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1 Made By Each Other: Organisms and Their Environment. To appear in a book symposium on John Odling-Smee’s, Kevin Laland’s and Marcus Feldman’s Niche Construction: The Neglected Process in Evolution in Biology and Philosophy. Kim Sterelny Philosophy, Victoria University of Wellington and The Australian National University Draft of June 2004 2 I. An Alternative to Externalism: The Niche Construction Hypothesis The standard picture of evolution, is externalist: a causal arrow runs from environment to organism, and that arrow explains why organisms are as they are (Godfrey-Smith 1996). Natural selection allows a lineage to accommodate itself to the specifics of its environment. As the interior of Australia became hotter and drier, phenotypes changed in many lineages of plants and animals, so that those organisms came to suit the new conditions under which they lived. Odling-Smee, Laland and Feldman, building on the work of Richard Lewontin, have shown that while sometimes appropriate, this is an inadequate conception of the relationship between organisms and the environments in which they live. Over time organisms alter their environment as well as being altered by their environments (Lewontin 1982; Lewontin 1983; Lewontin 1985). For example, animals modulate the effects of their physical and biological environment by building shelters: the beaver’s dam and lodge system, and termite mounds are two famous cases of animal structures, but they are few of many. There are many thousands of animals which make nests, burrows and other shelters. Likewise, animals make tools that give them access to resources from which they would otherwise be excluded: thus the Galapagos woodpecker finch uses a cactus needle to extract insects from crevasses in bark — insects that they would otherwise be unable to catch (Tebbich, Taborsky et al. 2001). Tool making is not as common as shelter-making, but it is common. For example many animals make traps: there are many species of pit-making antlions. Thus in part organisms make the world in which they live. They partially construct their own niches. Odling-Smee, Laland and Feldman argue that this has five major and under-appreciated consequences for biological theory. 1. Organism-Environment Matching. Niche construction is one source of the fit between organisms and environment. Lineages sometimes evolve in response to new conditions. But when environments change, lineages often shift in space to track their preferred environmental conditions. When this is not possible, the result is often extinction rather than accommodation to the new conditions (Bennett 1997). But a lineage can also adapt its new environment to it. In New Zealand, rabbits both tend to 3 prefer disturbed habitat, and to disturb the habitat in which they live, thus preserving the conditions they prefer. 2. Feedback and Evolutionary Cascades. When organisms adapt their environment rather than adapting to their environment, they often establish a feedback loop that results in evolutionary cascades. Thus the establishment of life in burrows selects for further evolutionary changes. In some cases these changes are extreme: living in mounds influences every facet of termite morphology, physiology and behaviour (Turner 2000). 3. Learning has evolutionary consequences. The skills an animal acquires in its life cannot be incorporated into its genome and transmitted genetically to the next generation. It does not follow, though, that such changes in individual phenotypes are of no evolutionary consequence: for these changes alter the selective forces acting on that animal, and hence make a difference to the generation-by-generation action of selection on a linage. Woodpecker finches typically learn to manipulate cactus spines (Tebbich, Taborsky et al. 2001), and so selection will favour those members of the population whose beak shape make them most adept in using spines to harvest resources. There is a change in the selective forces acting on these birds even though they must learn to use spines in every generation. The selective environment of the woodpecker finch is altered by the skills it acquires. 4. Ecological Inheritance. Organisms change not only their own environment but also that of the next generation. Many Australian plants germinate only after fires, and many of those very plants make fire more likely, through the nature of the litter they produce. For example, their leaves are high in volatile oil content; and the bark of many of these trees hangs from them rather than forming a moist, decaying litter on the ground. So these organisms make their environment more fire-prone both for themselves and for the next generations. Odling-Smee, Laland and Feldman think that such downstream effects constitute a special and separate inheritance system, ecological inheritance. Organisms transmit to their offspring altered physical and selective environments. They do so both by physical action on their biological and 4 non-biological environments and by niche choice: they effect their offspring’s lives by choosing where they will live and breed, and when they will be active. 