The term "social learning", as currently applied to animals, describes a
ragbag of heterogeneous processes, with a variety of functions, found in a
broad array of vertebrate and invertebrate species. A more narrow use of the
term would restrict it to those processes that might reasonably be regarded
as homologous to processes operating in human social learning, and that
mediate a general capacity to acquire information from others, regardless of
the nature of the information, its function, or the sensory modality
employed. Within the narrow category of social learning, humans probably
transmit more information vertically from parent to offspring than all other
species. Protocultural species typically depend primarily on horizontal
transmissions based on social enhancement, rather than on imitation or
teaching (Galef, 1988; Laland et al., 1993). A comparative perspective thus
implies that the earliest forms of social transmission were probably
horizontal. In contrast, humans appear to acquire large amounts of
information from their parents, and from the parental generation (Hewlett &
Cavalli-Sforza, 1986; Guglielmino et al., 1995), suggesting that the lineage
leading to Homo sapiens has been selected for increasing reliance on
vertical and oblique cultural transmission.

The theoretical analyses described above imply that a shift from transient
horizontal traditions towards increased transgenerational cultural
transmission reflects a greater constancy in the environment over time. Such
a shift is difficult to reconcile with the traditional evolutionary
perspective, since there is no evidence to suggest that environments have
become more constant over the last few million years, but rather the
opposite. Moreover, even if they had, other proto-cultural species would be
expected to show more vertical transmission too. However, the increasing
reliance of hominids on vertical transmission is consistent with our
perspective, since here, a significant component of the selective
environment is self-constructed by the species concerned, and this component
could have favoured vertical transmission. We are suggesting that our
ancestors constructed niches in which it "paid" them to transmit more
information to their offspring. The more an organism controls and regulates
its environment, and the environment of its offspring, the greater should be
the advantage of transmitting cultural information from parent to offspring.
For instance, by tracking or anticipating the movements of migrating or
dispersing prey, populations of hominids may have increased the chances that
a specific food source was available in their environments, that the same
tools used for hunting would always be needed, and that the skin, bones and
other materials from these animals would always be at hand to use in the
manufacture of further tools. Such activities create the kind of stable
social environment in which related technologies, such as food preparation
or skin processing methods, would be advantageous from one generation to the
next, and could be repeatedly socially transmitted from parent to offspring.
It is possible that, once started, vertical cultural transmission may become
an autocatalytic process: greater culturally generated environmental
regulation leading to increasing homogeneity of environment as experienced
by parent and offspring, favouring further vertical transmission. With new
cultural traits responding to, or building on, earlier cultural traditions,
niche construction sets the scene for an accumulatory culture. This might
result in offspring learning higher-order "packages" of cultural traits from
their parents, as appears to be the case in pre-industrial societies
(Hewlett & Cavalli-Sforza, 1986; Guglielmino et al., 1995).

Clearly, the transition from animal proto-culture to human culture involved
much more than a shift towards vertical transmission of information and the
development of an accumulatory culture. Nonetheless, it is clear that the
new evolutionary perspective portrayed in Figure 2c can generate novel
hypotheses that may help to reconstruct some aspects of the evolution of
human culture.

2.2. Example 2: Human Altruism, Cooperation and Conflict.

At present, standard evolutionary theory provides two principal explanations
for "altruistic" cooperation in organisms, kin selection (Hamilton, 1964)
and reciprocity (Trivers, 1985; Axelrod, 1984), as exemplified by solutions
such as tit-for-tat to prisoner�s dilemma type games (Axelrod, 1984) . These
ideas have been used to account for a lot of cooperation in nature but
neither is sufficient to explain the full gamut of human cooperation (Boyd &
Richerson, 1985; Richerson & Boyd, In Press) . Kin selection is restricted
to kin, while the evolution of cooperation based on reciprocity is probably
limited to group sizes of less than ten, because increasing the size of
interacting social groups reduces the likelihood that selection will favour
reciprocating strategies (Boyd & Richerson, 1988)3. It is also hard to
account for certain forms of human altruism, such as military heroism, in
terms of reciprocity or kin selection (Boyd & Richerson, 1985). Our
evolutionary framework, however, indicates that the suite of processes that
may be regarded as feasible evolutionary explanations for human cooperation
is considerably larger than kin selection and reciprocity alone.

