Niche Inheritance: A Possible Basis for Classifying ... Inheritance: A Possible Basis for Classifying Multiple Inheritance Systems in Evolution Next generation t t +1 Populations of

Niche Inheritance: A Possible Basis for ClassifyingMultiple Inheritance Systems in Evolution

John Odling-SmeeSchool of AnthropologyUniversity of [email protected]

AbstractThe theory of niche construction adds a second general inher-itance system, ecological inheritance, to evolution (Odling-Smee et al. 2003). Ecological inheritance is the inheritance,via an external environment, of one or more natural selec-tion pressures previously modified by niche-constructing or-ganisms. This addition means descendant organisms inheritgenes, and biotically transformed selection pressures in theirenvironments, from their ancestors. The combined inheritanceis called niche inheritance. Niche inheritance is used as a basisfor classifying the multiple genetic and non-genetic, inheri-tance systems currently being proposed as possibly significantin evolution (e.g., Jablonka and Lamb 2005). Implications ofniche inheritance for the relationship between evolution anddevelopment (EvoDevo) are discussed.

Keywordscultural inheritance, development, evolution, ecological in-heritance, epigenetic inheritance, niche construction, nicheinheritance

April 8, 2007; accepted September 30, 2007276 Biological Theory 2(3) 2007, 276–289. c©2008 Konrad Lorenz Institute for Evolution and Cognition Research

John Odling-Smee

Organisms do not live very long. Because they don’t, the onlyway they can affect evolution is by contributing to one ormore inheritance systems. In this connection standard evolu-tionary theory (SET henceforth) is restricting. It only recog-nizes a single general inheritance system, genetic inheritance(Mameli 2004). It therefore implies there is only one way inwhich organisms can contribute to evolution. In each gener-ation, variant organisms survive and reproduce differentiallyrelative to natural selection and chance, thereby causing “fit”organisms to transmit their genes to their descendents by ge-netic inheritance.

This restricted concept of inheritance constrains our un-derstanding of how evolution works, and how it relates toother processes in biology. For example, it has consistentlypromoted the separation of developmental biology from evo-lutionary biology. At least since Morgan (1919), evolutionarybiologists have assumed that the between generation trans-mission of genes by organisms through genetic inheritance issufficient to explain how evolutionary changes occur in popu-lations, regardless of the functions of those same genes withingenerations during the development of individual organisms(Amundson 2005).

A second consequence applies almost exclusively to hu-mans. It has long been recognized that the expression of humanphenotypes depends on cultural inheritance as well as geneticinheritance (Dawkins 1976; Cavalli-Sforza and Feldman 1981;Boyd and Richerson 1985). However, if human evolution, likethe evolution of all other species, depends exclusively on ge-netic inheritance, then the only way in which cultural inher-itance can affect human evolution must be by contributingto human variation, and therefore to differential survival andreproduction of diverse humans in each generation (Wilson1975).

The assumption that genetic inheritance is the only inher-itance system in evolution has recently been questioned, pri-marily because of new data stemming from molecular biology(e.g., Schlichting and Pigliucci 1998; Oyama et al. 2001; West-Eberhard 2003; Jablonka and Lamb 1995, 2005; Gilbert 2001,2004; Pigliucci and Preston 2004; Mameli 2004). Jablonkaand Lamb (2005), for example, propose four distinct inher-itance systems in evolution: genetic, epigenetic, behavioral,and symbolic. Adopting a different approach, Odling-Smeeet al. (2003) propose that, minimally, two general inheritancesystems in evolution are necessary: genetic inheritance andecological inheritance.

This proliferation of putative inheritance systems intro-duces some dangers. It could eventually advance our un-derstanding of evolution. It could even remove some long-standing “log-jams” that have prevented the achievement ofbroader syntheses in biology, for instance, by making it eas-ier to connect evolutionary biology to developmental biology(West-Eberhard 2003), a possibility discussed here. Or it could

help fuse ecosystem level ecology with evolution (O’Neill et al.1986; Jones and Lawton 1995; Holt 2005). However, it couldsimultaneously make it harder to model evolution formally,or to describe how each of the proposed inheritance systemsinteracts with the others. One clear threat is that the coherence,lucidity, and empirical potency of SET’s genetic inheritanceonly approach could be lost in a “riot” of competing inheri-tance systems.

Can such a riot be avoided? Is it possible to make senseof multiple evolutionary inheritance systems without a lossof potency by evolutionary theory? A necessary first step isto establish a taxonomy of inheritance systems that is bothsimple and clarifying. I shall attempt that here. First, I willuse niche construction theory (Odling-Smee et al. 2003) asa starting point, in an effort to establish a general theoreticalframework that is less hostile than SET to the idea that pluralinheritance systems exist in evolution. Second, I will use thisrevised theoretical framework as a basis for classifying diverseinheritance systems. Third, I will apply the resulting taxonomicscheme to the exceptionally difficult case of human evolution.The rationale for this last step is that the evolution of our ownspecies includes cultural inheritance, and probably involvesmore distinct inheritance systems than the evolution of anyother species. Therefore, if the proposed taxonomic schemeworks for human evolution, it should also work for evolutionin general.

Niche Construction

The theory of niche construction was first introduced to evo-lutionary biology by Lewontin (1982, 1983). Recently it hasgathered momentum (Odling-Smee 1988; Odling-Smee et al.1996, 2003; Laland et al. 1996, 1999, 2001; Lewontin 2000;Oyama et al. 2001; Sterelny 2003; Boni and Feldman 2005;Donohue 2005; Laland and Sterelny 2006). Figure 1 contrastsSET, without niche construction, to an extended version ofevolutionary theory that includes it.

In SET (Figure 1a), natural selection pressures in environ-ments (E) act on populations of diverse organisms (or pheno-types) to influence which individuals survive and reproduce,and pass on their genes to the next generation via a singleinheritance system, genetic inheritance. The adaptations of or-ganisms are treated as consequences of independent naturalselection pressures moulding organisms to fit pre-establishedenvironmental templates. The templates are dynamic becauseprocesses that are independent of organisms change the worldsto which organisms have to adapt. However, the changes thatorganisms bring about in their own worlds are seldom thoughtto have evolutionary significance.