5. Ecosystem Integration. A central and unresolved problem in ecological theory concerns the extent to which ecological communities are integrated systems rather than mere aggregates of individual agents who happen to live and die adjacent to one another. Niche construction does not resolve this problem, but it does make it clear that the individual-aggregate conception of communities understates the range of potentially important and stabilising interactions between organisms. For organisms do not affect only their own environments. They effect those of other populations. Some organisms are ecological engineers: when beavers build their dams, they alter waterflows and create small wetlands, thus creating habitat for many other organisms, but denying it to others. Trees, likewise are often important ecological engineers: physically stabilising the soils on which they grow, moderating many physical impacts, and providing shelters, resources, and living space for hosts of animals and epiphytes (Jones, Lawton et al. 1997). Moreover, this power of organisms to influence the world in which they live results in a kind of biological action at a distance. One population can influence another by changing important features of the physical environment. Australian inland river systems are prone to salination. Water-tables rise to the surface, and then dry in hot spells leaving a salt residue. But salination is influenced by the very vegetation it affects. Trees lower the water-table, reduce salination, and hence improve the prospects of a raft of salt-vulnerable species. These indirect ecological links expand the range of potential coevolutionary interactions in ecosystems. Populations act on one another via the physical changes they induce. Waste recycling is the cleanest example. Plants produce litter as a by-product of their life: fallen leaves, twigs, bark. A host of organisms live by consuming the litter, and as a consequence of these actions, they return crucial materials to the soil. This is absorbed by the vegetation, which in turn produces more litter (pp 318-322). These indirect effects are relevant not just to coevolutionary interactions. The conditions of life at one period of time in a river basin affect those conditions at later 5 periods not just by persisting in more or less altered forms, but also by sieving the basin’s future inhabitants. Thus the salt levels of a river basin at time T affect those levels at T+N, for salt tends to persist. But those levels will also affect later states indirectly. For example, salt can kill trees, selecting against vegetation that would tend to lower the water-table. Hence salt levels can change the local vegetation in ways that tend to cause further rises in those levels. The physical profile of the basin at time T influences its profile at T+N via its effects on the suite of niche constructors that act at T+N. The physical features filter the local populations of organisms, causing local extinctions and allowing new invasions. As a consequence of such changes, the collective power of organisms to act on the basin may change very significantly over time. I have no doubt that the central thesis of Niche Construction is right: organisms act on the environment, and those actions sometimes have major ecological and evolutionary consequences. However, I am not convinced that niche construction is as pervasive and as unified as Odling-Smee, Laland and Feldman suppose. On their view the paradigm cases of niche construction — the artefact building, ecological engineering of termites and other eusocial arthropods; the warren systems of rabbits, naked mole rats and other tunnel builders; the beaver’s dams and lodges — are the tip of an iceberg. They think that all living organisms are niche constructors, though those niche constructing activities can sometimes be ignored in formal evolutionary modelling. I am more inclined to think that Odling-Smee, Laland and Feldman’s conception of niche construction is too heterogeneous. They are lumpers: I am a splitter. In particular, I think it is crucial to distinguish between the mere effects of an organism’s actions on its environment, and the ability of agents to control their own environment, albeit partially, and only with respect to some environmental factors. Mere effects are often important. But they do not establish the evolutionary and ecological cascades that are the consequence of life in a partially designed world. Odling-Smee, Laland and Feldman recognise the differences between mere effects and designed change; between action on the biological and non-biological aspects of the environment, and the differences between niche choice and niche changing. Nonetheless they think 6 these differences can be accommodated within a unified thermodynamic framework. I shall return to lumping and splitting after considering that thermodynamic argument for the pervasiveness and unity of niche construction. If it fails, the issue turns on theoretical productivity. Are the various phenomena which Odling-Smee, Laland and Feldman identify productively conceived as variants of a single process? II. A Universal Ethology? Odling-Smee, Laland and Feldman argue that all organisms must engage in niche construction; it is an essential aspect of life. Living organisms are far-fromequilibrium systems, and to persist in their environments and reproduce, they must suck energy out of the system to do the work that is necessary to maintain the local environment in a far-from-equilibrium state. Organisms are energy-and-entropy pumps: they pump energy from the environment, and pump entropy into it. These thermodynamic preconditions of life define a universal ethology: a set of characteristics all living agents must have. 1. Organisms must be active: if organisms were not active they could not gather resources they need, or discard their wastes. To secure sources of energy, an agent must act. Likewise wastes do not just leak away of their own accord; they will accumulate where they are made, unless they are actively expelled. 2. Since niche construction requires energy, it must on average be profitable. A minimal condition of continued life is the energy gained by exploration and capture exceeds the costs of resource harvesting plus waste removal. Thus niche construction must usually enhance short-term fitness. 