After reading Gould and Lewontin’s “Spandrels of San Marco,” discuss its relationship to or implications for these topics:
– Grade and Clade
– Selection and Neutral Change
– Species and Speciation
as developed in lecture and lab. Discuss connections, including how the points you discuss weave through other answers to the question, “What is evolution?”
Proc. R. Soc. Lond. B 205, 581-598 (1979) 581
Printed in Creat Britain
The spandrels of San Marco and the Panglossian paradigm:
a critique of the adaptationist programme
BY S. J. GOULD AND R. C. LEWONTIN
Museum of Comparative Zoology, Harvard University,
Cambridge, Massachusetts 02138, U.S.A.
An adaptationist programme has dominated evolutionary thought in
England and the United States during the past 40 years. It is based on
faith in the power of natural selection as an optimizing agent. It proceeds
by breaking an organism into unitary ‘traits’ and proposing an adaptive
story for each considered separately. Trade-offs among competing
selective demands exert the onlv brake upon perfection; non-optimality
is thereby rendered as a result of adaptation as well. We criticize this
approach and attempt to reassert a competing notion (long popular in
continental Europe) that organisms must be analysed as integrated
wholes, with Bauplane so constrained by phyletic heritage, pathways of
development and general architecture that the constraints themselves
become more interesting and more important in delimiting pathways of
change than the selective force that may mediate change when it occurs.
We fault the adaptationist programme for its failure to distinguish current
utility from reasons for origin (male tyrannosaurs may have used their
diminutive front legs to titillate female partners, but this will not explain
why they got so small); for its unwillingness to consider alternatives to
adaptive stories; for its reliance upon plausibility alone as a criterion for
accepting speculative tales; and for its failure to consider adequately
such competing themes as random fixation of alleles, production of nonadaptive
structures by developmental correlation with selected features
(allometry, pleiotropy, material compensation, mechanically forced
correlation), the separability of adaptation and selection, multiple
adaptive peaks, and current utility as an epiphenomenon of non-adaptive
structures. We support Darwin’s own pluralistic approach to identifying
the agents of evolutionary change.
The great central dome of St Mark’s Cathedral in Venice presents in its mosaic
design a detailed iconography expressing the mainstays of Christian faith. Three
circles of figures radiate out from a central image of Christ: angels, disciples, and
virtues. Each circle is divided into quadrants, even though the dome itself is
radially symmetrical in structure. Each quadrant meets one of the four spandrels
in the arches below the dome. Spandrels – the tapering triangular spaces formed
by the intersection of two rounded arches at right angles (figure 1) – are necessary
architectural by-products of mounting a dome on rounded arches. Each spandrel
contains a design admirably fitted into its tapering space. An evangelist sits in the
[ 147 ]
582 S. J. Gould and R. C. Lewontin (Discussion Meeting)
upper part flanked by the heavenly cities. Below, a man representing one of the
four Biblical rivers (Tigris, Euphrates, Indus and Nile) pours water from a pitcher
into the narrowing space below his feet.
The design is so elaborate, harmonious and purposeful that we are tempted to
view it as the starting point of any analysis, as the cause in some sense of the
surrounding architecture. But this would invert the proper path of analysis. The
s S ! 6 _ …………………………………. ……….. . ] , , _ _ _ _ _~~~~~~~~~~. .. …
FIGURE 1. One of the four spandrels of St Mark’s; seated evangelist above,
personification of river below.
system begins with an architectural constraint: the necessary four spandrels and
their tapering triangular form. They provide a space in which the mosaicists
worked; they set the quadripartite symmetry of the dome above.
Such architectural constraints abound and we find them easy to understand
because we do not impose our biological biases upon them. Every fan vaulted
ceiling must have a series of open spaces along the mid-line of the vault, where
the sides of the fans intersect between the pillars (figure 2). Since the spaces must
exist, they are often used for ingenious ornamental effect. In King’s College Chapel
in Cambridge, for example, the spaces contain bosses altemately embellished with
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Critique of the adaptationist programme 583
the Tudor rose and portcullis. In a sense, this design represents an ‘adaptation’,
but the architectural constraint is clearly primary. The spaces arise as a necessary
by-product of fan vaulting; their appropriate use is a secondary effect. Anyone
who tried to argue that the structure exists because the alternation of rose and
portcullis makes so much sense in a Tudor chapel would be inviting the same
ridicule that Voltaire heaped on Dr Pangloss: ‘Things cannot be other than they
F~~~~~~~~~~~~~~~~~. ..i ..
FIGuRz 2. The ceiling of King’s College Chapel.
are… Everything is made for the best purpose. Our noses were made to carry
spectacles, so we have spectacles. Legs were clearly intended for breeches, and
we wear them.’ Yet evolutionary biologists, in their tendency to focus exclusively
on immediate adaptation to local conditions, do tend to ignore architectural
constraints and perform just such an inversion of explanation.
