AM. ZOOLOGIST, 9:261-267
(1969).
Of Foxes and Hedgehogs:
The Interface Between Organismal and Populational Biology—II
PETER MARLER
New York Zoological Society and Rockefeller University, New York, N. Y. 10021
My assignment is to consider the interface from the viewpoint of a populational
biologist—in so far as an animal behaviorist can represent that position—and I
should like to begin by quoting a zoologism from an essay that Isaiah Berlin
wrote in 1951 on Tolstoy. He tells us that,
"There is a line among the fragments of
the Greek poet, Archilochus, which says:
'The fox knows many things, but the
hedgehog knows one big thing.' Scholars
have differed about the correct interpretation of these dark words, which may mean
no more than that the fox, for all his
cunning, is defeated by the hedgehog's one
defense. But, taken figuratively, the words
can be made to yield a sense in which
they mark one of the deepest differences
which divide writers and thinkers, and, it
may be, human beings in general."
He goes on to propose that Tolstoy's
greatness stems from being a fox by nature
yet striving to be a hedgehog. I want to
suggest that a similar ideal may be appropriate for scientists as well. I think of the
typical organismal biologist as something
of a fox, elucidating the structural or
physiological basis of some property of the
organism, finding his ultimate satisfaction
in the completion of that undertaking, and
then seeking another knot to unravel. He
is inclined to be an empiricist. Ecologists,
evolutionary biologists, and some animal
behaviorists are more often, I think,
hedgehogs, grappling with unknowns
which the individual investigator can rarely hope to understand completely even in a
lifetime. Here we find more theorizing
and—dare I say it—a certain proclivity
towards mysticism. Thus, I wish to distinguish organismal and populational biologists on the basis of their predominant
261
methodology rather than on the basis of
their subject matter, although it is obvious
that the two are interdependent, and that
the biases of each are productive and appropriate to the nature of the problems
with which they deal.
It should be clear that I am not trying to
make a distinction between good and bad
research. I take it for granted that all good
research has relevance beyond its immediate context, whatever the level of analysis. I
am thinking, rather, of the strategy that
guides the choice of direction in which to
pursue a problem, once initiated. The inclination to pursue a reductionist approach is characteristically that of a fox. A
hedgehog will more readily look in the
other direction, to the more emergent
properties of the phenomenon under
study. Whether a biologist is working with
populations, or at the organizational or
molecular level, he can work creatively
with either approach, but populational biology seems to be a special haven for
hedgehogs, presumably because of the
nature of the problems in the area.
I want to press the case for breeding
more hybrids, or should I say for training
"fedgehoxes", who will be organismal biologists with an evolutionary approach to
their subject, and populational biologists,
bringing all of the special methods and
insights of organismal biologists to the
problems they study.
I feel some urgency about this need. All
over the country, and I suppose all over
the world, the curricula in introductory
biology are being revised to incorporate
the fruits of the revolution in molecular
biology. Inevitably some changes have to
be made to make way for the new material,
usually some facet of organismal biology.
262
PETER MARLER
In my experience, comparative anatomy is
one of the first casualties in the curriculum
for biologists. I understand that the
weight of new advances in medicine is
causing some neglect of human anatomy in
medical training. There are often, of
course, excellent reasons for this neglect.
Comparative anatomy is now, with some
exceptions, a pursuit of rather pure-bred
foxes, and not many of them at that. No
doubt the lectures are often dull. Can we
jettison this huge body of knowledge with
a clear conscience? I think that would be
tragic. T h e material needs to be reintegrated with other viewpoints, in courses
concerned with this hybrid zone between
organismal and populational biology, in
neurophysiology and behavior, evolution,
and physiological ecology. I found Malcom
Gordon's recent book, Animal
Function,
Principles and Adaptations, an exciting
step forward and no doubt others are moving in the same direction.
As in teaching, so in research, Dr.
Kennedy has given in the first paper in
this symposium many examples of the kind
of exciting advances that organismal biologists can accomplish if they bear in mind
the physical and social environments in
which the organism usually functions and
which have directed its evolution. I would
like to give a few instances where the populational biologist can usefully look to the
organismal biologist for new insights. Some
are obvious.
