A M . ZOOLOGIST, 12:739-753 (1972)
The Ciliate Protozoa and Other Organisms: Some Unresolved Questions
of Major Phylogenetic Significance*
JOHN O. CORLISS
Department of Zoology, University of Maryland, College Park, Maryland 20742
SYNOPSIS. Recently there has been renewed interest in the origin and subsequent evolution
of such "lower" forms of life as the eukaryotic protists. Concern is expressed that the most
significant questions to be asked may often be slighted in workers' attempts to find
answers to isolated problems in the phylogeny of these organisms. Stress is placed on
questions involving the ciliate Protozoa, following brief description of this intriguing
group and of approaches to their study. Is their nature cellular or acellular? Are they
closely related to other protozoan groups? How did they arise themselves and to what, if
any, metazoan assemblage did they possibly serve as ancestors? How united are the ciliates
among themselves? Related questions treated include the concepts of monophyly and
polyphyly (widely neglected or misunderstood by many practicing taxonomists) and the
possible reflection of phylogenetic considerations in practical schemes of higher-level
classification among various protistan groups. Throughout the paper, emphasis is placed
on formulation of relevant questions and on the value of the comparative approach to
their resolution; seldom are attempts made to provide detailed answers to the problems
posed. A plea is made for keeping an open mind in all research in this broad area.
INTRODUCTION
In recent years there has been a renewed
flurry of interest in the evolutionary histories of various eukaryotic protistan groups,
partly in attempts to find answers related to
their own possible intra-and inter-relationships and their own origins, partly to understand how some of them (e.g., the protozoa)
may be considered cells on the one hand
and complete organisms on the other, and
partly to suggest the origin of so-called
"higher" groups of plants and animals from
one or more of them. New technical ap-
proaches have accelerated the accumulation
of relevant new data, particularly at the
molecular level, and the field is justifiably
becoming a more attractive one.
The main purpose of the present essay,
however, is neither to add new facts per se
nor to supply any particularly new answers.
Rather, I am concerned with the major
relevant questions for which sound answers
must be sought, for I have a distinct feeling
that unless and until some of the basic
problems are clarified, or at least put into
proper perspective, we are hardly in a posi-
It is impossible to mention the names of all of the
students and colleagues with whom I have discussed
one or more of these controversial questions over the
years; yet I wish to express my general indebtedness
to them—for their patient listening and, perhaps too
infrequently, their rigorous cross-examination. Nor is
it appropriate to include specific citation to all of the
pertinent literature which I have perused, particularly in view of the limited amount of space which I
could devote here to each topic treated.
I should like to single out two colleagues for special mention, adding that they are to be held in no
way responsible for the views of mine expressed
here; but without the stimulation of discussions with
them and without their encouragement this paper
might never have been written. My gratitude, then,
to Dr. Eugene N. Kozloff, protozoologist and "lower"
invertebrate specialist, who courageously refuses to
conform to traditional ideas on the evolution and
739
classification of the forms he studies unless they seem
totally unassailable to him; and to Dr. Michael J.
Green berg, comparative invertebrate physiologist by
trade, who long ago impressed me with his appreciation of and admiration for our mutual friends
the protozoa by spending 90% of the time in the
first course he ever taught in invertebrate zoology
on almost totally protozoan-oriented problems not
unlike some of those discussed in this paper.
Support of National Science Foundation grant GB27050X is also gratefully acknowledged.
* This paper is the text of an undelivered Presidential Address. Publishing such a contribution has
long been a custom of the American Society of Zoologists; the tradition of its non-deliverance is a more
recent and perhaps transient one related to abandonment of our Annual Dinner during the past several
years.—Editor
740
JOHN O. CORLISS
tion to label any "answer" as an enduring
resolution to the problems involved. Even
the sequence of questions to be asked—at
least in the case of the principal topic of
this paper, the possible role and place of
ciliate Protozoa in the overall evolutionary
and hierarchical scheme of living things—
may be of significance.
Truly proper treatment of each of the
subtopics considered in following sections
would require book-length presentations;
held to brevity, I feel reasonably justified in
my hit-and-run tactics.
Eschewing details, I shall concentrate on
formulation of the questions, with indication of their complexities and interrelatedness and the value of the comparative approach to their solutions.
WHO ARE THE CILIATES?
Before turning to questions relating to
evolution, it might be helpful to describe,
very briefly, what we know in general about
the group of organisms under central discussion.