As a closer example, recently featured in some important biological literature
on adaptation, anthropologist Michael Harner has proposed (I977) that Aztec
human sacrifice arose as a solution to chronic shortage of meat (limbs of victims
were often consumed, but only by people of high status). E. 0. Wilson (1978) has
used this explanation as a primary illustration of an adaptive, genetic predisposition
for carnivory in humans. Harner and Wilson ask us to view an elaborate
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584 S. J. Gould and R. C. Lewontin (Discussion Meeting)
social system and a complex set of explicit justifications involving myth, symbol,
and tradition as mere epiphenomena generated by the Aztecs as an unconscious
rationalization masking the ‘real’ reason for it all: need for protein. But Sahlins
(1978) has argued that human sacrifice represented just one part of an elaborate
cultural fabric that, in its entirety, not only represented the material expression
of Aztec cosmology, but also performed such utilitarian functions as the maintenance
of social ranks and systems of tribute among cities.
We strongly suspect that Aztec cannibalism was an ‘adaptation’ much like
evangelists and rivers in spandrels, or ornamented bosses in ceiling spaces: a
secondary epiphenomenon representing a fruitful use of available parts, not a
cause of the entire system. To put it crudely: a system developed for other reasons
generated an increasing number of fresh bodies; use might as well be made of
them. Why invert the whole system in such a curious fashion and view an entire
culture as the epiphenomenon of an unusual way to beef up the meat supply.
Spandrels do not exist to house the evangelists. (Moreover, as Sahlins argues, it is
not even clear that human sacrifice was an adaptation at all. Human cultural
practices can be orthogenetic and drive towards extinction in ways that Darwinian
processes, based on genetic selection, cannot. Since each new monarch had to
outdo his predecessor in even more elaborate and copious sacrifice, the practice
was beginning to stretch resources to the breaking point, It would not have been
the first time that a human culture did itself in. And, finally, many experts doubt
Harner’s premise in the first place (Ortiz de Montellano 1978). They argue that
other sources of protein were not in short supply, and that a practice awarding
meat only to privileged people who had enough anyway, and who used bodies so
inefficiently (only the limbs were consumed, and partially at that) represents a
mighty poor way to run a butchery.)
We deliberately chose non-biological examples in a sequence running from
remote to more familiar: architecture to anthropology. We did this because the
primacy of architectural constraint and the epiphenomenal nature of adaptation
are not obscured by our biological prejudices in these examples. But we trust that
the message for biologists will not go unheeded: if these had been biological
systems, would we not, by force of habit, have regarded the epiphenomenal
adaptation as primary and tried to build the whole structural system from it?
2. THE ADAPTATIONIST PROGRAMME
We wish to question a deeply engrained habit of thinking among students of
evolution. We call it the adaptationist programme, or the Panglossian paradigm.
It is rooted in a notion popularized by A. R. Wallace and A. Weismann (but not,
as we shall see, by Darwin) towards the end of the nineteenth century: the near
omnipotence of natural selection in forging organic design and fashioning the best
among possible worlds. This programme regards natural selection as so powerful
and the constraints upon it so few that direct production of adaptation through
[ 150 ]
Crttique of the adaptationist programme 585
its operation becomes the primary cause of nearly all organic form, function, and
behaviour. Constraints upon the pervasive power of natural selection are recognized
of course (phyletic inertia primarily among them, although immediate architectural
constraints, as discussed in the last section, are rarely acknowledged). But they
are usually dimissed as unimportant or else, and more frustratingly, simply
acknowledged and then not taken to heart and invoked.
Studies under the adaptationist programme generally proceed in two steps:
(1) An organism is atomized into ‘traits’ and these traits are explained as
structures optimally designed by natural selection for their functions. For lack
of space, we must omit an extended discussion of the vital issue: ‘what is a trait?’
Some evolutionists may regard this as a trivial, or merely a semantic problem.
It is not. Organisms are integrated entities, not collections of discrete objects.
Evolutionists have often been led astray by inappropriate atomization, as D’Arcy
Thompson (1942) loved to point out. Our favourite example involves the human
chin (Gould I977, pp. 381-382; Lewontin 1978). If we regard the chin as a ‘thing’,
rather than as a product of interaction between two growth fields (alveolar and
mandibular), then we are led to an interpretation of its origin (recapitulatory)
exactly opposite to the one now generally favoured (neotenic).
(2) After the failure of part-by-part optimization, interaction is acknowledged
via the dictum that an organism cannot optimize each part without imposing
expenses on others. The notion of ‘trade-off’ is introduced, and organisms are
interpreted as best compromises among competing demands. Thus, interaction
among parts is retained completely within the adaptationist programme. Any
suboptimality of a part is explained as its contribution to the best possible design
for the whole. The notion that suboptimality might represent anything other than
the immediate work of natural selection is usually not entertained. As Dr Pangloss
said in explaining to Candide why he suffered from venereal disease: ‘It is indispensable
in this best of worlds. For if Columbus, when visiting the West Indies,
had not caught this disease, which poisons the source of generation, which frequently
even hinders generation, and is clearly opposed to the great end of Nature,
we should have neither chocolate nor cochineal.’ The adaptationist programme is
truly Panglossian. Our world may not be good in an abstract sense, but it is the
very best we could have. Each trait plays its part and must be as it is.