For example, anyone concerned with the
interrelationship between organisms and
their environment cannot afford to ignore
•what physiologists tell us about the sensory
world of animals. One could cite endless
examples. Let me give just one. Ethologists
find that some reactions are controlled by
surprisingly specific external stimuli, or socalled releasers, and much effort has gone
into behavioral experimentation to determine which stimulus-parameters are relevant. A good deal of this effort is often
wasted because of lack of appreciation of
the physiological operation of the sense
organs. 1 feel this to be true of some work
on visual releasers, for example, where appropriate cooperation with the physiologist
holds great promise. Similarly in audition, interplay between the organismal and
the populational biologist has tremendous
potential. Consider the songs of Orthoptera, particularly the tree crickets, as
studied by Walker (1957).
In favorable localities in the southeastern United States one can hear as
many as 20 different species of tree crickets calling at the same time. Although both
males and females can produce some
sounds, the most conspicuous contribution
to the din on summer evenings in such
places comes from what is known as the
calling song of the males, which serves the
function in these tree crickets of attracting females to males when they are ready
for mating. This attractiveness is readily demonstrated experimentally as Dr.
Thomas Walker has shown. A cage approximately three feet long is fitted with
loudspeakers at each end and a reproductive female is released in the center. One
loudspeaker transmits recordings of songs of
a male of her own species; the other, songs
of another species. She will quite reliably
move towards the song of her own kind.
This song functions, then, in reproductive
isolation, and such a function carries certain requirements. If females were to respond indiscriminately to the songs of any
males they heard, time would be wasted
and reproduction would be ineffective, for
hybrids would probably be poorly adapted
or infertile, if indeed they ever developed
into adult form. I should interject that
these strictures on hybrid viability are not
applicable to fedgehoxes which are cultural rather than genetic hybrids, although
a potential role in reproductive isolation
might be argued for some behavioral traits
of our more creative young people. In
crickets, however, a mechanism is clearly
required to restrict the female's choice to
sounds of her species.
Investigation reveals that males of each
species have a particular pulse rate in their
song, and it is to this rate that the female
responds. Experiments with artificial songs
OF FOXES AND HEDCEHOCS
show that it does not matter what the
frequency of pulses is, as long as the rate is
correct, a puzzle until it is recognized that
the tympanal organs are hardly if at all
responsive to variations in frequency, within the range that they can hear. Thus, the
behaviorist gains from knowledge of
physiological data. But there are further
questions that challenge the physiologist.
What is the neural basis of this speciesspecific responsiveness? Although the basic
behavioral situation is simple, there are
further refinements that require physiological explanation. The rate of many of the
metabolic processes of these crickets is of
course a function of temperature. The
pulse rate in the song changes with temperature, as implied by the name that
some species have earned of "thermometer
crickets". The changes in rate with temperature are quite drastic, and one might
think that this would throw a female seeking a mate into hopeless confusion. In fact,
the physiological mechanism which determines her responsiveness changes with
temperature in a fashion parallel to the
change in the pulse rate of the male's
song, thus avoiding confusion.
Incidentally this dependence on temperature provides neat proof that the pulse
rate is the only character to which females
are responding. The quality of the individual syllables or pulses in some species
sounds different to our ears, and it would
seem reasonable to suppose that the crickets themselves are even more sensitive to
such subtle characteristics. Suppose that
the male of a given species, A, normally
sings with a pulse rate of 50 pulses per
second at 70°F. We can take a male of
another species, B, whose pulse rate is normally slower than this and warm him up
until his pulse rate is also 50 per second.
This can be recorded and played to a female of species A at 70°F. She will respond
normally, even though the pulse structure
is that of another species.
Here and elsewhere, the sensory basis of
specific responsiveness to signals, whether
the particular Hash patterns in fireflies
263
(Buck, 1937; Lloyd, 1966) or the speciesspecific songs of birds, poses a host of basic
problems for the organismal biologist.
Some of the most exciting advances in sensory physiology, our President's work, for
example (Dethier, 1963) or that of Hartline and co-workers (Hartline, 1938; Hartline, Wagner, and Ratliff, 1956; Ratliff,
1965), Hubel and Wiesel (1959, 1962),
Barlow (1953«, b), and Maturana, Lettvin,
McCulloch, and Pitts (1960) on vision,
stem from appreciation of the behavioral
demands placed on sense organs in their
natural environment. With audition, Capranica (1965, 1968) and Frishkopf, Capranica, and Goldstein (1968) have made an exciting start in relating electrophysiological
studies of hearing in frogs to the neural basis of the specific responsiveness of bullfrogs
to playback or recorded calls of the males.