We suggest that any organism, O1, should be prepared to cooperate in ways
that benefit any other organism, O2, provided the total niche-constructing
outputs of O2, or any of O2�s decendents, modify resources in the
environment of O1, or any of O1�s decendents, with resulting fitness
benefits to O1 that exceed the cost of O1�s cooperation. This reasoning
applies to relatives, and implies that cooperation should be more likely
among kin that niche construct in mutually beneficial ways, and less likely
among kin that niche construct in mutually detrimental ways, than a strict
interpretation of Hamilton�s rule might suggest. The same logic also applies
to non kin. In fact it is obvious that reciprocal altruism is a special case
in which O1 and O2 are unrelated individuals of the same species that
directly modify each other�s environment. Recent analyses here suggest that
most cases currently described as reciprocal altruism, and many cases of kin
selection, are actually forms of intra-specific mutualism that are the
incidental outcomes of selfish behaviour (Mesterton-Gibbon & Dugatkin, 1992;
Connor, 1995). In addition our statement justifies a variant of reciprocal
altruism in which individuals do not trade altruistic acts with each other,
but rather an individual aids a second individual if the latter acts in ways
that benefit the first individual�s decendents.

Mutualisms and commensalisms also slot into this framework. Like altruism,
mutualism also depends on the modification of the selective environments of
recipient organisms by the niche-constructing activities of donor organisms.
However, in the case of mutualisms, O1 and O2 are individuals in different
species. The same is true of commensalisms, which for our purpose can be
regarded as asymmetric versions of mutualism. In commensalisms O1 cooperates
with O2 because O2 benefits O1 by ameliorating O1�s environment, but O2 is
unnaffected by O1, so O2 does not cooperate with O1.

Our general statement sketching the conditions under which organisms should
cooperate, may, under restricted circumstances, generalise to cases in which
O1, and O2 are groups of organisms, in one or more species. In many cases,
the niche-constructed by-products of several organisms are exploited by a
population. For example, shoals of fish, flocks of birds, and herds of
animals enjoy reduced predation risks, relative to solitary animals, merely
because their combined presence changes the selective environment of each
individual (Hamilton, 1971). Coordinated fish driving by cormorants, or seal
hunting by killer whales, provide examples of individuals coordinating their
niche construction so that it results in more effective food acquisition for
everyone (Connor, 1995).

Mutualistic interactions that result from the exploitation of incidental
by-products are more evolutionarily robust than altruistic interactions as,
because each individual is already acting selfishly, they are less likely to
be broken down by selfish cheaters. Organisms may also invest in others so
as to enhance the benefits which eventually return to themselves (Connor,
1995). A large amount of human cooperation can probably be explained in
terms of the exploitation and investment in the by-products of others, in
other words in terms of mutualisms resulting from human niche construction.
For example, barter and exchange are mutualistic interactions in which
individuals or organizations trade products for more desirable alternatives.
Moreover, human individuals and institutions "invest", metaphorically, or
even literally, in other individuals or institutions in order to enhance
their own returns.

One other possible explanation of cooperation in animals is the revised
group selection hypothesis proposed by Wilson and Sober (1994), about which
we have some reservations. In the past, much confusion has been caused by a
failure to distinguish between group selection for group or for individual
advantage (Wynne Edwards, 1962), or between "replicators" and "vehicles" 4
as the object of group selection (Wilson & Sober, 1994). Wilson and Sober
maintain that the fundamental question concerning group selection really
turns on whether social groups, or any other higher-level entities, can be
vehicles of selection, and not on whether they are replicators. They propose
a nested hierarchy of vehicles for genes (individual, group, metapopulation)
in which each level also includes a population of lower-level units.
Selection then acts at the lowest level for which there are fitness
differences. Thus, if there are no fitness differences between individuals,
there should be a "frame shift" (p. 592) to selection at the group level.