At this point, some evolutionists will protest that we are caricaturing their view
of adaptation. After all, do they not admit genetic drift, allometry, and a variety
of reasons for non-adaptive evolution? They do, to be sure, but we make a different
point. In natural history, all possible things happen sometimes; you generally do
not support your favoured phenomenon by declaring rivals impossible in theory.
Rather, you acknowledge the rival, but circumscribe its domain of action so
narrowly that it cannot have any importance in the affairs of nature. Then, you
often congratulate yourself for being such an undogmatic and ecumenical chap.
We maintain that alternatives to selection for best overall design have generally
been relegated to unimportance by this mode of argument. Have we not all heard
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586 S. J. Gould and R. C. Lewontin (Discussion Meeting)
the catechism about genetic drift: it can only be important in populations so
small that they are likely to become extinct before playing any sustained evolutionary
role (but see Lande I976).
The admission of alternatives in principle does not imply their serious consideration
in daily practice. We all say that not everything is adaptive; yet, faced
with an organism, we tend to break it into parts and tell adaptive stories as if
trade-offs among competing, well designed parts were the only constraint upon
perfection for each trait. It is an old habit. As Romanes complained about A. R.
Wallace in 1900: ‘Mr. Wallace does not expressly maintain the abstract impossibility
of laws and causes other than those of utility and natural selection…
Nevertheless, as he nowhere recognizes any other law or cause.. ., he practically
concludes that, on inductive or empirical grounds, there is no such other law or
cause to be entertained.’
The adaptationist programme can be traced through common styles of argument.
We illustrate just a few; we trust they will be recognized by all:
(1) If one adaptive argument fails, try another. Zig-zag commissures of clams
and brachiopods, once widely regarded as devices for strengthening the shell,
become sieves for restricting particles above a given size (Rudwick I964). A suite
of external structures (horns, antlers, tusks) once viewed as weapons against
predators, become symbols of intraspecific competition among males (Davitashvili
I96I). The eskimo face, once depicted as ‘cold engineered’ (Coon et al. I950),
becomes an adaptation to generate and withstand large masticatory forces (Shea
I977). We do not attack these newer interpretations; they may all be right. We do
wonder, though, whether the failure of one adaptive explanation should always
simply inspire a search for another of the same general form, rather than a consideration
of alternatives to the proposition that each part is ‘for’ some specific
(2) If one adaptive argument fails, assume that another must exist; a weaker
version of the first argument. Costa & Bisol (I978), for example, hoped to find a
correlation between genetic polymorphism and stability of environment in the
deep sea, but they failed. They conclude (I978, pp. 132, 133): ‘The degree of
genetic polymorphism found would seem to indicate absence of correlation with
the particular environmental factors which characterize the sampled area. The
results suggest that the adaptive strategies of organisms belonging to different
phyla are different.’
(3) In the absence of a good adaptive argument in the first place, attribute
failure to imperfect understanding of where an organism lives and what it does.
This is again an old argument. Consider Wallace on why all details of colour and
form in land snails must be adaptive, even if different animals seem to inhabit the
same environment (I899, p. 148): ‘The exact proportions of the various species of
plants, the numbers of each kind of insect or of bird, the peculiarities of more or
less exposure to sunshine or to wind at certain critical epochs, and other slight
differences which to us are absolutely immaterial and unrecognizable, may be of
[ 152 ]
Critique of the adaptationist programme 587
the highest significance to these humble creatures, and be quite sufficient to
require some slight adjustments of size, form, or colour, which natural selection
will bring about.’
(4) Emphasize immediate utility and exclude other attributes of form. Fully
half the explanatory information accompanying the full-scale Fibreglass Tyrannosaurus
at Boston’s Museum of Science reads: ‘Front legs a puzzle: how Tyrannosaurus
used its tiny front legs is a scientific puzzle; they were too short even to
reach the mouth. They may have been used to help the animal rise from a lying
position.’ (We purposely choose an example based on public impact of science to
show how widely habits of the adaptationist programme extend. We are not using
glass beasts as straw men; similar arguments and relative emphases, framed in
different words, appear regularly in the professional literature.) We don’t doubt
that Tyrannosaurus used its diminutive front legs for something. If they had
arisen de novo, we would encourage the search for some immediate adaptive
reason. But they are, after all, the reduced product of conventionally functional
homologues in ancestors (longer limbs of allosaurs, for example). As such, we do
not need an explicitly adaptive explanation for the reduction itself. It is likely to
be a developmental correlate of allometric fields for relative increase in head and
hindlimb size. This non-adaptive hypothesis can be tested by conventional
allometric methods (Gould (I974) in general; Lande (1978) on limb reduction) and
seems to us both more interesting and fruitful than untestable speculations based
on secondary utility in the best of possible worlds. One must not confuse the fact
that a structure is used in some way (consider again the spandrels, ceiling spaces
and Aztec bodies) with the primary evolutionary reason for its existence and
3. TELLING STORIES
‘All this is a manifestation of the rightness of things, since if there is a volcano
at Lisbon it could not be anywhere else. For it is impossible for things not to be
where they are, because everything is for the best’ (Dr Pangloss on the great
Lisbon earthquake of 1755 in which up to 50000 people lost their lives).
