26
THE ROLE OF WATER IN THE EVOLUTION OF
THE TERRESTRIAL VERTEBRATES
BY J. GRAY, M.A.,
King's College, Cambridge.
(From the Zoological Laboratory, Cambridge.)
(Received igth January 1928.)
(With Three Text-figures.)
As pointed out by Watson (1925) the main problems of evolution centre round the
possibility of deriving one morphological type from another without postulating
or necessitating any functional discontinuity of the organs involved. We have,
therefore, to assume that the changes in bodily structure attending evolution of
the earliest terrestrial vertebrates (from purely aquatic organisms) occurred in
such a way as to maintain the organism, at all times, in a state of physiological
efficiency. This particular phase of evolution must have been influenced if not
largely controlled by the fact that, whereas water is present in abundance in the
environment of a fish, it is not so present in the case of an animal living in air.
Since the tissues of all living vertebrates, irrespective of environment, contain
nearly 80. per cent, of their weight of water (Table I) it seems almost certain that
the terrestrial forms were evolved without seriously reducing the percentage of
water in their tissues.
Table I.
Vertebrate type
Dogfish
Trout
Goldfish
Frog
Newt
Salamander
Lizard
Sparrow
Fowl
Approx. % water in embryo,
or in non-bony adult tissues
81
84
75
80
79
78
72
78
83
If a fish, frog, newt, or salamander is removed from water and exposed to air,
the loss of water which occurs is both rapid and extensive; this suggests that the
acquisition of a skin which is relatively impermeable to water occurred after and
not before the origin of the earliest terrestrial types. Fig. 1 illustrates these facts in
respect to the newt, Triton cristatns. It is seen that a live newt loses water by
The Evolution of Terrestrial Vertebrates
27
evaporation from the skin as rapidly as one that is dead, and on being replaced in
an aquatic medium water is very rapidly reabsorbed by the same route. An animal
of this type may be said to be in dynamic equilibrium with the water in the surrounding environment. A typical reptile {Lacerta viridis), on the other hand, only very
slowly loses water when exposed to air (Fig. 2) and this character persists long
after the animal is killed; the organism is almost, in fact, in static equilibrium
with the water of its environment. This adaptation to conservation of water is
undoubtedly located in the dermis, since if the skin'of the lizard be removed the
tissues lose water as rapidly as do those of a newt or fish (Fig. 3).
ALIVE I N WATER
50
TRITON CRISTATUS
50
O
60
70
80
90
10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170
Time in hours
Figs, i and 3. Illustrating that when a newt is exposed to air it very rapidly loses water through
its skin, whereas the loss from a lizard is very much less.
Just as a lizard does not lose water through its skin, so it is unable to absorb
water rapidly by this organ. We find, in fact, that reptiles are the earliest type of
vertebrate which drinks water through the mouth and absorbs it by the alimentary canal. Typical amphibia on the other hand do not drink; they imbibe water
over the whole surface of their bodies. We may, therefore, conclude that vertebrate
terrestrial life remote from water became possible as soon as the adult organism
acquired a skin which was relatively impermeable to water.
Complete adaptation to terrestrial life includes the faculty of laying eggs on
land and of supplying the developing embryo with an adequate supply of water.
In a previous paper (Gray, 1926) it has been shown that the eggs of a fish {Salmo
fario) absorb a significant amount of water from their environment, and there are
good reasons for supposing that a similar phenomenon occurs in nearly every other
aquatic type of egg. Table II shows that in a variety of cases 50 percent, of the weight
J. GRAY
of vertebrate eggs is composed of solid materials; two-thirds of this material is
converted into embryonic tissues whose water content is roughly 80 per cent. It
is clear that a significant amount of water in the full time embryo must be derived
from the external medium.
Table II.
Type
Scyllium canicula
Salmofario
Ranafusca
R. temporaria
(Maja squinado)
{Sepia officinalis)
Tropidonotus
Gallus gallus
Moorhen
% solid material in the
yolky phase of the egg
Si'4
4i
41
A
42-6
43-6
47-3
567
49 ;
5i
60
S 5°
T3
•8 40
o
o
30
M
CO
O
20
s
o 10
\ I7ARQ with sk'm
10
40
20
30
50
Time in Hours
Fig. 3. Illustrating that the power, possessed by a lizard, of preventing loss of water from its tissues
is due to the properties of its skin.
It is necessary, therefore, to determine the means whereby the embryo of a reptile
or bird is supplied with an adequate supply of water, and secondly to consider
how such a type of egg could have been evolved from purely aquatic types without
any discontinuous change in function on the part of any essential organ.
There can be no doubt that the embryos of oviparous amniotes derive their
water supply from the so-called albumen deposited round the egg by the walls of
The Evolution of Terrestrial Vertebrates
29
the oviduct. This fact is illustrated by the figures in Table III which are largely
self-explanatory. In the sample of eggs used, the average egg weighed 58 gm., and
contained 38-7 gm. of water when newly laid. Of this water, 8*8 gm. were in the
volk and 29*9 gm. in the albumen. At the end of incubation the embryo contains
27'4gm. of water according to Murray's (1925) figures, so that at least two-thirds
of this is derived from the albumen.
Table III.
Water lost
in evaporation
Water gained
at 23 %
by
combustion
humidity
Albumen and
of yolk
(Calc. from
amniotic space
Murray)
Amount of water (in gm.) in
Day of
incubation
0
6
8
10
12
14
16
18
20
Embryo
(Murray)
0
o-4
I-I
2-5
4-6
79
I2'O
18-1
27-4
Yolk
8-5
8-45
8-4
8-2
7-8
6-9
5'3
2-3
i-o
29-9
27-2
25-4
23-0
20-4
16-9
12-6
9-2
2-2
0
2*4
3
'i
5-6
6-7
7-8
8-8
9-8
0
O'OI
0-05
O-I2
0-27
0-50
o-8o
1*2
2-O
That two-thirds of the water in the embryo is provided by the albumen is
shown by the fact that as incubation proceeds the amount of water in the albumen
falls steadily whilst the percentage of water in the yolk does not materially decrease
after the 10th day. It will be noticed that 70 per cent, of the water in the albumen
is required for the formation of the embryo leaving 30 per cent, available for
evaporation. I have calculated the loss due to this cause at 23 per cent, humidity,
since this appears to be a reasonable figure for the conditions of incubation of Gallus
gallus in its natural habitat.
As far as is known no reptilian or avian egg exists without an albuminous phase,
and we may assume that its function is not radically different from that performed
in the case of the chick. It is, therefore, fairly clear that the amniota have solved the
problem of providing their embryos with an adequate supply of water by enveloping
the egg with an aqueous mass of protein secreted by the walls of the oviduct.
Now it is hardly conceivable that the albuminous layer of the amniote egg arose
de novo as an adaptation to terrestrial life, for this would involve a sudden change
in the structure of the oviduct. By the principle of physiological continuity it is
much more reasonable to regard this essential layer as the equivalent of such homologous structures as are found in the anamniota. Among fishes, tertiary egg membranes rich in water are found in the Dipnoi, and they appear to be present in all
amphibia. These membranes apparently protect the egg against destruction by
predatory animals although there may be subsidiary functions associated with the
incubation of the embryo.
In most amphibia, where the tertiary envelope is of a mucoid nature, the full
water content of the envelope is not attained until after the egg has been deposited
in water, but interesting and suggestive modifications are found in the eggs of those
30
J.
GRAY
amphibia which deposit their eggs on land. In Phyllomedusa and in Rhacophorus
the protective function of the mucoid envelope is to a large extent replaced by other
devices, and it is difficult to resist the conclusion that the envelopes are themselves
largely devoted to the provision of water to the embryo. In Phyllomedusa hypochondrialis the eggs are deposited in the folds of a leaf. The mucilaginous egg
capsules rapidly liquefy after oviposition and provide a fluid medium in which the
eggs develop. Agar (1909) observed that a certain percentage of capsules contain
no eggs, and this suggests that the function of these membranes, if any, is to augment
the amount of water available for the larvae. The essential point is that the whole
of the water necessary for development is provided by the oviductal walls of the
mother. Similarly, the eggs of Rhacophorus schlegelii are laid in a subterranean
burrow. Having formed the burrow, the female secretes into it mucilage which,
by means of her feet, is rapidly worked into a froth. Into this froth the eggs are
laid, and as development proceeds the froth is gradually liquefied. Here again the
water for development is all derived from the female organs.
From these types it is not difficult to derive either the egg of a reptile with its
solid albumen phase or the egg of a typical bird where the fluid albumen has entirely
lost its power of protecting the embryo against predatory foes. It is interesting to
note that, far from requiring a supply of water from external sources, the eggs of
birds fail to develop unless a certain amount of water is actually lost by evaporation
during incubation (Chattock, 1925). A suggestive experiment by Weldon (1902)
indicates that the formation of an amnion is dependent on a loss of water by
evaporation1.
Since the mammals are derived from oviparous reptiles it is of interest to consider how the small eutherian egg can be derived from that of the latter group
without any break in the physiological functions of the organs concerned. A conceivable fine of origin is suggested by the eggs of Monotremes. The egg of these
forms has no true albumen layer and the yolky ovum lies close under the shell. As
it leaves the ovary, the egg is about 2 mm. in diameter, but during its passage down
the oviduct its bulk is enormously increased so that the yolky phase is about 14 mm.
in diameter before the shell is deposited (Caldwell, 1887). This 300-fold increase
in volume must largely be due to an absorption of water, although a certain increase in dry weight may well occur. The only significant difference between the
egg of aMonotreme and that of a reptile is that, in the former, the aqueous secretions
of the oviductal walls are passed straight into the yolky ovum itself instead of being
deposited on its surface as a separate phase. In eutherian mammals this process
has gone one step further since the water contained in the mother's blood is passed,
not into the ovum, but direct into the embryo.
If the arguments here presented are sound, there seems good evidence to show
that terrestrial vertebrates have descended from afish-likeancestor which possessed
a glandular oviduct. The secretions of these oviducts were at first utilised as a
1
Weldon incubated eggs in such a way as to replace the water normally lost by evaporation
without interfering with the processes of evaporation or respiration. In such eggs the amnion failed
to develop normally.
The Evolution of Terrestrial Vertebrates
31
protective covering to the eggs, but eventually they made it possible for the eggs
to develop OR land by providing an adequate supply of water to the embryo.
It is, perhaps, permissible to note that the evidence available is entirely experimental and it would seem reasonable to hope that the application of similar
methods might, if applied to the various organs of the body, provide useful evidence
of evolutionary change.
SUMMARY.
1. The origin of truly terrestrial vertebrates was associated with the development of a skin which is relatively impermeable to water. The skins of fishes and
of most amphibia are freely permeable to water, and water is readily lost when
the animals are exposed to ordinary atmospheric conditions. The skin of a lizard
on the other hand is relatively impermeable to water and the animal is therefore
able to withstand exposure to air without serious inconvenience.
2. Complete adaptation to terrestrial conditions involved the capability of
laying and incubating eggs on land. The eggs of fish and of typical amphibia absorb,
during development, considerable quantities of water from the external environment. The embryos of reptiles and of birds derive the equivalent of this water
from the albumen layer secreted round the ova by the walls of the oviduct.
3. Evidence is presented to show that the reptilian type of egg is to be derived
from that of a dipnoan or amphibian, where the egg is surrounded by a mucilaginous
or albuminous secretion of the walls of the oviduct.
4. The mammalian egg can be derived from that of a reptile by supposing that
the aqueous secretions of the oviduct are passed direct into the embryo instead of
forming a separate phase round the ovum. An intermediate type is found in
Monotremes where the secretions are passed into the ovum itself before the egg
is laid.
REFERENCES.
AGAR, W. E. (1909). Proc. Zool. Soc, 893.
CALDWEIX, W. H. (1887). Phil. Trans. Roy. Soc. 178, B, 463.
CHATTOCK, A. P. (1935). Phil. Trans. Roy. Soc. 213, B, 397.
GRAY, J. (1926). Brit.Journ. Exp. Biol. 4, 215.
MURRAY, H. A. (1925). Jowrn. Gen. Physiol. 9, 1.
WATSON, D. M. S. (1925). Phil. Trans. Roy. Soc. 214, B, 189.
WELDON, W. F. R. (1902). Biometrika, 1, 365.