PHYSIOLOQICAL ADAPTATION.
705
Physiological Adaptation. By C. F. A. PANTIN,
M.A. The Zoological
Laboratory, Cambridge. (Communicated by Dr. G. P. BIDDER.)
[Read 14th May, 1931.1
ONE of the first duties in any science is the description of the objects with which
that science deals. In Biology this demands an exact account of the living
organism in relation to its environment. But, whereas we can speak of the
morphological characters of an organism with considerable precision, tho
physiological characters which describe their functional significance and tho
adaptation of organism to environment remain ill-defined. The term ‘(physic)logical character ’’ covers many entirely different things, and it is 011r objec*t,
to consider their nature and the ways in which they bring about physiologicnl
adaptation to the environment.
I n the first place, it is necessary to define the term ‘(adaptation.” Few things
seem more evident than its existence, but its exact definition is not ea.;y.
Perhaps the definition given by Allen (1929) in his Hooker lecture is hesf :
“ By an adaptation we mean nothing more than a character of an organism
which has enabled a species to survive itself as such, or to survive until it is
transformed into another species. It is survival that gives the measlire of
adaptation.” This definition is simple and precise. At least in theory, it
allows the quantitative determination of adaptation by direct experiment.
It omits implications concerning the mode of origin of adaptations and
of their apparent “ purposiveness.” A character is adaptive as long 8 s
it increases sthe chance of survival, even when it does so under unusual
circumstances which the organism could never have been prepared to meet.
But we do not usually employ Allen’s definition in practice. When we state
that a particular character is an adaptation, we usually base our judgment
on certain qualitative impressions. These are, first, an apparent correlntioii
I)etween the occurrence of a ptrticular character and a particular environmental
feature, and, secondly, our perception of some functional relation between
them. Thus the occurrence of haemoglobin in animals is definitely correlated
with environments deficient in oxygen. We perceive albo a functional relation
based on the ability of haemoglobin to combine with oxygen. We therefow
argue that the occurrence of haemoglobin is an adaptation to an environment
poor in oxygen. Of two species of Cuczlmaria, C. elongata lives in miid which
may well be deficient in oxygen and its ccelomic fluid contains abundant
hzmoglobin corpuscles. On the other hand, C. saxicola, which lives among
rocks, possesses no hzemoglobin. The inference that the hEmoglobin ill
is an adaptation t o its environment seems natural,
c.
LINK. JOURN.-ZOOLOGY,
VOL. XXXVII.
49
706
MR. C. F. A. PANTIN ON
Such judgments may, in fact, be attempts to make a qualitative estimate of the
survival value of the character on a basis such as Allen’s definition. But
instead of performing direct experiments to determine survival value, we
attempt to infer their answer from what we know of the properties of the
environment and of the character concerned. I n this there is great danger.
Our knowledge of the environment of most organisms is very incomplete,
and our ignorance is too often filled in by precarious assumptions based on the
analogy of our own special environment. We cannot define “ adaptation ”
to conditions which we cannot specify, and our attempted functional interpretation may be wrong unless verified by experiment.
Numerous correlations are found without apparent functional explanation.
Many animals have free in their gut substances which yield hsmochromogens.
Such are the helicorubin in the crop of Helix and the similar substances present in
the digestive fluids of many Crustacea, of the worm Aphrodite, and other animals.
If an ingenious functional significance were suggested for this, we might be
tempted to consider it an adaptation. Because, in this case, no satisfactory
interpretation is forthcoming, we can without prejudice perceive how much the
truth of any such interpretation would require experimental verification.
I n many cases physiological adaptation seems clear. Krogh and Leitch
(1919) showed that the eel and pike, whicb can live in water somewhat deficient
in oxygen, possess hsmoglobins with a much higher avidity for oxygen than that
of the trout, which only survives in well-aerated water. But to dismiss such
cases as adaptations without a functional study of animal and environment
is to cloak ignorance. Planorhis and Arenicola both live under conditions
of oxygen deficiency. Both possess hsmoglobin with a high affinity for oxygen.
But its function i E different in the two cases. Leitch (1916) showed that in
Planorbis the ha?moglobin acts primarily as a carrier of oxygen from the surface
of the animal to the tissues, which comes into action when the external oxygen
pressure is so low that simple diffusion of oxygen no longer supplies the needs
of the animal. On the other hand, Barcroft and Barcroft (1924) found in
Arenicola that the function of the hsmoglobin is to provide a store upon
which the worm can draw during the period it remains sealed in its burrow
a t low tide.