We would not object so strenuously to the adaptationist programme if its
invocation, in any particular case, could lead in principle to its rejection for want
of evidence. We might still view it as restrictive and object to its status as an
argument of first choice. But if it could be dismissed after failing some explicit
test, then alternatives would get their chance. Unfortunately, a common procedure
among evolutionists does not allow such definable rejection for two reasons. First,
the rejection of one adaptive story usually leads to its replacement by another,
rather than to a suspicion that a different kind of explanation might be required.
Since the range of adaptive stories is as wide as our minds are fertile, new stories
can always be postulated. And if a story is not immediately available, one can
always plead temporary ignorance and trust that it will be forthcoming, as did
Costa & Bisol (1978), cited above. Secondly, the criteria for acceptance of a story
588 S. J. Gould and R. C. Lewontin (Discussion Meeting)
are so loose that many pass without proper confirmation. Often, evolutionists
use consistency with natural selection as the sole criterion and consider their work
done when they concoct a plausible story. But plausible stories can always be told.
The key to historical research lies in devising criteria to identify proper explanations
among the substantial set of plausible pathways to any modern result.
We have, for example (Gould I978) criticized Barash’s (I976) work on aggression
in mountain bluebirds for this reason. Barash mounted a stuffed male near the nests
of two pairs of bluebirds while the male was out foraging. He did this at the same
nests on three occasions at 10 day intervals: the first before eggs were laid, the
last two afterwards. He then counted aggressive approaches of the returning male
towards both the model and the female. At time one, aggression was high towards
the model and lower towards females but substantial in both nests. Aggression
towards the model declined steadily for times two and three and plummeted to
near zero towards females. Barash reasoned that this made evolutionary sense
since males would be more sensitive to intruders before eggs were laid than afterwards
(when they can have some confidence that their genes are inside). Having
devised this plausible story, he considered his work as completed (I976, pp. 1099,
‘The results are consistent with u. 3xpectations of evolutionary theory.
Thus aggression toward an intruding male (the model) would clearly be especially
advantageous early in the breeding season, when territories and nests are
normally defended … The initial aggressive response to the mated female is also
adaptive in that, given a situation suggesting a high probabiiity of adultery
(i.e. the presence of the model near the female) and assuming that replacement
females are available, obtaining a new mate would enhance the fitness of males…
The decline in male-female aggressiveness during incubation and fledgling stages
could be attributed to the impossibility of being cuckolded after the eggs have
been laid… The results are consistent with an evolutionary interpretation.’
They are indeed consistent, but what about an obvious alternative, dismissed
without test by Barash? Male returns at times two and three, approaches the
model, tests it a bit, recognizes it as the same phoney he saw before, and doesn’t
bother his female. Why not at least perform the obvious test for this alternative
to a conventional adaptive story: expose a male to the model for the first time
after the eggs are laid.
Since we criticized Barash’s work, Morton et al. (I978) repeated it, with some
variations (including the introduction of a female model), in the closely related
eastern bluebird Sialia sialis. ‘We hoped to confirm’, they wrote, that Barash’s
conclusions represent ‘a widespread evolutionary reality, at least within the genus
Sialia. Unfortunately, we were unable to do so.’ They found no ‘anticuckoldry’
behaviour at all: males never approached their females aggressively after testing
the model at any nesting stage. Instead, females often approached the male model
and, in any case, attacked female models more than males attacked male models.
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Critique of the adaptationist programme 589
‘This violent response resulted in the near destruction of the female model after
presentations and its complete demise on the third, as a female flew off with the
model’s head early in the experiment to lose it for us in the brush’ (1978, p. 969).
Yet, instead of calling Barash’s selected story into question, they merely devise
one of their own to render both results in the adaptationist mode. Perhaps, they
conjecture, replacement females are scarce in their species and abundant in
Barash’s. Since Barash’s males can replace a potentially ‘unfaithful’ female, they
can afford to be choosy and possessive. Eastern bluebird males are stuck with
uncommon mates and had best be respectful. They conclude: ‘If we did not
support Barash’s suggestion that male bluebirds show anticuckoldry adaptations,
we suggest that both studies still had “results that are consistent with the expectations
of evolutionary theory” (Barash 1976, p. 1099), as we presume any
careful study would.’ But what good is a theory that cannot fail in careful study
(since by ‘evolutionary theory’, they clearly mean the action of natural selection
applied to particular cases, rather than the fact of transmutation itself).
