Below is the unedited penultimate draft of: Laland, Kevin N., Odling-Smee, John and Feldman, Marcus W. (1999) Niche Construction, Biological Evolution and Cultural Change. Behavioral and Brain Sciences 23 (1): XXX-XXX. This is the unedited penultimate draft of a BBS target article that has been accepted for publication (Copyright 1999: Cambridge University Press U.K./U.S. -- publication date provisional) and is currently being circulated for Open Peer Commentary. This preprint is for inspection only, to help prospective commentators decide whether or not they wish to prepare a formal commentary. Please do not prepare a commentary unless you have received the hard copy, invitation, instructions and deadline information. For information on becoming a commentator on this or other BBS target articles, write to: [EMAIL PROTECTED] For information about subscribing or purchasing offprints of the published version, with commentaries and author's response, write to: [EMAIL PROTECTED] (North America) or [EMAIL PROTECTED] (All other countries). ---------------------------------------------------------------------------- ---- Niche Construction, Biological Evolution and Cultural Change. Kevin N Laland Sub-Department of Animal Behaviour, University of Cambridge, Madingley, Cambridge CB3 8AA, United Kingdom. http://www.zoo.cam.ac.uk/ [EMAIL PROTECTED] John Odling-Smee Institute of Biological Anthropology, University of Oxford, 58 Banbury Road, Oxford OX2 6QS, U.K. http://www.admin.ox.ac.uk/oxro/ad.htm [EMAIL PROTECTED] Marcus W Feldman Department of Biological Sciences, Herrin Hall, Stanford University, Stanford, CA 94305-5020, USA. http://www.stanford.edu/dept/biology [EMAIL PROTECTED] Abstract We propose a model to map the causal pathways relating biological evolution to cultural change. Building on conventional evolutionary theory, the model emphasises the capacity of organisms to modify sources of natural selection in their environment (niche construction); the evolutionary dynamic can also be broadened to incorporate ontogenetic and cultural processes, with phenotypes playing a much more active role in evolution. The model sheds light on hominid evolution, the evolution of culture, altruism and cooperation. Culture amplifies the capacity of human beings to modify sources of natural selection in their environments to the point where that capacity raises some new questions about the processes of human adaptation. Keywords Niche construction, gene-culture coevolution, human evolution, evolutionary psychology, sociobiology, adaptation. ---------------------------------------------------------------------------- ---- 1.0 AN EVOLUTIONARY FRAMEWORK FOR THE HUMAN SCIENCES The relationship between genetic evolution and culture raises two causal issues: The first is concerned with the extent to which contemporary human cultures are constrained or directed by our biological evolutionary heritage. The second explores whether hominid genetic evolution has itself been influenced by cultural activities. We contend that these issues are inextricably tied, and argue that the significance of evolutionary theory to the human sciences cannot be fully appreciated without a more complete understanding of how phenotypes in general, and human beings in particular, modify significant sources of selection in their environments, thereby codirecting subsequent biological evolution. Our principal goal is to delineate and explore the interactions between biological evolution and cultural change. Evolutionary biology has been widely invoked to account for human behaviour and social institutions. These explanations have generated sociobiology (Wilson, 1975; Trivers, 1985), human behavioural ecology (Borgerhoff Mulder, 1991) and evolutionary psychology (Barkow et al., 1992), as well as evolutionism and social Darwinism (Kuper, 1988). However, evolutionary approaches to human behaviour have provoked strong opposition, and the relevance of biological evolution to the human sciences remains widely disputed. Less familiar, but equally deserving of attention, are empirical data and theoretical arguments that human cultural activities have influenced human genetic evolution by modifying sources of natural selection and probably altering genotype frequencies in some human populations (Bodmer & Cavalli Sforza, 1976; Wilson, 1985; Durham, 1991; Feldman & Laland, 1996). Cultural traits, such as the use of tools, weapons, fire, cooking, symbols, language and trade, may also have played powerful roles in driving hominid evolution in general, and the evolution of the human brain in particular (Holloway, 1981; Byrne & Whiten, 1988; Dunbar, 1993; Aiello & Wheeler, 1995). It is probable that some cultural practices in contemporary human societies are still affecting human genetic evolution. Historically, evolutionary theory has suggested only two possible routes via which feedback from human cultural activities could influence human genetic evolution. Either human cultural activities may directly change the genes that humans pass on to their descendants by generating mutations, or they may change the probability of humans surviving and reproducing. The first alternative was ruled out by the failure of Lamarkism. The so-called "Weismann barrier" effectively stops genes from being affected by any of the acquired characteristics of phenotypes, including the culturally acquired characteristics of human beings. Modern molecular biologists do interfere with genes directly on the basis of their acquired scientific experiences, but this innovation is too recent to have had any impact on human genetic evolution. The failure of this route therefore left only the second alternative, which encouraged sociobiology�s claim that phenotypes of all species, including our own, reduce to "survival machines" or "vehicles" for their genes (Dawkins, 1989), and that the only role of phenotypes in evolution is to survive and reproduce differentially in response to natural selection and chance. This subordinate status for phenotypes does not cut off human culture from human genetic evolution entirely, since it still allows culture to contribute to human adaptations (Alexander, 1979), and hence to genotypic fitnesses. However, according to this perspective, culture has no power to co-direct human genetic evolution through active modification or creation of selection pressures. Other evolutionary biologists maintain that culture frequently does affect the evolutionary process, and some have begun to develop mathematical and conceptual models of gene-culture coevolution that involve not only descriptions of how human genetic evolution influences culture, but also of how human culture can drive or co-direct at least some genetic changes in human populations (Cavalli-Sforza & Feldman 1981; Boyd & Richerson, 1985; Durham, 1991; Feldman & Laland, 1996). These models include culturally biased non-random mating systems (e.g. Durham, 1991; Laland, 1994; Aoki & Feldman, 1997), the treatment of human socio-cultural or linguistic environments as sources of natural selection (Cavalli-Sforza & Feldman 1983; Aoki & Feldman 1987), and the impact of different cultural activities on the transmission of certain diseases such as malaria or Sickle-cell anaemia (Durham, 1991). The common element among these cases is that cultural processes change the human selective environment and thereby affect which genotypes survive and reproduce. Culture works on the basis of various kinds of transmission systems (Cavalli-Sforza & Feldman, 1981; Boyd & Richerson, 1985) which collectively provide humans with a second, non-genetic "knowledge-carrying" inheritance system. If the cultural inheritance of an environment-modifying human activity persists for enough generations to generate a stable selection pressure, it will be able to co-direct human genetic evolution. The culturally inherited traditions of pastoralism provide a case in point. Apparently, the persistent domestication of cattle, and