The main problem with this view is that it discour-ages consideration of the feedback in evolution caused bythe modification of environmental selection pressures by the

Biological Theory 2(3) 2007 277

Niche Inheritance: A Possible Basis for Classifying Multiple Inheritance Systems in Evolution

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Figure 1.a. Standard evolutionary theory. b. Extended evolutionary theory.

niche-constructing activities of organisms. All organisms,through their metabolisms, movements, behaviors, andchoices, partly define, create, and destroy their selective envi-ronments, and in doing so, they transform some of the naturalselection pressures in their environments that subsequentlyselect them (Lewontin 1983; Odling-Smee et al. 2003). Theadaptations of organisms cannot therefore be exclusively con-sequences of organisms responding to autonomous selectionpressures in environments. Sometimes they must involve or-ganisms responding to selection pressures that have previouslybeen transformed by their own, or their ancestors’, or eachother’s niche-constructing activities.

When niche construction is added, it extends evolutionarytheory as illustrated in Figure 1b. The evolution of organismsnow depends on both natural selection and niche construc-tion. Genes are transmitted by ancestral organisms to theirdescendents, as directed by the outcomes of natural selectionin the usual way. But selected habitats, modified habitats, andmodified sources of natural selection in those habitats are also

transmitted by the same organisms to their descendents, as aconsequence of their niche-constructing activities, through asecond general inheritance system in evolution, ecological in-heritance. Ecological inheritance comprises the inheritance ofone or more natural selection pressures, previously modifiedby the niche-constructing activities of organisms, in their ex-ternal environments (Odling-Smee et al. 2003). The selectiveenvironments encountered by organisms are therefore partlydetermined by independent sources of natural selection, forinstance, by climate, or physical and chemical events. How-ever, they are also partly determined by what organisms do,or previously did to their own, and each other’s selective envi-ronments, by niche construction.

Innumerable examples of niche construction are known.Animals manufacture nests, burrows, webs, and pupal cases;plants modify fire regimes, levels of atmospheric gases, andnutrient cycles; fungi decompose organic matter; and bacteriafix nutrients (Turner 2000; Odling-Smee et al. 2003; Schwilk2003; Hansell 2005; Meysman et al. 2006). There are also

278 Biological Theory 2(3) 2007

John Odling-Smee

examples of social niche construction in insects (Fredericksonet al. 2005) and primates (Flack et al. 2006), and of culturalniche construction in humans (Feldman and Cavalli-Sforza1989; Durham 1991; Laland et al. 2000; Balter 2005; Smith2007). For decades, ecologists have also realized that organ-isms can, and frequently do alter their environments in ecolog-ically significant ways. Today these phenomena are referredto by ecologists as ecosystem engineering (Jones et al. 1994,1997; Wright and Jones 2006).

Many kinds of niche construction have already been mod-eled both by standard, and non-standard, population geneticmodels. For example, niche construction is implicit in stan-dard models of frequency- and density-dependent selection(Futuyma 1998), habitat selection (Hanski and Singer 2001),maternal inheritance (Kirkpatrick and Lande 1989), extendedphenotypes (Dawkins 1982), indirect genetic effects and epis-tasis (Wolf et al. 2000), and co-evolution (Thompson 1994).Other models have explicitly investigated how niche construc-tion and ecological inheritance change the dynamics of theevolutionary process (Laland et al. 1996, 1999, 2001; Odling-Smee et al. 1996, 2003; Ihara and Feldman 2004; Hui and Yue2004; Boni and Feldman 2005; Borenstein et al. 2006; Silverand Di Paolo 2006). So far, all the latter models have foundniche construction to be evolutionarily consequential.

In spite of this work, the full significance of niche con-struction has been neglected. What has been missing, untilrecently, was a body of theory that recognizes niche construc-tion as a distinct causal process in evolution in its own right(Waddington 1969; Lewontin 1983; Odling-Smee et al. 2003;Laland and Sterelny 2006). Why has such a seemingly obviousprocess been marginalized in evolutionary theory for so long?

The Limitations of Standard Evolutionary Theory

The answer probably lies hidden in a seldom re-consideredfoundational assumption of SET concerning the role of envi-ronments in evolution. Odling-Smee (1988) called it a “refer-ence device” problem. Lewontin (1983) originally describedthe problem in terms of two pairs of coupled differential equa-tions.

The first pair (1) summarizes SET:

dO

dt= f (O,E), (1a)

dE

dt= g(E). (1b)

In (1) evolutionary change in organisms, dO/dt, is assumed todepend on both organisms’ states, O, and environmental states,E (1a). In contrast, environmental change, dE/dt, is assumed todepend exclusively on environmental states (1b). With many

caveats and complications, organisms are not generally re-garded as causing any evolutionarily significant changes intheir environments.

But, said Lewontin, this is not how evolution works. Hissecond pair of equations (2) summarizes how he thinks it doeswork:

dO

dt= f (O,E), (2a)

dE

dt= g(O,E), (2b)

Change in organisms, dO/dt, is assumed to depend on bothorganisms’ states and environmental states as before (2a), butenvironmental change, dE/dt, is now assumed to depend onboth environment states, and the environment-modifying ac-tivities of organisms (2b).

Philosopher Peter Godfrey-Smith (1996) drew attentionto the same problem when he described SET as an “external-ist” theory, because it uses the external environment as its soleexplanatory reference device. The standard theory seeks to ex-plain the internal properties of organisms, their adaptations,exclusively in terms of properties of their external environ-ments, natural selection pressures (Figure 1a).

The principal point the standard theory obscures is thatorganisms are active, as well as reactive (Waddington 1969;Lewontin 1983). To stay alive organisms must gain re-sources from their external environments by “informed,” “fuel-consuming” non-random “work” (Odling-Smee et al. 2003).Organisms are therefore compelled to choose and perturb spe-cific components of their environments. They are also com-pelled to change some of the selection pressures in their en-vironments by doing so. This point is captured by Lewontin’sequation 2b. In effect, this equation introduces a second “causalarrow” in evolution in addition to Darwin’s “causal arrow” ofnatural selection. Odling-Smee (1988) called Lewontin’s sec-ond causal arrow “niche construction.”

