Building the microbiome in health and disease: niche construction and social conflict in bacteria

Microbes collectively shape their environment in remarkable ways via the products of their metabolism. The diverse environmental impacts of macro-organisms have been collated and reviewed under the banner of ‘niche construction’. Here, we identify and review a series of broad and overlapping classes of bacterial niche construction, ranging from biofilm production to detoxification or release of toxins, enzymes, metabolites and viruses, and review their role in shaping microbiome composition, human health and disease. Some bacterial niche-constructing traits can be seen as extended phenotypes, where individuals actively tailor their environment to their benefit (and potentially to the benefit of others, generating social dilemmas). Other modifications can be viewed as non-adaptive by-products from a producer perspective, yet they may lead to remarkable within-host environmental changes. We illustrate how social evolution and niche construction perspectives offer complementary insights into the dynamics and consequences of these traits across distinct timescales. This review highlights that by understanding the coupled bacterial and biochemical dynamics in human health and disease we can better manage host health.     

Cultural niche construction and human evolution

Organisms frequently choose, regulate, construct and destroy important components of their environments, in the process changing the selection pressures to which they and other organisms are exposed. We refer to these processes as niche construction. In humans, culture has greatly amplified our capacity for niche construction and our ability to modify selection pressures. We use gene‐culture coevolutionary models to explore the evolutionary consequences of culturally generated niche construction through human evolution. Our analysis suggests that where cultural traits are transmitted in an unbiased fashion from parent to offspring, cultural niche construction will have a similar effect to gene‐based niche construction. However, cultural transmission biases favouring particular cultural traits may either increase or reduce the range of parameter space over which niche construction has an impact, which means that niche construction with biased transmission will either have a much smaller or a much bigger effect than gene‐based niche construction. The analysis also reveals circumstances under which cultural transmission can overwhelm natural selection, accelerate the rate at which a favoured gene spreads, initiate novel evolutionary events and trigger hominid speciation. Because cultural processes typically operate faster than natural selection, cultural niche construction probably has more profound consequences than gene‐based niche construction, and is likely to have played an important role in human evolution.     

Operationalizing niche construction theory with stone tools

One of the greatest difficulties with evolutionary approaches in the study of stone tools (lithics) has been finding a mechanism for tying culture and biology in a way that preserves human agency and operates at scales that are visible in the archaeological record. The concept of niche construction, whereby organisms actively construct their environments and change the conditions for selection, could provide a solution to this problem. In this review, we evaluate the utility of niche construction theory (NCT) for stone tool archaeology. We apply NCT to lithics both as part of the “extended phenotype” and as residuals or precipitates of other niche‐constructing activities, suggesting ways in which archaeologists can employ niche construction feedbacks to generate testable hypotheses about stone tool use. Finally, we conclude that, as far as its applicability to lithic archaeology, NCT compares favorably to other prominent evolutionary approaches, such as human behavioral ecology and dual‐inheritance theory.     

Cooperation and human cognition: the Vygotskian intelligence hypothesis

Nicholas Humphrey's social intelligence hypothesis proposed that the major engine of primate cognitive evolution was social competition. Lev Vygotsky also emphasized the social dimension of intelligence, but he focused on human primates and cultural things such as collaboration, communication and teaching. A reasonable proposal is that primate cognition in general was driven mainly by social competition, but beyond that the unique aspects of human cognition were driven by, or even constituted by, social cooperation. In the present paper, we provide evidence for this Vygotskian intelligence hypothesis by comparing the social-cognitive skills of great apes with those of young human children in several domains of activity involving cooperation and communication with others. We argue, finally, that regular participation in cooperative, cultural interactions during ontogeny leads children to construct uniquely powerful forms of perspectival cognitive representation.     

