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.     

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.     

The extended evolutionary synthesis: its structure,assumptions and predictions

Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways—one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the ‘extended evolutionary synthesis'' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism–environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.     

A generalised approach to the study and understanding of adaptive evolution

Evolutionary theory has made large impacts on our understanding and management of the world, in part because it has been able to incorporate new data and new insights successfully. Nonetheless, there is currently a tension between certain biological phenomena and mainstream evolutionary theory. For example, how does the inheritance of molecular epigenetic changes fit into mainstream evolutionary theory? Is niche construction an evolutionary process? Is local adaptation via habitat choice also adaptive evolution? These examples suggest there is scope (and perhaps even a need) to broaden our views on evolution. We identify three aspects whose incorporation into a single framework would enable a more generalised approach to the understanding and study of adaptive evolution: (i) a broadened view of extended phenotypes; (ii) that traits can respond to each other; and (iii) that inheritance can be non-genetic. We use causal modelling to integrate these three aspects with established views on the variables and mechanisms that drive and allow for adaptive evolution. Our causal model identifies natural selection and non-genetic inheritance of adaptive parental responses as two complementary yet distinct and independent drivers of adaptive evolution. Both drivers are compatible with the Price equation; specifically, non-genetic inheritance of parental responses is captured by an often-neglected component of the Price equation. Our causal model is general and simplified, but can be adjusted flexibly in terms of variables and causal connections, depending on the research question and/or biological system. By revisiting the three examples given above, we show how to use it as a heuristic tool to clarify conceptual issues and to help design empirical research. In contrast to a gene-centric view defining evolution only in terms of genetic change, our generalised approach allows us to see evolution as a change in the whole causal structure, consisting not just of genetic but also of phenotypic and environmental variables.     

THE NICHE CONSTRUCTION PERSPECTIVE: A CRITICAL APPRAISAL

Niche construction refers to the activities of organisms that bring about changes in their environments, many of which are evolutionarily and ecologically consequential. Advocates of niche construction theory (NCT) believe that standard evolutionary theory fails to recognize the full importance of niche construction, and consequently propose a novel view of evolution, in which niche construction and its legacy over time (ecological inheritance) are described as evolutionary processes, equivalent in importance to natural selection. Here, we subject NCT to critical evaluation, in the form of a collaboration between one prominent advocate of NCT, and a team of skeptics. We discuss whether niche construction is an evolutionary process, whether NCT obscures or clarifies how natural selection leads to organismal adaptation, and whether niche construction and natural selection are of equivalent explanatory importance. We also consider whether the literature that promotes NCT overstates the significance of niche construction, whether it is internally coherent, and whether it accurately portrays standard evolutionary theory. Our disagreements reflect a wider dispute within evolutionary theory over whether the neo‐Darwinian synthesis is in need of reformulation, as well as different usages of some key terms (e.g., evolutionary process).     

Evolutionary models of extended phenotypes

A variety of theoretical models incorporate phenotypes expressed in the external environment, but a core question is whether such traits generate dynamics that alter evolution. This has proven to be a challenging and controversial proposition. However, several recent modelling frameworks provide insight: indirect genetic effect (IGE) models, niche construction models, and evolutionary feedback models. These distinct approaches converge upon the observation that gene action at a distance generates feedback that expands the range of trait values and evolutionary rates that we should expect to observe in empirical studies. Such conceptual replication provides solid evidence that traits with extended effects have important evolutionary consequences, but more empirical work is needed to evaluate the predictive power of different modelling approaches.     

The extended evolutionary synthesis and human origins: Archaeological perspectives

Recent developments in evolutionary biology have led to a call for an extension of standard evolutionary theory, with its emphasis on processes such as selection and drift, into a much larger theoretical framework that includes processes such as niche construction, developmental plasticity, inclusive inheritance, and developmental bias. Skeptics argue that these processes are already subsumed within the standard theory and thus an extension is not required. Here, we outline what this evolutionary “rethink” might mean for the study of human origins. Specifically, can paleoanthropologists benefit from an extended theoretical toolkit? The papers in this special issue suggest it can be useful but may not be necessary, depending on the kinds of questions that are being asked.     

Hierarchy Theory of Evolution and the Extended Evolutionary Synthesis: Some Epistemic Bridges,Some Conceptual Rifts

Contemporary evolutionary biology comprises a plural landscape of multiple co-existent conceptual frameworks and strenuous voices that disagree on the nature and scope of evolutionary theory. Since the mid-eighties, some of these conceptual frameworks have denounced the ontologies of the Modern Synthesis and of the updated Standard Theory of Evolution as unfinished or even flawed. In this paper, we analyze and compare two of those conceptual frameworks, namely Niles Eldredge’s Hierarchy Theory of Evolution (with its extended ontology of evolutionary entities) and the Extended Evolutionary Synthesis (with its proposal of an extended ontology of evolutionary processes), in an attempt to map some epistemic bridges (e.g. compatible views of causation; niche construction) and some conceptual rifts (e.g. extra-genetic inheritance; different perspectives on macroevolution; contrasting standpoints held in the “externalism–internalism” debate) that exist between them. This paper seeks to encourage theoretical, philosophical and historiographical discussions about pluralism or the possible unification of contemporary evolutionary biology.     