We can now pin down the “reference device problem”more precisely. One of the causal arrows in equations 2, natu-ral selection, is fully compatible with the externalist assump-tion of SET because it is pointing in the “right” direction, fromenvironments to organisms. Hence, it is conceptually straight-forward to describe how external natural selection pressuresin environments cause adaptations in organisms. However, thesecond causal arrow in 2, niche construction, is pointing inthe “wrong” direction, from organisms to environments. Thatrenders niche construction incompatible with the externalistassumption of SET. It makes it difficult or impossible for evo-lutionary biologists to describe changes in natural selectionpressures, caused by prior niche-construction, as evolution-arily causal. Instead, SET is forced by its own explanatory



reference device, the external environment, to “explain away”all observed instances of niche construction as “nothing but”phenotypic, or possibly extended phenotypic (Dawkins 1982,2004) consequences of prior natural selection. SET can recog-nize niche construction as a consequence of evolution, but itcannot recognize it as a cause.

The solution adopted by niche construction theory was tochange the explanatory reference device. Instead of describingthe evolution of organisms only relative to natural selectionpressures in external environments, as in (1), Odling-Smeeet al. (2003) describe evolution relative to their “niches.”

N (t) = h(O,E) (3)

In (3), Nt represents the niche of a population of organ-isms O at time t, and the dynamics of Nt are driven by bothpopulation-modifying natural selection pressures in E, and bythe environment-modifying niche-constructing activities of thepopulation of organisms, O. Everything here is evolving. Thepopulation, O is evolving, as usual. O’s selective environment,E, is in part coevolving as a consequence of O’s genetically“informed”, or possibly “brain-informed” niche-constructingactivities. Finally, the niche relationship itself, N(t), is evolvingas a function of O’s and E’s interactions. Equation 3 subsumesLewontin’s equations, 2.

Because niches always include two-way interactions be-tween organisms and their environments (Chase and Leibold2003), this step is sufficient to allow an extended “interaction-ist” (Godfrey-Smith 1996) theory of evolution (Figure 1b) tobe substituted for the standard externalist theory (Figure 1a).The solution works because the niche concept offers a “neu-tral” explanatory reference device. The (OE) niche relationshipdoes not impose an a priori bias either in favor of natural se-lection and against niche construction, or vice-versa. Insteadit allows both the “causal arrows” in (2), natural selectionand niche construction, to be modeled as reciprocal causesin evolution (Laland and Sterelny 2006). Formal models cannow be built that capture (1) the modification of sources ofnatural selection in environments by prior niche construc-tion; (2) the subsequent selection of organisms by sourcesof selection modified by prior niche construction; and (3)changes in the adaptations, and hence in the subsequent niche-constructing activities of organisms, caused by prior natu-ral selection (Laland et al. 1996, 1999; Odling-Smee et al.2003).

Conceptually and empirically, it is only necessary torecognize that natural selection is not a property of au-tonomous external habitats, but a property of relativis-tic niches. On that basis, all the processes that modifyorganism-environment niche relationships, including both nat-ural selection and niche construction, become evolutionarilycausal.

Ecological Inheritance

Multiple consequences flow from this revision (Odling-Smeeet al. 2003). Here I will focus only on those that affect inheri-tance in evolution.

When niche construction is included as a co-directingcausal process in evolution, it not only contributes to the adap-tations of organisms, but it also causes a second general inheri-tance system in evolution, ecological inheritance. This occursbecause some of the environmental consequences caused bythe repeated niche-constructing activities of multiple genera-tions of organisms in their environments (e.g., the presenceof burrows, mounds, and dams or, on a larger scale, changedatmospheric states, soil states, substrate states, or sea states;Dietrich and Taylor Perron 2006; Meysman et al. 2006) ac-cumulate or persist in environments across generations. Whenthey do, they transform some of the natural selection pressuresencountered by later generations of organisms (Odling-Smeeet al. 2003).

The way ecological inheritance works is substantially dif-ferent from the way genetic inheritance works (Odling-Smee1988). First, ecological inheritance is transmitted, in the formof biotically modified sources of natural selection, throughthe medium of an external environment. It is not transmittedby reproduction. Second, unlike genetic inheritance, ecolog-ical inheritance does not depend on the transmission of dis-crete replicators between generations (Sterelny 2001, 2005;Dawkins 2004). It depends only on organisms bequeathing al-tered selective environments to their offspring, either throughthe physical perturbation of biological and non-biologicalcomponents of their environments, or by their choices of habi-tats. Third, in sexual populations genetic inheritance is trans-mitted by two parents only, during sexual reproduction, andfrom the point of view of the offspring, on a single occa-sion only. In contrast, an ecological inheritance may be trans-mitted by multiple organisms, to multiple other organisms,within and between generations, throughout the lifetimes ofthe niche-constructing organisms. Last, ecological inheritanceis not exclusively transmitted by genetic relatives. It can alsobe transmitted by other organisms, who share, or previouslyshared, a common ecosystem. These other organisms must beecologically related, but they are not always genetically relatedto the organisms receiving the inheritance.

The explicit inclusion of ecological inheritance in evo-lutionary theory replaces the single inheritance system inFigure 1a by the dual inheritance system in Figure 1b. InSET, Figure 1a, genes are transmitted between generations viagenetic inheritance, but nothing else is. In the extended versionof evolutionary theory, Figure 1b, organisms inherit genes, in-cluding naturally selected genes from their ancestors throughgenetic inheritance. They also inherit some ancestrally modi-fied natural selection pressures, in their environments, relativeto their genes, through ecological inheritance.


John Odling-Smee

Niche Inheritance

Ecological inheritance has important consequences for de-velopment as well as for evolution, and it could change theperceived relationship between evolutionary biology and de-velopmental biology. If, in each generation, each individualoffspring not only inherits genes, but also a previously chosenor modified local selective environment relative to its genes,then what each offspring must actually inherit is an initialorganism-environment relationship or “niche” from its ances-tors.

Niche inheritance is summarized in equation 4.

N (to) = h[OiEi] (4)

N(to) represents the niche state at the moment of origin of a neworganism. It needs to be emphasized that each inherited niche isnow an individual organism’s “personal” developmental niche,rather than a population’s evolutionary niche (Odling-Smee1988).

