TREE vol. 8, no.

5, May

44 Gliwicz, M.Z. and Sieniawska,

A. (1986)
Limnol. Oceanogr. 3 I, I 132-i I38
45 fones, M., Felt, C. and Guarda, S. (1991)
Freshwater Biol. 26, 35-44
46 Sullivan, B.K., Buskey, E., Miller, D.C. and
Ritacco, P.I. (1983) Mar. Biol. 77, 299-306
47 McNaught,
D.C. (1989) Hydrobiologia
188089, 117-121
48 Arts, M.T. and Sprules, W.C. (1987) Can. I
Fish. Aqoat. Sci. 44, 458-466
49 Buikema, A.L., Jr and Benfield,
E.F. (1979)

Much of the debate over applying the theory of evolution to the study of human
behaviour has died down because most
critics now realize that the political ramifications of sociobiology are no more, or no
less, than those of behaviourism, psychoanalysis or cognitive science. But controversy remains. It is scientific, and concerns
the proper way to do human sociobiology.
I contrast the perspective of those sociobiologists who use the approach of behavioural
ecology, and who have come to be known
as darwinian anthropologists or darwinian social scientists, with their critics, who
refer to themselves as evolutionary or darwinian psychologists, describe the research
methods that each uses, and ad if those

issues must also be confronted by those

studying animals.
Darwinian anthropologists
and
evolutionary
psychologists
accept
Williams conception of adaptation,
but they differ in their emphasis on
(I) the importance
of proximate
mechanisms, (2) the relevance of
current
fitness,
(3) the
role
of behaviour, and (4) the nature of
proximate mechanisms in the study
of adaptations.
These differences
lead them to place differential
importance on the ancestral environment in the study of behaviour.
Darwinian anthropology
Darwinian anthropologists
(DAs)
often assume that it is unnecessary
to invoke proximate mechanisms
when using evolutionary theory to
study behaviour. To quote Alexander2, Quite different sets of such
proximate mechanisms may lead to
what appears to be the same goal
in different individuals, or to different goals in the same individual at
different times and in different circumstances. (p. 18). These goals
Charles Crawford is at the Dept of Psychology, Simon
Fraser University, Burnaby. B.C., Canada V5A IS6.
0 1993, Elsewer

Sctence

Publlshers

perspectives
---

1993

Ltd (UK)

J. Fish. Res. Board Can. 36, 32 l-328

50 Cairns, I., fr, Heath, A.G. and Parker, B.C.
135-171
(1975) Hydrobiologia47,
51 Cooney, I.D., Gehrs, C.W. and Bunting,
D.L., II (1983) Effects of Temperature
and
Nutritional State on the Toxicity of Acridine
to the Calanoid Copepod, Diaptomus
clavipes Schacht, Environmental
Sciences
Division, Oak Ridge National
Laboratory
52 Lewis, P.A. and Horning, W.B., III (1991)
Environ. Toxicol. Chem. IO, I 35 I -I 357

53 Hanazato,

T.

( I99 I ) Limnol.

Oceanogr.

36,

165-171
54 Cochrane, B.J., irby, R.B. and Snell. T.W.
( 199 I ) Camp. Biochem. Physiol. 98C. 385-390
55 Carvalho, C.R. (I 9871 I. Anim. Ecol 56,
469-478
56 Hanazato. T. and Yasuno, M. ( I9891 Arch.
I 14,497-504
Hydrobiol.
57 Vanni, M.I. (1987) Ecol. Monogr. 57,61-68
58 Brooks, 1.L. and Dodson, S.I. I I9651
Science 150, 28-35

The Future of Sociobiology:

Babies or Studying

Counting
Proximate
Mechanisms

Charles B. Crawford
are not to be specified in terms of
hunger, fear, love or anger, but in
terms
of fitness.
To
quote
Alexander2 again, The theory of
lifetimes most widely accepted
among biologists is that individuals
have evolved to maximize the likelihood of survival not of themselves, but of their genes, and that
they do this by reproducing and
tending in various ways offspring
and other carriers of their own
and non
genes - descendent
descendent
relatives. (p. 38).
Because organisms are seen as
inclusive fitness maximizers, much
DA research focuses on reproductive differentials,
such as those
between high and low status males
in medieval Portuga13, or the number of surviving offspring of good
and poor hunters among the Ache,
a tribe of Paraguayan hunter gatherers4, or the conditions
under
which polyandry can be advantageous for some Tibetans5.
Darwinian anthropologists
argue
that, although the study of proximate mechanisms
may on occasion, as in kin recognition, help
us to understand adaptation, it is
behaviour that maximizes fitness,
and hence it should be the focus of
study. Irons discussion of culture is
phrased in terms of behaviour,
rather than ideas, beliefs, and
sentiments
because it is actual
behaviour that influences reproductive
success directly. Ideas,
beliefs, and sentiments, from the
point of view of behavioural biolo-

gy, are important to the extent that

they affect behaviour.b
Because of the emphasis
on
behaviour
and inclusive fitness
maximization, DAs see less need to
focus on the ancestral environment,

where adaptations evolved, and its

relation to the current environment,
where behaviour is studied. Crook
and Crook5 write, Where strategic
behaviour
maintaining fitness is
demonstrable
it may be argued
that humans, like for example gelada baboons..
have dispositions to
interact in ways that create social
organizations in which they reproduce successfully.
Figure I may help the reader to
understand the DA perspective. In
distinguishing the two perspectives
I believe it is helpful to distinguish
between the innate adaptation, the
genetically encoded design for the
development
of proximate mechanisms7, and the operational

adap-

the phenotypic psychological processes

actually producing
the behaviour. For DAs the innate
adaptation refers to the genetically
encoded ability to develop scenario building, flexible
learning,
and other mechanisms for maximizing inclusive fitness. Ancestral and
current behaviour
differ to the
extent that different behaviours are
required for tracking ancestral and
current fitness goals. Because the
distinction between the ancestral
and current environment
is not
emphasized it is not represented
in Fig. 1.
tation,

183

perspectives

TREE vol. 8, no. 5, May 7993

Specific ancestral
selection pressures
on a species

capacity for scenario building and

learning behaviours that maximized inclusive fitness

innate adaptation:

due to
interaction of innate flexible
learning capacities with environment
Operational adaptation

Developmental
environment
-------

Behaviour

Immediate
environment

Fig. I. The darwinian anthropologists

perspective on how an evolved innate adaptation, in conjunction
with the current developmental and immediate environments,
produces current behaviour.

behaviours
adaptive
and others
Evolutionary psychologists (EPs)~ nonadaptive,
(2) the mechanisms
criticize DAs on several grounds.
that natural selection shaped to
They argue, first, that although
produce the adaptive behaviours,
adaptations have evolved because
and (3) the ways that these evolved
mechanisms function nowO.
they provided ancestral organisms
Note the distinctions between
with greater lifetime reproductive
ancestral
and current
environsuccess
(LRS) than alternative
adaptations,
it is incorrect to say ments, between ancestral and current operational adaptations, and
that organisms evolved propensiancestral
and current
ties to maximize their inclusive fit- between
behaviour in Fig. 2. The innate
ness. The processes of evolution
adaptation,
genetically
encoded
are not the goals of organisms.
design-information
for the develSecond, they argue that although
behaviour is a manifestation of an opment of specific cognitive and
adaptation, behaviour itself is not emotional mechanisms useful to
ancestral individuals, is assumed
adaptation,
and
therefore
Ehaviour
should be studied to to be unchanged between anceselucidate
the naturally selected
tral and current
environments.
Ancestral and current operational
design of the proximate mechanisms producing it. Third, they argue
adaptations, the psychological prothat since the environment of evocesses actually producing behavlutionary adaptedness and the cur- iour, may differ because they are
formed through interactions of the
rent environment may differ considerably, reproductive differences
innate adaptation with the current
that contribute to fitness now cannot
environment during development,
be used for elucidating adaptations.
and because ancestral and current
developmental
environments may
Finally, they argue that since natural selection can only shape specific differ.
Ancestral and current behaviours
mechanisms for dealing with ancestral conditions, the human psyche may differ because (I) ancestral
and current developmental
enmust be comprised
of specific
mechanisms rather than being a vironments may differ producing
general
problem
solver.
Evol- different operational adaptations,
or (2) because, even if Pleistocene
utionary psychologists think of evoland current
operational
adaputionary psychology as the study
tations are identical, the distribuof: (I) the conditions in ancestral
tion of the immediate information
populations that rendered certain
Evolutionarypsychology