Human niche construction in interdisciplinary focus

Niche construction is an endogenous causal process in evolution, reciprocal to the causal process of natural selection. It works by adding ecological inheritance, comprising the inheritance of natural selection pressures previously modified by niche construction, to genetic inheritance in evolution. Human niche construction modifies selection pressures in environments in ways that affect both human evolution, and the evolution of other species. Human ecological inheritance is exceptionally potent because it includes the social transmission and inheritance of cultural knowledge, and material culture. Human genetic inheritance in combination with human cultural inheritance thus provides a basis for gene-culture coevolution, and multivariate dynamics in cultural evolution. Niche construction theory potentially integrates the biological and social aspects of the human sciences. We elaborate on these processes, and provide brief introductions to each of the papers published in this theme issue.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

Runaway cultural niche construction

Cultural niche construction is a uniquely potent source of selection on human populations, and a major cause of recent human evolution. Previous theoretical analyses have not, however, explored the local effects of cultural niche construction. Here, we use spatially explicit coevolutionary models to investigate how cultural processes could drive selection on human genes by modifying local resources. We show that cultural learning, expressed in local niche construction, can trigger a process with dynamics that resemble runaway sexual selection. Under a broad range of conditions, cultural niche-constructing practices generate selection for gene-based traits and hitchhike to fixation through the build up of statistical associations between practice and trait. This process can occur even when the cultural practice is costly, or is subject to counteracting transmission biases, or the genetic trait is selected against. Under some conditions a secondary hitchhiking occurs, through which genetic variants that enhance the capability for cultural learning are also favoured by similar dynamics. We suggest that runaway cultural niche construction could have played an important role in human evolution, helping to explain why humans are simultaneously the species with the largest relative brain size, the most potent capacity for niche construction and the greatest reliance on culture.     

Behavioural environments and niche construction: the evolution of dim-light foraging in bees

Most bees forage for floral resources during the day, but temporal patterns of foraging activity vary extensively, and foraging in dim-light environments has evolved repeatedly. Facultative dim-light foraging behaviour is known in five of nine families of bees, while obligate behaviour is known in four families and evolved independently at least 19 times. The light intensity under which bees forage varies by a factor of 10⁸, and therefore the evolution of dim-light foraging represents the invasion of a new, extreme niche. The repeated evolution of dim-light foraging behaviour in bees allows tests of the hypothesis that behaviour acts as an evolutionary pacemaker. With the exception of one species of Apis , facultative dim-light foragers show no external structural traits that are thought to enable visually mediated flight behaviour in low-light environments. By contrast, most obligate dim-light foragers show a suite of convergent optical traits such as enlarged ocelli and compound eyes. In one intensively studied species ( Megalopta genalis ) these optical changes are associated with neurobiological changes to enhance photon capture. The available ecological evidence suggests that an escape from competition for pollen and nectar resources and avoidance of natural enemies are driving factors in the evolution of obligate dim-light foraging.     

More 'altruistic' punishment in larger societies

If individuals will cooperate with cooperators, and punish non-cooperators even at a cost to themselves, then this strong reciprocity could minimize the cheating that undermines cooperation. Based upon numerous economic experiments, some have proposed that human cooperation is explained by strong reciprocity and norm enforcement. Second-party punishment is when you punish someone who defected on you; third-party punishment is when you punish someone who defected on someone else. Third-party punishment is an effective way to enforce the norms of strong reciprocity and promote cooperation. Here we present new results that expand on a previous report from a large cross-cultural project. This project has already shown that there is considerable cross-cultural variation in punishment and cooperation. Here we test the hypothesis that population size (and complexity) predicts the level of third-party punishment. Our results show that people in larger, more complex societies engage in significantly more third-party punishment than people in small-scale societies.     

How institutions shaped the last major evolutionary transition to large-scale human societies

What drove the transition from small-scale human societies centred on kinship and personal exchange, to large-scale societies comprising cooperation and division of labour among untold numbers of unrelated individuals? We propose that the unique human capacity to negotiate institutional rules that coordinate social actions was a key driver of this transition. By creating institutions, humans have been able to move from the default ‘Hobbesian’ rules of the ‘game of life’, determined by physical/environmental constraints, into self-created rules of social organization where cooperation can be individually advantageous even in large groups of unrelated individuals. Examples include rules of food sharing in hunter–gatherers, rules for the usage of irrigation systems in agriculturalists, property rights and systems for sharing reputation between mediaeval traders. Successful institutions create rules of interaction that are self-enforcing, providing direct benefits both to individuals that follow them, and to individuals that sanction rule breakers. Forming institutions requires shared intentionality, language and other cognitive abilities largely absent in other primates. We explain how cooperative breeding likely selected for these abilities early in the Homo lineage. This allowed anatomically modern humans to create institutions that transformed the self-reliance of our primate ancestors into the division of labour of large-scale human social organization.     

