-pathogen dynamics within the squash bug that could ultimately determine its ability to transmit pathogens and be leveraged to interrupt disease transmission in this system.

The Importance of Environmentally Acquired Bacterial Symbionts for the Squash Bug (Anasa tristis), a Significant Agricultural Pest.

Most insects maintain associations with microbes that shape their ecology and evolution. Such symbioses have important applied implications when the associated insects are pests or vectors of disease. The squash bug, Anasa tristis (Coreoidea: Coreidae), is a significant pest of human agriculture in its own right and also causes damage to crops due to its capacity to transmit a bacterial plant pathogen. Here, we demonstrate that complete understanding of these insects requires consideration of their association with bacterial symbionts in the family Burkholderiaceae. Isolation and sequencing of bacteria housed in the insects' midgut crypts indicates that these bacteria are consistent and dominant members of the crypt-associated bacterial communities. These symbionts are closely related to Caballeronia spp. associated with other true bugs in the superfamilies Lygaeoidea and Coreoidea. Fitness assays with representative Burkholderiaceae strains indicate that the association can significantly increase survival and decrease development time, though strains do vary in the benefits that they confer to their hosts, with Caballeronia spp. providing the greatest benefit. Experiments designed to assess transmission mode indicate that, unlike many other beneficial insect symbionts, the bacteria are not acquired from parents before or after hatching but are instead acquired from the environment after molting to a later developmental stage. The bacteria do, however, have the capacity to escape adults to be transmitted to later generations, leaving the possibility for a combination of indirect vertical and horizontal transmission.

A need to consider the evolutionary genetics of host-symbiont mutualisms.

Despite the ubiquity and importance of mutualistic interactions, we know little about the evolutionary genetics underlying their long-term persistence. As in antagonistic interactions, mutualistic symbioses are characterized by substantial levels of phenotypic and genetic diversity. In contrast to antagonistic interactions, however, we, by and large, do not understand how this variation arises, how it is maintained, nor its implications for future evolutionary change. Currently, we rely on phenotypic models to address the persistence of mutualistic symbioses, but the success of an interaction almost certainly depends heavily on genetic interactions. In this review, we argue that evolutionary genetic models could provide a framework for understanding the causes and consequences of diversity and why selection may favour processes that maintain variation in mutualistic interactions.

Evolution of animal immunity in the light of beneficial symbioses.

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'.

Bloody-minded parasites and sex: the effects of fluctuating virulence.

Asexual lineages can grow at a faster rate than sexual lineages. Why then is sexual reproduction so widespread? Much empirical evidence supports the Red Queen hypothesis. Under this hypothesis, coevolving parasites favour sexual reproduction by adapting to infect common asexual clones and driving them down in frequency. One limitation, however, seems to challenge the generality of the Red Queen: in theoretical models, parasites must be very virulent to maintain sex. Moreover, experiments show virulence to be unstable, readily shifting in response to environmental conditions. Does variation in virulence further limit the ability of coevolving parasites to maintain sex? To address this question, we simulated temporal variation in virulence and evaluated the outcome of competition between sexual and asexual females. We found that variation in virulence did not limit the ability of coevolving parasites to maintain sex. In fact, relatively high variation in virulence promoted parasite-mediated maintenance of sex. With sufficient variation, sexual females persisted even when mean virulence fell well below the threshold virulence required to maintain sex under constant conditions. We conclude that natural variation in virulence does not limit the relevance of the Red Queen hypothesis for natural populations; on the contrary, it could expand the range of conditions over which coevolving parasites can maintain sex.