The commonly known ciliates (reasonably
representative, in a general way, of the 6,000
or so described species: Corliss, 1961) are
quite easily recognizable as distinct from all
other cells and organisms. Essentially microscopic in size and generally clothed more or
less uniformly with locomotory cilia arranged in rows, they possess nuclei of two
kinds (one or more diploid micronuclei,
exhibiting gametic meiosis, and one or more
polyploid macronuclei, controlling display
of phenotypic characters) and are rarely
without an oral apparatus, often of considerable complexity. They undergo asexual
binary homothetogenic fission regularly,
under optimal conditions perhaps several
times a day, and periodically may exhibit
one of the sexual phenomena of conjugation, cytogamy, or autogamy. Multiple
mating type systems, within syngens, are
becoming known for a number of, but still
not many, species.
Ciliates show a wide tolerance for environmental conditions, occurring—-as a
group—in habitats ranging from open fresh-
and salt-water niches to sand and soil, and
from ectosymbiotic associations with (predominantly) invertebrate animals to internal parasites of (especially) the digestive
tract of both invertebrates and vertebrates.
Distribution is world-wide.
At the ultrastructural level many of the
component parts of a ciliate appear identical to those known for numerous kinds of
cells and (other) eukaryotic microorganisms
(membranes, endoplasmic reticulum, ribosomes, microtubules, fibers, basal bodies,
mitochondria, etc., though the Golgi apparatus is rare or underdeveloped in ciliates
and centrioles per se are absent). Particularly important is the infraciliature, the fine
structure of which is rapidly becoming well
known in diverse taxonomic groups. Contractile vacuoles (or expulsion vesicles),
with pores to the outside, are common.
Methods of feeding vary, depending on
gustatory proclivities (herbivorous, carnivorous, omnivorous, cannibalistic, etc.),
the presence or absence of a true oral opening, and the elaborateness of the buccal and
ancillary organelles when a mouth is
present. Feeding preference and other behavioral traits are exhibited.
Many ciliates possess compound ciliary
structures, in addition to or in place of
simple cilia; some are without cilia of any
kind, at least in certain stages of the life
cycle. Finally, in this extremely abbreviated
characterization, it should be mentioned
that many ciliates form cysts of one kind or
another as part of their whole life cycle;
some sedentary forms produce stalks; and
a number of species are able to construct
loricae, some quite remarkable. It is among
the last-mentioned species that a few fossil
forms have been described (Corliss, 1961).
METHODS OF STUDY
To acquire data about ciliates (and often
other protozoa) which may be helpful in
trying to answer questions of a phylogenetic
nature, several technical approaches may be
used and several areas or kinds of study are
important (Corliss, 1963, 1973a). Protozoologists have recognized for some time
PRESIDENTIAL ADDRESS
(Corliss, 1962a) that attention must be given
to non-morphological as well as morphological attributes of their organisms, although the former are often more difficult
to gather information about and to utilize
in taxonomic work.
There is obviously considerable overlapping in the "levels" or approaches treated
below; and it should be clear that a whole
constellation or combination of characteristics should be studied in parallel in any
proper comparative investigation. Data
should be gathered from populations of organisms. Statistical methods, and computer
techniques when applicable, ought to be
employed in analyses—and even in construction of overall protozoan taxonomic
schemes (Jahn and Bovee, 1967). And the
design of the problem ought to be as carefully planned as in purely experimental
research.
At the light microscopical level, the several known methods of silver impregnation
deserve special mention because they are
today considered to be nearly indispensable
in comparative morphological studies of
ciliates. They reveal many of the essential
elements of the ever-present infraciliature,
making particularly clear the patterns
formed by the kinetosomes and other argentophilic structures or organelles. Unique for
every species, the "cortical fingerprint" or
corticotype supplies invaluable data in
comparative taxonomic work (an explicit
example may be found in the numerous
works on the genus Telrahymena by the
writer and others: see the comprehensive
review by Corliss, 1973b). Other stains and
various specialized cytochemical-biochemical methods are also helpful in any thorough study, not to mention the importance
of examination of living material by several
kinds of microscopy and by microcinematography.
At the ultrastructural level, the knowledge available from examination of the fine
structure of many subunits of the ciliate cell
is of great potential value from the point of
view of comparative systematics. Although
much remains to be learned, the use of
transmission electron microscopy and, in
741
more recent years, scanning electron microscopy—and now from combined SEM-TEM
approaches—has already opened the door
to better understanding of certain minute
structures and organelles inscrutable under
the resolving powers of the light microscope.