the associated dairying activities, did alter the selective environments of some human populations for sufficient generations to select for genes which today confer greater adult lactose tolerance (Feldman & Cavalli Sforza, 1989; Durham, 1991). This approach is explicitly species specific. Although other species of animals have their �protocultures� (Galef, 1988), it has generally been assumed that Homo sapiens is the only extant species with cultural transmission stable enough to co-direct genetic evolution (Boyd & Richerson, 1985). If this is the case, �culture� can be used to explain little in primate evolution that happened prior to the appearance of powerful, accumulatory cultural inheritance. We think this particular human-centred perspective is misleading. Humans may be unique in their extraordinary capacity for culture, but they are not unique in their capacity to modify natural selection pressures in their environments. Many other species do the same, either on the basis of simple proto-cultural traditions, but mostly without any help from culture at all (Lewontin, 1983; Odling-Smee et al., 1996; Jones et al., 1997). We suggest that a deeper understanding of the relationship between genes and culture can be derived from evolutionary theory by demonstrating that humans are far from unique in being able to change their own selective environments. Human culture may allow humans to modify and construct their niches, with spectacular ecological and evolutionary consequences, but niche construction is both general and pervasive, and probably influences the ecology and evolution of many species. 1.1 Niche Construction Building on ideas initially developed by Lewontin (1983), we have previously proposed that biological evolution depends not only on natural selection and genetic inheritance, but also on "niche construction" (Odling-Smee, 1988, Odling-Smee, et al., 1996; Laland et al., 1996a). By niche construction we refer to the same processes that Jones et al. (1997) call "ecosystem engineering". Niche construction refers to the activities, choices and metabolic processes of organisms, through which they define, choose, modify and partly create their own niches1. For instance, to varying degrees, organisms choose their own habitats, mates, and resources and construct important components of their local environments such as nests, holes, burrows, paths, webs, dams, and chemical environments. Many organisms also partly destroy their habitats, through stripping them of valuable resources, or building up detritus, processes we refer to as negative niche construction. In addition, organisms may niche construct in ways that counteract natural selection, for example by digging a burrow or migrating to avoid the cold, or they may niche construct in ways which introduce novel selection pressures, for example by exploiting a new food resource which may subsequently select for a new digestive enzyme. They may also do both, for instance if counteractive niche construction itself establishes a novel selection pressure by acting on a second trait, for example, when nest building is further elaborated to enhance defence. In every case, however, the niche construction modifies one or more sources of natural selection in populations� environments, and in doing so generates a form of feedback in evolution that is not yet fully appreciated (Lewontin, 1983; Odling-Smee et al., 1996; Laland et al., 1996a). There are numerous examples of organisms choosing or changing their habitats, or of constructing artefacts, leading to an evolutionary response (Odling-Smee et al., 1996; Laland et al., 1996a). For instance, spiders construct webs which have led to the subsequent evolution of various camouflage, protection and communication behaviours on the web (Edmunds, 1974; Preston-Mafham & Preston-Mafham, 1996). Similarly, ants, bees, wasps and termites, construct nests which often themselves become the source of selection for many nest regulatory, maintenance and defence behaviour patterns. Many ant and termite species regulate temperature by plugging nest entrances at night, or in the cold, by adjusting the height or shape of their mounds to optimise the intake of the sun�s rays, or by carrying their brood around their nest to the place with the optimal temperature and humidity for the brood�s development (Frisch, 1975; Hansell, 1984). The construction of artefacts is equally common among vertebrates. Many mammals (including badgers, gophers, ground squirrels, hedgehogs, marmots, monotrema, moles, mole rats, opossum, prairie dogs, rabbits and rats) construct burrow systems, some with underground passages, interconnected chambers, and multiple entrances (Nowak, 1991). Here too there is evidence that burrow defence, maintenance, and regulation behaviours have evolved in response to selection pressures that were initiated by the construction of the burrow (Nowak, 1991). In all of the above examples there is often strong comparative evidence suggesting that nest building is ancestral to the nest elaboration, defence and regulatory behaviour (Hassell, 1984; Nowak, 1991; Preston-Mafham & Preston-Mafham, 1996). Most cases of niche construction, however, do not involve the building of artefacts, but merely the selection or modification of habitats (Odling-Smee, 1988). For instance, many insects choose particular host plants as oviposition sites, greatly influencing the developmental (and hence selective) environment of the emerging larvae (e.g. Jaenike, 1982). Nor is niche construction confined to animals. Plants too can change the chemical nature, the pattern of nutrient cycling, the temperature, the humidity, the fertility, the acidity, and the salinity of their soils (Ellis & Mellor, 1995) and the patterns of light and shade in their habitats (Holmgren et al., 1997). For instance, pine and chaparral species increase the likelihood of forest fires by accumulating oils or litter (Mount, 1964). In this case a probable evolutionary consequence is that these species have evolved a resistance to fire, while some species require a fire before their seeds will germinate (Whelan, 1995). Niche constructing organisms may also substantially modify the environment of their offspring, and even more distant descendants. Thus generations of organisms not only inherit genes from their ancestors, but also a legacy of natural selection pressures which have been modified by ancestral niche construction. This legacy of modified selection pressures has previously been labelled an "ecological inheritance" by Odling-Smee (1988). Major differences between genetic inheritance and ecological inheritance include that the former is transmitted internally from only one (asexual) or two (sexual) parents to offspring via reproduction, whereas the latter persists, or is actively maintained from one generation to the next, in the external environment, by multiple organisms. Below we illustrate this legacy of modified selection pressures, by choosing a series of increasingly complicated examples, starting with the simplest case, in which the effects of niche construction are confined to a single generation. All organisms constantly interact with their local environments, and they constantly change them by doing so. If, in each generation, populations of organisms only modify their local environment idiosyncratically, or inconsistently, then there will be no modification of natural selection pressures, and hence, no significant evolutionary consequence. If, however, in each generation, each organism repeatedly changes its own environment in the same way, perhaps because each individual inherits the same genes causing it to do so, then the result may be a modification of natural selection. The environmental consequences of such niche construction may be transitory, and may still be restricted to single generations, but if the same environmental change is re-imposed for sufficient generations it can serve as a significant source of