3. Niche construction involves discrimination. Since environments and organisms vary, the type of niche constructing that is profitable will vary too, and hence an organism’s niche constructing behaviour must be controlled by systems welldesigned for its local environment. This design is the result of selection editing the DNA carried by the organism: “unconstrained, random or haphazard nicheconstructing acts could not provide any organism with a basis for staying alive because it is astronomically impossible for any far-from-equilibrium system to maintain itself by chance alone” (p177) 4. Niche construction is predictive. Niche construction is active, and actions must be initiated prior to any feedback from the environment. Thus agents act on the basis of information, on the basis of search plans. Though these may be rudimentary; “in this limited and in most species entirely noncognitive sense, niche construction must be preparative or predictive in character” (p178). 7 I am unconvinced that these thermodynamic conditions define a universal ethology. Life itself does not require active, future-oriented search by individual agents. To think it does is to conflate evolutionary facts about lineages with proximate facts about individual organisms. Consider the difference between fixed and inducible defences. Some plants have a fixed resource allocation to defensive chemicals. Others have mechanisms of inducible defence: if they get specific signals, they crank up their production of defensive chemicals (Herms and Mattson 1992). Plants are not cognitive agents, but those with inducible defences are in an important sense predictive agents (Godfrey-Smith 1996). Those with a fixed investment predict only at the level of the lineage, for individual response is determined by the level of threat registered by selection on the lineage as a whole. But individual agents in such lineages are not predicting the level of threat. Likewise consider a suspension feeder that sorts food from non-food by its sifting apparatus: food sticks, non-food does not. There has been evolutionary sorting to build such a system. But the agent itself is not actively sorting. A filter-feeder has not even the most rudimentary search plan. Passive filter-feeding is not random or haphazard; it is the result of prior selection on the lineage. The design of a filter-feeder’s filtering apparatus is an inductive bet that future environments will resemble past ones. But it involves no search plan at the level of individual agency. A notion of individual agency that counts filter-feeders and fixed investment defenders as actively searching their environment or predicting its future is too weak. Moreover, I do not think it follows that because actions must in general be profitable, organisms must typically be shaping their environment in ways that improve the organism-environment fit. I do not think that profitability implies control. It is true that actions must indeed normally be profitable. But they are profitable not because of their effects on the agent’s environment, but because of their effects on the agent itself. Odling-Smee, Laland and Feldman’s own thermodynamic perspective implies that actions do not typically create an ordered environment. On average, life pumps entropy into the environment making it, if anything, worse. In particular, the ordinary ecological impacts of an agent on its environment must typically make that agent’s environment worse because they involve the extraction of resources. They are 8 consumptive acts. Per capita impacts will typically be negligible, but to the extent that they are not, they make resources scarcer and thus degrade the local habitat. Consumption pays despite its effects on the environment, not because of them: the agent extracts a sufficient price for degrading its environment. Thermodynamic considerations suggest that acting on the environmental is an inevitable aspect of life. But these very considerations indicate that these impacts are typically mere effects: they make the environment more disordered and less friendly, rather than consist in an extension of the agent’s control over aspects of its world. Thus the ordinary ecological life of an agent has effects quite unlike those of termite mounds and the other paradigm cases of niche construction with which we began. These structures are manifestations of control. Agents must invest energy and information in shaping and maintaining artefacts, but as Odling-Smee, Laland and Feldman note, these structures will not subvert, resist, or escape from control (p 188). Nor are they consumed by the routine metabolic needs of their makers. And hence changes an agent makes to its non-biological environment may well be extensions of control over its environment, not mere effects on it. Environments themselves become partially designed and feedback loops can then be selected to make these changes more robust, reliable and far-reaching. In contrast, ecological interaction between organisms typically takes place in contested space. Mutualisms and similarly cooperative interactions are important, and one important message of Niche Construction is that these can be important even when they are indirect, mediated by alterations of physical aspects of the environment. Even so, the biological world of an agent is unlikely to be designed by that agent. When organisms interact, many agents with conflicting agendas are trying to engineer their interactions to suit their own interests. Agents will not typically be able to impose their own stamp on their biological world, any more than a pub after an all-in brawl reflects any agent’s control. The effects of organisms on less contested environmental dimensions are likely to be importantly different from the effects of agent action in contested environmental dimensions. This distinction between control and mere effects will be important in the following sections. I begin with the distinction between individual and collective effects on the 9 environment. Collective effects are enormously important biologically, but their evolutionary dynamics differs sharply from those of individual niche construction. III. Agent and Population Niche Construction There is an important contrast between beavers and termites on the one hand, and another environmental impact of life’s activities which is clearly consequential: soil formation and nutrient cycling. On forest floors, a vastly numerous and taxonomically