This concept of niche inheritance differs from standardideas of inheritance in two ways. First, in SET the devel-opment of offspring organisms is assumed to begin with theinheritance by each organism of a “start-up” kit of genes,that subsequently “unfolds” in the context of an independentenvironment, in the course of the organism’s development(Lewontin 1983). In niche construction theory, however, thedevelopment of an organism begins with the inheritance of a“start-up” [OE] relationship, or niche, that combines both agenetic and an ecological inheritance. Subsequently, these twoinheritance systems “interact,” and their interactions are in partregulated by the phenotypically plastic, niche-constructing or-ganisms themselves during their development (Oyama et al.2001; West-Eberhard 2003; Pigliucci and Preston 2004).

Second, niche inheritance depends on two transmissionchannels between generations, instead of one (Figure 1b). Thefirst channel is closely associated with reproduction and is re-served by SET for genetic inheritance only. The second chan-nel is the external environment through which an ecologicalinheritance is transmitted. Minimally, in addition to inheritedgenes, each inherited niche, for each offspring, must includethe inheritance of an initial environmental “address” in spaceand time, often influenced by parental choices. In many speciesthe parents also ensure that a “resource package” is present attheir offspring’s initial address. For instance, phytophagous in-sects not only supply their offspring with eggs, but they oftenchoose specific host plants on which to lay their eggs, the cho-sen plants subsequently serving as energy and matter resourcesfor their offspring. In addition to what its parents supply, an or-ganism’s start-up niche may also include other environmentalresources, due to the niche-constructing activities of other, less

closely related organisms. For example, when termites build amound, they modify the mean, and reduce the range of tem-perature and humidity experienced by the developing larvaeby their collective niche-constructing activities (Hansell 2005;Laland and Sterelny 2006).

Niche inheritance is therefore richer than SET’s genetic-inheritance-only version of inheritance, and less restricting. Itmay therefore provide a friendlier basis for incorporating andclassifying the multiple inheritance systems in evolution thatare currently being proposed (West-Eberhard 2003; Jablonkaand Lamb 2005). It is this idea that I want to explore in therest of this article.

The Dimensions of Niche Inheritance

In order to explore it, we must first describe the principalsub-components of niche inheritance. For that, we need somedescriptive dimensions. We can derive two of them by furtherunpacking the relativity of the [OE] niche relationship. Onedimension can be derived from the relationship between theinternal and external environments of organisms. This relation-ship demarcates the two transmission channels through whichthe different components of niche inheritance are transmitted(Figure 1b). A second dimension is derived from the relation-ship between whatever “semantic information” (Odling-Smeeet al. 2003) is inherited by organisms from their ancestors andthe diverse natural selection pressures in their environmentsthat selected that information. The latter must include selectionpressures previously modified by ancestral niche construction.I will provisionally assume that these selection pressures arethemselves derived from energy and matter resources in theenvironments of organisms. Let us start with the transmissionchannels.

Channel 1 connects the internal environments of parentorganisms to the internal environments of offspring organ-isms, directly, via the mechanisms of reproduction. Ultimatelychannel1 is reducible to cell division and cell fusion. Channel1 was originally discovered by Schwann and Virchow in the19th century, and it gave rise to cell theory. Any kind of in-heritance that travels between organisms, from cell to cell, orfrom O to O directly during reproduction will be treated as aChannel 1 type inheritance.

Channel 2 connects possibly multiple, ancestral niche-constructing organisms to descendent organisms indirectly,through the modification of selection pressures in an externalenvironment. Any kind of inheritance that does not travel be-tween organisms, from cell to cell directly, will be treated asa Channel 2 type inheritance. Channel 2 works is the way thatecological inheritance works, from O to E, and back to O.

These definitions assume it is easy to demarcate the in-ternal and external environments of organisms in the contextof their [OE] niche relationships. However, the demarcation is



not always easy. For example, it would seem straightforwardto define any individual organism, O, by whatever boundaryexists between the organism and its environment, E. Thus, inthe case of a single celled organism, the boundary is its cellwall or membrane. O’s external environment E is then every-thing outside the same boundary. Depending on the focus ofinterest, however, there can be complications. For example, ina multi-celled organism the external environment of most cellsincludes the other cells in the metazoan’s body. Hence, in so-matic cell division inside a metazoan body, for example, whena parent liver cell in an animal gives rise to two daughter livercells, the transmission of heritable resources is direct, fromcell to cell, and therefore through Channel 1. However, the ex-ternal environment now becomes the rest of the liver, the restof the metazoan’s body, plus the metazoan organism’s externalenvironment. It follows that demarcating between an internaland external environment depends on how “the organism,” orpart organism that is the current focus of interest, is defined.Assuming “the organism,” O, can be defined sufficiently well,then relative to O, an external environment, E, can also bedefined.

It may also be difficult to distinguish between heritable in-formational resources, versus the heritable energy and matterresources that are the principal components of niche inheri-tance, and the primary sources of the natural selection pres-sures that select for semantic information in organisms. Here,several points need clarifying.

First, the distinction between informational resources andenvironmental energy and matter resources traces back to theorigin of life. To survive and reproduce, organisms must takephysical energy and matter from their environments. Theymust also dump physical detritus back in their environments.However, organisms cannot do either of these things unlessthey are adapted to their environments. Moreover, organismscannot be adapted unless they are sufficiently informed a pri-ori by adaptive semantic information. The “catch 22” is thatorganisms cannot be informed a priori without also possessingsufficient energy and material resources a priori to pay a fitnesscost for the acquisition, storage, and use of adaptive seman-tic information, including the “de novo” selection of “new”adaptive information by natural selection (Odling-Smee et al.2003; Bergstrom and Lachmann, 2004). So which came first,physical resources or semantic information, metabolism orreplication? This is the classic origin of life problem and it isstill not fully resolved (Fry 2000). But it does illustrate howfundamental and ancient is the distinction between semanticinformation and energy and material resources in evolution.

It is also notoriously difficult to define semantic informa-tion. Here, I will only attempt a working definition: Semanticinformation is anything that reduces uncertainty about selec-tive environments, relative to the fitness goals of organisms.Hence, the “meaningfulness” of whatever semantic informa-

tion is encoded in inherited genes ultimately derives from theability of those genes to “inform” organisms, relative to theirfitness goals and natural selection pressures, in such ways thatadapted organisms can tap into energy and matter resources intheir environments. This definition deliberately refrains fromspecifying the physical carriers of semantic information. Inprinciple, the carriers could be genes, or other molecules, orneurons, or in humans, cultural symbols. All that matters isthat the semantic information, carried by any carrier, can po-tentially influence the fitness of organisms.