Continued improvements may be expected
in preservation, sectioning, staining, coating, etc. of materials desirable for study.
(Studies and reviews are coming out so
rapidly from so many laboratories that the
reader is referred to current numbers of
appropriate journals—Journal of Cell Biology, to name just one—for latest developments in the broad field of cellular ultrastructure.)
At what might be termed the general
physiological level, many of the data derivable today from refined growth and nutritional studies (see Hall, 1967, for comprehensive review), enzyme investigations,
amino acid metabolism, responses to a
variety of stimuli, locomotion, osmoregulation, membrane permeability, serological
experiments, etc. are most useful in gaining
an understanding of the nature of ciliates,
both as cells and as complete organisms.
The recent volume edited by Kidder (1967)
is rich in appropriate references to work in
these fields.
At the sophisticated molecular and genetic levels (conveniently combined here),
perhaps ultimately the best single source of
reliable data for comparative studies, advances are still slow and undeveloped, in
general, with respect to the ciliate Protozoa
and their evolutionary relationships at
the higher taxonomic levels. Nevertheless, there are already clear indications that
the approaches included under this broad
heading, when tied in with the two preceding methodologies, are yielding highly fruitful data pertinent to affinities among organisms at the lower (species and subspecies)
levels (see Allen, 1967, and references
therein). But the widespread lack of discoverable sexuality among the protozoa
creates a problem of its own (e.g., see Sonneborn, 1957): did such organisms have it
and lose it, or have they never had it at all?
Ecological and other so far non-specified
742
JOHN O. CORLISS
considerations,
perhaps
unjustifiably
lumped together as a single approach at the
whole organism and community levels,
should be used in combination with
methods listed in preceding paragraphs in
order to serve as a broad source of additional-but-overlapping data. The cosmopolitan nature of the Ciliophora, as a group,
and their wide tolerance to varying conditions in the physico-chemical environment
(Faure-Fremiet, 1967; Noland and Gojdics,
1967) make them less favorable objects of
comparative study, with rare exception,
than many metazoan taxa from the general
points of view of such factors as habitat
preference, zoogeographic distribution, and
geographic isolation. This is not to deny the
value of more intensive pursuit of protozoological problems in these areas, using
the more refined methods of the modern
community ecologist, etc. The vast realm of
parasitism—host-parasite relationships, etc.
—probably also best fits under this broad
ecological umbrella, with certain special aspects more appropriate under general physiology (above), however.
Urged here is attention to morphogenetic
factors and to dynamic aspects in the life
cycle or ontogeny of the organism under
study, no matter whether the actual methodological approach is descriptive and cytological or experimental and physiological or
biochemical (see reviews by Hanson, 1967;
Tartar, 1967). Only in relatively recent
years have ciliate protozoologists interested
in systematics and evolution started to
realize the significance of data derived from
tracing out the dynamics of the infraciliary
patterns during such phenomena as cell division and stomatogenesis (Corliss, 1967,
1968). An explicit example of its application
to high-level taxonomic considerations may
be found in the provocative work of Small
(1967), although its broad usage was established and the stage set for future workers
in the truly pioneering investigations of the
late E. Faure'-Fremiet in the 1930's and
1940's (see Corliss, 19726, for discussion of
the lasting contributions of this remarkable
man), culminating in his modest but milestone paper on the comparative systematics
of all ciliates (Faure-Fremiet, 1950). When
the data obtained are used in phylogenetic
investigations, one may think of them as
comprising, in effect, "evidence from embryology."
GENERAL HAZARDS AND PITFALLS
One more introductory consideration
must be given at least brief attention.
Often workers interested in evolutionary
problems involving microorganisms do not
seem to appreciate that the same over-riding
problems which face the students of the socalled "higher" organisms face them as well
(Canella, 1964; Corliss, 1968). Worse still,
the microbiologist or protozoologist, with
rare exceptions (see any protozoological
text; also such a work as Schopf, 1972),
lacks some of the kinds of materials held
indispensable by, for example, the vertebrate evolutionist: viz., fossils. Thus, the
all-important time-factor can be only a
subject for speculation; serial lineages cannot be proven; missing links cannot be
identified with any certainty; homologies
may not be as apparent; convergence
or parellel evolution cannot be distinguished infallibly; rates of evolution cannot be estimated with reliability; conditions
of monophyly or polyphyly (see a subsequent section of this paper) can never be
proven; past environmental conditions and
their selective pressure effects must remain
tantalizingly unknown. A sobering outlook
indeed! Little wonder that microorganisms
are despairingly left to one side by many
writers of treatises on systematics, evolution,
and phylogeny, authors whose own stocksin-trade are typically higher plants or vertebrate animals.
