The human gut harbors a large and complex community of beneficial microbes that remain stable over long periods. This stability is considered critical for good health but is poorly understood. Here we develop a body of ecological theory to help us understand microbiome stability. Although cooperating networks of microbes can be efficient, we find that they are often unstable. Counterintuitively, this finding indicates that hosts can benefit from microbial competition when this competition dampens cooperative networks and increases stability. More generally, stability is promoted by limiting positive feedbacks and weakening ecological interactions. We have analyzed host mechanisms for maintaining stability-including immune suppression, spatial structuring, and feeding of community members-and support our key predictions with recent data.
Bacteria often live within matrix-embedded communities, termed biofilms, which are now understood to be a major mode of microbial life. The study of biofilms has revealed their vast complexity both in terms of resident species composition and phenotypic diversity. Despite this complexity, theoretical and experimental work in the past decade has identified common principles for understanding microbial biofilms. In this Review, we discuss how the spatial arrangement of genotypes within a community influences the cooperative and competitive cell-cell interactions that define biofilm form and function. Furthermore, we argue that a perspective rooted in ecology and evolution is fundamental to progress in microbiology.
■ Abstract Although best known for cooperation, insect societies also manifest many potential conflicts among individuals. These conflicts involve both direct reproduction by individuals and manipulation of the reproduction of colony members. Here we review five major areas of reproductive conflict in insect societies: (a) sex allocation, (b) queen rearing, (c) male rearing, (d) queen-worker caste fate, and (e) breeding conflicts among totipotent adults. For each area we discuss the basis for conflict (potential conflict), whether conflict is expressed (actual conflict), whose interests prevail (conflict outcome), and the factors that reduce colony-level costs of conflict (conflict resolution), such as factors that cause workers to work rather than to lay eggs. Reproductive conflicts are widespread, sometimes having dramatic effects on the colony. However, three key factors (kinship, coercion, and constraint) typically combine to limit the effects of reproductive conflict and often lead to complete resolution. INTRODUCTIONObservation of an insect society readily reveals cooperation. Workers actively work for the good of the colony as they forage, guard, build, and nurse. Detailed study reinforces this impression. Workers cooperate to forage and defend by means of sophisticated communication signals (56,113). In some species cooperation includes extreme altruism, with defending workers sacrificing their lives as they deploy detachable stings or chemical-filled exploding abdomens to deter intruders (56,113). However, sophisticated cooperation in one area of social life does not preclude conflict in another. Egg laying, brood rearing, and queen-worker caste development, for example, can all be associated with significant conflict. Indeed, potential conflict in insect societies is inevitable because insect societies are almost always families, not clones. Nevertheless, conflict in insect colonies is less obvious 0066-4170/06/0107-0581$20.00 581 Annu. Rev. Entomol. 2006.51:581-608. Downloaded from arjournals.annualreviews.org by University of Massachusetts -Amherst on 10/14/09. For personal use only. 582RATNIEKS FOSTER WENSELEERS than cooperation, which suggests that conflict may often be resolved or weak. What factors enable insect societies to resolve their conflicts? In this review, we discuss the large body of work devoted to this question, which has focused primarily on the eusocial Hymenoptera (bees, ants, and wasps). INCLUSIVE FITNESS THEORY: EXPLANATION FOR BOTH COOPERATION AND CONFLICTInclusive fitness theory (47) provides a general explanation for reproductive division of labor in eusocial insects, with some individuals forgoing direct reproduction to help rear the offspring of other colony members. The intermediate levels of relatedness typically found in insect societies provide a strong incentive for altruism, and kin are also close at hand and can readily be helped by defense or food collection. Ironically, the same theory also led to the realization that insect societies are subject to internal conflic...
The human body carries vast communities of microbes that provide many benefits. Our microbiome is complex and challenging to understand, but evolutionary theory provides a universal framework with which to analyse its biology and health impacts. Here we argue that to understand a given microbiome feature, such as colonization resistance, host nutrition or immune development, we must consider how hosts and symbionts evolve. Symbionts commonly evolve to compete within the host ecosystem, while hosts evolve to keep the ecosystem on a leash. We suggest that the health benefits of the microbiome should be understood, and studied, as an interplay between microbial competition and host control.