Perspective: seven reasons (not) to neglect niche construction

The niche-construction perspective within evolutionary biology places emphasis on the changes that organisms bring about in their selective environments. Advocates of this viewpoint argue that there is both accuracy and utility in treating niche construction as an evolutionary process in its own right, rather than merely as a product of evolution. Here we discuss and assess seven putative weaknesses of the niche-construction perspective. Niche construction has been neglected or rejected on the grounds that (1) it is not prevalent, (2) its study is not tractable, (3) it is not a process, (4) it is caused by natural selection, (5) it does not change our understanding of evolution in any fundamental way, (6) it does not bring about adaptation, and (7) it is not a single phenomenon. In each case, we critically evaluate the theoretical standing of these arguments and consider the empirical evidence that can be brought to bear on the debate. We conclude that none of these are strong criticisms of the niche-construction perspective and maintain that there are compelling reasons for treating niche construction as a major evolutionary process.     

基于生态位构建的n-种群集合种群动态分析

生态位构建是指任何有机体具有的对环境的修复作用,其可能对集合种群的动态与分布产生深刻的影响.尝试性的将生态位构建概念引入集合种群的续存与动态这一复杂问题的研究中,建立了具有生态位构建作用的多物种集合种群的数学模型.模拟结果表明:随着生态位构建能力的增强,种群的续存能力和平衡态大小都有所增加;在此过程中,生态序的变化具有一定的规律性,分别呈现灭绝数为零的 1、 3、 5、 7和 9的协同演化.     

Evolution of lactase persistence: an example of human niche construction

Niche construction is the process by which organisms construct important components of their local environment in ways that introduce novel selection pressures. Lactase persistence is one of the clearest examples of niche construction in humans. Lactase is the enzyme responsible for the digestion of the milk sugar lactose and its production decreases after the weaning phase in most mammals, including most humans. Some humans, however, continue to produce lactase throughout adulthood, a trait known as lactase persistence. In European populations, a single mutation (-13910*T) explains the distribution of the phenotype, whereas several mutations are associated with it in Africa and the Middle East. Current estimates for the age of lactase persistence-associated alleles bracket those for the origins of animal domestication and the culturally transmitted practice of dairying. We report new data on the distribution of -13910*T and summarize genetic studies on the diversity of lactase persistence worldwide. We review relevant archaeological data and describe three simulation studies that have shed light on the evolution of this trait in Europe. These studies illustrate how genetic and archaeological information can be integrated to bring new insights to the origins and spread of lactase persistence. Finally, we discuss possible improvements to these models.     

Human behavioral ecology and niche construction

We examine the relationship between niche construction theory (NCT) and human behavioral ecology (HBE), two branches of evolutionary science that are important sources of theory in archeology. We distinguish between formal models of niche construction as an evolutionary process, and uses of niche construction to refer to a kind of human behavior. Formal models from NCT examine how environmental modification can change the selection pressures that organisms face. In contrast, formal models from HBE predict behavior assuming people behave adaptively in their local setting, and can be used to predict when and why people engage in niche construction. We emphasize that HBE as a field is much broader than foraging theory and can incorporate social and cultural influences on decision‐making. We demonstrate how these approaches can be formally incorporated in a multi‐inheritance framework for evolutionary research, and argue that archeologists can best contribute to evolutionary theory by building and testing models that flexibly incorporate HBE and NCT elements.     