The original, or "naive", group selection hypothesis failed, primarily
because the processes that maintain group differences and select between
groups are typically weak compared with the processes that break down group
differences and select within groups (Williams, 1966). If group-level
adaptations are based on the cooperation of altruists, then any individual
who refuses to cooperate can reap the benefits without paying the costs, and
selfish strategies should be favoured by natural selection. It is not clear
how Wilson and Sober can surmount this obstacle to explain the cooperation
of large groups of individuals, since they have not proposed any feasible
process that could have reduced individual differences within groups, yet
promoted differences between groups, during hominid evolution. Here it may
be worth reflecting on the fact that group-level cooperation typically
depends on niche construction, because group-level adaptations are generally
expressed outside of human bodies. Groups may remain cohesive because it
pays each individual to invest in mutually beneficial niche construction.

Although we recognize some utility in the replicator-vehicle distinction,
and in Wilson and Sober�s hierarchical approach, we regard it as a
distortion. The entities that are selected, and between which there are
fitness differences, are not well described as "vehicles", or even
"interactors" (Hull, 1988), but rather are "organism-environment systems".
Similarly, what is replicated, from one generation to the next, is a complex
of information (both genetic and cultural) and some environmental (including
developmental) resources (Gray, 1992; Oyama, 1985). Once these distortions
are removed, it becomes easier to see how a form of group selection could
help account for some human cooperation.

The hypothesis that comes closest to a solution comes from gene-culture
coevolutionary theory, and places explicit emphasis on culturally inherited
niche construction. In this hypothesis, proposed by Boyd and Richerson
(1985), group selection works at the cultural level, with group-level
cultural traits being selected. They place emphasis on a "when in Rome do as
the Romans do" conformity, where individuals adopt the behaviour of the
majority. The significance of this "conformist transmission" is that it
minimises behavioural differences within groups, while maintaining
differences between groups. Thus group selection of cultural variation "for
the good of the group" is possible because if an altruistic cultural trait
becomes frequent in a cultural group, the transmission process should
subsequently discriminate against selfish individuals. Group selection of
cultural rather than genetic variation, requires a "frame shift" of
replicator, because it is not genes that are selected for, but rather groups
of individuals expressing a particular culturally transmitted idea. Since
cultural selection between groups may favour beliefs that benefit the group
at the expense of the individual, Boyd and Richerson provide a new
explanation for human cooperation.

Several properties of cultural inheritance, as opposed to genetic
inheritance, make Boyd and Richerson�s idea attractive. One is that cultural
inheritance, unlike genetic inheritance, may depend on more than two
parents. It is therefore possible for individuals to be sensitive to the
most frequent cultural traits in their society, and to conform to them.
Second, group selection of cultural variants can be faster than group
selection of genetic variants, because cultural death does not imply the
physical death of all the people in a culture. A threatened or defeated
people may switch to the traits of a new conquering culture, either
voluntarily, or under duress. Thus, unlike Wilson and Sober�s group
selection, here migration will not weaken the process. Third, symbolic group
marker systems, such as totem animals, human languages, and flags, make it
considerably easier for cultures to maintain their identities, and to resist
imported cultural traits from immigrants, than it is for local gene pools,
or demes, to maintain their identity by resisting gene flow (Boyd &
Richerson, 1985). Fourth, cultural transmission of information about
cheaters (e.g. gossip) reduces the efficacy of non-cooperative strategies
(Dugatkin, 1992).