heterogeneous guild of organisms consumes fallen litter and as a consequence of their collective acts, resources (for example: nitrogen and phosphorus) are returned to the soil, to be reabsorbed by the litter-providing trees. Soil formation and nutrient cycling show how centrally organisms contribute to the conditions which make life possible. The oxygenisation of the earth’s atmosphere is an even more dramatic case. Even so, these are mass effects. These organisms collectively influence their world. Yet organism by organism, they make no real difference to their own micro-niche. A beetle’s munching on a fallen leaf contributes only in a small way to the local recycling of nutrients in its particular patch. These litter-eaters have minute per capita effects. More importantly yet, as Dawkins argues, differences in a beetle’s contribution to the cycle do not effect its own prospects. A beetle that chewed leaves into tinier fragments, thus speeding up the cycle, would not itself benefit from an incremental improvement more than any other litter-eater in the local area (Dawkins forthcoming)). That is not true of, for example, termites and beavers. These have large per capita effects (so long as we think of the termite collective as the ecological agent). Moreover, their effects do not fall equally on the population at large. The consequences of changes in a local stream system will fall most directly on the beavers who caused those changes. This difference makes a crucial difference in the evolutionary dynamics we expect. Agent by agent, the litter-eaters do not make their world: if the nutrient cycle changes — even if it changes as a result of some change in their mass action — it will be experienced by each individual agent as a case of autonomous change in the environment. For an individual litter-eater, the litter-comsuming guild is part of the 10 environment and a part it cannot change. There still can be feedback in the system: mass effects on nutrient cycling can have biological consequences for the litterconsumers which cause further changes in their capacity to recycle1. Litter-eaters can be selected for an evolutionary response to the changes that they collectively cause, but they cannot be selected to modulate those changes. For none has its individual fitness raised or lowered by variations in its own environmental effects. Beavers and termites, in contrast are adapted to influence their environment. These are ecological engineers by design: in some respects, their environment is in part orderly, stable, and organised for the same reason that their phenotypes are. Litter-consuming niche construction only looks like beaver niche construction if we allow ourself to think of populations as the niche constructing agents: and yet they are not evolutionary agents in the same sense individual organisms are evolutionary agents. Thus in thinking about the effects of organisms on their environments, it is important not to tacitly frame-shift between individuals and populations. The same moral emerges from thinking about social behaviour and social environments. The social environment, broadly defined, is selectively important to almost all agents. The sex ratio; the structure of the population (for example, whether it is divided into a large number of small semi-isolated populations); the competitive strategies and abilities of others in the local population; the mate choice dispositions of the opposite sex — all this plays a role in determining an agent’s fitness. Moreover, it is widely accepted that these features of the environment are evolutionarily labile. While standard evolutionary theory has typically treated the environment as the fixed background of change in a lineage, that assumption has been relaxed in modelling the evolutionary upshot of interactions between conspecifics. Neither evolutionary games theory nor frequency dependent selection treat the environment of other choice-making agents as fixed. For that reason, Odling-Smee, Laland and Feldman treat these models as special cases of niche construction (pp 120-124); 189-190). I think that is lumping: frame-shifting between individual and population effects. If we have in mind the individual agent, the rest of the population is the environment. 1 Imagine for example that a particular kind of litter accumulates because it cannot be recycled due to a chance extinction in the community, and this accumulation causes further losses (the litter is toxic) and thus the whole cycle becomes less and less effective. 11 But in this case, the individual organisms are not niche constructing. Differences in sexual strategy is one of the phenomenon to which frequency-dependent models have been applied. For example, in some fish species there are two male strategies: a territory guarding display of maleness, and female-mimicking sneak strategy. In normal circumstances, a fish cannot change its environment by shifting, say, between the sneaky-male and the guarding-male sexual strategies. If the social environment is very patchy and divided into very small groups, a male changing to the sneaky-male strategy may able change the local ratio. But standard frequency dependent models of the evolution of social behaviour do not assume that the agent’s own decisions change their local environment. More importantly, even if an agent’s choice makes a difference to the local ratio, there is an important sense in which this does not change the selective environment. It does not change the equilibrium ratio of sneaks to guards. If the local environment is out of equilibrium, the right choice will enhance his fitness, but that fitness enhancement does not depend on his choice changing his social environment. On the assumption that evolutionary agents are individual organisms, the per capita effect of each agents action is typically not niche altering. It will not usually change the local ratio, and it will not change the equilibrium ratios that determine the long-run dynamics of