4. THE MASTER’S VOICE RE-EXAMINED
Since Darwin has attained sainthood (if not divinity) among evolutionary
biologists, and since all sides invoke God’s allegiance, Darwin has often been
depicted as a radical selectionist at heart who invoked other mechanisms only in
retreat, and only as a result of his age’s own lamented ignorance about the
mechanisms of heredity. This view is false. Although Darwin regarded selection
as the most important of evolutionary mechanisms (as do we), no argument from
opponents angered him more than the common attempt to caricature and trivialize
his theory by stating that it relied exclusively upon natural selection. In the last
edition of the Origin, he wrote (I872, p. 395):
‘As my conclusions have lately been much misrepresented, and it has been
stated that I attribute the modification of species exclusively to natural selection,
I may be permitted to remark that in the first edition of this work, and subsequently,
I placed in a most conspicuous position – namely at the close of the
Introduction -the following words: “I am convinced that natural selection
has been the main, but not the exclusive means of modification.” This has been
of no avail. Great is the power of steady misinterpretation.’
Romanes, whose once famous essay (I900) on Darwin’s pluralism versus the
panselectionism of Wallace and Weismann deserves a resurrection, noted of this
passage (i900, p. 5): ‘In the whole range of Darwin’s writings there cannot be
found a passage so strongly worded as this: it presents the only note of bitterness
in all the thousands of pages which he has published.’ Apparently, Romanes did
not know the letter Darwin wrote to Nature in 1880, in which he castigated Sir
Wyville Thomson for caricaturing his theory as panselectionist (i88o, p. 32):
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590 S. J. Gould and R. C. Lewontin (Discussion Meeting)
‘I am sorry to find that Sir Wyville Thomson does not understand the principle
of natural selection … If he had done so, he could not have written the following
sentence in the Introduction to the Voyage of the Challenger: “The character
of the abyssal fauna refuses to give the least support to the theory which refers
the evolution of species to extreme variation guided only by natural selection.”
This is a standard of criticism not uncommonly reached by theologians and
metaphysicians when they write on scientific subjects, but is something new
as coming from a naturalist… Can Sir Wyville Thomson name any one who
has said that the evolution of species depends only on natural selection? As far
as concerns myself, I believe that no one has brought forward so many observations
on the effects of the use and disuse of parts, as I have done in my ” Variation
of Animals and Plants under Domestication”; and these observations were
made for this special object. I have likewise there adduced a considerable body
of facts, showing the direct action of external conditions on organisms.’
We do not now regard all of Darwin’s subsidiary mechanisms as significant or
even valid, though many, including direct modification and correlation of growth,
are very important. But we should cherish his consistent attitude of pluralism
in attempting to explain Nature’s complexity.
5. A PARTIAL TYPOLOGY OF ALTERNATIVES TO THE
In Darwin’s pluralistic spirit, we present an incomplete hierarchy of alternatives
to immediate adaptation for the explanation of form, function, and behaviour.
(1) No adaptation and no selection at all. At present, population geneticists are
sharply divided on the question of how much genetic polymorphism within
populations and how much of the genetic differences between species is, in fact,
the result of natural selection as opposed to purely random factors. Populations
are finite in size and the isolated populations that form the first step in the
speciation process are often founded by a very small number of individuals. As a
result of this restriction in population size, frequencies of alleles change by genetic
drift, a kind of random genetic sampling error. The stochastic process of change in
gene frequency by random genetic drift, including the very strong sampling process
that goes on when a new isolated population is formed from a few immigrants, has
several important consequences. First, populations and species will become
genetically differentiated, and even fixed for different alleles at a locus in the complete
absence of any selective force at all.
Secondly, alleles can become fixed in a population in spite of natural selection.
Even if an allele is favoured by natural selection, some proportion of population,
depending upon the product of population size N and selection intensity s, will
become homozygous for the less fit allele because of genetic drift. If Ns is
large this random fixation for unfavourable alleles is a rare phenomenon, but if
Critique of the adaptationist programme 591
selection coefficients are on the order of the reciprocal of population size (Ns = 1)
or smaller, fixation for deleterious alleles is common. If many genes are involved
in influencing a metric character like shape, metabolism or behaviour, then the
intensity of selection on each locus will be small and Ns per locus may be small.
As a result, many of the loci may be fixed for non-optimal alleles.
Thirdly, new mutations have a small chance of being incorporated into a
population, even when selectively favoured. Genetic drift causes the immediate
loss of most new mutations after their introduction. With a selection intensity s,
a new favourable mutation has a probability of only 2s of ever being incorporated.
Thus, one cannot claim that, eventually, a new mutation of just the right sort for
some adaptive argument will occur and spread. ‘Eventually’ becomes a very long
time if only one in 1000 or one in 10000 of the ‘right’ mutations that do occur
ever get incorporated in a population.
(2) No adaptation and no selection on the part at issue; form of the part is a
correlated consequence of selection directed elsewhere. Under this important
category, Darwin ranked his ‘mysterious’ laws of the ‘correlation of growth’.