More negatively, conformist transmission may potentially be exploited by
powerful individuals, groups, or institutions, that dominate the
dissemination of information through societies, to promote their own
interests. Powerful "cultural parents" may stand to gain from persuading
other less powerful humans to conform, perhaps by recruiting extra
assistance in modifying environments in ways in which they, rather than the
helpers benefit. These processes may be amplified by tool use, for instance
by the technology of the modern media, by weapons, by art, or by deceit.
Religious, commercial and political propaganda, for example, may all be used
to persuade, trick or coerce conformity from others against their own
individual interests, yet in favour of the interests of a dominant class of
cultural transmitters.

We can also reverse our earlier logic to suggest that any organism O1,
should act in a hostile manner, to the disadvantage of any other organism
O2, provided the total niche-constructing outputs of O2, or of any of O2�s
descendents, modify resources in the environment of O1, or any of O1�s
descendents, to the detriment of O1, if the resulting reduction in the
fitness costs to O1 of O2�s outputs exceeds the cost of O1�s agonistic
behaviour. It is easy to see how this reasoning might account for a great
deal of aggressive behaviour, including a form of reciprocal hostility, in
which individuals and their descendents trade antagonistic acts. In other
words, we predict that organisms should actively harm other organisms by
investing in niche construction that destroys other organism�s selective
environments, provided the fitness benefits that accrue to the investing
organisms from doing so, are greater than their fitness costs. Since this is
a general idea, it should extend to the human cultural level, with the
qualification that at this level other processes may be operating.


2.3 Example 3: Selfish Phenogenotypes and Multiple-Process Adaptation

2.3.1. Units of Selection in Human Evolution: A prima facie problem with our
multiple-processes-in-evolution approach is that it raises questions about
the currency of human evolution. Should cultural traits be measured in terms
of reproductive success only, as the sociobiologists advocate, or should
they be measured by a cultural transmission rate parameter as well as, or
instead of genes? This problem was one of the earliest hurdles faced by
contemporary gene-culture theory. Initially genetic and cultural processes
were treated as independent, with separate fitness scores and transmission
coefficients allocated for natural selection and cultural transmission.
However, it rapidly became clear that genes and cultural traits can interact
in the same way that two genetic loci can interact, to generate associations
of genotype and cultural phenotype in non-random frequencies (Feldman &
Cavalli-Sforza, 1984). This means that treating genetic and cultural
processes as independent is a distortion. A straightforward, pragmatic
solution is to allocate fitnesses and transmission rate parameters directly
to combinations of genotypes and cultural traits, a package known as a
'phenogenotype'. For instance, in Feldman and Cavalli-Sforza�s (1989)
theoretical exploration of the coevolution of lactose tolerance and milk
usage, one phenogenotype was a milk using individual expressing two copies
of the allele conferring lactose tolerance, while another was a non-milk
using individual which no such alleles. For human sociobiologists, the most
appropriate way to think about evolution is from the perspective of the
gene: those characteristics that have been favoured by selection are the
expression of the "selfish genes"(Dawkins, 1989) that were best able to
increase their representation in the next generation. For gene-culture
coevolutionary theory, the logic is the same, but the replicator is
different: Instead of the selfish gene there is the "phenogenotype". Those
human characteristics that have been favoured in the face of both natural
selection and cultural transmission are the expression of the phenogenotypes
that were best able to increase their representation in the next generation,
by whatever process. As an intuitive shorthand, a phenogenotype can be
thought of as a human with a package of genes and experience. In this sense,
the phenogenotype approach re-establishes the organism (or rather, classes
of organism) as the central unit of human evolution, not as vehicle but as
replicator. In fact, what is really replicated is a bio-cultural complex,
with a composite array of information (acquired through multiple processes,
and stored at different levels) and inherited resources. However, we
recognize the need for simple conceptual and formal models that have the
utility to explore and shed light on the dynamics of such systems, and we
regard the phenogenotype approach as the best method currently on the
market5.