the population. If we sum the effects of all the agents then those effects are of course significant. They do determine the actual ratios, and hence whether and in what respects the population is out of equilibrium. But then we have no distinction between agent and environment. IV Extended Phenotypes and Environmental Effects There is a broad sense of niche construction, according to which any important effect of agents and populations on their environment is niche construction. I have contrasted that sense with a narrower one in which agents construct niches only when they adapt their local microenvironments. But this narrow sense invites an important challenge. Artefacts seem to be the most striking and undeniable examples of niche construction. Yet rabbit warrens, naked mole rat burrow systems, beaver dams, and termite mounds are only examples of action on the environment if we count these structures as part of the environment, not part of the agent. Dawkins’ extended phenotype analysis raises the option of treating animal artefacts as part of the 12 organism, not part of its world (Dawkins 1982a; Dawkins 1994). Not all artefacts fit into Dawkins’ extended phenotype model. The tool of the woodpecker finch seems to be an expression of adaptive plasticity: of a novel yet adaptive phenotype. It is not likely to be a capacity that evolved incrementally through the assembly of dedicated developmental resources. In contrast, nests are aspects of a bird’s extended phenotype. Birds are great builders. Many species build strong, soft, weatherproof, and often camouflaged nests of twigs, leaves, moss, spider web, fur and much else. For example, one Australian gerygone (gerygones are small insect-eaters) constructs a nest that is suspended over water and which looks for all the world like a small clump of flood debris ((Serventy 1982) pp 178-179). These hanging nests are part of the bird's phenotype. They are as developmentally stable, as heritable, and as predictable in their ecological effects as other traits. And they are adaptive complexes, and like other adaptive complexes, this nest almost certainly evolved incrementally. From this perspective, nest evolution presents an evolutionary problem of the same kind as other complex adaptations. To understand it, we need to decompose its evolutionary trajectory into a sequence of small changes, each of which, in the relevant environment, was an incremental improvement. However, if the evolutionary dynamics of extended phenotype adaptations are just like those of other complex adaptations, then the evolution of nests and burrows is not an instance of agent’s changing their environments, it is simply an instance of adaptation to the environment. When the average phenotype in a lineage changes, moving closer to the local optimum, the adaptive landscape is not changing: rather, the lineage is changing its position in the adaptive landscape: it is climbing a hill. Ordinary phenotype evolution is in itself a change in the adaptive landscape. Arguably, the same is true of the evolution of an extended phenotype: ancestral gerygones were under selection to keep their eggs and nestlings warm and hidden. The same is true of contemporary gerygones. Evolutionary change in the gerygone lineage has altered the impact of the environment on the agent, not the environment itself. If we take extended phenotypes to be just a special case of ordinary phenotype traits, their influence on fitness is not an instance of niche construction. So there are two ways of describing artefacts. The niche construction team has chosen one way. Agents in part control their environment by making artefacts. Dawkins’ ideas suggest a second way: artefacts are part of a 13 lineage’s evolutionary response to an (unaltered) environment. Are these both legitimate perspectives on artefact evolution? If so, what is the distinctive advantage of the niche construction perspective? If not, what factors make one perspective correct? Treating artefacts as part of the agent’s phenotype is not an option for artefacts whose construction is an expression of phenotypic plasticity: tool use in the woodpecker finch (the hypothesis runs) is not itself an adaptation, and is not an aspect of the bird’s phenotype. The relevant phenotype trait is the learning ability through which the tool use is acquired. Even so, according to this line of argument, the most convincing examples of niche construction disappear. They are examples of phenotypic development, not of the influence of phenotype on the environment. On this line of thought, Dawkins’ extended phenotype analysis shows that the physiological boundary between organism and agent is of no deep evolutionary significance. His examples of parasite-host manipulation show that the world within the skin is not a safe and as benign as one might have supposed. The existence of disease has always made clear that organic systems could be destructively invaded: the barrier could be pierced. But parasitic manipulation shows that it can be infiltrated too. Even when the basic metabolism of an agent has not been compromised, the internal environment is less benign, less protected. On the other hand, the world without can be designed: it can be an extension of gene power. Genes act on their environment to improve their prospects of replication, and from the perspective of the gene, cells tissues, nests, burrows are just more environment (Dawkins 1994). Thus Dawkins’ analysis raises an important question about boundaries and their significance for Odling-Smee, Laland and Feldman’s analysis. This is a difficult and unresolved problem, but my best guess is that despite control beyond the skin, barriers are of real evolutionary importance. Even so, the niche construction perspective must live with the idea that boundaries, and with the organism/environment distinction, are leaky, evolutionarily contingent, and in some cases indeterminate. It is important to the niche construction case that the gerygone-nest