Like Arenicola, the Sabellid worms possess a respiratory pigment, in this case
chlorocruorin. These worms are tubicolous, and one might he tempted to
ascribe to the pigment an adaptational significance similar to the hsmoglobin
of Arenicola. But Fox (1926) has shown that the affinity of the chlorocruorins
for oxygen is so low that they are not even fully saturated when in equilibrium
with air. We can only say we do not know their functional significance.
Though physiological adaptation is a reality, the very facility with which
hypotheses can be formed when knowledge of both environment and function
is uncertain shows how necessary it is that experimental verification should
immediately follow. Without verification the hypotheses purport to give
knowledge we do not possess,
1'HYSIOLOQICAL .4DAPTATION.
707
So long as this is continually borne in mind t h e search for adaptational
significancc of physiological characters is very productive. Recent work
on the effect of temperature on the enzymes oi various invertebrates illustrates
this. Experiments of a few hours' durationwith the enzymes of the mammalian
gut show that the '' optimum " temperature a t which the greatest amount
of substrate is digested coincides with the normal temperature of the body.
But i11 variour; marine invertebrates, experiments of 2-3 hours) duration showed
optimum enzyme action at temperatures of from 40" to 60" C. These are
far abovc the death-point of the animals (20"-30"C.).
The idea that, despite appearances, the properties of these digestive enzymes
might, nevertheless, be closely related to the Conditions of oxistence of the
;tnimals led Berrill (1929) to reconsider the problem. He drew attention to the
well-known fact that the " optimum " temperaturr of an enzyme depends
on the duration of the experiment : the greater the duration the greater is the
clentruction of enzymc at high temperatures, so that the longer the experiment
lusts the lower is the appwent optimum temperatiire. For the amylase of the
Tunicate, l'ethywn, the optimum conversion of starch after one hour occurred
a t 45" C. But after 57 hours the optimum temperature was as low as 13" C.
Now a t a temperature of 10"C., which is near that of the normal environment,
the food requised 50-55 hours t o pass through the gut. It therefore follows
that the enzyme is utilised as economically as possible under natural conditions.
Similar conditions have been shown to obtain in Subella (Nicol, 1930) and in
PPcten (Graham, 1931).
But, despite the intercst of these observations, the problem is still far from
concluded. Provided the amount of digestion effected by the enzyme a t
orclinasy temperatures be unaltered, no disadvantage would seem to exist if,
in addition, it were able to withstand abnormally high temperatures without
rapid destruction. We know, a t present, no reason why an enzyme should
not possess this property and yet retain a digestive efficiency a t lower temperatures equal to that of thc unstable enzymes actually found in these animals.
Such an enzymc would be even more efficient a t a higher temperature than
;it that of the normal environment : the " optimum " might be above the deathpoint. It is true that this property would never be of use to the animal, but,
since the efficiency a t ordinary temperatures is supposedly unaltered, t h k would
seem of no disadvantage to the animal. Nevertheless, this condition does not
seem to occur.
What the investigations have shown is that certain physiological characters
are directly related to environmental conditions. But the problem of their
adaptive value-that is, how far they would affect survival-is not concluded.
It is important to notice that the next stage of this problem must involve
purely laboratory experiments on the physical properties of enzymes. In the
study of function under natural conditions, the liiologist may not neglect thr
physical nature of the systems concerned, even though this involves experiments
under artiiicial conditions quite foreign to those found in Nature.
708
MR. C. F. A . PANTIN ON
Having surveyed some of the grounds on which physiological adaptation
may be inferred, we may consider the nature of the physiological characters
by which it is specified. The living organism comprises material structures
of different orders of complexity, varying from tissues and cells to particular
kinds of molecules which compose them. A variety of active processes takes
place in these structures, and their existence depends on them. Conversely,
the structures themselves have been brought into existence by such processes.
By these processes certain states are actively maintained by the organism.
These structures, processes, and states endow the organism with certain
properties, so that when subjected to a particular experimental treatment
it reacts in certain definite ways.
Morphological characters simply refer to material structures. Rut among
physiological characters entirely different kinds of things are apt to be taken
according to what aspect of the living organism happens to strike the observer.
For convenience they may be considered in four groups : physiological “ strnct,ures,” such as molecules of a respiratory pigment ; “ processes,” particularly
those of metabolism ; “ states ” actively maintained by the organism, such
as the ionic composition of the blood ; “properties,” such as limits of
temperature or pH within which the organism can survive. Of these, the
structures and the properties of the whole organism are most usually seized
upon, and attention will be directed chiefly towards them.
Like morphological structures, physiological structures are material bodies.