184

inputs to them may differ. In the

first case, for example, Pleistocene
and current educational practices
may differ I2, leading to somewhat
different
ancestral
and current
intellectual abilities. To illustrate
the second case, suppose
that
both
Pleistocene
and
current
children have the same operational adaptation for adjusting their
aggression to the level of the aggression they observe. Since the
distribution of aggression seen by
children on TV may differ from that
which Pleistocene
children
observed in their environment, the
same operational adaptation may
produce more aggression in current
children.
Because both ancestral and current operational adaptations
and
behaviour may differ, behaviours
that contributed
to ancestral fitness may not contribute to current
fitness, and behaviours that contribute to current fitness may not
have contributed to ancestral fitness. Therefore,
EPs argue that
making comparisons between fitness differences, a major research
tactic of DAs, is not useful for
studying adaptations.
The focus,
they argue, must be on the naturally selected design of proximate
mechanisms.
I believe
the key difference
between DAs and EPs is their view
of the innate adaptation. Darwinian
anthropologists
see the human
psyche as built of a relatively small
number of genetically conditioned
domain-general
mechanisms
enindividuals
to develop
abling
strategies, such as flexible learning
and scenario building, that in conjunction with tendencies to maximize inclusive fitness, produce the
operational adaptation that deals
with problems in the current environment. This view of the human
psyche, as a kind of modified tabula rasa, is congenial to most mainstream social scientists. (I have
found that for many psychologists,
anthropologists
and sociologists,
giving up the tabula rasa view of
the human psyche is much more
problematic
than accepting that
evolutionary theory can be profitably employed in the study of
human behaviour.)
Evolutionary
psychologists argue that the evolution of the mental apparatus does
not differ from the evolution of

TREE vol. 8, no. 5, May 7993

Specific ancestral
selection pressures
on a species

other adaptations.
Hence, there is
no more reason to believe that the
brain is a tabula
rasa than to
believe that the stomach is a general digester designed
to track the
foods an organism may encounter.

Then
/

f
3
/mate adaptation: information processing
mechanisms instantiated in neural hardware

Differencesin researchstrategies
In its pure form, DA focuses on
differences in LRS between individuals
encountering
different
environments, and uses the methods
of behavioural
ecology to study
these differences.
EP, in its purest
form, uses the methods
of evolutionary biology and experimental
psychology to study the naturally
selected
design of psychological
mechanisms.
Consider how these
two types
of researcher
might
approach
the
Triverstesting
Willard hypothesis about the allocation of parental
investment
to
male and female progeny.
Trivers and Willard argued that if
(I) variance of male LRS exceeded
that of female LRS, (2) the relative
health and dominance of mothers is
passed on to their progeny, and (3)
healthy or dominant
males obtain
more matings than males lacking
these attributes,
then (4) females
will be selected to allocate investment in progeny as a function of
their health or dominance. CluttonBrock et al., in a comprehensive
study of red deer (Cervus elaphus),
found considerable
support for the
hypothesis.
Sons born to mothers
above
median
rank were
more
reproductively
successful than their
daughters, while daughters born to
subordinate
mothers
were more
reproductively
successful than their
sons. Moreover, the ratio of sons to
daughters
produced
by dominant
mothers was higher than for subordinate mothers.
Because the sex
ratio
and
reproductive
success
were key dependent
variables
in
this study, it is similar to some
studies of sex allocation done by
DAs and described by Sieff.
evolutionary
An
psychologist
attempting
to test the TriversWillard hypothesis would first conmodel relating
struct a selection
sexual dimorphism
in variance in
reproductive
success in males and
females
and health or status of
mother to the benefits of differential investment
in sons and daughterslb. Varying the parameters
of
the model would provide a des-