I shall further assume that, in the case of genetic in-heritance, natural selection causes semantic information tobe carried by heritable genes, simply through the persis-tence of selected genes. By persisting across generations, se-lected “fit” genes register “fit” outcomes of previous organism-environment interactions and, in effect, become primitive“memories” (Odling-Smee 1983, 1988; Odling-Smee et al.2003). Semantic information is always relative because its“meaning” is ultimately derived from a relationship betweenthe fitness needs of organism and selection pressures in theirenvironments, including selection pressures previously modi-fied by niche construction. Conversely, environmental energyand matter “resources” are also relative, because they are recip-rocally defined by how they relate to whatever semantic infor-mation happens to be carried by specific organisms. Whetherthey are positive or negative, harmful or beneficial, energy andmatter resources are only “resources” relative to those specificorganisms that carry the semantic information that makes themso. Relative to other organisms that carry different semanticinformation, and therefore different adaptations, exactly thesame resources may be completely irrelevant (Lewontin 1982,1983; Odling-Smee et al. 2003).

A third problem relates to which transmission channel car-ries what kind of resource. By strongly identifying genes withinformation, and by reserving Channel 1 for genetic inheri-tance only, SET encourages the idea that Channel 1 transmitsgenetically encoded semantic information only. That idea ismisleading because some nongenetic components of “start-upniches,” including some energy and matter resources, are alsotransmitted by Channel 1, from cell to cell, during reproduc-tion. For example, in insects and birds the eggs supplied by“mothers” to their offspring carry some energy and matter re-sources in the form of cytoplasm and protein in egg yolks, aswell as semantic information (Sapp 1987; Amundson 2005).

Similarly, Channel 2 may appear to transmit physical en-ergy and matter resources only, in the form of modified naturalselection pressures. However, this too is misleading, because itis possible for ecological inheritance to transmit semantic in-formation, as well as modified energy and matter resources, be-tween generations. Semantic information is transmitted when-ever an ecological inheritance includes other organisms thatare themselves inheritors and carriers of semantic information,


John Odling-Smee

and when the semantic information they carry is modified byniche-constructing organisms. This point is complex and re-quires elaboration.

Previously, in our formal models of niche construction(Laland et al. 1996, 1999, 2001), the resource transmitted be-tween generations by ecological inheritance was notated by R,where R symbolized any environmental resource that could bemodified by niche construction. R could therefore be an abi-otic environmental component, for example a soil state, or awater hole. Or it could be an artefact built by an organism,for example, a termite nest, or a beaver dam. Or it could bea biotic environmental component, for example another or-ganism, from either the same or a different population as theniche-constructing organism itself. All these initial modelswere kept as simple as possible, partly by restricting R to en-ergy and matter resources only. That restriction, however, isneither necessary nor, in the longer term, desirable. Eventu-ally, it is likely to be useful to distinguish between physicalresources, Rp, and informational resources, Ri.

Many other organisms in the environments of niche-constructing organisms are likely to contain both Rp andRi resources relative to the adaptations of the focal organ-isms. Moreover, both the Rp and Ri contained by other or-ganisms may be altered, or exploited, or defended againstby niche-constructing organisms. For instance, another organ-ism may simply act as a physical resource, Rp, say a fooditem, for a niche-constructing organism. Alternatively, a niche-constructing organism may “manipulate” (e.g., the brood par-asitism of cuckoos; Davies et al. 1998; Combes 2001) or moreor less efficiently “copy” (e.g., social learning in animals; Fra-gaszy and Perry 2003) the semantic information, Ri, carriedin either the genome or the brain of some other organism,via some kind of communication. Similarly a parasite, say, avirus, may insert its own parasite DNA into its host’s DNAand by doing so manipulate the physiology or the behavior ofits host (Combes 2001). When this happens, the parasite doesnot immediately gain any physical resource or Rp by its nicheconstruction. What it gains in the first instance is a degree ofcontrol over its host’s phenotype by corrupting the semanticinformation, Ri, in its host’s genome or brain. Subsequently,the parasite may gain Rp as well by causing its host to supplyit with a physical resource. For instance, a gall produced bya plant benefits the parasite, at some cost to its host (Combes2001; West-Eberhard 2003).

Benign forms of communication are also possible, and inmany animals they are common. For example, it may “pay” aparent animal to transmit some of the information it carries inits brain to its offspring via social learning. It may also pay anoffspring to solicit and “copy” information held in the brainsof its parents, or its peers, or of other organisms in its socialgroup (Fragaszy and Perry 2003; Reader and Laland 2003;Odling-Smee 2006).

It follows that when the source of a natural selection pres-sure comprises other organisms in the external environmentsof niche-constructing organisms, the niche-constructing or-ganisms can potentially modify either the Rp or the Ri that iscarried by other organisms, or both. Rp can be modified by theconventional kinds of niche construction we have previouslymodeled (Odling-Smee et al. 2003). Ri, however, is invariablymodified by some kind of between-organism communication,henceforth “communicative niche construction.”

Unlike conventional niche construction, communicativeniche construction cannot modify a natural selection pressuredirectly. It can only modify natural selection indirectly, in twosteps instead of one. The first step involves communicativeniche construction causing a change in the semantic informa-tion, Ri, carried either by the niche-constructing organismsthemselves, for instance by the niche-constructing organismscopying some of the information carried by other organisms,or by the niche-constructing organisms changing the semanticinformation carried by other organisms. For instance, niche-constructing organisms may corrupt the semantic informationcarried by other organisms, as in the virus example. Noneof this is sufficient to modify any selection pressure in anyorganism’s environment.

A second step is also necessary as a consequence of thefirst. If communicative niche construction modifies the seman-tic information, Ri, carried by either the niche-constructingorganisms or by the other organisms, and if the modified se-mantic information subsequently translates into a change ofphenotypic or extended phenotypic expression, including theexpression of different niche-constructing activities in any ofthese organisms, then the resulting physical change in Rpcould eventually be sufficient to modify a natural selectionpressure in the environments of either the niche-constructingorganisms, or of the other organisms, or both. For example,animals frequently change the behaviors of other animals intheir own or other species by communicating with them, forinstance, by giving alarm calls to conspecifics, or by send-ing “stotting” signals to “would-be” predators. Animals cantherefore modify biotic sources of natural selection in theirenvironments by communication (Maynard Smith and Harper2003).