selection. Web spiders provide an example. Individual spiders repeatedly build webs in their local environments, generation after generation, presumably because they repeatedly inherit genes expressed in web construction. The consistent presence of a web in each spider�s environment has, over many generations, fed back to become the source of new natural selection pressures for further phenotypic changes in the population of spiders, such as the marking of the web to enhance crypsis, differential responses to the frequency of web vibration, or the building of dummy spiders in their webs by Cyclosa to divert the attention of bird predators away from themselves (Preston-Mafham & Preston-Mafham, 1996). Although this feedback from niche construction influences the natural selection of genes from one generation to the next, it does not introduce an ecological inheritance to evolution, because no consequence of niche construction affects the next generation via the external environment. In more complicated cases, inherited genes may be expressed in a modification of the environments of offspring, rather than in organisms� own environments. Here, the consequences of niche construction are effectively transmitted from one generation to the next via an external environment, in the form of parentally modified natural selection pressures. This transmittal is sufficient to establish an ecological inheritance. For example, cuckoo parents repeatedly select host nests for their offspring, thereby bequeathing modified selection pressures as well as genes to their chicks. These modified selection pressures have probably favoured adaptations in the offspring of cuckoos, such as their short incubation periods, or the behavioural ejection by cuckoo chicks of host eggs from the parasitized nests (Krebs & Davies, 1993). Parents in vast numbers of species, across broad taxa, act in ways that influence the developmental environments of their offspring, for example, by providing them with benign nest environments or with food. This kind of extra-genetic inheritance, between two succeeding generations, is now widely recognised, and can be modelled as a "maternal" inheritance (Feldman & Cavalli Sforza, 1976; West et al., 1988; Kirkpatrick & Lande, 1989; Wolf, et al.,1998). Maternal inheritance, however, is itself only a restricted case of a more general phenomenon, because the effects of niche construction readily generalise from two generations, to multiple generations, and from mothers only, to multiple ancestors of both sexes. For example, through their burrowing activities, their dragging organic material into the soil, their mixing organic material with inorganic material, and their casting, which serves as the basis for microbial activity, earthworms dramatically change both the structure and chemistry of soils (Darwin, 1881; Lee, 1985). As a result, contemporary earthworms live in worlds that have been partly niche-constructed by many generations of ancestors. Other earthworm phenotypes, such as epidermis structure, or the amount of mucus secreted, have probably coevolved with such niche-constructing behaviour. Figure 1: (a) The standard evolutionary perspective: populations of organisms transmit genes from one eneration to the next, under the direction of natural selection. (b) With niche construction: phenotypes modify their local environments (E) through niche construction. Each generation inherits both genes and a legacy of modified selection pressures (ecological inheritance) from ancestral organisms. Figure 1 shows how niche construction and ecological inheritance interact with natural selection and genetic inheritance. Figure 1a represents the standard evolutionary perspective: populations of organisms transmit genes from one generation to the next, under the direction of natural selection. Figure 1b extends this perspective to acknowledge that phenotypes modify their local environments through niche construction. Genes are transmitted by ancestral organisms to their descendants, exactly as the standard theory describes, but in addition, phenotypically selected habitats, phenotypically modified habitats, and artefacts, persist, or are actively or effectively "transmitted", by these same organisms to their descendants via their local environments. The environments encountered by descendent organisms are not just "templates" to which organisms adapt. Environments are partly determined by independent environmental events (for instance, climatic, geological or chemical events), but also partly by ancestral niche construction. The evolutionary significance of niche construction hangs primarily on the feedback that it generates. Many organisms modify their own selection pressures, such that environment-altering traits coevolve with traits whose fitness depends on alterable sources of natural selection in environments. Such feedback cycles may be indirect, so that they operate via a series of other environmental components, which may be biotic, such as other coevolving populations, or abiotic, for example, the soil, or a water resource (Odling-Smee et al., 1996). These indirect routes can become complicated, and may even incorporate entire biogeochemical cycles in ecosystems. The changes that organisms cause in their niches, and the resulting dynamics, are seldom investigated in empirical evolutionary studies, or incorporated into population genetic models. One theoretical construct which captures some, but not all, of the consequences of niche construction is Dawkins� (1982) �extended phenotype�. Dawkins argues that genes can express themselves outside the bodies of the organisms that carry them. For instance, the beaver's dam is an extended phenotypic effect of beaver genes. Like any other aspect of the phenotype, extended phenotypes play an evolutionary role by influencing the chances that the genes responsible for the extended phenotypic trait will be passed onto the next generation. Dawkins emphasises just this one aspect of the evolutionary feedback from niche construction. However, the beaver�s dam sets up a host of selection pressures which feed back to act not only on the genes responsible for the extended phenotype, but also on other genes which may influence the expression of other traits in beavers such as their teeth, tail, feeding behaviour, their susceptibility to predation or disease, their social system, and many other aspects of their phenotypes. It may also affect many future generations of beavers that may 'inherit' the dam, its lodge, and the altered river, as well as many other species of organisms that now have to live in a world with a lake in it. Other topics in population biology are concerned with the evolutionary consequences of the changes that organisms bring about in their own, and in other populations', selective environments. For example, habitat selection, frequency- and density-dependent selection and coevolution involve phenotypic effects which may feed back to affect fitness (Maynard-Smith, 1989). So far, however, most analyses of these subjects have focused only on those loci that influence the production of the niche-constructing phenotype itself. What is missing is an exploration of the feedback effects on other loci, exploring how traits that alter selection pressures coevolve with other traits favoured by these changed selection pressures. We have begun the development of a body of theory that sets out to explore the evolutionary consequences of niche construction in a systematic manner (Laland et al., 1996a). Our theoretical analysis, which employed a two-locus, population-genetic model, uncovered a number of interesting evolutionary consequences of the feedback from niche construction. We found that the selection resulting from niche construction may sometimes override independent sources of selection, driving populations along alternative evolutionary trajectories, and may even initiate new evolutionary episodes in an unchanging external environment. Niche