Human Niche Construction in Interdisciplinary Focus

Downloaded from rstb.royalsocietypublishing.org on February 14, 2011 Human niche construction in interdisciplinary focus Jeremy Kendal, Jamshid J. Tehrani and John Odling-Smee Phil. Trans. R. Soc. B 2011 366, 785-792 doi: 10.1098/rstb.2010.0306 References This article cites 46 articles, 16 of which can be accessed free http://rstb.royalsocietypublishing.org/content/366/1566/785.full.html#ref-list-1 Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;366/1566/785 Subject collections Articles on similar topics can be found in the following collections behaviour (1807 articles) evolution (2433 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2011 The Royal Society Downloaded from rstb.royalsocietypublishing.org on February 14, 2011 Phil. Trans. R. Soc. B (2011) 366, 785–792 doi:10.1098/rstb.2010.0306 Introduction Human niche construction in interdisciplinary focus Jeremy Kendal1,*, Jamshid J. Tehrani1 and John Odling-Smee2 1Centre for the Coevolution of Biology and Culture, Department of Anthropology, University of Durham, South Road, Durham DH1 3LE, UK 2School of Anthropology, University of Oxford, 51/53 Banbury Road, Oxford OX2 6PE, UK 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. Keywords: niche construction; gene–culture coevolution; cultural evolution; human evolution 1. INTRODUCTION Evolution entails networks of causation and feed- Niche-construction theory (NCT) originated as a back in which previously selected organisms drive branch of evolutionary biology that emphasizes the environmental changes, and organism-modified capacity of organisms to modify their environment environments subsequently select for changes in and thereby influence their own and other species’ organisms. evolution [1]. The defining characteristic of niche con- NCT provides both a philosophical shift in the way struction is not the modification of environments per we view and understand evolutionary processes as well se, but rather organism-induced changes in selection as a testable scientific theory. While the effects of niche pressures in environments [1]. The effects of niche construction on the evolutionary process have often construction have been documented across a wide been neglected in the past, it is also important to range of species including animals manufacturing note that many aspects of NCT are already incorpor- nests, burrows and webs, and plants modifying nutri- ated in standard theories of evolutionary biology, ent cycles. The papers presented in this special issue ecology, developmental biology and the human explore the phenomenon in Homo sapiens, for whom sciences. However, rather than aiming just to relabel endogenous causes of evolutionary dynamics are or reclassify established theories such as gene–culture impossible to ignore. coevolution or ecosystem engineering, NCT is put to NCT differs from standard evolutionary theory better use when formulating new hypotheses, or build- (SET) in recognizing that the evolution of organisms ing a more general evolutionary framework within is co-directed by both natural selection and niche con- which other theories can be subsumed. NCT provides struction. While genetic variation is subject to natural mechanisms by which currently disconnected bodies selection through differential survival and reproductive of theory, such as evolutionary and developmental success, the selective environments themselves are biology (‘evo-devo’) [1,3,4], or human cultural evol- partly determined by modifications made by niche- ution and structuration theory ([5], see below) can constructing organisms. Hence NCT recognizes be united [6]. natural selection and niche construction as reciprocal Here, we review the fundamental principles of con- causal processes in evolution, and treats the adapta- temporary NCT, initially in the context of biological tions of organisms as products of both processes [2]. evolution, before showing how the theory incorporates cultural evolutionary processes, and how it provides a framework for consilience between the natural and * Author for correspondence ([email protected]). the social sciences [7]. Where appropriate, we give One contribution of 13 to a Theme Issue ‘Human niche short summaries of each of the contributing papers construction’. in this theme issue. 785 This journal is q 2011 The Royal Society Downloaded from rstb.royalsocietypublishing.org on February 14, 2011 786 J. Kendal et al. Introduction. Human niche construction 2. FUNDAMENTAL PRINCIPLES OF NICHE environments, natural selection pressures. SET is CONSTRUCTION also fully consistent with the traditional view An early advocate of the niche construction perspec- expounded by Mayr [11], who regarded natural selective, Lewontin [8], neatly summarized the differences tion as the ultimate cause of phenotypic characters between standard evolutionary theory and NCT in [12]. It is a view that devalues so-called proximate two pairs of coupled differential equations. His first causes, including developmental processes such as pair (equations 2.1a,b) summarizes SET: learning, and human cultural processes in evolutionary biology [13,14]. In SET, niche-construction effects dO ¼ f ðO; EÞð2:1aÞ caused by developmental or proximate processes can dt be regarded as the expression of phenotypic plasticity and [15], or sometimes as extended phenotypes [16], but ultimately they still have to be explained by prior dE natural selection [17]. ¼ gðEÞ: ð2:1bÞ dt For many purposes, SET is sufficient, but it is insufficient when genetic selective environments are In equation (2.1a), evolutionary change in organ- modified as a function of phenotypic variation derived isms, dO/dt, depends on both organisms’ states, O, from so-called proximate processes such as learning. and environmental states, E. In equation (2.1b), For example, human cultural variation, depending lar- environmental change, dE/dt, depends exclusively on gely on differential social transmission of information environmental states. In general, organisms are not through social learning, may result in cultural niche- treated as the cause of any evolutionarily significant constructing practices that modify the natural selection changes in their environments, with the exception of of some human genes. As the selected genes may also cases such as frequency dependent selection, habitat influence human cultural practices, the assignment of selection, maternal inheritance and coevolution. ‘causation’ becomes complex. NCT replaces SET’s Instead adaptive evolutionary change is assumed to dichotomous proximate and ultimate distinction with be governed exclusively by a single ‘causal arrow’, ‘reciprocal causation’. Adaptations of organisms natural selection. depend on natural selection that is modified by niche However, SET underestimates the significance of construction, and niche construction that is selected the fact that, to stay alive, organisms must be active by natural selection [1,2]. In this light, niche construc- as well as reactive relative to their environments. tion is a mechanism of endogenous causation, reciprocal Organisms must gain resources from their external to natural selection in the evolutionary process. environments by genetically informed, or in animals, NCT asserts that, as a consequence of ancestral possibly brain informed, fuel consuming, non- niche construction, offspring inherit not only genes, random work [3]. They must perturb specific com- but an ecological inheritance, in the form of modified ponents of their environments, often at locations local selective environments relative to genetic fitness. chosen by the organisms themselves, and they must Overall, each offspring actually inherits an initial excrete detritus to their environments throughout organism–environment relationship, or ‘niche’, from their lives [1]. Organisms are, therefore, compelled its ancestors such that: to modify some natural selection pressures in their environments by the accumulating consequences of NðtÞ¼hðO; EÞ; ð2:3Þ their activities. Lewontin captured this point by his second pair (equations 2.2a,b) of equations that, in where N(t) represents the niche of a population of effect, summarize NCT: organisms O at time t in an environment E. The dO dynamics of N(t) are driven by the interaction ¼ f ðO; EÞð2:2aÞ dt of both population-modifying natural selection

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