Which evolutionary model best explains the culture of honour?

The culture of honour hypothesis offers a compelling example of how human psychology differentially adapts to pastoral and horticultural environments. However, there is disagreement over whether this pattern is best explained by a memetic, evolutionary psychological, dual inheritance, or niche construction model. I argue that this disagreement stems from two shortcomings: lack of clarity about the theoretical commitments of these models and inadequate comparative data for testing them. To resolve the first problem, I offer a theoretical framework for deriving competing predictions from each of the four models. In particular, this involves a novel interpretation of the difference between dual inheritance theory and cultural niche construction. I then illustrate a strategy for testing their predictions using data from the Human Relations Area File. Empirical results suggest that the aggressive psychological phenotype typically associated with honour culture is more common among pastoral societies than among horticultural societies. Theoretical considerations suggest that this pattern is best explained as a case of cultural niche construction.     

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.     

Genes,culture, and the human niche: An overview

The sharp distinction between biological traits and culturally based traits, which had long been standard in evolutionary approaches to behavior, was blurred in the early 1980s by mathematical models that allowed a co‐dependent evolution of genetic transmission and cultural information. Niche‐construction theory has since added another contrast to standard evolutionary theory, in that it views niche construction as a cause of evolutionary change rather than simply a product of selection. While offering a new understanding of the coevolution of genes, culture, and human behavior, niche‐construction models also invoke multivariate causality, which require multiple time series to resolve. The empirical challenge lies in obtaining time‐series data on causal pathways involved in the coevolution of genes, culture, and behavior. This is a significant issue in archeology, where time series are often sparse and causal behaviors are represented only by proxies in the material record.     

Unmodern Synthesis: Developmental Hierarchies and the Origin of Phenotypes

The question of whether the modern evolutionary synthesis requires an extension has recently become a topic of discussion, and a source of controversy. We suggest that this debate is, for the most part, not about the modern synthesis at all. Rather, it is about the extent to which genetic mechanisms can be regarded as the primary determinants of phenotypic characters. The modern synthesis has been associated with the idea that phenotypes are the result of gene products, while supporters of the extended synthesis have suggested that environmental factors, along with processes such as epigenetic inheritance, and niche construction play an important role in character formation. We argue that the methodology of the modern evolutionary synthesis has been enormously successful, but does not provide an accurate characterization of the origin of phenotypes. For its part, the extended synthesis has yet to be transformed into a testable theory, and accordingly, has yielded few results. We conclude by suggesting that the origin of phenotypes can only be understood by integrating findings from all levels of the organismal hierarchy. In most cases, parts and processes from a single level fail to accurately explain the presence of a given phenotypic trait.     

Assessing the prospects for a return of organisms in evolutionary biology

An argument has been raised from various perspectives against the Modern Synthesis (MS) in the past two decades: it has forgotten organisms. Niche construction theorists (Odling-Smee et al. 2003), developmental biologists like West-Eberhard (2003) and Evo-Devo elaborated various views which concur on a rehabilitation of the explanatory role of organisms, formerly neglected by an evolutionary science mostly centered on genes. This paper aims at assessing such criticisms by unraveling the specific arguments they use and evaluating how empirical findings may support them. In the first section, I review the usual critiques about the way MS treats organisms and show that the organisms-concerned critique is multifaceted, and I use the controversy about units of selection in order to show that purely conceptual and empirical arguments have been mixed up when organisms were concerned. In the second section, I consider successively the challenges raised to evolutionary MS by structuralist biologists and then the developmentalist challenge mostly raised by Evo-Devo. I distinguish what is purely conceptual among those criticisms and what mostly relies on recent empirical findings about genome activation, inheritance, and epigenetics. The last section discusses another program in MS, namely "evolutionary transitions" research, as enquiry into the emergence of organisms.     

EvoDevo and niche construction: building bridges

Evolutionary developmental biology and niche-construction theory have much in common, despite independent intellectual origins. Both place emphasis on the role of ontogenetic processes in evolution. The same historical events shaped them, and similar philosophical and sociological barriers hindered their respective advances. Both perspectives maintain that neo-Darwinism needs a theory of macroevolutionary variation and that such a theory can now be adduced from developmental biology. Some proponents of both EvoDevo and niche construction propose additional evolutionary mechanisms, and specify a key role for stable extra-genetic forms of inheritance. Similarly, proponents of each lay emphasis on "reciprocal causation" in the relationship between organism and environment. We illustrate here how EvoDevo and niche construction could gain "added value" from each other, and demonstrate how the niche-construction perspective potentially provides a useful conduit to integrate evolutionary and developmental biology.     