On its own, a single cell cannot exert more than a microscopic influence on its immediate surroundings. However, via strength in numbers and the expression of cooperative phenotypes, such cells can enormously impact their environments. Simple cooperative phenotypes appear to abound in the microbial world, but explaining their evolution is challenging because they are often subject to exploitation by rapidly growing, non-cooperative cell lines. Population spatial structure may be critical for this problem because it influences the extent of interaction between cooperative and non-cooperative individuals. It is difficult for cooperative cells to succeed in competition if they become mixed with non-cooperative cells, which can exploit the public good without themselves paying a cost. However, if cooperative cells are segregated in space and preferentially interact with each other, they may prevail. Here we use a multi-agent computational model to study the origin of spatial structure within growing cell groups. Our simulations reveal that the spatial distribution of genetic lineages within these groups is linked to a small number of physical and biological parameters, including cell growth rate, nutrient availability, and nutrient diffusivity. Realistic changes in these parameters qualitatively alter the emergent structure of cell groups, and thereby determine whether cells with cooperative phenotypes can locally and globally outcompete exploitative cells. We argue that cooperative and exploitative cell lineages will spontaneously segregate in space under a wide range of conditions and, therefore, that cellular cooperation may evolve more readily than naively expected.
Biofilms are densely packed communities of microbial cells that grow on surfaces and surround themselves with secreted polymers. Many bacterial species form biofilms, and their study has revealed them to be complex and diverse. The structural and physiological complexity of biofilms has led to the idea that they are coordinated and cooperative groups, analogous to multicellular organisms. We evaluate this idea by addressing the findings of microbiologists from the perspective of sociobiology, including theories of collective behavior (self-organization) and social evolution. This yields two main conclusions. First, the appearance of organization in biofilms can emerge without active coordination. That is, biofilm properties such as phenotypic differentiation, species stratification and channel formation do not necessarily require that cells communicate with one another using specialized signaling molecules. Second, while local cooperation among bacteria may often occur, the evolution of cooperation among all cells is unlikely for most biofilms. Strong conflict can arise among multiple species and strains in a biofilm, and spontaneous mutation can generate conflict even within biofilms initiated by genetically identical cells. Biofilms will typically result from a balance between competition and cooperation, and we argue that understanding this balance is central to building a complete and predictive model of biofilm formation.
Summary The budding yeast, Saccharomyces cerevisiae, has emerged as an archetype of eukaryotic cell biology. Here we show that S. cerevisiae is also a model for the evolution of cooperative behavior by revisiting flocculation, a self-adherence phenotype lacking in most laboratory strains. Expression of the gene FLO1 in the laboratory strain S288C restores flocculation, an altered physiological state, reminiscent of bacterial biofilms. Flocculation protects the FLO1-expressing cells from multiple stresses, including antimicrobials and ethanol. Furthermore, FLO1+ cells avoid exploitation by non-expressing flo1 cells by self/non-self recognition: FLO1+ cells preferentially stick to one another, regardless of genetic relatedness across the rest of the genome. Flocculation, therefore, is driven by one of a few known “green beard genes”, which direct cooperation towards other carriers of the same gene. Moreover, FLO1 is highly variable among strains both in expression and in sequence, suggesting that flocculation in S. cerevisiae is a dynamic, rapidly-evolving social trait.
Microbial cells secrete numerous enzymes, scavenging molecules, and signals that can promote the growth and survival of other cells around them [1-4]. This observation is consistent with the evolution of cooperation within species [5], and there is now an increasing emphasis on the importance of cooperation between different microbial species [4, 6]. We lack, however, a systematic test of the importance of mutually positive interactions between different species, which is vital for assessing the commonness and importance of cooperative evolution in natural communities. Here, we study the extent of mutually positive interaction among bacterial strains isolated from a common aquatic environment. Using data collected from two independent experiments evaluating community productivity across diversity gradients, we show that (1) in pairwise species combinations, the great majority of interactions are net negative and (2) there is no evidence that strong higher-order positive effects arise when more than two species are mixed together. Our data do not exclude the possibility of positive effects in one direction where one species gains at the expense of another, i.e., predator-prey-like interactions. However, these do not constitute cooperation and our analysis suggests that the typical result of adaptation to other microbial species will be competitive, rather than cooperative, phenotypes.
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