Niche construction in the light of niche theory

Ecological niche construction, the process whereby an organism improves its environment to enhance its growth and persistence, is an important missing element of niche theory. Niche theory has mainly focused on niche-deteriorating processes, such as resource consumption, predation and competition, which have negative effects on population growth. Here, we integrate niche construction explicitly into modern niche theory. We use a graphical approach to analyse how a species' niche-improving impacts interplay with niche-deteriorating impacts to modify its response to the environment. In a model of two consumers that compete for one limiting resource and one predator, we show how niche construction modifies the traditional niche-deteriorating impacts of its agent or of competing species, and hence the potential for species coexistence. By altering the balance between intraspecific and interspecific competitive effects, niche construction can either generate net interspecific facilitation or strengthen interspecific competition. The adaptive benefit derived from niche construction also strongly affects the realized niche of a niche-constructing species.     

Stalk size and altruism investment within and among populations of the social amoeba

Reproductive division of labour is common in many societies, including those of eusocial insects, cooperatively breeding vertebrates, and most forms of multicellularity. However, conflict over what is best for the individual vs. the group can prevent an optimal division of labour from being achieved. In the social amoeba Dictyostelium discoideum, cells aggregate to become multicellular and a fraction behaves altruistically, forming a dead stalk that supports the rest. Theory suggests that intra‐organismal conflict over spore–stalk cell fate can drive rapid evolutionary change in allocation traits, leading to polymorphisms within populations or rapid divergence between them. Here, we assess several proxies for stalk size and spore–stalk allocation as metrics of altruism investment among strains and across geographic regions. We observe geographic divergence in stalk height that can be partly explained by differences in multicellular size, as well as variation among strains in clonal spore–stalk allocation, suggesting within‐population variation in altruism investment. Analyses of chimeras comprised of strains from the same vs. different populations indicated genotype‐by‐genotype epistasis, where the morphology of the chimeras deviated significantly from the average morphology of the strains developed clonally. The significantly negative epistasis observed for allopatric pairings suggests that populations are diverging in their spore–stalk allocation behaviours, generating incompatibilities when they encounter one another. Our results demonstrate divergence in microbial social traits across geographically separated populations and demonstrate how quantification of genotype‐by‐genotype interactions can elucidate the trajectory of social trait evolution in nature.     

Niche construction,human behavior,and the adaptive‐lag hypothesis

Niche construction is the process whereby organisms modify selective environments, thereby affecting evolution. The niche‐construction perspective is particularly relevant to researchers using evolutionary methods to interpret human behavior and society. On the basis of niche‐construction theory, we argue against the hypothesis that modern humans experience an atypically large adaptive lag. We stress that humans construct their world largely to suit themselves and frequently buffer adaptive lag through cultural niche construction. Where they are unable to do that, natural selection of genes rapidly ensues. Our argument has implications for evolutionary psychology and human behavioral ecology, and suggests that the methods of the latter are potentially applicable to all human societies, even postindustrial ones.     

Reciprocity,culture and human cooperation: previous insights and a new cross-cultural experiment

Understanding the proximate and ultimate sources of human cooperation is a fundamental issue in all behavioural sciences. In this paper, we review the experimental evidence on how people solve cooperation problems. Existing studies show without doubt that direct and indirect reciprocity are important determinants of successful cooperation. We also discuss the insights from a large literature on the role of peer punishment in sustaining cooperation. The experiments demonstrate that many people are ‘strong reciprocators’ who are willing to cooperate and punish others even if there are no gains from future cooperation or any other reputational gains. We document this in new one-shot experiments, which we conducted in four cities in Russia and Switzerland. Our cross-cultural approach allows us furthermore to investigate how the cultural background influences strong reciprocity. Our results show that culture has a strong influence on positive and in especially strong negative reciprocity. In particular, we find large cross-cultural differences in ‘antisocial punishment’ of pro-social cooperators. Further cross-cultural research and experiments involving different socio-demographic groups document that the antisocial punishment is much more widespread than previously assumed. Understanding antisocial punishment is an important task for future research because antisocial punishment is a strong inhibitor of cooperation.