2.3.2. Multiple-Process Adaptation: Controversy has surrounded the
sociobiological postulate that human beings typically behave in ways that
increase their inclusive genetic fitness (Sahlins, 1976; Montagu, 1980). It
is trite to point out that the processes that underlie culture are
adaptations, and that socially learned information, and cultural
inheritance, may increase reproductive success. Mathematical models that
have explored the evolution of social learning reveal that it is a truism of
the modelling exercise that the capacity for social learning cannot be
favoured unless it generally increases some measure of fitness. Obviously,
the same is true of knowledge-gaining ontogenetic processes. So what
characteristics of human culture could allow humans to behave in a
maladaptive way, or to transmit maladaptive information?

One of the most important findings to emerge from gene-culture
coevolutionary theory is that there are a variety of mechanisms by which
culture can lead to the transmission of information that result in a fitness
cost relative to alternatives. Cavalli-Sforza and Feldman (1981) provided
theoretical confirmation of the intuitive notion that cultural traits
associated with a viability or fecundity deficit may still increase in
frequency in a population if there is strong conversion of individuals to
the same trait. Boyd and Richerson (1985) found that, where individuals
adopt the behaviour of influential or successful members of their society,
maladaptive cultural variants can spread, even if associated with a
substantial viability disadvantage. Other gene-culture models reach the same
conclusion (Feldman & Laland, 1996).

Our perspective suggests that, in each generation, populations of organisms
persistently construct or reconstruct significant components of their
environments. This means that, as they evolve, organisms may, in effect,
drag part of their own environments along with them, thereby transforming
their own "adaptive landscapes". If ontogenetic processes, culture, and
counteractive niche construction in general, have consistently damped out
the need for a genetic response to changes in the population�s environment,
hominid populations may have become increasingly divorced from their
ecological environments. At the same time, our hominid ancestors may
increasingly have responded to novel selection pressures initially generated
by inceptive niche construction, and subsequently dominated by cultural
traditions. In this case, the common conception that modern human
populations are adapted to an ancestral Pleistocene environment (Barkow et
al., 1992) can only be partly correct. In particular, components of the
social environment, for example, traits related to family, kinship and
social stratification, may have been increasingly vertically transmitted by
culture to the extent that contemporary human populations may have become
largely divorced from local ecological pressures. Support for this argument
comes from Guglielmino�s et al.�s (1995) study of variation in cultural
traits among 277 contemporary African societies, in which most traits
examined correlated with cultural (linguistic) history, rather than ecology.

In the short term organisms typically niche construct in ways that enhance
their immediate fitness, but in the long term organisms can also "niche
destruct" relative to their own genes. For example, they can build up
polluting detritus, or strip their environments of non-renewable, or too
slowly renewing, resources, until they have made their own environments
hostile to themselves and to their offspring (Diamond 1993). Among plants,
this process typically leads to auto-ecological succession, while animals
typically respond by dispersing to other environments. Failure to respond to
the feedback from negative niche construction is a possible recipe for
extinction.

Could humans drive themselves to extinction? There are two reasons for
supposing that this is a possibility. First, culture greatly enhances the
human capacity for niche construction. For example, science based technology
is currently making an enormous impact on the human environment. It has made
many new resources available via both agriculture and industry, it has
influenced human population size and structure via hygiene, medicine and
birth control, it has drastically changed human warfare, it is drastically
reducing biodiversity, and it may already have resulted in the degradation
of large areas of our global environment. These are all potential sources of
modified natural selection pressures. Second, human cultural processes can
work much faster than human genetic processes, generating new adaptive
problems at a faster rate than the human genetic processes can respond to.
In these circumstances, human culture might drive either local, or general,
self-induced extinctions.

In many respects, this is a reoccurrence of an old evolutionary problem.
Many relatively long-lived species encounter rates and types of
environmental change, whether self-induced or independent, that exceed the
capacity of their genes to handle, and they frequently go extinct. Clearly,
one way in which human beings could adapt to culturally induced
environmental changes is through quicker acting responses at some
non-genetic level, especially through further cultural change.