Manning (1967) commented on the fruitfulness of this approach in his recent and
excellent little book on animal behavior,
noting that the training in behavior that
physiologists receive often goes no farther
than the classical reflexes. It is still the
exceptional individual who crosses interdepartmental boundaries to get some experience in broader aspects of animal behavior.
We could make the same point with regard to reproductive physiology and other
aspects of endocrinology. It would be ridiculous for anyone studying processes of
reproduction in nature to neglect recent
advances in this aspect of organismal biology. The work of Beach, Hinde, and
Lehrman, for example is based on the premise that to understand the behavior, you
must take account of the associated endocrine changes (e.g., Beach, 1965; Hinde,
1967; Lehrman, 1961). And conversely,
such work, carefully done, can pose new
problems for the endocrinologist.
One example is Adler's discovery that a
female rat who is exposed to the customary
multiple intromissions by the male before
he ejaculates is more likely to bear young
than a female who simply gets a single
intromission with ejaculation. Further
study reveals that two mechanisms are in-
264
PETER MARLER
volved. Implantation is more likely to be
successful in the former because the intromissions initiate a neuroendocrine reflex
that results in the secretion of progesterone. In addition, the pre-ejaculatory intromissions facilitate entry of sperm into
the cervix, possibly by stimulating the release of oxytocin. Interestingly enough, in
species in which there are typically several
intromissions prior to ejaculation, such as
rats, hamsters, and mice, the female has a
short estrous cycle without a true luteal
phase. In the chinchilla and the guinea pig,
on the other hand, the male typically ejaculates with but one intromission, and females have a long luteal phase and sufficient levels of progesterone without copulatory stimulation (Adler, in press).
The open discussion on maternal behavior conducted by Dr. Jay Rosenblatt at the
A.A.A.S. meeting in Dallas (1968), brought
to light the inadequacy of the present hormonal picture of pregnancy and parturition to explain, for example, the ease with
which parental behavior can be induced in
virgin rats by exposure to pups, even in a
virgin which has been both gonadectomized and hypophysectomized.
With environmental physiology too,
there is obvious interplay with the ecologist—in fact there are already fedgehoxes
in this field, but there are many foxes
too—and here also a case could be made
for more traffic between organismal and
populational biologists. Suppose that a
difference is demonstrated in tolerance for
desiccation in two populations of some
species, which correlates with habitat, how
should one proceed? A reductionist view of
such physiological mechanisms is clearly
fruitful. Another possibility is to take the
populational biologist's approach and try
to retrace the history of difference. This is
very difficult to do and one reason is that
we still do not really know how to identify
the unit on which selection operates, that
is something more than the individual, but
less than the population (Mayr, 1963). It
has been called a "deme" but we have
practically no idea what a "deme" actually
is for all but a few species.
As a behaviorist, this question interests
me very much. Many of you must be aware
of Dr. Wynne-Edwards' stimulating and
thought-provoking book, Animal Dispersion in Relation to Social Behavior, that
caused such a stir in 1962. He surveys a
great deal of social behavior from a new
viewpoint, suggesting functions in control
of the population. He concludes that since
on occasion some individuals refrain from
reproduction, endanger their own survival,
or even sacrifice themselves in order that
others may survive and reproduce, a new
process of selection must be postulated
which he calls group-selection.
The critics were not slow in expressing
reluctance to even entertain such a notion
until existing concepts were proved wanting. Much of the criticism was cogent
(Lack, 1966; Wiens, 1966; Williams, 1966;
McLaren, 1967). Some of the phenomena
discussed, such as territoriality, can be explained adequately by the impact of classical natural selection on the individual
(Brown, 1964; Crook, 1965). In any case,
they pointed out that natural selection operates not on the individual alone, but on
the individual and his close kin (Smith,
1964; Brown, 1966). They indicate that
much of what Wynne-Edwards describes
can be explained as a result of kinselection, and in particular, Hamilton
(1964a, b), a populational geneticist, was
provoked to develop two papers on the
genetical theory of social behavior that are
full of stimulating ideas. He draws attention to many complex social phenomena,
in social insects for example, that can be
explained on the basis of kin-selection—
and in solitary insects as well—provided we
can assume that neighbors are likely to be
close relatives.