The same logic distinguishes between different kindsof coevolution. If other organisms are utilized by niche-constructing organisms exclusively as Rp, for instance food,as in standard models of predator-prey coevolution, then thetwo coevolving populations are likely to influence each oth-ers’ phenotypes directly, and their genes indirectly. However,if other organisms are used by niche-constructing organismsprimarily as Ri, as often happens in host-parasite coevolution,then a niche-constructing population may first influence thegenetics, or possibly the brains of the other organisms, andthen their expressed phenotypes. For example, in host-parasite



Table 1. The components of niche inheritance.

Transmission What is Type of inheritance Processes affected by theChannel transmitted system inheritance system

Channel 1 Semantic information (1a) Genetic inheritance Development/Welsmann/Evolution barrierInternaI Environment Epigenetic inheritance

(e.g.) Chromatin marks Development → Evolution sometimesMethylation patternsRNAiMaternal effects

Energy/matter (1b)(e.g.) Cytoplasmic inheritance Development → Evolution sometimes?

Other maternal effectsChannel 2 Semantic information (2a) Inheritance of modified selective environments Development → EvolutionExternaI Environment Energy/matter (e.g.) Behavioral traditions

Communication systems(2b) Inheritance of modified selective environments Development → Evolution(e.g.) Physically perturbed environments

coevolution, a parasite may change the semantic informationcarried by its host directly, for instance, by inserting its DNAin its host’s DNA. That may then alter its host’s subsequentbehavior (Combes 2001).

Classifying Inheritance Systems in Evolution

Equipped with these two dimensions of niche inheritance, in-ternal versus external transmission channels, and heritable se-mantic information versus heritable physical resources, can theconcept of niche inheritance be used to classify multiple inher-itance systems in evolution? Table 1 is an attempt to provide apositive answer to this question.

Several authors have reviewed the plural inheritance sys-tems that are now being proposed as evolutionarily significant(e.g., West-Eberhard 2003; Jablonka and Lamb 2005). Thescheme I will use here is Jablonka and Lamb’s (J&L’s) set offour inheritance systems, (1) genetic, (2) epigenetic, (3) be-havioural, and (4) symbolic. The advantage of their scheme isthat it is sufficiently broad to subsume all kinds of non-geneticas well as genetic inheritance systems in evolution. Table 1classifies the first three of J&L’s systems. Their fourth system,human symbolic inheritance, is discussed in a later section.

Table 1 uses both the two transmission channels, the in-ternal versus the external environment, and the two principalcomponents of niche inheritance, semantic information versusenergy and matter, to generate a 2 × 2 table, with four cells, 1a,1b, 2a and 2b. Each tabular cell (differentiated from biologicalcells) is then assigned the type(s) of inheritance proposed tobelong to it. Some illustrative examples of non-genetic inher-itance are also given in each cell.

Many of these assignments are straightforward. For exam-ple, if naturally selected genes encode semantic information(Maynard Smith 2000; Odling-Smee et al. 2003), then ge-netic inheritance indisputably belongs to Cell 1a. Given that

J&L (2005: 147) define epigenetic inheritance as the “trans-fer of information from cell to cell,” even though it might bepossible to define epigenetic inheritance more broadly, un-der their definition, epigenetic inheritance clearly belongs toCell 1a too. Examplar phenomena discussed by J&L underthe heading of epigenetic inheritance are also shown in Cell1a. They include chromatin markings, methylation patterns,RNAi (interference), and some maternal effects, for examplethe inheritance of maternal mRNA (Davidson 2006).

Cell 1b includes cytoplasmic inheritance, and some otherphysical resources that are transmitted by mothers to theiroffspring during reproduction, primarily via eggs. These re-sources include proteins, and components of membranes(Davidson 2006).

Cell 2a refers to J&L’s third inheritance system, behavioraltraditions, primarily in animals, and to the communication ofsemantic information between animals through social learn-ing (Fragaszy and Perry 2003). Since behavior is expressed inexternal environments, the phenomena in Cell 2a frequentlyinvolve both niche construction and ecological inheritance,the latter in the form of modified natural selection pressuresin the external environments of descendent organisms. J&Lemphasize this themselves in their book (p. 236). Cell 2a alsoincludes one kind of niche construction (not shown), describedby Sterelny (2003: 153) as “epistemic engineering.” Epistemicengineering refers to changes in “the informational characterof the next generation’s environment” caused by the niche-constructing activities of prior generations. Sterelny is primar-ily referring to human epistemic engineering, but it occurs inother animals too. Candidate examples include mammalianscent marks and insect pheromone trails.

Cell 2b refers to more conventional kinds of ecologicalinheritance, namely to the modification of natural selectionpressures in environments by niche construction by physicalperturbation or physical relocation (Odling-Smee et al. 2003).


John Odling-Smee

Table 1 demonstrates that it is not always easy to allocatecandidate non-genetic inheritance systems to single Cells. Thissuggests there is either something wrong with Table 1, or thatsome putative non-genetic inheritance systems may actuallyinclude more than one kind of inheritance. A good example isthe inheritance of maternal effects. Mousseau (2006: 19) pointsout that maternal effects are defined in a variety of ways, andhe himself defines them broadly as “all sources of offspringphenotypic variance due to mothers above and beyond thegenes that she herself contributes.” Depending on how they aredefined, maternal effects, and possibly some paternal effectstoo, could be assigned to all the cells in Table 1.

One particularly awkward example concerns the inher-itance of bacterial communities from mothers. Gut bacteriaare critical for mammalian development (Hooper et al. 2001;Xu and Gordon 2003), because bacteria induce gene expres-sion in intestinal epithelia, the genes subsequently activatingpathways that allow intestinal capillaries to form and permitlipids to be transported through the cells (Hooper et al. 2001;Stappenbeck et al. 2002). Humans inherit their gut microbialcommunities from their mothers’ vagina and the faeces at birth(Ley et al. 2006). It might therefore seem natural to assign thisinheritance to reproduction and to Channel 1 in Table 1. How-ever, bacteria are separate organisms from both human infantsand their mothers, so mothers are probably better describedas external environments for both the bacteria and their ownfoetuses. If so, bacterial inheritance must be transmitted viaChannel 2, not Channel 1. This raises a further problem. Inmammals, bacteria potentially provide both a Ri and a Rp. In-sofar as the development of a mammal’s gut depends on geneexpression regulated by bacterial genes, bacterial inheritancebelongs to Cell 2a. However, insofar as bacterial inheritanceaids subsequent mammalian digestive processes, it belongs toCell 2b.

