On the evolutionary feedback between genes and their extended effects in dispersal-limited groups where ecological (or cultural) inheritance is non-random within groups

Organisms continuously modify their living conditions via extended genetic effects on their environment, microbiome, and in some species culture. These effects can impact the fitness of current but also future conspecifics due to non-genetic transmission via ecological or cultural inheritance. In this case, selection on a gene with extended effects depends on the degree to which current and future genetic relatives are exposed to modified conditions. Here, we detail the selection gradient on a quantitative trait with extended effects in a patch-structured population, when gene flow between patches is limited and ecological inheritance within patches can be biased towards offspring. Such a situation is relevant to understand evolutionary driven changes in individual condition that can be preferentially transmitted from parent to offspring, such as micro-environments (e.g., nests), pathogens or microbiome, and culture. Our analysis quantifies how the interaction between limited gene flow and biased ecological inheritance influences the joint evolutionary dynamics of traits together with the conditions they modify, helping understand adaptation via non-genetic modifications. As an illustration, we apply our analysis to a gene-culture coevolution scenario in which genetically-determined learning strategies coevolve with adaptive knowledge. In particular, we show that when social learning is synergistic, selection can favour strategies that generate remarkable levels of knowledge under intermediate levels of both vertical cultural transmission and limited dispersal. More broadly, our theory yields insights into the interplay between genetic and non-genetic inheritance, with implications for how organisms evolve to transform their environments.

Eco-evolutionary dynamics in metacommunities: ecological inheritance, helping within- and harming between-species

Understanding selection on intra- and inter-specific interactions that take place in dispersal-limited communities is a challenge for ecology and evolutionary biology. The problem is that local demographic stochasticity generates eco-evolutionary dynamics that are generally too complicated to make tractable analytical investigations. Here, we circumvent this problem by approximating the selection gradient on a quantitative trait that influences local community dynamics, assuming that such dynamics are deterministic with a stable fixed point. We nonetheless incorporate unavoidable kin selection effects arising from demographic stochasticity. Our approximation reveals that selection depends on how an individual expressing a trait-change influences: (1) its own fitness and the fitness of its current relatives; and (2) the fitness of its downstream relatives through modifications of local ecological conditions (i.e., through ecological inheritance). Mathematically, the effects of ecological inheritance on selection are captured by dispersal-limited versions of press-perturbations of community ecology. We use our approximation to investigate the evolution of helping within- and harming between-species when these behaviours influence demography. We find that individually costly helping evolves more readily when intra-specific competition is for material resources rather than for space because in this case, the costs of kin competition are paid by downstream relatives. Similarly, individually costly harming between species evolves when it alleviates downstream relatives from inter-specific competition. Beyond these examples, our approximation can help better understand the influence of ecological inheritance on a variety of eco-evolutionary dynamics in metacommunities, from consumer-resource and predator-prey coevolution to selection on mating systems with demographic feedbacks.

Niche Construction

Niche construction is the process whereby organisms, through their activities and choices, modify their own and each other’s niches. Examples of niche construction include the building of nests, burrows, and mounds and alternation of physical and chemical conditions by animals, and the creation of shade, influencing of wind speed, and alternation of nutrient cycling by plants. Here the “niche” is construed as the set of natural selection pressures to which the population is exposed (discussed in Ecology). By transforming natural selection pressures, niche construction generates feedback in evolution, on a scale hitherto underestimated and in a manner that alters the evolutionary dynamic. Niche construction also plays a critical role in ecology, in which it supports ecosystem engineering and eco-evolutionary feedbacks and, in part, regulates the flow of energy and nutrients through ecosystems. Niche construction theory is the body of formal (e.g., population genetic, population ecology) mathematical theory that explores niche construction’s evolutionary and ecological ramifications. Many organisms construct developmental environments for their offspring or modify environmental states for other descendants, a process known as “ecological inheritance.” In recent years, this ecological inheritance has been widely recognized as a core component of extra-genetic inheritance, and it is central to attempts within evolutionary biology to broaden the concept of heredity beyond transmission genetics. The development of many organisms—and the recurrence of traits across generations—has been found to depend critically on the construction of developmental environments by ancestors. Historically, the study of niche construction has been contentious because theoretical and empirical findings from niche construction theory appear to challenge some orthodox accounts of evolution. Many researchers studying niche construction embrace an alternative perspective in which niche construction is regarded as a fundamental evolutionary process in its own right, as well as a major source of adaptation. This perspective is aligned intellectually with other progressive movements within evolutionary biology that are calling for an extended evolutionary synthesis. In addition to ecology and evolution, niche construction theory has had an impact on a variety of disciplines, including archaeology, biological anthropology, conservation biology, developmental biology, earth sciences, and philosophy of biology.

Effects of Ecological Inheritance on Coevolution of Cooperative Behaviors and Physically Niche Constructing Behaviors

Niche construction is a process whereby organisms that modify their own or others’ niches through their ecological activities. Recent studies have revealed that changes in social structures of interactions caused by social niche construction of individuals can affect seriously the evolution of cooperation. However, such a social niche also could be changed indirectly by a modification of their physical environment. Our purpose is to clarify the coevolution of cooperative behavior and physically niche-constructing behavior that modifies social niche indirectly. For this purpose, we constructed an evolutionary model in which each individual has not only a strategy for a spatial Prisoner’s Dilemma but also has traits for a niche-constructing behavior for modifying its physical environment that can limit social interactions between neighboring individuals. By conducting evolutionary experiments, we show that a cyclic coevolution between cooperative behavior and niche-constructing behavior occurred in the situation with no or low degree of ecological inheritance, in which the constructed niche could not be inherited in succeeding generations at all. Conversely, when the degree of ecological inheritance was high, the evolution of cooperation was promoted by the emerged environmental structure constructed by the evolved niche-constructing behavior. We also show that the condition for each scenario to occur depends on the settings of the payoff parameters as well as the degree of ecological inheritance.