examples are one end of a spectrum: such nests are not just intricate, co-adapted and obviously the result of cumulative adaptation. They are as reliable and identifiable a feature of gerygones as 14 their calls or feather patterns. That is why it is possible to write field guides to nests. Even when niche construction is an extension of adaptive control over the immediate environment, niche construction is often less regular, stable, and intricate than gerygone nests. In this respect, a number of Odling-Smee, Laland and Feldman’s other examples are more typical. Desert isopods disperse as adults to build a breeding tunnel, where they will breed. Not many succeed: the dispersal is dangerous, and successful burrows are dug only where there is high soil moisture content. Somewhat unexpectedly, highly eroded soils with a high rock content increase soil moisture content. For undisturbed soils have a hard micro-organism compacted crust, from which water runs off. The isopods break up this crust, thus improving water retention at their own microlocation, and improving their survival chances (pp 227-231). But there is no exact, regular and repeated pattern of water works around the burrows. Likewise the combustibility of eucalypt litter is no accident. Even so, it does not consist in regular, repeatable, well-formed faggots. Thus there are many examples of adaptive niche construction that do not involve a barrier marking a boundary between the adaptively engineered environment and no man’s land. Only when there is a barrier between the designed and the wild parts of the environment is there is a temptation to think of extended phenotype traits as aspects of the agent’s ordinary phenotype. For physical barriers really do seem to make a difference. Outside the barrier surrounding an agent, we find a war of all against all. The space between skins is a no-man’s land, controlled by no-one; designed for no-one; littered with the detritus of biological struggle. Despite their permeability and the extension of control into the world, physical barriers often coincide with the limits of gene power. Within we have a set of organised, designed, interdependent, co-adapted components; the joint products of a single genotype. Within the skin, components interact with other components. Cells, tissues, and organs, interact with other cells, tissues and organs. In general, cells and cell systems do not interact with anything beyond the skin: only the organism does that. Thermodynamic considerations also show the evolutionary importance of barriers: every organism is a system far from thermodynamic equilibrium, and is maintained at its far-from-equilibrium condition only by the expenditure of energy and by a barrier to the free flow of energy and material from the organism to the environment. 15 Thus despite the exertion of control through artefacts, mutualisms and similar sources of power over the environment, barriers matter. Physical boundaries only partially correlate with control, and there will be ambiguous cases that can be described either way. Nevertheless, there is probably a reasonably principled organism-environment boundary. Despite that boundary, organisms sometimes exert partial adaptive control over important aspects of their local environment. In the limit, but only in the limit, that control is so pervasive, systematic, and central to the organism’s life history, that we can regard the engineered aspects of the environment as an extended phenotype which is part of the agent. But that is niche construction at its exceptional limit. V Inheritance and Ecological Inheritance As they are standardly conceived, inheritance mechanisms are similarity-sustaining mechanisms. To a first approximation, inheritance is the transmission of developmental resources from one generation to the next, resources which explain why offspring resemble their parents. Dawkins has persuasively argued that a certain type of similarity making is of especial importance to evolution: high-fidelity transmission that nevertheless preserves and transmits occasional changes occurring in one generation to the next. Inheritance mechanisms which meet this “replicator condition” are important to the cumulative evolution of complex adaptations. They typically transmit a phenotype accurately enough for it to re-appear in the next generation. But should a change appear and survive, it will be transmitted to the next generation and hence will be available for selection. Gene flow across the generations is of special importance because it meets this condition. Offspring resemble their parents because they inherit genes from them. But even more importantly, a variant form of a gene can both make a phenotypic difference and be transmitted accurately to the next generation (Dawkins 1982a; Sterelny 2001; Dawkins forthcoming). Agents act not just on their own environment but on the environment of the next generation. Hence their agency has intergenerational effects. According to OdlingSmee, Laland and Feldman, these intergenerational effects are systematic and important enough to constitute an inheritance system: ecological inheritance. Just as 16 Odling-Smee, Laland and Feldman have an inclusive definition of niche construction, so too they have an inclusive definition of ecological inheritance. For them, any activity of generation N that changes the selective environment of generation N+ 1 is ecological inheritance. So when a flock of mammoths, caught on a newly cut-off island by rising sea levels, overgrazes the local vegetation and lumbers the next generation with a degraded environment, that is ecological inheritance. The New Zealand bird fauna is occasionally supplemented by new birds blown across from Australia; most recently by small insect-eaters known as a silvereyes. When a pair was first blown across from Australian to New Zealand and then breed in those new conditions, those birds transmitted a new selective environment to their young. Cultural inheritance