The DevoEvo Consequences of Niche Inheritance

The final column on the right of Table 1 concerns whether anyof the component inheritance systems shown in the body ofthe table might change our understanding of the relationshipbetween developmental biology (Devo), and evolutionary bi-ology (Evo) in the EvoDevo relationship. One question thathas never gone away is whether any of the acquired charac-teristics, or any of the activities expressed by the phenotypesof developing organisms during their lives, can subsequentlyaffect the evolution of their descendents in innovative or adap-tive ways (Schlichting and Pigliucci 1998; Oyama et al. 2001;West-Eberhard 2003; Pigliucci and Preston 2004; Jablonkaand Lamb 2005).

Niche inheritance is immediately followed by niche regu-lation. Niche regulation involves phenotypically plastic, niche-constructing organisms, interacting with their local environ-

ments, in developmental [OE] niche relationships, throughouttheir lives, on behalf of their fitness needs. Successful nicheregulation eventually leads to surviving and reproducing “fit”organisms bequeathing niche inheritances in their turn to thenext generation. Niche regulation is provisionally described byboth Developmental Systems Theory (Oyama et al. 2001) andthe theory of phenotypic plasticity (Schlichting and Pigliucci1998; Gilbert 2001; Pigliucci and Preston 2004). The ques-tion is whether any of the component inheritance systems inniche inheritance can carry any kind of “acquired” variationsfrom parent organisms to their offspring, as a consequenceof the niche-regulating interactions of parent organisms withtheir environments. (The arrows in the final column of Table1 indicate candidate DevoEvo connections.) Let us considereach of the inheritance systems in cells 1a, 1b, 2a and 2b inturn.

According to SET, the first entry, genetic inheritance (Cell1a), affects the development of individual organisms, but ev-erything else that happens to, or is caused by the developingphenotypes themselves during their development is evolution-arily irrelevant. This is because there is no capacity for somato translate back into DNA. That version of Lamarckism isuntrue (Jablonka and Lamb 2005). All that counts is the trans-mission of genes by “fit” organisms to the next generation. Noother connections between “Devo” and “Evo” are recognizedby SET. This point is symbolized by the two slashed lines inTable 1. Amundson (2005) has shown how this disconnectionhas historically been attributed to a series of putative “barriers”between “Devo” and “Evo.” The best known barrier is the oneshown in Table 1, “Weismann’s,” derived from the early seg-regation of germ line from somatic cells during development(see also Maynard Smith 2000).

Such disconnection between Devo and Evo is now thoughttoo severe, particularly by developmental biologists, and it isbeing challenged by the non-genetic inheritance systems inTable 1 (West- Eberhard 2003; Jablonka and Lamb 2005). Thesecond entry in Table 1, epigenetic inheritance, provides oneexample. The notion that epigenetic variation, as well as ge-netic variation (Cell 1a), can be transmitted across generationswas controversial for decades, but there has recently been anaccumulation of empirical support for the idea (Bird 2002,2007; Jablonka and Lamb 2005; Reik 2007). For instance, thepeloric form of the toadflax Linaria is caused by an epige-netically inherited methylation pattern, yet this phenotype hasbeen stably inherited for over 200 years (Jablonka and Lamb2005; Bird 2007). Methylation differences in the gene for theglucocorticoid receptor are apparently also transmitted fromgeneration to generation in rats. Methylation differences ap-pear to be responsible for different abilities in rats to handlestress (Weaver et al. 2004), enabling the gene to be transcribedin the brains of some rats, where the gene is unmethylated, butnot in others.



Provisional evidence also exists for some evolutionaryconsequences of cytoplasmic inheritance and the inheritanceof some maternal effects. In the past, prominent evolutionarybiologists such as Morgan and Dobzhansky rejected cyto-plasmic inheritance as being of any importance in evolution(Amundson 2005). However, it is now established that amother’s experience of her environment sometimes leads tovariations in her growth, condition, and physiological statethat are subsequently transmitted to her offspring via cytoplas-mic factors (e.g., via yolk amount or hormones (Mousseauand Fox 1998a, 1998b). More generally, Mousseau (2006) hassummarized how and when transmitted maternal effects canhave evolutionary as well as developmental consequences.

All the remaining inheritance systems in Cells 2a and2b in Table 1 depend on niche construction. Elsewhere, wehave shown, with examples, that: (1) Niche construction is ex-pressed by individual organisms throughout their lives, and istherefore itself a developmental process. (2) Niche construc-tion can have subsequent evolutionary as well as developmen-tal consequences. (3) Niche construction does have evolution-ary consequences whenever prior niche construction causes thesubsequent modification of one or more natural selection pres-sures in the environments of populations, if the environmentalmodification is sustained for sufficient generations (Odling-Smee et al. 2003; Laland and Sterelny 2006).

In this respect, there is a further general point. Table 1 in-troduces a second channel (Channel 2) via which the ecologicalcomponents of niche inheritance are transmitted. But Channel2 is not affected by any of the “barriers” that apply to Chan-nel 1. For example, there is nothing equivalent to Weismann’sbarrier in an external environment. Potentially, this point hasconsiderable consequences for the DevoEvo relationship. In-sofar as (1) any of the inheritance systems in Table 1 affectsphenotypic variance and plasticity during development; (2)any form of phenotypic variance and plasticity translates intoniche construction; and (3) the expressed niche constructionsubsequently modifies one or more natural selection pressuresin the environments of later generations of a population viaChannel 2, then all the inheritance systems in Table 1 couldcontribute to the evolution of populations, as well as to thedevelopment of individual organisms.

Human Cultural Inheritance

J&L’s fourth system is human symbolic inheritance. Humanevolution depends on cultural inheritance as well as all theother inheritance systems in Table 1, and the transmission ofcultural inheritance depends, to a considerable degree, on sym-bols and language (Cavalli-Sforza and Feldman 1981; Durham1991; Deacon 1997; Richerson and Boyd 2005).