Today, we speak of pleiotropy, allometry, ‘material compensation’ (Rensch 1959,
pp. 179-187) and mechanically forced correlations in D’Arcy Thompson’s sense
(1942; Gould 1971). Here we come face to face with organisms as integrated
wholes, fundamentally not decomposable into independent and separately optimized
Although allometric patterns are as subject to selection as static morphology
itself (Gould i966), some regularities in relative growth are probably not under
immediate adaptive control. For example, we do not doubt that the famous 0.66
interspecific allometry of brain size in all major vertebrate groups represents a
selected ‘design criterion,’ though its significance remains elusive (Jerison 1973).
It is too repeatable across too wide a taxonomic range to represent much else than
a series of creatures similarly well designed for their different sizes. But another
common allometry, the 0.2 to 0.4 intraspecific scaling among homeothermic
adults differing in body size, or among races within a species, probably does not
require a selectionist story though many, including one of us, have tried to
provide one (Gould 1974). R. Lande (personal communication) has used the
experiments of Falconer (1973) to show that selection upon body size alone yields
a brain-body slope across generations of 0.35 in mice.
More compelling examples abound in the literature on selection for altering the
timing of maturation (Gould 1977). At least three times in the evolution of arthropods
(mites, flies and beetles), the same complex adaptation has evolved, apparently
for rapid turnover of generations in strongly r-selected feeders on superabundant
but ephemeral fungal resources: females reproduce as larvae and grow the next
generation within their bodies. Offspring eat their mother from inside and emerge
from her hollow shell, only to be devoured a few days later by their own progeny.
It would be foolish to seek adaptive significance in paedomorphic morphology per
se; it is primarily a by-product of selection for rapid cycling of generations. In
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592 S. J. Gould and R. C. Lewontin (Discussion Meeting)
more interesting cases, selection for small size (as in animals of the interstitial
fauna) or rapid maturation (dwarf males of many crustaceans) has occurred by
progenesis (Gould I977, pp. 324-336), and descendant adults contain a mixture
of ancestral juvenile and adult features. Many biologists have been tempted to
find primary adaptive meaning for the mixture, but it probably arises as a byproduct
of truncated maturation, leaving some features ‘behind’ in the larval
state, while allowing others, more strongly correlated with sexual maturation,
to retain the adult configuration of ancestors.
(3) The decoupling of selection and adaptation.
(i) Selection without adaptation. Lewontin (I979) has presented the following
hypothetical example: ‘A mutation which doubles the fecundity of individuals
will sweep through a population rapidly. If there has been no change in efficiency
of resource utilization, the individuals will leave no more offspring than before,
but simply lay twice as many eggs, the excess dying because of resource limitation.
In what sense are the individuals or the population as a whole better adapted
than before? Indeed, if a predator on immature stages is led to switch to the species
now that immatures are more plentiful, the population size may actually decrease
as a consequence, yet natural selection at all times will favour individuals with
(ii) Adaptation without selection. Many sedentary marine organisms, sponges
and corals in particular, are well adapted to the flow regimes in which they live.
A wide spectrum of ‘good design’ may be purely phenotypic in origin, largely
induced by the current itself. (We may be sure of this in numerous cases, when
genetically identical individuals of a colony assume different shapes in different
microhabitats.) Larger patterns of geographic variation are often adaptive and
purely phenotypic as well. Sweeney & Vannote (1978), for example, showed that
many hemimetabolous aquatic insects reach smaller adult size with reduced
fecundity when they grow at temperatures above and below their optima. Coherent,
climatically correlated patterns in geographic distribution for these insects – so
often taken as a priori signs of genetic adaptation – may simply reflect this
‘Adaptation’ – the good fit of organisms to their environment – can occur at
three hierarchical levels with different causes. It is unfortunate that our language
has focused on the common result and called all three phenomena ‘adaptation’:
the differences in process have been obscured and evolutionists have often been
misled to extend the Darwinian mode to the other two levels as well. First, we
have what physiologists call ‘adaptation’: the phenotypic plasticity that permits
organisms to mould their form to prevailing circumstances during, ontogeny.
Human ‘adaptations’ to high altitude fall into this category (while others, like
resistance of sickling heterozygotes to malaria, are genetic and Darwinian).
Physiological adaptations are not heritable, though the capacity to develop them
presumably is. Secondly, we have a ‘heritable’ form of non-Darwinian adaptation
in humans (and, in rudimentary ways, in a few other advanced social species):
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Critique of the adaptationist programme 593
cultural adaptation (with heritability imposed by learning). Much confused
thinking in human sociobiology arises from a failure to distinguish this mode from
Darwinian adaptation based on genetic variation. Finally, we have adaptation
arising from the conventional Darwinian mechanism of selection upon genetic
variation. The mere existence of a good fit between organism and environment is
insufficient evidence for inferring the action of natural selection.
(4) Adaptation and selection but no selective basis for differences among
adaptations. Species of related organisms, or subpopulations within a species,
often develop different adaptations as solutions to the same problem. When
‘multiple adaptive peaks’ are occupied, we usually have no basis for asserting
that one solution is better than another. The solution followed in any spot is a
result of history; the first steps went in one direction, though others would have
led to adequate prosperity as well. Every naturalist has his favourite illustration.
