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Open accessJournal ArticleDOI: 10.1073/PNAS.2016487118

On the evolutionary origins of host-microbe associations

02 Mar 2021-Proceedings of the National Academy of Sciences of the United States of America (National Academy of Sciences)-Vol. 118, Iss: 9
Abstract: Many microorganisms with high prevalence in host populations are beneficial to the host and maintained by specialized transmission mechanisms. Although microbial promotion of host fitness and specificity of the associations undoubtedly enhance microbial prevalence, it is an open question whether these symbiotic traits are also a prerequisite for the evolutionary origin of prevalent microbial taxa. To address this issue, we investigate how processes without positive microbial effects on host fitness or host choice can influence the prevalence of certain microbes in a host population. Specifically, we develop a theoretical model to assess the conditions under which particular microbes can become enriched in animal hosts even when they are not providing a specific benefit to a particular host. We find increased prevalence of specific microbes in a host when both show some overlap in their lifecycles, and especially when both share dispersal routes across a patchy habitat distribution. Our results emphasize that host enrichment per se is not a reliable indicator of beneficial host-microbe interactions. The resulting increase in time spent associated with a host may nevertheless give rise to new selection conditions, which can favor microbial adaptations toward a host-associated lifestyle, and, thus, it could be the foundation for subsequent evolution of mutually beneficial coevolved symbioses.

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Topics: Population (52%)
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Open accessJournal ArticleDOI: 10.1038/S41396-021-01039-0
22 Jun 2021-The ISME Journal
Abstract: The concept of fitness is often reduced to a single component, such as the replication rate in a given habitat. For species with multi-step life cycles, this can be an unjustified oversimplification, as every step of the life cycle can contribute to the overall reproductive success in a specific way. In particular, this applies to microbes that spend part of their life cycles associated to a host. In this case, there is a selection pressure not only on the replication rates, but also on the phenotypic traits associated to migrating from the external environment to the host and vice-versa (i.e., the migration rates). Here, we investigate a simple model of a microbial lineage living, replicating, migrating and competing in and between two compartments: a host and an environment. We perform a sensitivity analysis on the overall growth rate to determine the selection gradient experienced by the microbial lineage. We focus on the direction of selection at each point of the phenotypic space, defining an optimal way for the microbial lineage to increase its fitness. We show that microbes can adapt to the two-compartment life cycle through either changes in replication or migration rates, depending on the initial values of the traits, the initial distribution across the two compartments, the intensity of competition, and the time scales involved in the life cycle versus the time scale of adaptation (which determines the adequate probing time to measure fitness). Overall, our model provides a conceptual framework to study the selection on microbes experiencing a host-associated life cycle.

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3 Citations


Open accessPosted ContentDOI: 10.1101/2021.09.21.461237
24 Sep 2021-bioRxiv
Abstract: Background. Our current view of nature depicts a world where macroorganisms dwell in a landscape full of microbes. Some of these microbes not only transit but establish themselves in or on hosts. Although hosts might be occupied by microbes for most of their lives, a microbe-free stage during their prenatal development seems to be the rule for many hosts. The questions of who the first colonizers of a newborn host are and to what extent these are obtained from the parents follow naturally. Results. We have developed a mathematical model to study the effect of the transfer of microbes from parents to offspring. Even without selection, we observe that microbial inheritance is particularly effective in modifying the microbiome of hosts with a short lifespan or limited colonization from the environment, for example by favouring the acquisition of rare microbes. Conclusion. By modelling the inheritance of commensal microbes to newborns, our results suggest that, in an eco-evolutionary context, the impact of microbial inheritance is of particular importance for some specific life histories.

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Topics: Microbiome (50%)


Journal ArticleDOI: 10.1016/J.MIB.2021.08.001
Arne Traulsen1, Michael Sieber1Institutions (1)
Abstract: Microbial populations typically show a large degree of intra-population diversity. This diversity is intertwined with the structure of the population. Here, we discuss endogenous and exogenous drivers of population structure in microbes and how the population structure can affect evolutionary dynamics and vice versa. Endogenous structure, which can be genetic or demographic, is driven by the ecology and evolutionary dynamics within the population. Exogenous structure is typically driven by the spatial and temporal properties of the environment. A particular interesting case arises when also this exogenous structure experiences feedbacks from the microbial population.