The fact that these may be molecules provides no fundamental distinction
between them except order of complexity. Indeed, comparative anatomy
cannot logically be limited to structures above an arbitrary size. Just as gross
anatomy extends to the cellular nature of tissues, and the structure of the cell
to its microscopically visible constituents, so the study of form must extend
further t o the ultimate molecular morphology of cell-structures. Atoms and
electrons are the common material of all living organisms.
It is in the
structure of the molecule that specific differentiation &st becomes apparent.
For this reason the description of molecular structure occupies a position
of peculiar importance in the systematic description of organisms. We may
not limit such description to macroscopic structures simply on the ground that
its extension involves the biologist in methods with which he is unfamiliar.
Nuttall’s (1904) classical work on blood-immunity indicated that in different
animals complex molecules may undergo differentiation that is quite comparable
to specific morphological differentiation, and follows phylogenetic relationship
in the same way.
We are apt to consider morphological characters as infinitely plastic in their
capacity for differentiation. Yet this cannot be true of molecular structures,
becabse they are composed of units:
Despite this limitation, immense
variety is possible. Proteins are the most complex constituents of protoplasm. The molecule is composed of amino-acids, of which there are known
some twenty-one different kinds. Their molecular weight is probably always
PRYSIOLOOICAL ADAPTATION.
709
1, 2, 3, or 6X34,500 (Svedberg, 1930). Since the average molecular weight
of an amino-acid is (30 to 100, i t follows that each protein molecule is it11
sggregate of units each containing some 350 amino-acids. The number of
ways in which twenty-one different kinds of object can be a,rranged in series
to form units of 350 is about
These in turn can be arranged to form
aggregates of 6 , 3 , 2 ,and 1units in about lOZ7Ooways. This number is, therefore,
the general order of the different proteins which might be possible to our
prvscnt knowledge. It is inconceivably great. (According to Eddington
electrons in the whole Universe !) Almost infinite graditthere are only
tioiis of protein structure are rendered possible. Nevertheless, the whole
nature of the molecule is limited, because it is composed of units. Though
organisms have evolved proteins with specific gradations of structiir(h,
evolutionary modification must have occurred by abrupt steps of one or morc
iimino-acids.
The limitations imposed by molecular structure are very clear in substarices
such as the respiratory pigments, which subserve a unique function. These
are remarkably limited in kind. Only four classes are definitely known which
are able to combine reversibly with oxygen. These are : the hzmoglobins,
the chlorocruorins, the hBmerythrins, and the hernocyanins. The first three
contain iron and the last copper. All the members of one class are closely
related compounds of characteristic structure, and are quite dist,inct from the
other classes.
I n considering these pigments some striking features appear. WhcIl
i ~ animal
~ i
develops a respiratory pigment it seems strictly limited to one of four
classes of molecule. Further, the same pigment is independently evol\wl
in entirely distinct groups of animals. We have here a character of great
adaptational significance, which has evolved repeatedly and which could not
possibly be developed gradually. Only in the complete molecule do the
peciiliarly valuable oxygen-carrying powers emerge. However perfectly the
presence of hemoglobin may appear t o adapt the anima,l to its environment,
it codd only have arisen by the sudden appearance of the complete molecule.
The analysis of these systems is of interest. The molecule of hsmoglobin
is a combination of a particular iron-porphyrin compound with protein. The
protein varies in different organisms and causes small variations in the physical
properties of the molecule. The iron-porphyrin compound has a unique
structure, identical in a11 haemoglobins. This same compound also appears
in all kinds of protoplasm in free hematins, hsmochromogens, and the respiratory substance cytochrome. It seems, therefore, that the occurrence of
hsmoglobin is determined by the fact that ohly limited materials are available
in protoplasm for the construction of a respiratory pigment. Since the ironporphyrin compounds only require a particular combination with certain
proteins to yield hsmoglobin, this substance appears repeatedly.
The limitations of the materials available in protoplasm arise from the
properties of matter. I n the periodic table very few elements are available
710
ME. C . F. A. PANTIN ON
for the construction of protoplasm, and each has highly special properties.
It is the special properties of iron that render hsmoglobin possible ; no other
element can adequately take its place.
Our consideration of physiological structure forcibly makes 11s consider that
protoplasmic materials comprise a limited number of standard parts of liinitcvl
properties. Only certain molecules can be constructed from these to meet ally
special function. No infinitely graded adaptation is possible in thew uiiitH,
SO that special structures must appear fully developed 01' not a t all. Owing
to the numerous unit,s employed, an immensc number of gradations ill
properties may be observed in related complex molecules such as the proteins.
But these molecules can only be made of certain kinds of units and only modified
by whole units a t a time. We realise that the organism can never be infinitely
plitstic, All its structures are makeshifts which meet environmental requirements within the limits of the standard parts available for their construction.