Nevertheless, I have a positive point to
make here. For even while one should be
fully cognizant of the traps and snares
enumerated above, it is still legitimate to
postulate unknown relationships and even
unknowable phylogenetic lines without
such an effort's "degenerating into a kind of
scholarly indoor past-time," as an experimental biologist of note once scornfully
labeled it. Evidence from extant forms
as well as from fossil material, if
gathered properly and treated judiciously,
PRESIDENTIAL ADDRESS
can be of genuine value, especially if one
keeps in mind that "conclusions" drawn
should be realized as tentative at best.
The indispensable time-factor itself
may be taken care of in part, by acceptance
of the following assumption (Corliss, 1968):
that some groups of present-day protozoa
have gone essentially unchanged in certain
key characteristics, at least, for many, many
aeons, while others have not. Thus, members of the former groups resemble ancestral forms or more primitive species more
closely than do the others which have
evolved more rapidly and show more
change, especially in some readily observable important features. This is not a
radical hypothesis; indeed, it is also often
applied to species of metazoan organisms.
Extreme caution is necessary, however, for
we can never know what groups have become extinct along the way, where they
may have fitted into the evolutionary
scheme, and what their affinities might have
been with respect to the various groups
still with us today.
CILIATES: CELLS OR ACELLS?
An early question, probably the first, to
be asked, it seems to me, is whether or not
the Protozoa (and let's confine ourselves
solely to the Ciliophora for the moment) are
cellular (essentially unicellular) or acellular
organisms. For if they are to be considered
totally non-cellular their possible evolutionary relationship to other organisms may
require an entirely different approach than
if they are simply unicellular. Thus, I cannot agree with the many biologists who
lightly dismiss the question as being a
"purely semantic" one.
I believe that the electron microscope, in
particular, has dealt a crippling blow to the
assumption that because a ciliate is a whole
organism it cannot (also) be considered a
cell. The ultrastructural similarity, even
identity sensn lato, of many of the component parts of a ciliate with those of cells
of multicellular organisms (including plants)
reinforces the proposition that homologous
organelles are very likely present. Basal
bodies, mitochondria, endoplasmic reticu-
743
lum, ribosomes, and microtubules will serve
as scattered examples (Pitelka, 1963). Phenomena such as cytoplasmic fission and nuclear mitosis and meiosis, not to mention
possession of often identical enzyme systems
and biosynthetic pathways in general, furnish further impressive support of the basic
cellular nature of ciliate Protozoa.
The complexities of subcellular organization in ciliates, their dual nuclear system
with polyploid macronuclei, their frequent
display of more or less unique properties
such as contractile vacuoles (rarely seen outside the Protista), stalks, sculptured pellicles, and elaborate cortical infraciliary systems, not to mention often highly complex
ciliary organelles, may all be related, simply,
to two facts: (1) their simultaneous existence
as "morphological" cells and as whole, independent organisms carrying on all of the
physiological functions characteristic of
multicellular species (be they carried oxit in
the latter by cells, tissues, organ-systems, or
the organism as an integrated unit); and (2)
their undoubtedly extremely long presence
on earth, which has allowed plenty of time,
through mutation, adaptation, natural selection, etc., to have built up within their
bodies an unparalleled degree of subcellular
differentiation appropriate to their longrange survival.
Definitions, admittedly, do come into the
picture; they can be unwisely restrictive, in
my opinion, if care is not exercised in their
composition. (Gregg, 1959, has interestingly
treated aspects of this subject from a logician's point of view.) For example, 1 cannot
accept the characterizations of a cell offered
by Dobell (1911), Hyman (1940), and Baker
(1948), since they arbitrarily exclude protozoa by their very narrowness. This may be
noted in the following quotations (pertinent
parts only) from the three authors cited: a
cell is "part of an organism and not a whole
organism"; it is "one nucleated division
[part] of an organism"; it possesses "a single
nucleus formed by the telophase transformation of a haploid or diploid set of anaphase
chromosomes." Not only do these rigid definitions deliberately exclude the protozoa
(though Baker's would admit uninucleate
744
JOHN O. CORLISS
First perhaps we should ask the question,
are non-ciliate Protozoa cells? Many groups,
such as numerous amoebae and flagellates,
"look like" cells even more strikingly than
do ciliates, especially because of possession,
commonly, of but a single nucleus, mitosis
often with centrioles and spindle fibers, and
frequently an apparent simplicity in cytoarchitecture in general. Compare the rhizopod amoeba and the mammalian leukocyte.