He develops some of his arguments from
J. B. S. Haldane and R. A. Fisher with
whom he shares an interest in the relation
of the individual to the group in cases of
cryptic and aposematic insects. Here there
is indeed evidence for group-effects. David
O F FOXES AND HEDGEHOGS
Blest, for example, hypothesized with regard to the post-reproductive survival of
Saturniid moths in Panama that the longer
a cryptic species survives after reproducing the greater the chance it will be found
by a predator, so encouraging the predator
to look for more and thus endangering
the safety of others that may still be reproductive. "Group"-selection should thus
shorten post-reproductive survival for
cryptic species and should have the reverse
effect on aposematic species. Field study
yielded the predicted results, females of
cryptic species surviving one to two days
after egg-laying and aposematic species up
to nine days (Blest, 1963).
This is a simple case where longevity of
the individual may be affected by events at
the level of the population, and no doubt
many other aspects of organismal biology
can become similarly involved. Until we
know how close kin are distributed in
nature this subject remains difficult to explore. It seems at least conceivable that
clusters of related kin are quite large in
some cases, with a degree of inbreeding
within such groups. If this should prove
correct, then such is the unit on which the
organismal biologist should focus when
studying, say, variation in water metabolism with habitat, if he is to discover how
such adaptations actually evolve.
Another reason I am excited by this subject is my belief that it contains the seeds
of a revolution in our thinking about social organization in animals and its evolution. Let me give three examples.
First, the most elegant one comes from
Selander's work with house mice. One
great difficulty confronting the populational biologist is that of determining who is
fathering whose children, a problem not
unknown in human society. When paternity is contested, one of the first things we do
is to check blood groups—in other words
to use the methods of the organismal and
molecular biologist to look for direct
chemical evidence of genetic relationship.
It begins to appear that such methods as
starch-gel electrophoresis of proteins in the
265
blood serum and other tissues can uncover sufficient polymorphism to give a good
chance of reconstructing the recent reproductive relationships of the members of
natural animal populations as well.
Building on the work of Lewontin
(1962), Anderson (1964), Petras (1967a,
b, c; Reimer and Petras, 1967) and others,
Selander has concluded an exhaustive analysis of biochemical polymorphisms in
house mice, living mainly in barns. The
essential points are first the extraordinarily
limited gene flow not only between barns
separated by a few yards, but even between
clusters of animals within the same barn
only five feet apart. The second is the indication that the basic unit corresponds with
the social unit—a tribe of a dominant
male, four or five adult females and some
subordinate males, and subadults—and the
implication that the coherence of these
groups maintained by territorial behavior
constitutes a significant barrier to gene
flow, and makes for a somewhat inbred
group of close kin (Selander and Yang, in
press). If, as seems conceivable, subordinate males do less breeding than the dominant, we are brought back to one of
Wynne-Edwards' points—the great interest
to us of the occurrence of individuals that
refrain from breeding—but in a context
that makes it more comprehensible if they
are all common kin, and perhaps contributing to the fitness of the tribe as a whole.
Still uncertain is the adaptive significance of these biochemical variations.
Random drift may occur under such conditions, but I understand Selander is convinced that some have adaptive significance. Here is a perfect opportunity for
collaboration between organismal and
populational biologists to work out the
physiological correlates of such gene differences and to demonstrate both the way in
which natural selection actually operates
to generate physiological races and to
bridge the gap between discovery of a difference in genotype and establishment of a
correlation with differences in overt behavior and physiology.
266
PETER MARLER
T h e same approach may help to explain
the significance of many other aspects of
social behavior. For example, in many
higher primates the basic social unit is a
coherent troop with many adult animals.
There is some evidence for a degree of
inbreeding here and a suggestion that a
few males do most of the mating. Yet the
evidence is hard to come by and one is
reluctant to accept the notion that some
individuals relinquish to others the right
to father young. I was therefore intrigued
to discover evidence of a quite different
type from another kind of organismal biologist—the physical anthropologist, Buettner-Janusch—looking at hemoglobins and
transferrins in the blood of baboons. Once
more there is sufficient variation in the
transferrins in one geographical area to
permit inferences about mating systems.