construction may influence the amount of genetic variation in a population, by affecting the stability of polymorphic equilibria. Moreover, because of the multi-generational properties of ecological inheritance, niche construction can generate unusual evolutionary dynamics. For instance, timelags were found between the onset of a new niche-constructing behaviour, and the response of a population to a selection pressure modified by this niche construction. These timelags generated an evolutionary inertia, where unusually strong selection is required to move a population away from an equilibrium, and a momentum, where populations continue to evolve in a particular direction even if selection pressures change or reverse. Although these findings are novel, they are consistent with those of related theoretical analyses. For instance, Robertson (1991) concluded that, because adapted organisms are both consequences of, and sources of, natural selection, both positive and negative feedback loops should be pervasive in evolution. These feedback loops introduce major instabilities, associated primarily with positive feedback cycles, and hyper stabilities, associated with negative feedback cycles. Feedback can produce "lock-in" effects, in which very small initial differences between alternative adaptations in species, can be powerfully amplified by positive feedback loops resulting from a frequency-dependent fitness advantage to the most common variant. This variant may then rapidly become dominant, driving all competitors extinct. Theoretical analyses of maternal inheritance also report unusual evolutionary dynamics, such as timelags in the response to selection, and evolutionary momentum (Feldman & Cavalli-Sforza, 1976; Kirkpatrick & Lande, 1989). This small, but growing, body of theory suggests that niche construction and ecological inheritance may be of greater evolutionary importance than generally conceived. In our view, the capacity of populations of organisms to modify their selective environment through niche construction, and the fact that many of these changes persist for multiple generations, demand an adjustment in understanding of the evolutionary dynamic, because they suggest that a description of evolutionary change relative only to independent environments is rather restrictive. In the presence of niche construction, adaptation ceases to be a one-way process, exclusively a response to environmentally imposed problems: instead it becomes a two-way process, with populations of organisms setting as well as solving problems. (Lewontin, 1983; Odling-Smee, et al., 1996). Evolution consists of mutual and simultaneous processes of natural selection and niche construction. We have outlined the principal evolutionary consequences of niche construction elsewhere (Odling-Smee et al., 1996; Laland et al., 1996a). Our goal here is to spell out the repercussions of this perspective for the human social sciences. We maintain that a focus on niche construction has important implications for the relationship between genetic evolution and cultural processes. The replacement of a single role for phenotypes in evolution by a dual role immediately takes away from human culture its claim to a unique status with respect to its capacity to modify natural selection. Humans can and do modify many natural selection pressures in their environments, but the same may be said of many species, and most do so without the help of culture. Moreover, this dual role for phenotypes implies that a complete understanding of the relationship between genes and culture must acknowledge not only genetic and cultural inheritance, but also take account of the legacy of modified selection pressures in environments. To illustrate these points, we need to take a fresh look at how human culture relates to human evolution in the light of niche construction. 1.2 The Relationship between Evolution and Culture. There is considerable disagreement over the relationship between evolution and culture. In Figure 2, we set out to elucidate how three independent approaches, human sociobiology, contemporary gene-culture coevolutionary theory, and our own proposed extension of gene-culture coevolutionary theory, model these interactions. Figure 2: The relationship between biological evolution and cultural change. (a) Sociobiology: Culture is treated as the expression of naturally selected genes, like any other feature of the phenotype. (b) Gene-culture coevolutionary theory: Culture is treated as shared ideational phenomena (ideas, beliefs values, knowledge), that are learned, and socially transmitted between, as a cultural inheritance. Cultural activities may modify some natural selection pressures in human environments, and thereby bias the transmission of some selected human genes. (c) Extended gene-culture coevoutionary framework: Niche construction from all ontogenetic processes modify human selective environments, generating a legacy of modified natural selection pressures which are bequeathed by human ancestors to their descendants. This figure best captures the causal logic underlying the relationship between biological evolution and cultural change. 1.2.1 Human Sociobiology: The conceptual model in Figure 2a represents the perspective of much human sociobiology (Wilson, 1975; Alexander, 1979; Trivers, 1985), and is built upon the standard evolutionary viewpoint portrayed in Figure 1a. Here the potential interactions between biological evolution and cultural change are extremely simple. "Culture" is treated as the expression of naturally selected genes, like any other feature of the phenotype. According to the sociobiological standpoint, the only way in which development and culture can affect genetic evolution is by influencing the adaptations of individual organisms, and hence the probability that different individuals in a population will survive and reproduce to pass on their genes to the next generation. However, this initial conceptual model is too restricted, and leaves us with a rather poor understanding of how human genetic evolution interacts with human cultural life. For instance, the sociobiological perspective largely neglects cultural inheritance, and ignores the fact that cultural activities can modify selection pressures in human environments (Bodmer & Cavalli-Sforza, 1976; Durham, 1991; Feldman & Laland, 1996). The scheme portrayed in Figure 2a, has also fostered the equally simple contrary view, maintained by many of the critics of sociobiology (Sahlins, 1976; Montagu, 1980) that, at least in modern humans, cultural inheritance is so powerful, that in many cases it no longer interacts with genetic inheritance at all, but overrules it. This position fails to explain many relevant data which indicate that to varying degrees, human cultural processes are constrained by human genes, and could not work unless they were, since they need "a priori" knowledge in the form of evolved, genetically-encoded information, to get started (Daly & Wilson, 1983; Durham, 1991; Barkow et al., 1992). For example, there is now considerable evidence that evolved linguistic predispositions, as well as other generative capacities, exist in human brains, and presumably they are subject to developmental processes that are constrained by genes (Barkow et al., 1992; Pinker, 1994). Therefore, culture cannot always be meaningfully decoupled from genetics. However, it is important to recognize that genetic influences on human behaviour are rarely straightforward, and that these influences may dissipate, or become obscure, when human relationships and social institutions are brought into focus (Hinde, 1987). 