Human cultural inheritance has previously been modeledin diverse ways by a variety of theories (Laland and Brown

2002). None is fully compatible with Table 1. For example,one early approach, classical sociobiology (Wilson 1975), isfirmly based on SET. Accordingly, it assumes that the onlyinheritance system in evolution is genetic inheritance. Hencefor sociobiology, the only way any culturally inherited trait canaffect human evolution is by biasing the contributions madeby culturally variant humans to genetic inheritance.

An alternative approach, advocated by gene-culture co-evolutionary theorists, does recognize that cultural inheritancecan play a more significant role in human evolution (Cavalli-Sforza and Feldman 1981; Boyd and Richerson 1985; Durham1991; Richerson and Boyd 2005). This approach demonstratesthat inherited cultural behaviors, for example the dairy farmingof pastoralists (Enattah et al. 2002), can sometimes transformhuman selective environments in ways that do select for dif-ferent human genes. That led to “dual inheritance” modelsof human evolution incorporating both genetic and culturalinheritance. Laland et al. (2000, 2001) subsequently addedboth cultural niche construction and ecological inheritance tothese dual inheritance models, thereby generating a “triple in-heritance” model of human evolution incorporating genetic,cultural, and ecological inheritance systems. But triple inher-itance is also incompatible with Table 1, because it proposesthree instead of two transmission channels. However, becauseit includes ecological inheritance, it does suggest a possiblefurther model that is compatible.

Originally, Laland et al. (2000) proposed three separateinheritance systems in human evolution, only because the sameauthors had previously modeled ecological inheritance exclu-sively in terms of Rp. Since human cultural inheritance isprimarily concerned with the transmission of semantic infor-mation in the form of cultural “knowledge,” it is obviouslynot compatible with such an over-restricted version of eco-logical inheritance. It was for this reason that we previouslyassigned human cultural inheritance a separate status. How-ever, if ecological inheritance includes both Rp and Ri, as Ihave been arguing here, then a separate status for cultural in-heritance is not necesary. Instead, it becomes possible to treatboth the inheritance of cultural knowledge and the inheritanceof material culture as just different cultural components of aninclusive human ecological inheritance system.

Doing so reduces Laland et al.’s triple inheritance modelto the new dual inheritance model of human gene-culture co-evolution in Figure 2. Figure 2 is fully compatible with bothFigure 1b and Table 1. It indicates that both semantic infor-mation, inclusive of human cultural knowledge, and physicalresources, inclusive of human material culture, can be trans-mitted between generations by both Channels 1 and 2. Figure 2therefore suggests that even though human cultural inheritanceis exceptionally interesting, because human knowledge cangenerate exceptionally potent kinds of cultural niche construc-tion in both human “epistemic engineering” (Sterelny 2003;


John Odling-Smee

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Figure 2.Dual inheritance in human gene-culture co-evolution via Channel 1 and Channel 2.

Tomasello et al. 2005) and human “ecosystem engineering”(Boogert et al. 2006), it is not a special case requiring a separatestatus. On the contrary, human cultural inheritance is just an-other component of human ecological inheritance. Like all theother components of niche inheritance, it belongs in Table 1.

Conclusion

This still leaves some issues outstanding. I will signpost twoof them, but will make no attempt to do more here.

One issue concerns the relationship between informa-tional resources (Ri) and energy and matter resources (Rp)again. It is a very difficult relationship to work out, partlybecause relativistic systems are always difficult, and partlybecause even though semantic information is always carriedby some kind of physical carrier, semantic information on theone hand, versus energy and matter resources on the other, su-perficially appear to obey different thermodynamic rules. AsSterelny (2003: 153) put it, “Information is unlike meat. Afterpassing on to you my stone-working technique I still have it.”

The true relationship between information versus energyand matter is an ongoing problem for physicists and biologists(Bekenstein 2003; Bergstrom and Lachmann 2004), and it isunlikely to be resolved soon.

A second issue concerns fitness. In one respect, there isno change. Niches are defined by their organisms, so it makeslittle difference whether fitness is assigned to organisms, or totheir interactive niche relationships. Fitness is a relative con-cept anyway. But in a second respect, there may be a differ-ence. Conventionally, fitness is measured by the contributionsorganisms make to genetic inheritance only. So convention-ally, there is only one “currency” in evolution, genetic fitness.Niche inheritance, however, suggests that all the other inher-itance systems in Table 1 may contribute to the fitness of

organisms too, and they may introduce other fitness curren-cies, for instance ecological or “economic” currencies, thatare not readily convertible to the base evolutionary currencyof genetic fitness.

A simple example is the selection of mates by femalesin animal species. Females are usually expected to choosemales that signal they carry “fit” genes by advertising theirhealth, or their capacity to support a “handicap” (Zahavi 1975).However, if an experimenter were to arrange a choice betweena genetic “wimp” (poor Ri resources), artificially assignedcontrol over extremely rich physical (Rp) resources, versusa genetic “Adonis” (good Ri resources), artificially assignedextremely poor (Rp) resources, who would she choose? Theanswer is by no means a foregone conclusion. (Charmantierand Sheldon 2006).

A more complicated example arises from the tensions thatexist between genetic and cultural processes in human gene-culture coevolution (Figure 2). Cultural niche construction isnot always adaptive (Laland, et al. 2001). The Fore’s cannibal-ism, for instance, increased their vulnerability to kuru disease(Durham 1991). Similarly, both the Easter Island and Green-land Norse communities probably contributed to their owndownfall through culturally “acquired,” maladaptive, “niche-destructing” practices (Diamond 2005).

This raises a novel question. Do humans inherit two kindsof semantic information carrying different, and sometimes in-compatible “meanings? “Cultural meaning” is the apparentproduct of cultural selection and decision processes (Cavalli-Sforza and Feldman 1981; Durham 1991; Richerson and Boyd2005). “Genetic meaning” is established by natural selection.Both kinds of “meaning” occur in the context of interactivehuman niches, where both natural and cultural selection pro-cesses are constantly being modified by both cultural and non-cultural human niche construction. Are they compatible? It is



a question that goes beyond traditional nature versus nurturetype questions and it indicates another reason why a morecomprehensive approach to inheritance in evolution is proba-bly necessary. The concept of niche inheritance could supply it.

AcknowledgmentI should like to thank Doug Erwin, Marc Feldman, Kevin Laland, KimSterelny, Pete Richerson, and two anonymous referees for their valuable crit-icisms of an earlier draft of this paper.

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