In the West Indian land snail Cerion, for example, populations living on rocky
and windy coasts almost always develop white, thick and relatively squat shells
for conventional adaptive reasons. We can identify at least two different developmental
pathways to whiteness from the mottling of early whorls in all Cerion,
two paths to thickened shells and three styles of allometry leading to squat shells.
All 12 combinations can be identified in Bahamian populations, but would it
be fruitful to ask why – in the sense of optimal design rather than historical
contingency – Cerion from eastern Long Island evolved one solution, and Cerion
from Acklins Island another?
(5) Adaptation and selection, but the adaptation is a secondary utilization of
parts present for reasons of architecture, development or history. We have already
discussed this neglected subject in the first section on spandrels, spaces and
cannibalism. If blushing turns out to be an adaptation affected by sexual selection
in humans, it will not help us to understand why blood is red. The immediate
utility of an organic structure often says nothing at all about the reason for its being.
6. ANOTHER, AND UNFAIRLY MALIGNED, APPROACH TO EVOLUTION
In continental Europe, evolutionists have never been much attracted to the
Anglo-American penchant for atomizing organisms into parts and trying to
explain each as a direct adaptation. Their general alternative exists in both a
strong and a weak form. In the strong form, as advocated by such major theorists
as Schindewolf (1950), Remane (1971), and Grasse (1977), natural selection under
the adaptationist programme can explain superficial modifications of the Bauplan
that fit structure to environment: why moles are blind, giraffes have long necks,
and ducks webbed feet, for example. But the important steps of evolution, the
construction of the Bauplan itself and the transition between Bauplane, must
involve some other unknown, and perhaps ‘internal’, mechanism. We believe that
English biologists have been right in rejecting this strong form as close to an appeal
20 [159 ] Vol. 205 B.
594 S. J. Gould and R. C. Lewontin (Discussion Meeting)
But the argument has a weaker – and paradoxically powerful – form that has
not been appreciated, but deserves to be. It also acknowledges conventional
selection for superficial modifications of the Bauplan. It also denies that the
adaptationist programme (atomization plus optimizing selection on parts) can do
much to explain Baupldne and the transitions between them. But it does not
therefore resort to a fundamentally unknown process. It holds instead that the
basic body plans of organisms are so integrated and so replete with constraints
upon adaptation (categories 2 and 5 of our typology) that conventional styles of
selective arguments can explain little of interest about them. It does not deny
that change, when it occurs, may be mediated by natural selection, but it holds
that constraints restrict possible paths and modes of change so strongly that the
constraints themselves become much the most interesting aspect of evolution.
Rupert Riedl, the Austrian zoologist who has tried to develop this thesis for
English audiences (1977 and I975, now being translated into English by R.
‘The living world happens to be crowded by universal patterns of organization
which, most obviously, find no direct explanation through environmental conditions
or adaptive radiation, but exist primarily through universal requirements
which can only be expected under the systems conditions of complex organization
itself … This is not self-evident, for the whole of the huge and profound thought
collected in the field of morphology, from Goethe to Remane, has virtually
been cut off from modern biology. It is not taught in most American universities.
Even the teachers who could teach it have disappeared.’
Constraints upon evolutionary change may be ordered into at least two categories.
All evolutionists are familiar with phyletic constraints, as embodied in
Gregory’s classic distinction (1936) between habitus and heritage. We acknowledge
a kind of phyletic inertia in recognizing, for example, that humans are not
optimally designed for upright posture because so much of our Bauplan evolved
for quadrupedal life. We also invoke phyletic constraint in explaining why no
molluscs fly in air and no insects are as large as elephants.
Developmental constraints, a subcategory of phyletic restrictions, may hold the
most powerful rein of all over possible evolutionary pathways. In complex
organisms, early stages of ontogeny are remarkably refractory to evolutionary
change, presumably because the differentiation of organ systems and their
integration into a functioning body is such a delicate process, so easily derailed
by early errors with accumulating effects. Von Baer’s fundamental embryological
laws (i8z8) represent little more than a recognition that early stages are both
highly conservative and strongly restrictive of later development. Haeckel’s
biogenetic law, the primary subject of late nineteenth century evolutionary
biology, rested upon a misreading of the same data (Gould I977). If development
occurs in integrated packages, and cannot be pulled apart piece by piece in
evolution, then the adaptationist programme cannot explain the alteration of
developmental programmes underlying nearly all changes of Bauplan.
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Critique of the adaptationist programme 595
The German palaeontologist A. Seilacher, whose work deserves far more attention
than it has received, has emphasized what he calls ‘ bautechnischer’, or architectural,
constraints (Seilacher I 970). These arise not from former adaptations retained in
a new ecological setting (phyletic constraints as usually understood), but as
architectural restrictions that never were adaptations, but rather the necessary
consequences of materials and designs selected to build basic Baupline. We devoted
Dtwlcelalype Yoldia TYpO Fabuilna Type oecurtuseTpe
FIGURE 3. The range of divaricate patterns in molluscs. E, F, H, and L are non-functional in
Seilacher’s judgement. A-D are functional ribs (but these are far less common than nonfunctional
ribs of the form E). G is the mimetic Arca zebra. K is Corculum. See text for
the first section of this paper to non-biological examples in this category. Spandrels
must exist once a blueprint specifies that a dome shall rest on rounded arches.