1.2.2. Gene-Culture Coevolution: Dissatisfaction with both sociobiology, and the critics of sociobiology, eventually led to the development of gene-culture coevolutionary theory2 (Cavalli-Sforza & Feldman, 1981; Boyd & Richerson, 1985; Durham, 1991), portrayed in Figure 2b. Gene-culture coevolution is still based on standard evolutionary theory (Figure 1a), except that here the interactions between human genetic evolution and culture become richer. Culture is treated as shared information (ideas, beliefs, values) that is learned, expressed in cultural activities, and socially transmitted between individuals in the form of a cultural inheritance. This concept of culture is deliberately restricted, abandoning more diffuse and all-encompassing notions of culture common in the human sciences (e.g. Tylor, 1871), while building on ideational perspectives, in an attempt to operationalize the units of cultural transmission (Durham, 1991). The novelty of the gene-culture approach is that it assumes that some human cultural activities may feed back to modify some selection pressures in human environments, and thus cultural transmission may affect the fate of some selected human genes. Thus, in Figure 2b, the relevant aspect of human selective environments is defined as cultural. This selection arises from the impact of cultural activities on human environments and is sufficient to allow humans some power to co-direct their own evolution. The conceptual model in Figure 2b extends Figure 2a, yet it still over simplifies the causal pathways connecting genes and culture, because it requires that cultural inheritance should affect the fate of some human genes directly, in the absence of any other mediating process. In most cases where gene-culture coevolutionary theory has been applied, this assumption is reasonable. Culture may bias human mating patterns non randomly, it may bias other human interactions, such as trade or warfare, or it may bias the choice of which infants are selected for infanticide (Boyd & Richerson, 1985; Laland, 1994; Kumm et al., 1994). The assumption that human cultural inheritance can directly bias human genetic inheritance may also be acceptable even when the source of the natural selection pressure that is modified by culture is no longer human, provided the relationship between whatever cultural trait is being expressed, and whatever natural selection pressure it is modifying, is sufficiently direct. For example, the trait that affected human genetic evolution in the lactose tolerance case was milk usage (Durham, 1991). Here, gene-culture theory is again applicable, because the link between milk usage and its genetic consequences are sufficiently simple to allow it to be modelled without bringing in any intermediate variables (Feldman & Cavalli-Sforza, 1989) . 1.2.3. Gene-Culture Coevolution plus Niche Construction: The gene-culture coevolutionary approach, however, fails in more complicated situations. Take, for example, the case of Kwa-speaking yam cultivators in West Africa, who increased the frequency of a gene for Sickle-cell anaemia in their own population as a result of the indirect effects of yam cultivation. These people traditionally cut clearings in the rainforest, creating more standing water and increasing the breeding grounds for malaria carrying mosquitoes. This, in turn, intensifies selection for the Sickle-cell allele, because of the protection offered by this allele against malaria in the heterozygotic condition (Durham 1991). Here the causal chain is so long that simply plotting the cultural trait of yam cultivation against the frequency of the Sickle-cell allele would be insufficient to yield a clear relationship between the cultural trait and allele frequencies (Durham 1991). The crucial variable is probably the amount of standing water in the environment caused by the yam cultivation, but standing water is an ecological variable, not a cultural variable, and it partly depends on factors (i.e. rainfall) that are beyond the control of the population. So here the simplifying assumption of a direct link between cultural and genetic inheritance distorts reality too much to allow their interaction to be modelled in the standard way. This time the two human inheritance systems can only interact via an intermediate, abiotic, ecological variable, which should be included to complete the model. This shortcoming leads us to propose an extended gene-culture coevolutionary theory, a conceptual version of which is shown in Figure 2c. The novelty here is the replacement of the genetic-inheritance scheme, described by standard evolutionary theory (Figure 1a), as the proper basis of gene-culture coevolution, by the extended evolutionary scheme incorporating niche construction, summarised in Figure 1b. Thus in Figure 2c, niche construction from all ontogenetic and cultural processes modifies human selective environments. Culturally modified selection pressures are now regarded, not as unique, but as just a part of a more general legacy of modified natural selection pressures which are bequeathed by human ancestors to their descendants. Hence, instead of being exclusively responsible for allowing us to co-direct our own evolution in contrast to what happens in every other species, culture now becomes merely the principal way in which we humans do the same thing that most other species do. 1.3. Multiple Processes in Evolution We now take a closer look at the set of processes by which populations of complex organisms, such as humans, acquire adaptive information, and how this information is expressed in niche construction. It is now widely recognised that several of the major evolutionary transitions involved changes in the way information is acquired, stored and transmitted (Szathmary & Maynard Smith, 1995). This is reflected in Figure 3, where we acknowledge that populations of complex organisms can acquire relevant semantic "information", or more accurately "knowledge" (Holland, 1992), through a set of information-acquiring processes (Holland, 1992), operating at three different levels, and with the knowledge gained being influenced by niche-constructed environments at each level. In various combinations, these are the processes which supply all organisms with the knowledge that organises their adaptations. Every species is informed by naturally selected genes, many are also informed by complex, information-acquiring ontogenetic processes such as learning or the immune system, while hominids, and perhaps a few other species, are also informed by culture. It is generally recognised that any comprehensive treatment of the gene-culture relationship requires the inclusion of all three sets of processes because the links between genetic evolution and culture cannot be understood without some reference to the intermediate ontogenetic processes, such as individual learning, that connect them (Plotkin & Odling-Smee 1981; Boyd & Richerson, 1985; Durham, 1991; Feldman & Laland, 1996). Figure 3: This figure zooms in on one of the boxes labelled "populations of phenotypes" in Figure 2. Human evolution results from information-acquiring processes at three levels. Adaptation in populations of complex organisms, such as humans, depends on population genetic processes, information-acquiring ontogenetic processes, and cultural processes, all of which can generate niche construction. The most phylogenetically ancient process ultimately responsible for niche construction is genetic evolution. As a consequence of the differential survival and reproduction of individuals with distinct genotypes, genetic evolution results in the acquisition, inheritance and transmission of genetically encoded "knowledge" by individuals in populations. Each individual inherits this genetic information from its ancestors, which then translates into developmental processes, expressing different phenotypes in different environments, the so-called "norm of reaction". Each individual may also contribute to the modification of its population�s selective environment by genetically guided niche construction. Many species have also evolved a set of more complicated ontogenetic processes, that allow individual organisms to acquire another kind of information. These processes are themselves products of genetic evolution, but are