Modeling host-associating microbes under selection
TL;DR: In this article, the authors investigate a simple model of a microbial lineage living, replicating, migrating and competing in and between two compartments: a host and an environment, and 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.
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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TL;DR: In this article , weak or variable selection on microbial symbiotic associations, horizontal transmission, and low costs of adaptation to novel host habitats are predicted to promote the expansion or maintenance of microbial niches.
Abstract: Our understanding of host influence on microbial evolution has focused on symbiont specialization and the genomic streamlining that often accompanies it. However, a vast diversity of symbiotic lineages facultatively interact with hosts or associate with multiple hosts. Yet, there are no clear expectations for how host association influences the niche of these symbionts or their evolution. Here, we discuss how weak or variable selection on microbial symbiotic associations, horizontal transmission, and low costs of adaptation to novel host habitats are predicted to promote the expansion or maintenance of microbial niches. This broad perspective will aid in developing better and more general predictions for evolution in microbial symbioses.
4 citations
22 Sep 2021
TL;DR: In this article, the authors used non-invasive procedures to detect microbial communities in saliva, oral swabs and brushings from the distal esophagus, and may provide an alternative means of BE detection.
Abstract: Esophageal adenocarcinoma (EAC) claims the lives of half of patients within the first year of diagnosis, and its incidence has rapidly increased since the 1970s despite extensive research into etiological factors. The changes in the microbiome within the distal esophagus in modern populations may help explain the growth in cases that other common EAC risk factors together cannot fully explain. The precursor to EAC is Barrett’s esophagus (BE), a metaplasia adapted to a reflux-mediated microenvironment that can be challenging to diagnose in patients who do not undergo endoscopic screening. Non-invasive procedures to detect microbial communities in saliva, oral swabs and brushings from the distal esophagus allow us to characterize taxonomic differences in bacterial population abundances within patients with BE versus controls, and may provide an alternative means of BE detection. Unique microbial communities have been identified across healthy esophagus, BE, and various stages of progression to EAC, but studies determining dynamic changes in these communities, including migration from proximal stomach and oral cavity niches, and their potential causal role in cancer formation are lacking. Helicobacter pylori is negatively associated with EAC, and the absence of this species has been implicated in the evolution of chromosomal instability, a main driver of EAC, but joint analyses of microbiome and host genomes are needed. Acknowledging technical challenges, future studies on the prediction of microbial dynamics and evolution within BE and the progression to EAC will require larger esophageal microbiome datasets, improved bioinformatics pipelines, and specialized mathematical models for analysis.
4 citations
TL;DR: The theory states that, when mass is conserved in the course of fragmentation, the evolutionarily optimal reproduction mode is fragmentation into exactly two, typically equal, parts and shows conditions which promote evolution of asymmetric division or fragmentation into multiple pieces.
Abstract: Significance Cells and simple cell colonies reproduce by fragmenting their bodies into pieces. Produced newborns need to grow before they can reproduce again. How big a cell or a cell colony should grow? How many offspring should be produced? Should they be of equal size or diverse? We show that the simple fact that the immediate mass of offspring cannot exceed the mass of parents restricts possible answers to these questions. For example, our theory states that, when mass is conserved in the course of fragmentation, the evolutionarily optimal reproduction mode is fragmentation into exactly two, typically equal, parts. Our theory also shows conditions which promote evolution of asymmetric division or fragmentation into multiple pieces.
3 citations
TL;DR: A review of recent applications of experimental and computational methods toward the elucidation of metabolic interactions in plant-associated microbiomes can be found in this article , where the authors highlight how the continued integration of multiple methods can further reveal the general ecological characteristics of plant microbiomes, as well as provide strategies for applications in areas such as improved plant protection, bioremediation, and sustainable agriculture.
2 citations
TL;DR: This review focuses on the mechanisms underlying the early stage of beneficial bacterium-invertebrate associations, from initial contact to the establishment of the symbionts in a specific location of the host’s body.
Abstract: Beneficial associations with bacteria are widespread across animals, spanning a range of symbiont localizations, transmission routes, and functions. While some of these associations have evolved into obligate relationships with permanent symbiont localization within the host, the majority require colonization of every host generation from the environment or via maternal provisions. SUMMARY Beneficial associations with bacteria are widespread across animals, spanning a range of symbiont localizations, transmission routes, and functions. While some of these associations have evolved into obligate relationships with permanent symbiont localization within the host, the majority require colonization of every host generation from the environment or via maternal provisions. Across the broad diversity of host species and tissue types that beneficial bacteria can colonize, there are some highly specialized strategies for establishment yet also some common patterns in the molecular basis of colonization. This review focuses on the mechanisms underlying the early stage of beneficial bacterium-invertebrate associations, from initial contact to the establishment of the symbionts in a specific location of the host’s body. We first reflect on general selective pressures that can drive the transition from a free-living to a host-associated lifestyle in bacteria. We then cover bacterial molecular factors for colonization in symbioses from both model and nonmodel invertebrate systems where these have been studied, including terrestrial and aquatic host taxa. Finally, we discuss how interactions between multiple colonizing bacteria and priority effects can influence colonization. Taking the bacterial perspective, we emphasize the importance of developing new experimentally tractable systems to derive general insights into the ecological factors and molecular adaptations underlying the origin and establishment of beneficial symbioses in animals.
2 citations
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TL;DR: Measures of variation that are standardized by the trait mean are appropriate for making comparisons of genetic variation for quantitative characters to compare evolvabilities, or ability to respond to selection, and to make inferences about the forces that maintain genetic variability.