Ancestral
developmental
environment
---------

Operational adaptation in ancestral

environment due to innate information
processing mechanisms responding to
environment during development
/

*
-t-------Now

Immediate
ancestral
environment

Ancestral behaviour
_-___--_------_----------------

Operational adaptation in current

environment due to innate information
processing mechanisms responding to
environment during development

Current
developmental
environment

Immediate
current
environment

Current behaviour
Fig. 2. The evolutionary psychologists perspective on how the evolved innate adaptation in conjunction
with the current developmental
and immediate environments
produces current behaviour. Because
there is a clear distinction between ancestral and current environments
and between ancestral and current operational adaptations (although not between ancestral and current innate adaptations) ancestral
and current behaviour may differ considerably. Although ancestral behaviour contributed to ancestral
fitness, and hence the evolution of the innate adaptation, current behaviour need not contribute to current fitness.

cription of how sex allocation might

have been selected for in a particular species. The model would be
used in conjunction
with information about the natural history of
the species to explore the parameter space of the independent
variables to determine whether a window of opportunity
could have
existed
for the evolution
of the
putative adaptation.
If the results
of the modelling suggested that the
evolution
of the
adaptation
is
plausible, a theory of the nature of
the adaptation,
specified in terms
of decision rules assumed to be
instantiated
in neural
hardware,
would be formulated.
The dependent variables would be outputs
from the decision process affecting
nursing time, amount of protection
from predators, etc., given to sons
and daughters, rather than fitness
measures or behaviours
assumed
to enhance fitness. Attitudes,
val-

ues, intentions and motives would

be measured in human studies. A
decision rule might be something
like: If subordinate
and physically
weak, be more responsive to the
needs of daughters than of sons;
but if strong and dominant
be
more attentive
to the needs of
sons than of daughters. It would be
necessary to formulate a theory of
the relation between ancestral and
current environments.
Such a theory requires a model
of how the crucial independent
variables,
which are measures of
adaptation-relevant
external
and
internal
environmental
variables,
are represented
to the ancestral
adaptation.
Dominance,
for example, might have been represented
in terms of posture, frequency of
unreciprocated
threat displays, or
resources held by different ancestral individuals. Once the decision
rules that describe the adaptation
185

perspectives

TREE vol. 8, no. 5, May 7993

are specified, and the way the environmental

inputs to them are
represented
to the psyche, the
evolutionary psychologist can use
the
methods
of experimental
psychology to test predictions from
the overall model.
The logic of such an experiment
is laid out in Fig. 3. In the case of
red deer, an experiment
might
involve
manipulating
status
or
health and measuring variables
related to differential investment
in sons and daughters. To strengthen
the inferences
about the adaptation, predictions from other evolutionary
explanations
are recommended.
Clutton-Brock et a/.
noted that their results could also
be explained on the basis of the
vulnerable-male
hypothesis. Thus,
their results might be explained as
a cost of sexual selection: male red
deer may have been selected to
divert energy from growth of their
immune system to growth of their
antlers, making them more vulnerable to stress. What appears to be
sex allocation might be nothing
more than a fortuitous effect of sexual selection. A series of controlled
experiments should enable the EP
to eliminate alternative hypotheses.
If the results of the controlled
experiments
do not support the
proposed explanation, the EP must
attempt to determine where the
problem lies. It could reside in the
formulation of the selection model,
the description
of the decision
rules that describe the adaptation,
the way the crucial environmental