is a form of ecological inheritance too: a rat that acquires a new food preference — say, stored human foods — and transmits that preference to her young via chemical cues in her milk has changed the selective environment of her young. For they will now be exposed to both the costs and benefits of foraging on that particular food source. Finally, the evolution of extended phenotypes is often also a form of ecological inheritance. Nests and nesting hollows, obviously, are very different developmental environments than an unprotected scrape on the ground. My response to this broad conception of ecological inheritance is the same as my reaction to their equally broad conception of niche construction: viz, that it is too broad. These intergenerational effects all matter, but they are very different. As I see it, Odling-Smee, Laland and Feldman’s conception of ecological inheritance amalgamates three very different intergenerational evolutionary effects. 1. Genes (and perhaps other developmental resources) have “norms of reaction”. That is, in different environments, the same gene will have different phenotypic effects. One set of mechanisms of ecological inheritance are important because they expose a larger fraction of these norms of reaction to selection. 2. Another set of mechanisms of ecological inheritance themselves transmit similarity-producing developmental resources from one generation to the next. They constitute distinct inheritance channels. 3. A third set of mechanisms of ecological inheritance result in developmental environments being engineered to make the transmission of developmental resources more reliable and relevant to a greater array of phenotypic traits. They increase the fidelity and power of existing inheritance channels. 17 I said above that mechanisms explain parent-offspring similarities. Yet the “norm of reaction” mechanisms are not similarity-making mechanisms at all. Rather, they explain why later generations differ from earlier generations. Ecological inheritance understood this way explains why mammoths shrunk on northern islands; why islanddwelling birds are more confiding than their continental relatives; why animals that live in ecological association with humans behave quite differently from their independently-living relatives. Mechanisms of niche choice do not in themselves result in parent-offspring similarities2. Yet they are they have important evolutionarily consequences. For similarity-making developmental resources have “norms of reaction”. If we vary the environment, we will vary their phenotypic effect. Thus the phenotypic effects of genes are sensitive to context, though the extent and type of sensitivity varies widely. A reaction norm for a gene plots its phenotypic effects in a range of potential environments. Different alleles can be phenotypically equivalent in some but not all of their potential environments (Lewontin 2000). This is probably true of other developmental resources. Thus niche choice is important because it extends the range of environments in which conserved and transmitted developmental resources must develop. If more potential environments are actual, then a larger fraction of a gene’s reaction norm is evolutionarily consequential. Thus more developmental resources are exposed to differential selection. Niche choice — switching from one environment to another — has this effect but so does any activity of one generation that results in the next generation developing in a significantly changed environment. When a hominid population stopped moving and began to live amongst its own wastes, the next generation both developed in a different environment and was exposed to a whole new suite of pathogens. Genes were newly visible to selection, both because their developmental contexts were different and they had different phenotypic upshots and because the selective environment were different. In short, niche choice and niche change are forms of ecological inheritance that result in the population gene pool being filtered in new ways. 2 They result in similarity only if there is some additional mechanism that ensures that offspring and parents make the same choices; for example, as with seabirds that return to breed on the same island that they hatched. 18 In contrast, other forms of ecological inheritance just are similarity-sustaining mechanisms. Imprinting is one such mechanism. When a mother rat suckles her pups, chemical residues in her milk that derive from her food prime her young with similar tastes. So the mother rat’s ordinary ecological activities — her foraging choices — in combination with these mechanisms of the social transmission of information result in parent-offspring similarities and hence influence the selective environment the young rats face. They escape some dangers of trial and error learning, but they inherit their mother’s new cost/benefit foraging trade-off along with her feeding phenotype. Finally, other forms of ecological inheritance amplify other similarity-sustaining mechanisms. Rich, conserved, accurately transmitted variation allows cumulative selection to build adaptive complexes. But similarity-and-difference making inputs from one generation to the next are context sensitive in their effects. Thus genes are similarity-makers but only if the crucial causal context stays the same, generation by generation. Two competing alleles have consistent effects on their own replication prospects only in specific genetic, cellular, and developmental contexts. This contextsensitivity makes the evolution of extended phenotypes an important aspect of ecological inheritance. Genes can be selected for outside-the-skin effects only if the outside-the-skin causal contexts reliably re-occur, just as they can be selected for inside-the-skin effects only if the physiological context reliably re-occurs. To the extent that organisms control their environment, the environment can become a stable, repeatable background context in which varying