Ecological and evolutionary consequences of niche construction for its agent

Niche construction can generate ecological and evolutionary feedbacks that have been underinvestigated so far. We present an eco-evolutionary model that incorporates the process of niche construction to reveal its effects on the ecology and evolution of the niche-constructing agent. We consider a simple plant-soil nutrient ecosystem in which plants have the ability to increase the input of inorganic nutrient as an example of positive niche construction. On an ecological time scale, the model shows that niche construction allows the persistence of plants under infertile soil conditions that would otherwise lead to their extinction. This expansion of plants' niche, however, requires a high enough rate of niche construction and a high enough initial plant biomass to fuel the positive ecological feedback between plants and their soil environment. On an evolutionary time scale, we consider that the rates of niche construction and nutrient uptake coevolve in plants while a trade-off constrains their values. Different evolutionary outcomes are possible depending on the shape of the trade-off. We show that niche construction results in an evolutionary feedback between plants and their soil environment such that plants partially regulate soil nutrient content. The direct benefit accruing to plants, however, plays a crucial role in the evolutionary advantage of niche construction.     

The extended evolutionary synthesis and the role of soft inheritance in evolution

In recent years, a number of researchers have advocated extending the modern synthesis in evolutionary biology. One of the core arguments made in favour of an extension comes from work on soft inheritance systems, including transgenerational epigenetic effects, cultural transmission and niche construction. In this study, we outline this claim and then take issue with it. We argue that the focus on soft inheritance has led to a conflation of proximate and ultimate causation, which has in turn obscured key questions about biological organization and calibration across the life span to maximize average lifetime inclusive fitness. We illustrate this by presenting hypotheses that we believe incorporate the core phenomena of soft inheritance and will aid in understanding them.     

Why Gupta <Emphasis Type="BoldItalic">et al.</Emphasis>’s critique of niche construction theory is off target

Gupta et al., in their article in this issue (‘Niche construction in evolutionary theory: the construction of an academic niche?’. doi: 10.1007/s12041-017-0787-6), lament ‘serious problems with the way science is being done’ and suggest that ‘niche construction theory exemplifies this state of affairs.’ However, their aggressively confrontational but superficial critique of niche construction theory (NCT) only contributes to these problems by attacking claims that NCT does not make. This is unfortunate, as their poor scholarship has done a disservice to the evolutionary biology community through propagating misinformation. We correct Gupta et al.’s misunderstandings, stressing that NCT does not suggest that the fact that organisms engage in niche construction is neglected, nor does it make strong claims on the basis of its formal theory. Moreover, the treatment of niche construction as an evolutionary process has been highly productive, and is both theoretically and empirically well-validated. We end by reflecting on the potentially deleterious implications of their publication for evolutionary science.     

The evolutionary consequences of niche construction: a theoretical investigation using two-locus theory

This paper addresses the joint evolution of environment-altering (niche constructing) traits, and traits whose fitness depends on alterable sources of natural selection in environments. We explore the evolutionary consequences of this niche construction using a two-locus population genetic model. The novel conclusions are that niche construction can (1) cause evolutionary inertia and momentum, (2) lead to the fixation of otherwise deleterious alleles, (3) support stable polymorphisms where none are expected, (4) eliminate what would otherwise be stable polymorphisms, and (5) influence disequilibrium. The results suggest that the changes that organisms bring about in their niche can themselves be an important source of natural selection pressures, and imply that evolution may proceed in cycles of selection and niche construction.     

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 extended phenotype(s): a comparison with niche construction theory

While niche construction theory locates animal artefacts in their constructors’ environment, hence treating them as capable of exerting selective pressure on both the constructors and their descendants, the extended phenotype concept assimilates artefacts with their constructors’ genes. Analogous contrasts apply in the case of endoparasite and brood parasite genes influencing host behaviour. The explanatory power of these competing approaches are assessed by re-examining the core chapters of Richard Dawkins’ The Extended Phenotype. Because animal artefacts (chapter 11) have multiple evolutionary consequences for their constructors, the extra-body effects of a gene seemingly include feedback effects on multiple other genes, a result which is more consistent with niche construction theory than with selfish gene theory. In the case of endoparasite genes influencing host behaviour (chapter 12), Dawkins’ argument leaves out what appears to be the key explanatory component, namely the role of the host’s own bodily systems in making it possible for such genes to exist. For action at a distance (chapter 13), it is unclear whether the key genes have extended effects because they sit in the body of the manipulating organism, or alternatively do not have such effects because they sit in the body of its victim. It is argued that niche construction theory offers a superior explanation in all three cases, regardless of whether the extended phenotype concept is interpreted in selfish gene or selfish organism terms.