nevertheless distinct from it. They comprise "facultative" or "open" developmental processes, based on specialised information-acquiring subsystems in individual organisms, such as the immune system in vertebrates, or brain-based learning in animals, and they are capable of additional, individually-based, information acquisiton. Here the information acquiring entity is no longer an evolving population but is instead each individual organism in a population. As a result, the adaptive knowledge acquired through these ontogenetic processes cannot be inherited because all the knowledge gained by individuals during their lives is erased when they die. Nonetheless, processes such as learning can still be of considerable importance to subsequent generations because learned knowledge can guide niche construction. A few species, including many vertebrates, have also evolved a capacity to learn from other individuals, and to transmit some of their own learned knowledge to others. In humans this ability is facilitated by a further set of processes (e.g. language), which collectively underlie culture. Culture adds a second knowledge inheritance system to the evolutionary process through which socially learned information is accrued, stored, and transmitted between individuals. Here, the information-acquiring entity is again a group of interacting organisms rather than an individual. Although all cultural knowledge is traceable to the innovation and learning by particular individuals (with ontogenetic processes the ultimate source), major cultural changes may also occur through learning from neighbouring groups or immigrants, and may come with a baggage of associated ideological or organisational requirements. Within a population, individuals share at least some of their learned knowledge with others, within and between generations. This information sharing can depend on several kinds of cultural inheritance, including vertical (from parents), horizontal (from peers), oblique (from unrelated older individuals), indirect (e.g. from key individuals) and frequency-dependent (e.g. from the majority) cultural transmission systems (Cavalli Sforza & Feldman, 1981; Boyd & Richerson, 1985). Cultural inheritance therefore requires at least one non-genetic channel of communication among organisms via which learned knowledge can be shared and spread. It probably also requires that organisms can decompose their store of cultural "knowledge" into discrete transmittable "chunks" (Feldman & Cavalli-Sforza, 1976), or "memes" (Dawkins, 1989), perhaps equivalent to psychologist�s "schemata", either in simple or compound form (Holland, et al., 1986; Plotkin, 1996). In practice, in every species that is capable of sharing learned information, cultural inheritance depends on some kind of social learning (Galef, 1988; Durham, 1991), while in humans, it may also depend on language (Pinker, 1994). Much of human niche construction is dominated by socially learned knowledge and cultural inheritance, but the transmission and acquisition of this knowledge is itself dependent on pre-existing information acquired through genetic evolution or complex ontogenetic processes. Thus, while the variants that occur during genetic evolution, (i.e. mutations), are random (or at least, blind relative to natural selection), those acquired through ontogenetic processes are not. As well as being selected by ontogenetic processes, any knowledge gain by individuals is guided by genetic information. For example, animals are genetically predisposed to respond to both specific internal cues (e.g. hunger) and environmental contexts (e.g. sensory cues indicating food is nearby) by generating appropriate behaviour patterns from their repertoires. Hence, during learning, animals typically demonstrate "a priori" biases in their associations and patterns of behaviour that are most likely to be adaptive (Seligman 1970; Bolles, 1970). In addition, those associations and patterns of behaviour that animals do learn critically depend on which stimuli are perceived as reinforcing (pleasant or painful) under the influence of species-specific motivational systems, and these perceptual and motivational processes are constrained by genes (Hinde & Stevenson Hinde, 1973; Plotkin & Odling-Smee, 1981). This means that the behaviours of an animal, the associations it forms, the antibodies it generates, the developmental pathways it takes, are typically, although not universally, functional and adaptive. By the same reasoning, as well as being selected by cultural processes, cultural knowledge is guided and constrained by both genetic information and by ontogenetic processes (Odling-Smee, 1994). Social learning and transmission are affected by individual reinforcement histories and past associations partly because the cultural selective processes are themselves guided by what Durham (1991) calls "primary (or developmental) values", as well as by socially transmitted cultural values. Therefore, with some caveats that we discuss in the final section, we expect that the ideas, values, and acquired knowledge that comprise a culture would usually be adaptive. We have now come some way from the simple, sociobiological descriptions of gene-culture interactions, captured by Figure 2a. We have brought together two different bodies of theory, gene-culture coevolution and niche construction. As a result, there is a proliferation of interactions between niche-constructing processes, biological evolution and culture, shown in Figure 2c. This proliferation is summarised in Table 1, which illustrates each interaction with an example, organised in terms of the sources and consequences of niche construction. Source of Niche Construction Feedback to Biological Evolution Feedback to Cultural Change Population Genetic Processes eg. web spiders marking web or building dummy spiders (Edmunds, 1974) eg. sex differences in human mating behaviour (Daly & Wilson, 1983, Barkow et al., 1992) Information acquiring Ontogenetic Processes eg. woodpecker finch, by learning to grub with a tool, alleviates selection for a woodpecker's bill (Alcock, 1972, Grant, 1986) eg. learning and experience, influence the adoption of cultural traits (Durham, 1991) Cultural Processes eg. dairy farming selects for lactose tolerance (Feldman & Cavalli-Sforza, 1989) eg. the invention of writing leads to other innovations such as printing, libraries, e-mail Table 1: Niche construction resulting from population genetic processes, information-acquiring ontogenetic processes, and cultural processes, can influence both biological evolution and cultural change. The point is illustrated by a single example in each cell. We believe that due recognition of the role of niche construction in the evolutionary dynamic should advance our understanding of the relationship between human culture and human genetic evolution. As such, our perspective may be regarded as part of a movement working towards a framework for integrating biology and the behavioural sciences (Hinde 1987; Durham, 1991). 2.0. ILLUSTRATING THE FRAMEWORK What happens to those evolutionary and cultural issues that concern the human sciences when our new framework is substituted for the standard evolutionary perspective? In this section we will start to answer this question by describing some examples of how the feedback that occurs in our extended version of gene-culture coevolution might work. The examples we have chosen are hominid evolution, altruism and cooperation, and the processes of human adaptation. 