Abstract: There are two distinct reasons for making comparisons of genetic variation for quantitative characters. The first is to compare evolvabilities, or ability to respond to selection, and the second is to make inferences about the forces that maintain genetic variability. Measures of variation that are standardized by the trait mean, such as the additive genetic coefficient of variation, are appropriate for both purposes. Variation has usually been compared as narrow sense heritabilities, but this is almost always an inappropriate comparative measure of evolvability and variability. Coefficients of variation were calculated from 842 estimates of trait means, variances and heritabilities in the literature. Traits closely related to fitness have higher additive genetic and nongenetic variability by the coefficient of variation criterion than characters under weak selection. This is the reverse of the accepted conclusion based on comparisons of heritability. The low heritability of fitness components is best explained by their high residual variation. The high additive genetic and residual variability of fitness traits might be explained by the great number of genetic and environmental events they are affected by, or by a lack of stabilizing selection to reduce their phenotypic variance. Over one-third of the quantitative genetics papers reviewed did not report trait means or variances. Researchers should always report these statistics, so that measures of variation appropriate to a variety of situations may be calculated.
1,786 citations
TL;DR: Novel hypotheses for how nutrient selection, immune activation and other mechanisms control the biogeography of bacteria in the gut are considered, and the relevance of this spatial heterogeneity to health and disease is discussed.
Abstract: Animals assemble and maintain a diverse but host-specific gut microbial community. In addition to characteristic microbial compositions along the longitudinal axis of the intestines, discrete bacterial communities form in microhabitats, such as the gut lumen, colonic mucus layers and colonic crypts. In this Review, we examine how the spatial distribution of symbiotic bacteria among physical niches in the gut affects the development and maintenance of a resilient microbial ecosystem. We consider novel hypotheses for how nutrient selection, immune activation and other mechanisms control the biogeography of bacteria in the gut, and we discuss the relevance of this spatial heterogeneity to health and disease.
1,637 citations
TL;DR: The principle of natural selection as the motive force for evolution was framed by Darwin in terms of a "struggle for existence" on the part of organisms living in a finite and risky environment, but the logical skeleton of his argument turns out to be a powerful predictive system for changes at all levels of biological organization.
Abstract: The principle of natural selection as the motive force for evolution was framed by Darwin in terms of a "struggle for existence" on the part of organisms living in a finite and risky environment. The logical skeleton of his argument, however, turns out to be a powerful predictive system for changes at all levels of biological organization. As seen by present-day evo lutionists, Darwin's scheme embodies three principles (Lewontin 1) : 1. Different individuals in a popUlation have different morphologies, physiologies, and behaviors (phenotypic variation). 2. Different phenotypes have different rates of survival and reproduc tion in different environments (differential fitness). 3. There is a correlation between parents and offspring in the contribu tion of each to future generations (fitness is heritable). These three principles embody the principle of evolution by natural selec tion. While they hold, a population will undergo evolutionary change. It is important to note a certain generality in the principles. No particular mechanism of inheritance is specifi'ed, but only a correlation in fitness between parent and offspring. The population would evolve whether the correlation between parent and offspring arose from Mendelian, cytoplasmic, or cultural inheritance. Conversely, when a population is at equilibrium under selection (for example, a stable polymorphism due to heterozygous superiority), there is no correlation in fitness between parent and offspring, no matter what the mechanism of inheritance. Nor does Principle 2 specify the reason for the differential rate of contribution to future generations of the different phenotypes. It is not necessary, for example, that resources be in short supply for organisms to struggle for existence. Darwin himself pointed out that "a plant at the edge of a desert is said to struggle for life against the drought." Thus, although Darwin came to the idea of natural selection from consideration of Malthus', essay on overpopulation, the element of competition between organisms for a resource in short supply is not integral to the argument. Natural selection occurs even when two bacterial strains are growing logarithmically in an excess of nutrient broth if they have different division times. The generality of the principles of natural selection means that any enti ties in nature that have variation, reproduction, and heritability may evolve. For example, if we replace the term individual with the term population and
1,571 citations
TL;DR: It is demonstrated that the elementary processes of mutation and selection alone are suifficient to promote rapid proliferation of new designs and support the theory that trade-offs in competitive ability drive adaptive radiation.
Abstract: Successive adaptive radiations have played a pivotal role in the evolution of biological diversity1,2,3. The effects of adaptive radiation are often seen4,5,6, but the underlying causes are difficult to disentangle and remain unclear7,8,9. Here we examine directly therole of ecological opportunity and competition in driving genetic diversification. We use the common aerobic bacterium Pseudomonas fluorescens10, which evolves rapidly under novel environmental conditions to generate a large repertoire of mutants11,12,13. When provided with ecological opportunity (afforded by spatial structure), identical populations diversify morphologically, but when ecological opportunity is restricted there is no such divergence. In spatially structured environments, the evolution of variant morphs follows a predictable sequence and we show that competition among the newly evolved niche-specialists maintains this variation. These results demonstrate that the elementary processes of mutation and selection alone are suifficient to promote rapid proliferation of new designs and support the theory that trade-offs in competitive ability drive adaptive radiation14,15.
1,181 citations
TL;DR: The history of adaptation theory is surveyed, focusing on the rise and fall of various views over the past century and the reasons for the slow development of a mature theory of adaptation.
Abstract: Theoretical studies of adaptation have exploded over the past decade. This work has been inspired by recent, surprising findings in the experimental study of adaptation. For example, morphological evolution sometimes involves a modest number of genetic changes, with some individual changes having a large effect on the phenotype or fitness. Here I survey the history of adaptation theory, focusing on the rise and fall of various views over the past century and the reasons for the slow development of a mature theory of adaptation. I also discuss the challenges that face contemporary theories of adaptation.
1,120 citations