developmental inputs can have consistent, varying effects. This allows for the selection of one in favour of another. Parent extended phenotypes are offspring developmental environments: they systematise developmental contexts, and allow rival alleles (and other developmental resources) to be exposed to selection. Those genes will have a more consistent phenotypic effects, for developmental environments will be more standardised, and for the same reason their fitness consequences will be more consistent. If nests, trees hollows, beach scrapes or cliff edges are reliably part of the causal context in which genes influence development, then the phenotypic and fitness differences those distinct environments induce will be visible to selection. Notice, then, that designing the environment has a very different consequences from niche choice. It shrinks the range of environments in which a given gene develops, narrowing the relevant region 19 of the its norm of reaction (but perhaps also shifting it by comparison to previous generations). But when two alleles have distinct profiles in that narrowed region, the selective importance of their difference is magnified. For the alleles will typically rather than occasionally generate distinct phenotypes. Thus this form of ecological inheritance acts to amplify the importance of similaritymaking inheritance mechanisms, by making those mechanisms operate more reliably and extending the range of phenotypic traits that they can induce in the next generation. This form of ecological inheritance involves the design-like control of the next generation’s developmental environment, control that enhances the fidelity of transmission. This is most obvious in the case of the cultural transmission of information. Parental activity patterns can entrench social learning, making the transmission of crucial information more reliable and of higher fidelity (Avital and Jablonka 2000; Jablonka and Lamb forthcoming). I have argued at length that this mechanism is extremely important in hominid evolution (Sterelny 2003). But the mechanisms is also important in the transmission of symbiotic microorganisms. These microorganisms are sometimes transmitted by specific internal morphological adaptations, but transmission often depends on parental behaviours that are designed to infect their offspring: for example, feeding their young faecal material that is enriched with the microorganisms they need to digest their food (O'Neil, Hoffman et al. 1997; Sterelny 2004). I suspect this mechanism is equally important for genebased traits: many genes have adaptive effects on phenotypes only through the engineering of developmental environments. Generation N engineers the developmental environment of N + 1 and thus extends the array of stable effects of the genes they transmit. Engineering downstream environments allows out-of-thebody effects of genes, socially transmitted information, and symbiotic microorganism to flow more reliably and to have more predictable effects on generation N+1. In conclusion, this is a powerful, deep and important book. Odling-Smee, Laland and Feldman have developed Lewontin’s original insight and have shown niche construction is a mechanism of major evolutionary importance. But I think that the 20 difference between niche design and mere niche effect, likewise, is of fundamental importance: these are not two variants of a single process3. References Avital, E. and E. Jablonka (2000). Animal Traditions: Behavioural Inheritance in Evolution. Cambridge, Cambridge University Press. Bennett, K. D. (1997). Evolution and Ecology: The Pace of Life. Cambridge, Cambridge University Press. Dawkins, R. (1982a). The Extended Phenotype. Oxford, Oxford University Press. Dawkins, R. (1994). "Burying the Vehicle." Behavioral and Brain Sciences 17: 617. Dawkins, R. (forthcoming). "Extended Phenotype – But Not Too Extended. A reply to Laland, Turner and Jablonka." Biology and Philosophy. Godfrey-Smith, P. (1996). Complexity and the Function of Mind in Nature. Cambridge, Cambridge University Press. Herms, D. and W. Mattson (1992). "The Dilemma of Plants: to Grow or Defend." Quarterly Review of Biology 67(3): 283-335. Jablonka, E. and M. Lamb (forthcoming). Evolution in Four Dimensions. Cambridge, Mass, MIT Press. Jones, C., J. Lawton, et al. (1997). "Positive and Negative Effects of Organisms as Physical Ecosystems Engineers." Ecology 78: 1946-1957. Lewontin, R. (1985). Adaptation. The Dialectical Biologist. R. Levins and R. Lewontin. Cambridge, Harvard University Press: 65-84. Lewontin, R. C. (1982). Organism and Environment. Learning, Development and Culture. H. C. Plotkin. New York, Wiley: 151-170. Lewontin, R. C. (1983). "The Organism as the Subject and Object of Evolution." Scientia 118: 65-82. Lewontin, R. C. (2000). The Triple Helix. Cambridge, Mass, Harvard University Press. O'Neil, S., A. Hoffman, et al., Eds. (1997). Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford, Oxford University Press. 3 Thanks to Brett Calcott and Peter Godfrey-Smith for their comments on an earlier version of this paper, comments which have much improved its intelligibility. 21 Serventy, V., Ed. (1982). The Wrens and Warblers of Australia. National Photographic Index of Australian Wildlife. Sydney, Angus and Robinson. Sterelny, K. (2001). Niche Construction, Developmental Systems and the Extended Replicator. Cycles of Contingency. R. G. Gray, P And Oyama, S. Cambridge, MIT Press: 333-350. Sterelny, K. (2003). Thought in a Hostile World. New York, Blackwell. Sterelny, K. (2004). Symbiosis, Evolvability and Modularity. Modularity in Development and Evolution. G. Schlosser and G. Wagner. Chicago, University of Chicago Press: 490-516. Tebbich, S., M. Taborsky, et al. (2001). "Do Woodpecker Finches Acquire Tool-use By Social Learning." Proceedings of the Royal Society of London, Series B 268: 1-5. Turner, J. S. (2000). The Extended Organism: The Physiology of Animal-Built Structures. Cambridge, Harvard University Press.