Unfortunately there are well known snags with this kind of solution. First,
the population may not recognise the source of the novel, culturally induced
selection pressure. This was the case with the Fore of Papua New Guinea who
maintained a cannibalistic tradition despite the fact that it perpetuated a
deadly disease (Durham 1991). Second, the required corrective technology may
not always be available, or may be too costly to introduce. For example, in
theory the Kwa could have responded to the increased selection by malaria by
the cultural control of this disease, but in fact they lacked the technology
to do so. Third, the feedback from cultural niche construction may be
indirect, which may make it difficult to recognise any longer term negative
consequences of the niche construction. Rogers (1995) documents how the
adoption of wet rice cultivation in Madagascar had a range of diffuse
indirect effects only manifest several generations later, including changes
in tribal government, patterns of warfare and the role of the father.
Fourth, responding to cultural change with further cultural change always
risks introducing a "runaway" situation, in which each new solution
generates the next problem, at an ever accelerating rate. The phenomenon of
antibiotic resistance is a recent example (Ewald, 1994).

3.0 CONCLUDING REMARKS

In the preceding sections we have begun to develop a new type of
evolutionary framework for the human sciences by emphasing niche
construction, and ontogenetic and cultural processes. We have also
illustrated the conceptual model with a number of ideas, related to sample
topics. Our hope is that these suggestions will encourage others to use the
evolutionary framework we are proposing in this paper, either to take some
of the ideas we have already discussed further, to the point where they can
be empirically tested, or to generate other hypotheses of their own.

Notes.

1 Here "construction" refers to a physical modification of the environment
and not to the perceptual processes responsible for constructing a mental
representation of the world from sensory inputs.

2 Although in their book, Genes, Mind and Culture, Lumsden and Wilson (1981)
labelled their models "gene-culture coevolutionary theory", their approach
had more in common with conventional sociobiology than the modern
gene-culture coevolutionary theory (Feldman & Cavalli-Sforza, 1976; Boyd &
Richerson, 1985).

3 Boyd and Richerson (1992) established that punishment allows reciprocity
to evolve in large groups, if reciprocators respond to noncooperation by
withholding future cooperation, and also punish others that do not punish
noncooperators. However, they also established that there is no guarantee
that the cultural traits stabilized by punishment will enhance individual or
group fitness.

4 Dawkins (1989) coined the terms "replicator" and "vehicle" to distinguish
between the �immortal� genes, that are replicated each generation, and the
transient, vehicular organisms that house them. Dawkins also makes the point
that there may be other kinds of replicator, for instance, culturally
learned beliefs or traits, or "memes", which may be selected by processes
analogous to natural selection, a point anticipated by Cavalli-Sforza &
Feldman (1973), and central to contemporary gene-culture coevolutionary
theory.

5 The "phenogenotype" is simply a convenient tool for operationalizing the
modelling of gene-culture coevolution. We anticipate that, in some
circumstances, the relationship between genetic information, culturally
acquired information, and the behavioural phenotype may eventually prove too
complex to be handled in this way. For instance, in the past, gene-culture
modellers have chosen to parameterize either the frequency of a behaviour
pattern or of acquired information, as convenient. Such switching between
symbolically encoded information and phenotype is legitimate only where
there is a tight correspondence between information and behaviour (Cronk,
1995). Where this correspondence is weak, gene-culture methods might have to
be developed further, for example, by introducing a coefficient into the
models that represents the extent to which individuals with a particular
combination of genes and acquired information are likely to express a
particular behavioural phenotype.



Acknowledgements

We are grateful to Robert Hinde, Adam Kuper, Richard Lewontin, Henry
Plotkin, Peter Richerson, and Kate Robson-Brown for helpful comments on an
earlier draft of this manuscript. Kevin Laland was supported by a Royal
Society University Research Fellowship, and Marcus Feldman by NIH grant
GM28016.

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