It seems that adaptation of these structures can only be evolved by the natl1r:~l
nelection of abrupt variations-a condition precisely satisfied by Mentlelja~i
mutation. Provided the properties of the structure depend equally on a large
number of units, slight variation in many directions is possible. But if thc
nature of one particular unit is all-important in determining the Iiroperties
of the whole structure, successful variation becomes possible only along certain
lines, as in the repeated evolution of hzemoglobin. It is noteworthy that even
in complex morphological structures evidence for parallel evolution anti for
orthogenetic trends necessarily rests upon the results of one particular ~TOC+SS--in this cbse the deposition of calcium compounds.
Within the limits of this essay it is not possible to discuss tho itdaptatioii
of physiological processes and of the staijes they maintain. Their evolritioii
and adaptive significance is of a different nature from that of molecular or gross
morphological structure. Indeed, it is the latter alone that have undergone
evolution and adaptation in the ordinary sense. For the processes and states
only exist at any moment as a consequence of structure. Thus if we say that
the ionic composition of the blood of a n animal is adapted to the maintenance
of the tissue-cells, it is, in fact, the surface membranes and excretory organs
that have actually undergone evolutionary adaptation. Consequently adaptive
significance of blood composition cannot be discussed till we have adequate
k1iowledge of the structures which maintain it (Pantin, 1931).
Adaptation seems peculiarly evident in the physiological properties of the
animal as a whole. These properties are inevitably noticed in any systematic
description of the organism in its environment. Their interpretation is
necessarily the most complicated, because they invoIve every character of the
organism. An example of such properties is provided by the temperature
range of survival of an organism. This range is closely related t o the normal
environmental temperature. Mayer (1914) showed in Aurelia that the limits
of survival in the same species of organism may differ greatly according to
the normal environmental temperature where the organisms are found.
PHYSIOLOQICAL ADAPTATION.
711
The adaptation of organisms to temperature is peculiar in that the deathpoint seems always but little above the highest temperahre t o which the
organism is normally subject. But experiments similar to those of Mayer,
and of Dallinger (1887)) show that over a long period a species can, in fact,
become gradually adapted to withstand temperatures far above the deathpoint when taken from a cold environment, so that the normal closeness of the
death-point to the environmental temperature must be actively brought about
by the organism. It is not easy to see, from the point of view of survival,
wherein failure to withstand abnormally high temperatures can be the result
of adaptation. Provided survival is satisfactory a t normal temperatures, there
seems no disadvantage in ability to withstand much higher temperatures, even
though they be never encountered. Animals do not seem to possess this ability.
A search for the adaptational significance of temperature limits would be of the
greatest interest. Perhaps the attention that has been paid to the evaluation
of temperature-coefficients in organisms has obscured the very great importance of studying the factors which determine the temperature-limits.
I n all such cases what we require is more accurate description of the organism
and its environment. Only in the field can the conditions of existence of thc
animal be truly determined. But to determine the adaptabional significancc
of its characters to these conditions, their physical nature must he analysed
in the laboratory, even though the experiments may seem far removed from thr
actual conditions or' the animal.
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1929. The Origin of Adaptations. Hooker Lecture. Proc. Linn. Sor.
Session 141, p. 119.
BARCROFT,
J., & BAFWROFT,H. 1924. The Blood-pigment of Arenicola. Proc. Roy. SOC.
B, xcvi, p. 28.
BERRILX,,
N. J. 1929. Digestion in Ascidians and the Influence of Temperature. Brit.
Journ. Exp. Biol. vi,p. 275.
DALLIN~ER,
W. H. 1887. Presidential Address. Journ. Roy. Microscop. SOC. (1887),
p. 186.
Fox, H. M. 1926. Chlorocruorin : a Pigment allied to Hemoglobin. Proc. Roy. SOC.B,
xcix, p. 199.
GRAHAM,A. 1931. The optimum Hydrogen-Ion Concentration and Temperature of the
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KROQI~,
A., & LEITCR,L. 1919. The Respiratory Function of tho Blood in Fishes.
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NICOL,
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NUTTALL,G. H. F. 1904. Blood Immunity and Blood Relationship. Cambridge Univ.
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PANTIN,
C. F. A. 1931. The Origin of the Composition of the Body Fluids in Animals.
Biological Reviews, vi, p. 459.
S V E D B E R ~T.
, 1930. Ultrmentrifugale Di~~rsitiitsbestimmungenan F:iwehlGsungen,
Koll. Zeitt. li, p. 10.
ALLEN, E. J.