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Topics: Population (61%), Evolutionary dynamics (60%), Evolutionary ecology (57%) ... show more

Open accessJournal ArticleDOI: 10.1111/1751-7915.13976
Abstract: Microbial technology is exceptional among human activities and endeavours in its range of applications that benefit humanity, even exceeding those of chemistry. What is more, microbial technologists are among the most creative scientists, and the scope of the field continuously expands as new ideas and applications emerge. Notwithstanding this diversity of applications, given the dire predictions for the fate of the surface biosphere as a result of current trajectories of global warming, the future of microbial biotechnology research must have a single purpose, namely to help secure the future of life on Earth. Everything else will, by comparison, be irrelevant. Crucially, microbes themselves play pivotal roles in climate (Cavicchioli et al., Nature Revs Microbiol 17: 569-586, 2019). To enable realization of their full potential in humanity's effort to survive, development of new and transformative global warming-relevant technologies must become the lynchpin of microbial biotechnology research and development. As a consequence, microbial biotechnologists must consider constraining their usual degree of freedom, and re-orienting their focus towards planetary-biosphere exigences. And they must actively seek alliances and synergies with others to get the job done as fast as humanly possible; they need to enthusiastically embrace and join the global effort, subordinating where necessary individual aspirations to the common good (the amazing speed with which new COVID-19 diagnostics and vaccines were developed and implemented demonstrates what is possible given creativity, singleness of purpose and funding). In terms of priorities, some will be obvious, others less so, with some only becoming revealed after dedicated effort yields new insights/opens new vistas. We therefore refrain from developing a priority list here. Rather, we consider what is likely to happen to the Earth's biosphere if we (and the rest of humanity) fail to rescue it. We do so with the aim of galvanizing the formulation and implementation of strategic and financial science policy decisions that will maximally stimulate the development of relevant new microbial technologies, and maximally exploit available technologies, to repair existing environmental damage and mitigate against future deterioration.

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Open accessJournal ArticleDOI: 10.1073/PNAS.1218525110
Abstract: In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal–bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal–bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.

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1,711 Citations


Journal ArticleDOI: 10.1038/2011145A0
J. Maynard Smith1Institutions (1)
01 Mar 1964-Nature
Abstract: WYNNE-EDWARDS1,2 has argued persuasively for the importance of behaviour in regulating the density of animal populations, and has suggested that since such behaviour favours the survival of the group and not of the individual it must have evolved by a process of group selection. It is the purpose of this communication to consider how far this is likely to be true.

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Topics: Kin selection (64%), Group selection (59%), Green-beard effect (52%)

1,498 Citations


Open accessJournal ArticleDOI: 10.1073/PNAS.0602530103
Arne Traulsen1, Martin A. NowakInstitutions (1)
Abstract: We propose a minimalist stochastic model of multilevel (or group) selection. A population is subdivided into groups. Individuals interact with other members of the group in an evolutionary game that determines their fitness. Individuals reproduce, and offspring are added to the same group. If a group reaches a certain size, it can split into two. Faster reproducing individuals lead to larger groups that split more often. In our model, higher-level selection emerges as a byproduct of individual reproduction and population structure. We derive a fundamental condition for the evolution of cooperation by group selection: if b/c > 1 + n/m, then group selection favors cooperation. The parameters b and c denote the benefit and cost of the altruistic act, whereas n and m denote the maximum group size and the number of groups. The model can be extended to more than two levels of selection and to include migration.

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750 Citations


Journal ArticleDOI: 10.1146/ANNUREV.MICRO.51.1.47
Abstract: ▪ Abstract Xenorhabdus and Photorhabdus spp. are gram negative gamma proteobacteria that form entomopathogenic symbioses with soil nematodes. They undergo a complex life cycle that involves a symbiotic stage, in which the bacteria are carried in the gut of the nematodes, and a pathogenic stage, in which susceptible insect prey are killed by the combined action of the nematode and the bacteria. Both bacteria produce antibiotics, intracellular protein crystals, and numerous other products. These traits change in phase variants, which arise when the bacteria are maintained under stationary phase conditions in the laboratory. Molecular biological studies suggest that Xenorhabdus and Photorhabdus spp. may serve as valuable model systems for studying signal transduction and transcriptional and posttranscriptional regulation of gene expression. Such studies also indicate that these bacterial groups, which had been previously considered to be very similar, may actually be quite different at the molecular level.

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Topics: Photorhabdus (66%), Xenorhabdus (65%), Photorhabdus luminescens (59%) ... show more

536 Citations


Journal ArticleDOI: 10.1086/283200
Abstract: When an animal eats "spoiled" or "rotten" food of any kind, it runs a largely unknown risk (except in the case of grains) of being injured by toxins or microbe-produced antibiotics, getting food wi...

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491 Citations


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