Five baboon troops showed striking and
rather consistent differences in the distribution of the several transferrin phenotypes—implying considerable genetic isolation between the troops
(BuettnerJanusch, 1963). Again there might be
drift, or could it be that such a pattern of
social and genetic organization permits
some degree of physiological specialization
to local conditions?
As a final example, let me mention my
own point of departure on this line of
thinking, the significance of dialects in
bird song. In at least one case, Zonotrichin
leucophrys, we have evidence that songlearning encourages males and probably
females to settle and breed in the area of
birth (Mailer, in press). My colleague Dr.
Fernando Nottebohm (in press) has
suggested recently that here again some
genetic specialization to local conditions
may be encouraged—an explanation consistent with his discovery that song-dialects in
a South American relative, the chingolo,
Zonotrichia capensis, differ more strikingly across transitions in type of habitat than
within homogeneous areas. If this speculation proves correct, this will be another
aspect of social behavior that relates at
least in part to the genetic structuring of
local populations.
I have obviously exploited the occasion
of this discussion to speculate. However, I
am reassured to know that others are thinking along similar lines—many whose names
I have not mentioned, such as Dr. Ehrlich. Aside from the specific examples
and hypotheses it seems clear to me that
neither the organismal biologist, nor the
populational biologist, can afford to ignore
the other's discipline. One might also
press for more mixing within disciplines,
especially where these are divided by artificial departmental boundaries. For example, the genetics and ecology of populations are often taught in different departments, sometimes even in different schools,
one in agriculture and the other in
science. Everyone loses by such a separation. More unification of the sophisticated
theorizing and laboratory experience of
the populational geneticist with the field
know-how of the ecologist holds exciting
promise.
The facts already known, the methods
used, and the concepts that guide their
application, all invite attempts to increase
traffic between the disciplines, as well as
with the molecular biologist, and the
teacher's role in encouraging such "fedgehoxes" is a vital one. If we do it right, the
distinctions between such disciplines should
disappear. When we see that happening
we shall know that we have really accomplished something.
REFERENCES
Anderson, P. K. 1964. Lethal alleles in Mus musculus: local distribution and evidence for isolation
of denies. Science 145:177-178.
Adler, X. T. 1968. Effects of the male's copulatory
behavior in the initiation of pregnancy in the
female rat. Anat. Rec. 160:305.
Adler, N. T. 1969. The role of the male's copulatory behavior in successful pregnancy of the female
rat. |. Comp. Physiol. Psychol. (In press).
Barlow, H. B. 1953a. Action potentials from the
frog's retina. J. Physiol. 119:58-68.
Barlow, H. B. 1953/;. Summation and inhibition in
the frog's retina. ). Physiol. 119:69-88.
Beach, F. A. 1965. Sex and behavior. John Wiley
and Sons, Xew York.
O F FOXES AND HEDCEHOCS
267
Berlin. I. 1957. The hedgehog and the fox. George
mals. In W. C. Young, [ed.]. Sex and internal
Weidenfeld and Nicholson, Ltd., England.
secretions. Williams and Wilkins, Baltimore.
Lewontin. R. C. 1962. Interdeme selection controlBlest, A. D. 1963. Longevity, palatability and natuling a polymorphism in the house mouse. Am.
ral selection in five species of new world SaturNaturalist 96:65-78.
niid moth. Nature 197:1183-1186.
Lloyd, J. E. 1966. Studies on the flash communicaBrown, J. L. 1964. The evolution of diversity in
tion systems in Photinus fireflies. Univ. Mich.
avian territorial systems. Wilson Bull. 76:160-169.
Museum Zool. Misc. Publ. 130:1-95.
Brown, ). L. 1966. Types of group selection. Nature
Manning, A. 1967. An introduction to animal be211:870.
havior. Addison Wesley, Mass.
Buck, J. B. 1937. Studies on the firefly. II. The
Marler, P. 1969. A comparative approach to vocal
signal system and color vision in Pholimis pyralis. Physiol. Zool. 10:412-419.
learning: song development in white-crowned
sparrows. J. Com p. Physiol. Psychol. (In press).
Buettner-Janusch, J. 1963. Hemoglobins and transferrins of baboons. Folia Primat. 1:73-87.
Malurana, H. R.. J. Y. Lettvin, W. S. McCulloch,
and W. H. Pitts. 1960. Anatomy and physiology
Capranica, R. R. 1965. The evoked vocal response
of vision in the frog (liana pipiens). J. Gen.
of the bullfrog. M.I.T. Press, Cambridge, MassaPhysiol. 43:129-175.
chusetts.
Capranica, R. R. 1968. The vocal repertoire of the
Mayr, E. 1963. Animal species and evolution.
bullfrog (Rema catesbeiana). Behaviour 31:302Belknap Press, Mass.
325.
McLaren, I. A. 1967. Seals and group selection.
Ecology 48:104-110.
Crook, J. H. 1965. The adaptive significance of
avian social organizations. Symp. Zool. Soc. LonNottebohm, F. 1969. The song of the Chingolo,
don 14:181-218.
Zonotrichia capensis, in Argentina: description
and evaluation of a system of dialects. Condor
Dethier, V. G. 1963. The physiology of insect senses.
(In press).
John Wiley and Sons, New York.
Petras, M. L. 1967a. Studies of natural population
Frishkopf, L. S., R. R. Capranica, and M. H.
of Mus. I. Biochemical polymorphisms and their
Goldstein, Jr. 1968. Neural coding in the bullbearing on breeding structure. Evolution 21:259frog's auditory system—a teleological approach.
274.
Proc. IEEE 56:969-980.
Petras, M. L 19676. Studies of natural population
Gordon, M. S., C. A. Bartholomew, A. D. Grinncll,
of i\(us. II. Polymorphism at the T locus. EvoluC. B. J0rgensen, and F. N. White. 1968. Animal
tion 21:466-478.
function: principles and adaptations. Macmillan
Petras, M. L. 1967c. Studies of natural population
Co., New York.
Hamilton, W. D. 1964o. The genetical evolution of of Mus. III. Coat color polymorphism. Canad. J.
Genet. Cytol. 9:287-296.
social behaviour. I. J. Theoret. Biol. 7:1-16.
Hamilton, \V. D. 1964b. The genetical evolution of Ratlilf, F. 1965. Mach bands: quantitative studies
on neural networks in the retina. Holden Day,
social behaviour. II. J. Theoret. Biol. 7:17-52.
Hartline, H. K. 1938. The response of single optic Inc., San Francisco.
nerve fibers of the vertebrate eye to illumination Reimer, J. D., and M. L. Petras. 1967. Breeding
structure of the house mouse, Mus musculus, in
of the retina. Am. J. Physiol. 121:400-415.
a population cage. J. Mammal. 48:88-99.
Hartline, H. K., H. G. Wagner, and F. Ratlilf. 1956.
Selander, R. K., and S. Y. Yang. 1969. Biochemical
Inhibition in the eye of Limulus. J. Gen. I'hysiol.
genetics and behavior in wild house mouse popu39:651-673.
lations. In G. Lindzey and D. Thiessen, [ed.],
Hinde, R. A. 1967. Aspects of the control of avian Contributions to behavior-genetic analysis: the
reproductive development within the breeding mouse as a prototype. Appleton, Century, Crofts,
season. Proc. XIV Intern. Ornithol. Congr. New York. (In press)
135-153.
Walker, T. J. 1957. Specificity in the response of
Hubel, D. H., and T. N. Wiesel. 1959. Receptive female tree crickets (Orthoptera, Gryllidae, Oefields of single neurones in the cat's striate cor- canthinae) to calling songs of the males. Ann.
tex. J. Physiol. 148:574-591.
Entomol. Soc. Am. 50:626-636.
Hubel, D. H., and T. N. Wiesel. 1962. Receptive
Wiens, J. A. 1966. On group selection and Wynnefields, binocular interaction and functional arEdwards' hypothesis. Am. Scientist 54:273-287.
chitecture in the cat's visual cortex. J. Physiol.
Williams, G. C. 1966. Adaptation and natural selec160:106-154.
tion. Princeton Univ. Press, Princeton, New JerLack, D. 1966. Population studies of birds. Clarensey.
don Press, Oxford.
Wynne-Edwards, V. C. 1962. Animal dispersion in
Lehrman, D. S. 1961. Gonadal hormones and parrelation to social behaviour. Oliver and Boyd,
ental behavior in birds and infrahuman mamLondon.