Architectural constraints can exert a far-ranging influence upon organisms as well.
The subject is full of potential insight because it has rarely been acknowledged at
In a fascinating example, Seilacher (I972) has shown that the divaricate form
of architecture (figure 3) occurs again and again in all groups of molluscs, and in
brachiopods as well. This basic form expresses itself in a wide variety of structures:
raised ornamental lines (not growth lines because they do not conform to the
[ 161 ] 20-2
596 S. J. Gould and R. C. Lewontin (Discussion Meeting)
mantle margin at any time), patterns of coloration, internal structures in the
mineralization of calcite, and incised grooves. He does not know what generates
this pattern and feels that traditional and nearly exclusive focus on the adaptive
value of each manifestation has diverted attention from questions of its genesis
in growth and also prevented its recognition as a general phenomenon. It must
arise from some characteristic pattern of inhomogeneity in the growing mantle,
probably from the generation of interference patterns around regularly spaced
centres; simple computer simulations can generate the form in this manner
(Waddington & Cowe I969). The general pattern may not be a direct adaptation
Seilacher then argues that most manifestations of the pattern are probably
non-adaptive. His reasons vary, but seem generally sound to us. Some are based
on field observations: colour patterns that remain invisible because clams possessing
them either live buried in sediments or remain covered with a periostracum so
thick that the colours cannot be seen. Others rely on more general principles:
presence only in odd and pathological individuals, rarity as a developmental
anomaly, excessive variability compared with much reduced variability when the
same general structure assumes a form judged functional on engineering grounds.
In a distinct minority of cases, the divaricate pattern becomes functional in
each of the four categories (figure 3). Divaricate ribs may act as scoops and
anchors in burrowing (Stanley I970), but they are not properly arranged for
such function in most clams. The colour chevrons are mimetic in one species
(Pteria zebra) that lives on hydrozoan branches; here the variability is strongly
reduced. The mineralization chevrons are probably adaptive in only one remarkable
creature, the peculiar bivalve Corculum cardissa (in other species, they either
appear in odd specimens or only as post-mortem products of shell erosion). This
clam is uniquely flattened in an anterio-posterior direction. It lies on the substrate,
posterior up. Distributed over its rear end are divaricate triangles of mineralization.
They are translucent, while the rest of the shell is opaque. Under these windows
dwell endosymbiotic algae!
All previous literature on divaricate structure has focused on its adaptive
significance (and failed to find any in most cases). But Seilacher is probably right
in representing this case as the spandrels, ceiling holes and sacrificed bodies of
our first section. The divaricate pattern is a fundamental architectural constraint.
Occasionally, since it is there, it is used to beneficial effect. But we cannot understand
the pattern or its evolutionary meaning by viewing these infrequent and
secondary adaptations as a reason for the pattern itself.
Galton (I909, p. 257) contrasted the adaptationist programme with a focus on
constraints and modes of development by citing a telling anecdote about Herbert
‘Much has been written, but the last word has not been said, on the rationale
of these curious papillary ridges; why in one man and in one finger they form
whorls and in another loops. I may mention a characteristic anecdote of Herbert
[ 162 ]
Critique of the adaptationist programme 597
Spencer in connection with this. He asked me to show him my Laboratory
and to take his prints, which I did. Then I spoke of the failure to discover the
origin of these patterns, and how the fingers of unborn children had been
dissected to ascertain their earliest stages, and so forth. Spencer remarked that
this was beginning in the wrong way; that I ought to consider the purpose the
ridges had to fulfil, and to work backwards. Here, he said, it was obvious that
the delicate mouths of the sudorific glands required the protection given to them
by the ridges on either side of them, and therefrom he elaborated a consistent
and ingenious hypothesis at great length. I replied that his arguments were
beautiful and deserved to be true, but it happened that the mouths of the ducts
did not run in the valleys between the crests, but along the crests of the ridges
We feel that the potential rewards of abandoning exclusive focus on the
adaptationist programme are very great indeed. We do not offer a council of
despair, as adaptationists have charged; for non-adaptive does not mean nonintelligible.
We welcome the richness that a pluralistic approach, so akin to
Darwin’s spirit, can provide. Under the adaptationist programme, the great
historic themes of developmental morphology and Bauplan were largely abandoned;
for if selection can break any correlation and optimize parts separately,
then an organism’s integration counts for little. Too often, the adaptationist
programme gave us an evolutionary biology of parts and genes, but not of organisms.
It assumed that all transitions could occur step by step and underrated the
importance of integrated developmental blocks and pervasive constraints of
history and architecture. A pluralistic view could put organisms, with all their
recalcitrant, yet intelligible, complexity, back into evolutionary theory.
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[ 164 ]
After reading Gould and Lewontin’s “Spandrels of San Marco,” discuss its relationship to or implications for these topics: