Download On the Origin of the Metazoa By AC HARDY

On the Origin of the Metazoa
By A. C. HARDY
{From the Department of Zoology and Comparative Anatomy, Oxford)
SUMMARY
A new view is expressed regarding the possible evolution of the Metazoa from
unspecialized and relatively simple Metaphyta, instead of from colonial or partitioned
Protozoa.
T
HIS is a short paper to present a very simple idea regarding the origin of
the Metazoa, one which, as far as I am aware, has not been expressed
before. It is in a sense a corollary to the views expressed by my old friend and
colleague Dr. J. R. Baker in his article on 'the Status of the Protozoa' (1948); indeed, the idea owes its origin to that article for it occurred to me after reading it.
Baker, it will be remembered, defines a cell as 'a mass of protoplasm,
largely or completely bounded by a membrane, and containing within it a
single nucleus formed by the telophase transformation of a haploid or diploid
set of anaphase chromosomes'. He argues that while some Protozoa, such as
the Ciliophora and certain Radiolaria, are not cells in the sense of this definition, there are many which can properly be regarded as unicellular organisms.
He stresses that there is no fundamental difference between the cleavage of an
egg and the multiplication of a unicellular protozoon by division. At the end
of his article he discusses the evolution of Metazoa from Protozoa. It is well
known that there are two schools of thought regarding this question. On the
one hand, there are those who hold that the Metazoa were derived from a group
of protozoan cells which had failed to separate after repeated division, i.e.
from a colony of cells which have gained a new and corporate individuality;
on the other hand, there are those who believe that the origin of the manycelled condition was due to the development of partitions within a multinucleate protozoon. Baker discusses both sides of the controversy and points
out how it is more difficult for the zoologist to imagine the evolution of a
metazoon from a protozoan colony than it is for the botanist to imagine a
similar step in the evolution of multicellular plants. Since my suggestion
springs directly from his argument of this point, I will, with his kind permission, quote him at some length. He writes as follows:
'It may be remarked that while such forms as Volvox raise a storm of controversy
among zoologists, they are not regarded as unusual by botanists, who are familiar
with such colonial forms in groups other than the phytomonads. Botanists regard
them as composed of cells, which are comparable on one hand with the individuals
of what they call unicellular species, and on the other with the cells of higher but
related forms, in which there is somatic differentiation (heterotrichous forms and
other algal metaphytes).
[Quarterly Journal of Microscopical Science, Vol. 94, part 4, pp. 441-443, Dec. 1953.]
442
Hardy—On the Origin of the Metazoa
'If we seek the reason why zoologists are more divided in this controversy than
botanists, we shall surely find it in a fundamental difference between plants and
animals. In the lower plants each group tends to present both unicellular and metaphytic representatives, and botanists are repeatedly confronted with the intermediate
forms. Metaphytes, in fact, have obviously originated independently many times,
so that no one would propose the word "Metaphyta" in any classification that was
supposed to be based on evolutionary principles. With animals it is far different.
Zoologists have not got intermediates again and again before their eyes. In the great
group of Rhizopods, for example, there is no example of a multicellular form (the
word "cell" being here used as denned above). It would not appear that anyone has
discussed the reason for this striking difference between plants and animals. The
following suggestion may be made. The unicellular plant absorbs nutriment from
all sides equally, and when, in the course of ontogeny or phylogeny, it becomes a
metaphyte, there is no fundamental change in this respect: a cell divides without
separation and the two products continue to absorb nutriment over most of their
surfaces. The passage from the unicellular form to the metaphyte is therefore easy.
In the case of animals, however, there is an important change when a unicellular
form becomes a metazoon: a new method of feeding must be adopted. We see this
particularly clearly in the ontogeny of Dendrocoelum. The blastomeres feed at first
saprozoically, but at last a profound change occurs: a set of digestive organs originates,
and a new method of nutrition begins. Most animals overcome this difficulty in
ontogeny by placing enough reserve food-stuffs within the single-celled stage to
make feeding unnecessary. It is easy to see what evolutionary difficulties must be
presented when a new system of nutrition must be acquired before advance can
occur. The difficulties would be greatest when a protozoon had a localized mouth.
If the products of division of such an animal were to adhere together and each were to
acquire its own mouth, no advance would be made towards the evolution of a metazoan alimentary canal. This suggests that the Metazoa may have arisen from primitive Protozoa, unprovided with localized organs of assimilation. These considerations seem to make it clear why intermediates between unicellular animals and
Metazoa are rare, while intermediates between unicellular plants and metaphytes
are common. (The colonial phytomonads are, of course, only regarded as animals
by zoologists on account of their motility: their nutrition, it need scarcely be said, is
holophytic or saprophytic.)'
We are concerned here with the origin of the true Metazoa, leaving on one
side the sponges, sometimes called the Parazoa, which with their more limited
integration may well have been quite independently derived from aggregations
of choanoflagellate-like protozoa. The simple idea I want to suggest is that the
Metazoa have not been derived from the Protozoa at all, but from relatively
simple metaphytes which, after they had evolved from protophytes began,
perhaps as a result of a shortage of phosphates and nitrates, to capture and
feed upon other small organisms as do the higher insectivorous plants. Among
the Protista it is clear that animals have evolved from plants more than once;
in several different groups of Protophyta, as Fritsch (1935) has so well shown,
we can arrange parallel series passing from holophytic forms at one end to
holozoic forms at the other. In addition to such changes among the flagellates
of the class Euglenineae, Fritsch points out and compares these parallel
Hardy—On the Origin of the Metazoa
443
evolutionary lines in four different classes of the simpler algae: Chlorophyceae,
Xanthophyceae, Chrysophyceae, and Dinophyceae. If animals have evolved
from plants several times at the unicellular level, is it not possible that animals
might, at least once, have been so derived from plants at a not too specialized
multicellular level ? This suggestion may perhaps be worth bearing in mind
because it does get over the very real difficulty which Baker has pointed out,
that of how a metazoon could have evolved from a colony of protozoa, each, as
individuals, already adapted for the capture of prey.
It would be unprofitable to elaborate the idea in much detail. The many
different devices evolved by the various carnivorous plants to enable them to
secure their food suggest how such a metazoan organism may have been derived. It is not difficult to imagine a spherical volvox-like metaphyte developing a little pocket-like invagination in which small protozoa or protophyta
might collect, die, and provide breakdown products to be absorbed by the cells
lining the cavity. Such little pockets would be analogous with the bladders of
Utricularia which capture water-fleas. How similar in general action, although
different in physiological detail, are the 'tentacles' which capture flies on the
leaf of the sundew Drosera to those which capture Crustacea on the polyps
of a hydroid! The gradual transition from a simple metaphyte to a simple
polyp-like metazoon—a bladder-like cavity with tentacles—seems no more
difficult to conceive than the evolution of the higher animal-like insectivorous
plants; we have only to imagine the process going so far as to cut out all photosynthesis, thus making the organism holozoic—as indeed has occurred repeatedly at the unicellular level of the flagellates and algae.
If the Metazoa should have evolved from Metaphyta then the findings of
Gohar (1940) are of special interest; he claims to have shown that Alcyonarians
of the family Xeniidae feed entirely upon the photosynthetic products of their
symbiotic algae and never capture animals for food at all; by a circuitous
route they appear now to be metazoa which are on their way back to becoming
metaphytes and must, if the whole colony is to grow, be taking in nutritive
salts from outside for the growth of their enclosed plant cells. (It is perhaps just possible, but most unlikely, that the zooxanthellae of the Anthozoa,
which cannot be cultured outside their 'host', might be plant cells remaining
as a legacy from the original metaphytic days and not separate symbiotic
algae as in other such associations.)
I do not wish here to enter into the controversy between the former two
opposing views as to the origin of the Metazoa; the sole purpose of this short
communication is to state a third possible view for consideration. I am indebted to Dr. J. R. Baker not only for his article which gave rise to this idea,
but for his interest in the suggestion and his discussion of it.
REFERENCES
BAKER, J. R., 1948.
Nature, 161, 548, 587.
FRITSCH, F. E., 1935. The structure and reproduction of the algae, Vol. i. Cambridge.
GOHAR, H . A. F., 1940. Publications of the Marine Biological Station of Ghardaqa, No. 2,
23. (Cairo.)
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