2.1 Example 1: Hominid Evolution Archeologists and anthropologists currently seek to reconstruct the evolutionary history of modern humans from the fossil and molecular data, in the context of standard evolutionary theory (Figure 1a). Since this theory does not incorporate niche construction, it encourages the idea that human evolution must have been directed solely by independent natural selection pressures in human selective environments, that is by selection pressures that have not been modified by niche construction. These selection pressures may sometimes include those arising from hominid social interactions (e.g. Byrne & Whiten, 1988; Durham 1991; Dunbar, 1993; Foley 1995), but they do not include other sources of selection in the external environment that have been modified by ancestral hominid niche constructors. When human adaptation is treated not only as dependent on natural selection, but also on niche construction (Figure 2c), the suite of hypotheses about the causes, rates and processes of evolutionary change is considerably enlarged. 2.1.1. Processes of Human Evolution: Consider the possible ways in which a new evolutionary episode might be initiated in hominid evolution. For illustrative purposes only we consider a suite of explanations for the divergence of the lineages leading to the Pongidae and Hominidae families in the late Miocene, and we assume two ancestral populations in allopatry. The subsequent divergence of these two populations could have been triggered by any of the following events. First, each population could have been exposed to different external environments with different selection pressures, leading to allopatric speciation in the manner proposed in standard evolutionary theory. Alternatively, both populations may have been exposed to the same novel selective pressures, say a changed habitat, but only one population, say the ancestors of the Pongidae, was able to respond with counteractive niche construction by retreating to a still unchanged habitat, while the Hominidae ancestors remained where they were and became adapted to the new environment. Third, both populations may have responded to the same novel selection pressures with counteractive niche construction, but in different ways, each subsequently generating a different array of novel modified selection pressures which fed back on themselves. Fourth, the divergence might have been initated by inceptive niche construction on the part of one population, by which we mean by a novel form of niche construction, initiated by a change in organisms in one population, possibly because of a mutation, or a new cultural discovery, which subsequently caused, rather than resulted from, a change in the environment. For instance, this might have entailed one population discovering a new habitat, or discovering a new form of niche construction, most likely because of the spread of a newly learned behaviour (West-Eberhard, 1987; Bateson, 1988; Plotkin, 1988). Culture, or proto-culture, say on the part of the Hominidae, may have initiated some novel biological evolutionary change (Feldman & Cavalli Sforza, 1976; Boyd & Richerson, 1985; Wilson, 1985). Fifth, the ancestors of both lineages may have initiated different kinds of inceptive niche construction, again with no key environmental event triggering their divergence. This enlarged suite of processes operating in hominid evolution raises the possibility that some new traits might pay for their own fitness costs through niche construction. One possible example is the evolution of the (large) human brain. The mass-specific metabolic rate of the human brain is about nine times higher than the average metabolic rate of the human body as a whole, but there is no elevated basal metabolic rate in humans which would pay for it (Aiello & Wheeler, 1995). Aiello and Wheeler (1995) found that this was possible because the human gut, and in particular, the gastro-intestinal tract, requires fewer energetic resources. They hypothesized that our ancestors could afford a reduction in gut size because they used their brains to improve their diets in proportion to their loss of gut. Aiello and Wheeler suggest that this probably happened in two different episodes of brain evolution, the first coinciding with the appearance of the genus Homo, approximately two million years ago, and supported by increased meat eating, the second coinciding with the appearance of archaic Homo sapiens during the latter half of the Middle Pleistocene, and supported by the cultural invention of cooking, and therefore by the externalisation of part of the digestive processes. This is an example of how a trait, the human brain, might have evolved despite fitness costs by paying for itself by its "inventive" niche construction. Big brains would not be adaptive without niche construction. If niche construction were an important evolutionary agent, then for any clade of organisms, it should also be possible to predict a priori which phenotypic traits (which we will call "recipient characters" because they are receptive of selection pressures that have been modified by niche construction) might have been selected as adaptive in environments that have been niche constructed. Pertinent characters, and environmental states, could be measured in populations of closely-related organisms that do and do not exhibit this niche construction. It would then be possible to use comparative methods to determine if a selected recipient character change correlates with a particular niche construction activity, if the niche constructing activity is ancestral to the recipient character, and whether the recipient character in question is derived. If we are correct, there should be a significant relationship between the pertinent environmental state and the recipient character only when the niche constructing activity is also present. Since the same logic applies at the cultural level, this method could be applied to hominids, or contemporary human populations, where it may shed light on the relationship between particular genes and memes. For instance, in the Kwa, there is only a strong correlation between amount of standing water and incidence of Sickle-cell anaemia in populations that grow yams. In this case, a cultural practice has left a measurable genetic signature, in the form of a different allele frequency. In theory, it is therefore possible that genetic signatures for other cultural practices, evident in archaeological or ethnographic records, could be identified and used as evidence for the presence or absence of the cultural trait in particular populations, or to trace the diffusion of the cultural practice across geographic regions. If so, advances in molecular techniques could eventually aid this line of inquiry. 2.1.2. Rates of evolution: Niche construction may also have influenced the rate of hominid evolution. Much attention has focused on how cultural transmission affects evolutionary rates. Allan Wilson and colleagues have argued that changes in niche, resulting from complex social behaviour and cultural (or proto-cultural) transmission, may generate a "behavioral drive", which accelerates morphological evolution by fixing a greater proportion of genetic mutations (Wilson 1985). Wilson notes that there is a monotonic relationship between relative brain size and rate of anatomical evolution among vertebrates, which he argues is consistent with his behavioral drive hypothesis. However, theoretical analyses suggest that cultural processes may act both to accelerate and decelerate evolution (Feldman & Cavalli-Sforza 1976). These apparently contradictory findings make better sense in the light of our new perspective, because culture is a powerful medium for human niche construction, and niche construction can both counteract and support evolutionary change. If cultural innovations modify natural selection pressures, then genetic change due to modified natural selection is likely to follow. If, as seems likely, the rate of change of cultural niche construction is rapid relative to independent changes in the environment, biological evolutionary rates may be accelerated. A number of gene-culture coevolutionary models have found that, as cultural transmission may homogenise a population�s behaviour, and because culturally transmitted traits can spread through populations rapidly compared with genetic variants, culture can generate atypically strong