Niche Construction Affects the Variability and Strength of Natural Selection.

Consideration of the properties of the sources of selection potentially helps biologists account for variation in selection. Here we explore how the variability of natural selection is affected by organisms that regulate the experienced environment through their activities (whether by constructing components of their local environments, such as nests, burrows, or pupal cases, or by choosing suitable resources). Specifically, we test the predictions that organism-constructed sources of selection that buffer environmental variation will result in (i) reduced variation in selection gradients, including reduced variation between (a) years (temporal variation) and (b) locations (spatial variation), and (ii) weaker directional selection relative to nonconstructed sources. Using compiled data sets of 1,045 temporally replicated selection gradients, 257 spatially replicated selection gradients, and a pooled data set of 1,230 selection gradients, we find compelling evidence for reduced temporal variation and weaker selection in response to constructed compared to nonconstructed sources of selection and some evidence for reduced spatial variation in selection. These findings, which remained robust to alternative data sets, taxa, analytical methods, definitions of constructed/nonconstructed, and other tests of reliability, suggest that organism-manufactured or chosen components of environments may have qualitatively different properties from other environmental features.

How culture shaped the human genome: bringing genetics and the human sciences together.

Researchers from diverse backgrounds are converging on the view that human evolution has been shaped by gene-culture interactions. Theoretical biologists have used population genetic models to demonstrate that cultural processes can have a profound effect on human evolution, and anthropologists are investigating cultural practices that modify current selection. These findings are supported by recent analyses of human genetic variation, which reveal that hundreds of genes have been subject to recent positive selection, often in response to human activities. Here, we collate these data, highlighting the considerable potential for cross-disciplinary exchange to provide novel insights into how culture has shaped the human genome.

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 ways­one 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.

The role of internal and external constructive processes in evolution.

The architects of the Modern Synthesis viewed development as an unfolding of a form already latent in the genes. However, developing organisms play a far more active, constructive role in both their own development and their evolution than the Modern Synthesis proclaims. Here we outline what is meant by constructive processes in development and evolution, emphasizing how constructive development is a shared feature of many of the research developments central to the developing Extended Evolutionary Synthesis. Our article draws out the parallels between constructive physiological processes expressed internally and in the external environment (niche construction), showing how in each case they play important and not fully recognized evolutionary roles by modifying and biasing natural selection.

Ornamental plant domestication by aesthetics-driven human cultural niche construction.

Unlike plants that were domesticated to secure food, the domestication and breeding of ornamental plants are driven by aesthetic values. Here, we examine the major elements of the extended evolutionary synthesis (EES) theory that bridges the gap between the biology of ornamental plant domestication and the sociocultural motivations behind it. We propose that it involves specific elements of cumulative cultural evolution (CCE), plant gene-human culture coevolution (PGHCC), and niche construction (NC). Moreover, ornamental plant domestication represents an aesthetics-driven dimension of human niche construction that coevolved with socioeconomic changes and the adoption of new scientific technologies. Initially functioning as symbolic and aesthetic assets, ornamental plants became globally marketed material commodities as a result of the co-dependence of human CCE and prestige-competition motivations.

Conceptual Barriers to Progress Within Evolutionary Biology.

In spite of its success, Neo-Darwinism is faced with major conceptual barriers to further progress, deriving directly from its metaphysical foundations. Most importantly, neo-Darwinism fails to recognize a fundamental cause of evolutionary change, "niche construction". This failure restricts the generality of evolutionary theory, and introduces inaccuracies. It also hinders the integration of evolutionary biology with neighbouring disciplines, including ecosystem ecology, developmental biology, and the human sciences. Ecology is forced to become a divided discipline, developmental biology is stubbornly difficult to reconcile with evolutionary theory, and the majority of biologists and social scientists are still unhappy with evolutionary accounts of human behaviour. The incorporation of niche construction as both a cause and a product of evolution removes these disciplinary boundaries while greatly generalizing the explanatory power of evolutionary theory.

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.

Niche construction, sources of selection and trait coevolution.

Organisms modify and choose components of their local environments. This 'niche construction' can alter ecological processes, modify natural selection and contribute to inheritance through ecological legacies. Here, we propose that niche construction initiates and modifies the selection directly affecting the constructor, and on other species, in an orderly, directed and sustained manner. By dependably generating specific environmental states, niche construction co-directs adaptive evolution by imposing a consistent statistical bias on selection. We illustrate how niche construction can generate this evolutionary bias by comparing it with artificial selection. We suggest that it occupies the middle ground between artificial and natural selection. We show how the perspective leads to testable predictions related to: (i) reduced variance in measures of responses to natural selection in the wild; (ii) multiple trait coevolution, including the evolution of sequences of traits and patterns of parallel evolution; and (iii) a positive association between niche construction and biodiversity. More generally, we submit that evolutionary biology would benefit from greater attention to the diverse properties of all sources of selection.

Why Gupta et al.'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.

More on how and why: a response to commentaries.

We are grateful to the commentators for taking the time to respond to our article. Too many interesting and important points have been raised for us to tackle them all in this response, and so in the below we have sought to draw out the major themes. These include problems with both the term 'ultimate causation' and the proximate-ultimate causation dichotomy more generally, clarification of the meaning of reciprocal causation, discussion of issues related to the nature of development and phenotypic plasticity and their roles in evolution, and consideration of the need for an extended evolutionary synthesis.

Niche construction theory: a practical guide for ecologists.

Niche construction theory (NCT) explicitly recognizes environmental modication by organisms ("niche construction") and their legacy overtime ("ecological inheritance") to be evolutionary processes in their own right. Here we illustrate how niche construction theory provides usedl conceptual tools and theoretical insights for integrating ecosystem ecology and evolutionary theory. We begin by briefly describing NCT, and illustrating how it deifers from conventional evolutionary approaches. We then distinguish between two aspects ofniche construction--environment alteration and subsequent evolution in response to constructed environments--equating the first of these with "ecosystem engineering." We describe some of the ecological and evolutionary impacts on ecosystems of niche construction, ecosystem engineering and ecological inheritance, and illustrate how these processes trigger ecological and evolutionary feedbacks and leave detectable ecological signatures that are open to investigation. FIinally, we provide a practical guide to how NCT could be deployed by ecologists and evolutionary biologists to aeplore ecoeoolutionay dynamics. We suggest that, by highlighting the ecological and evolutionay ramifications of changes that organisms bring about in ecosystems, NCT helps link ecosystem ecology to evolutionary biology, potentially leading to a deeper understanding of how ecosystems change over time.

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.

Cause and effect in biology revisited: is Mayr's proximate-ultimate dichotomy still useful?

Fifty years ago, Ernst Mayr published a hugely influential paper on the nature of causation in biology, in which he distinguished between proximate and ultimate causes. Mayr equated proximate causation with immediate factors (for example, physiology) and ultimate causation with evolutionary explanations (for example, natural selection). He argued that proximate and ultimate causes addressed different questions and were not alternatives. Mayr's account of causation remains widely accepted today, with both positive and negative ramifications. Several current debates in biology (for example, over evolution and development, niche construction, cooperation, and the evolution of language) are linked by a common axis of acceptance/rejection of Mayr's model of causation. We argue that Mayr's formulation has acted to stabilize the dominant evolutionary paradigm against change but may now hamper progress in the biological sciences.