Experimentally
manipulated
inputs to proximate

variables are represented

to the
decision rules, or the experimental
procedures for data collection.
Finally, if both the selection
model and experimental
studies
support the existence of the putative adaptation,
EPs would recommend naturalistic observational
studies to explore how the adaptation is expressed in a variety of
current environments.
Note that
the results of the observational
studies are contingent on assumptions about the ancestral adaptation and its relation to the current
environment17. For example, an EP
would claim that the interpretation
of the study by Clutton-Brock et al.
is contingent on the assumption
that the red deer of Rhum are living in an environment similar to
that in which they evolved. If they
were not (say, because they were
being artificially provisioned), the
decision
processes
might not
respond according to the TriversWillard hypothesis
because
of
insufficient effective environment
cues to activate the adaptation.
The modelling, controlled experiments, and observational
studies
should give the researcher a reasonably
comprehensive
understanding of the putative adaptation.
Commentary
The evolutionary
psychologists
have raised a number of important
points that are having considerable
impact on the way many of us do
our research.
Since
darwinian
anthropology
is basically animal

Trivers - Willard
hypothesis

mechanisms:

Vulnerable male
hypothesis
-

Status of mother
Resources of mother

in terms of:

I
Health of mother

Predictions about outputs

from proximate
mechanisms tested

??

Nursing time

??

Support in conflicts
with conspecifics

??

Defense against
predators

I-

for sons and daughters

Fig. 3. Design for experimental

studies of putative proximate mechanisms for allocating resources to
sons and daughters. Note that the design is strengthened
by including predictions from alternative evolutionary hypotheses,
in this case the Trivers-Willard
hypothesis and the vulnerable-male
hypothesis.
Because the design includes random assignment of subjects to treatments
it can be used to make
causal statements about the putative adaptation.

186

behavioural
ecology applied
to
human behaviour, one wonders if
some of the critique does not also
apply to studies of animal behaviour. Is it legitimate to construct
explanations entirely in terms of
ultimate causes of behaviour, or
must another level of analysis, such
as the cognitive, be introduced?
Must animal behavioural ecologists
begin testing hypotheses
about
animals mental apparatus? Have
animal behavioural ecologists paid
sufficient attention to the relation
between
the ancestral environment, where adaptations evolved,
and the current environments where
they are studied? Do hypotheses
stated in terms of fitness maximization in current environments provide an adequate
basis for the
study of adaptation?
References
1 Williams, CC. (1966) Adaptation and
Natural Selection: A Critique of Some
Current Evolutionary
Thought, Princeton
University Press
2 Alexander, R.D. (1987) The Biology of
Moral Systems, Aldine de Gruyter
3 Boone, I.L. (1988) in Human Reproductive
Behavior: A Darwinian Perspective (Betzig,
L., Borgerhoff-Mulder,
M. and Turke, P., eds),
pp. 201-220, Cambridge University Press
4 Hill, K. and Kaplan, H. (1988) in Human
Reproductive
Behavior A Darwinian
Perspective (Betzig, L., Borgerhoff-Mulder,
M. and Turke, P., eds), pp. 277-306,
Cambridge University Press
5 Crook, I. and Crook, S. (1988) in Human
Reproductive
Behavior: A Darwinian
Perspective (Betzig, L., Borgerhoff-Mulder,
M. and Turke, P.. eds), pp. 97-1 14,
Cambridge University Press
6 Irons, W. (1979) in Evolutionary Biology
and Human Social Behavior: An
AnthropologicalPerspective
(Chagnon, N.A.
and Irons, W., eds), pp. 4-38, Duxbury Press
7 Cosmides, L. and Tooby, J. in Biological
Perspectives on Motivated and Cognitive
Activities (Wong, R., ed.), Ablex (in press)
8 Symons, D. ( 1987) Sociobiology and
Psychology: Ideas, Issues, and Applications
(Crawford, C., Smith, M. and Krebs, D., eds),
pp. 121-146, Erlbaum Associates
9 Symons, D. (1989) Ethel. Sociobioi
IO,
131-144
10 Crawford, C. and Anderson, 1. (1989) Am.
Psycho/. 44, 1449-l 459
1I Tooby, I. and Cosmides, ). (1990) Ethoi
Sociobiol. I I, 375-424
12 Bernard, 1. ( 1988) Primates in the
Classroom: An Evolutionary Perspective,
The University of Massachusetts Press
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I79,90-92
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Guinness, FE. (1986) AnIm. Behav. 34,460-471
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15. I