selection (Feldman & Laland, 1996). It is widely recognised that culture can also shield genetic variants of low fitness from selection (Boyd & Richerson, 1985; Feldman & Laland, 1996). For instance, improved levels of health care and sanitation are examples of culturally mediated counteractive niche construction that damp out selection against individuals with some gene-related disorders, who may survive and reproduce in the modified environment. In fact, ontogenetic processes may also damp out selection, for example, if individuals develop antibodies that counter disease, or learn to avoid parasites or predators (Bateson, 1988; Plotkin, 1988). In addition, the recent culturally enhanced mobility of peoples, facilitates greater mixing of genes between populations, eradicating differences, and slowing down the divergence of populations. Moreover, a new culturally induced environmental change may be responded to exclusively by a new cultural adaptation. For example, even though smoking during pregnancy probably has a significant effect on the survival rate of offspring, the spread of tobacco smoking is unlikely to select for genes for resistance to smoking-related disease, because advances in medical technology allow smokers and their offspring to survive, and because campaigns to prohibit smoking are increasing awareness of its dangers. Under such circumstances, culture is unlikely to affect the rate of genetic evolution. More generally, organisms have evolved many niche-constructing behaviours that allow them to regulate the environment in such a way as to buffer out particular natural selection pressures. Niche construction that mitigates a selection pressure may allow populations to maintain greater levels of genetic variation at those loci that would have been affected by selection had the population not expressed that particular niche-constructing traits, because it shields such variation from selection. For example, in mammals genetic variation in the ability to deal with heat, through body size, or shape of ears or tail, may be exposed to less intense selection in populations that escape extreme temperatures in burrows, than in those that do not. However, if the counteractive niche construction breaks down, say a new predator forces the mammals into the open, the presence of significant levels of variation in genes affecting heat exchange may facilitate rapid genetic evolution. In other words, for specific traits, counteractive niche construction may sometimes facilitate periods of evolutionary stasis, punctuated by rapid genetic change. Moreover, following such change, since the niche construction of many organisms, particularly "keystone" species, modifies the selective environments of other species, subsequent niche construction could trigger a cascade of evolutionary events that realign ecosystems (Jones et al., 1997). Although we do not anticipate all macroevolutionary patterns to be dominated by punctuated equilibria, niche construction does provide a novel, readily observable, and testable micro-evolutionary process to account for punctuated macro-evolutionary trends in particular traits, frequently observed in the fossil record (Eldredge & Gould, 1972). The particular significance of this for human evolution is that, as unusually potent niche constructors, hominids should be particularly resistant to genetic evolution in response to changing environments, while at the same time capable of dramatic evolutionary change following major innovations. If we assume that hominid niche construction is more flexible than that of other mammals, and that culture enhances the capacity of humans to alter their niches, such that the more technically advanced a culture the greater its capacity for counteractive niche construction, then a number of hypotheses follow. First, consider Vrba�s (1992) hypothesis of "turnover pulses". We would expect hominids to show less response to fluctuating climates than other mammals. We would also expect more technologically advanced hominids to exhibit less of a response to fluctuating climates than less technologically advanced homininds. Second, consider Bergmann�s and Allen�s Rules. These rules suggest, respectively, that populations in warmer climates will be smaller bodied and have bigger extremities than those in cooler climates. Again we would expect hominids to show less correspondence to these rules than other mammals. We would also expect more technically advanced humans (e.g. moderns) to exhibit less correspondence to these rules than less technically advanced humans (e.g. Neanderthals), assuming that the latter must have been less well equipped than the former to invest in counteractive niche construction. Third, by the same logic, we would expect an inverse relationship between "robusticity" and the capacity for expressing counteractive niche construction. Fourth, it should be possible to reverse the inference, and to use the fossil record to infer something about the niche constructing capabilities of animals, including hominids. Here we suggest the greater the phenotypic (as opposed to extended phenotypic) response to environmental change by hominids, the more restricted must have been their capacity for niche construction. We are well aware that some related ideas have been proposed before (see Lewin, 1998), but we think that our niche construction perspective could provide a basis for new and much more detailed predictions along these lines, based on a more comprehensive understanding of the underlying processes, and therefore for further empirical work. 2.1.3. The Evolutionary Roots of Culture: Modern culture did not suddenly emerge from some pre-cultural Hominid ancestor (Plotkin, 1996). The psychological processes and abilities that underlie culture have evolved over millions of years, and can often be found in rudimentary form in animals. Cultural inheritance depends on the transmission of learned "knowledge" among individuals by one or more kinds of social learning (Cavalli-Sforza & Feldman, 1981; Durham, 1991). Hence a first step towards an understanding of the evolution of culture is to consider the evolution of social learning. Over the past 15 years a variety of mathematical analyses have been conducted, exploring the adaptive advantages of social learning, relative to learning asocially, or expressing an unlearned pattern of behaviour that has been adapted over the course of genetic evolution (Boyd & Richerson, 1985; Rogers, 1988; Cavalli-Sforza & Feldman, 1983; Aoki & Feldman 1987; Bergman & Feldman, 1995; Laland et al., 1996b; Feldman, et al. 1996). Despite a plurality of methods, this body of theory has reached a surprising consensus as to when social learning is expected to be favoured. When environments change very slowly, adaptive knowledge should be gained at the level of population genetics because there are only modest demands for knowledge updating, which can easily be met by genetic systems responding to gradually changing selection pressures. In contrast, where environmental change is very rapid, or when there are sudden environmental shifts, tracking by individual learning should be favoured, as should horizontally (within-generation) transmitted information. In such environments, the genetic system will change too slowly to cope, while social learning from the parental generation is likely to be too error prone, as individuals would pick up outdated information. It is when individuals encounter intermediate rates of environmental change that social learning from parents should be favoured. Here, "intermediate" means when changes are not so fast that parents and offspring experience different environments, but not so slow that appropriate genetically transmitted behaviour could evolve instead. _______________________________________________ Crashlist resources: http://website.lineone.net/~resource_base To change your options or unsubscribe go to: http://lists.wwpublish.com/mailman/listinfo/crashlist