Many photosynthetic flagellates are strikingly like unicellular algae (indeed, so classified by botanists), themselves very likely
directly related to colonial and various
multicellular algae and, logically, to even
"higher" green plants. (Botanists, incidentally, seem less uncertain over the probable evolutionary significance of colonial
organization of organisms than do
zoologists: understandable in light of the
very nature of plants.)
Ultrastructurally, there is again ample
support for homologies, unless coincident
similarity in structure of certain organelles,
such as flagella, by "organic design" in
order to perform identical functions (e.g.,
see Grimstone, 1959) is an acceptable alternative explanation.
Mononucleate protozoa were mentioned
above, yet many non-ciliates are also multinuclear (even if all the nuclei are of the
same kind); and a few are definitely multicellular in some stage of the life cycle. This
is true, e.g., in various cnidosporidians,
though these enigmatic forms rest very insecurely among the Protozoa in the views
of many protozoologists today. So although,
in my opinion, non-ciliates, like ciliates,
are built on the cellular plan of organization, they are not restricted to unicellularity: truly colonial and multicellular
forms may also exist among them (Corliss,
1957).
But, yet, are ciliates reasonably considered
to
be closely related to the superficially
CILIATES: PROTOZOA OR WHAT?
somewhat similar zooflagellate protozoan
Protozoa are often given a prominent group or not? Have millions of years of
position on the evolutionary tree of life. probable separation widened the evoluBut the taxonomic limits of their own phy- tionary gap (if indeed it didn't exist as a
lum are seldom defined with precision. The wide one from the very beginnings of the
relationship of ciliates to other protistan two groups) to a degree suggesting very
groups remains an important considera- high-level taxonomic separation today? This
is important, even if in fact quite unresolvtion.
forms), in spite of their possession of so
many substructures in common with cells
of multicellular organisms, but it must be
admitted that they also exclude many "real"
cells from being recognized as cells: not
only ova and spermatozoa, mature mamalian erythrocytes, and binucleated liver
(and other such) cells but, most startling of
all, all cells (from multicellular origins) culturable in clonal lines in test tubes and
flasks! Now that, today, separate and individual cells can be so grown in populations,
using the older "tissue-culture" techniques
in refined ways, must we accept a definition
of a cell which would absurdly oblige us to
call all such experimental laboratory material non-cellular?
If phylogeneticists wish to exclude ciliates
from trie very large category of organisms
built on the cellular plan of organization,
whether the cells involved occur singly, in
colonies, or in more permanent multicellular arrangements, they must keep in mind
the evolutionary gulf so created when they
attempt to trace lines all the way from the
origin of life on earth through protistan
groups to such highly evolved creatures as
man.
Thus, though the subject cannot be developed in extenso here, the value of considering ciliates as cells (maybe supercells?)
would seem to outweigh heavily their treatment as unique and isolated acellular microorganisms with independent origins of all
organelles, so many of which are strikingly
like those found in other members of the
(cellular) biotic world. Certainly, "cell"
and "organism" are not mutually exclusive
terms, although the late Libbie H. Hyman
(1940, and still in 1959) and several other
leading biologists apparently have not appreciated and do not appreciate the logic
of this observation.
PRESIDENTIAL ADDRESS
able, because the possible relationship of
either group to other plant and animal
assemblages may be totally different, depending on the answer. For example, if
they are in effect totally unrelated, then
flagellates might have given rise to metazoan
forms and ciliates might have sprung from
certain metazoa (or not); viz., flagellates—*
metazoa—»ciliates (or simply flagellates—*
metazoa). But if they are closely related,
then one or the other (presumably though
not necessarily) might have produced the
metazoa via the other; viz.,flagellates—*ciliates—>metazoa. Other combinations are also
possible. And, of course, either group might
be a dead-end specialized offshoot. Will
data from study of homologies allow a
choice from among these several alternatives?
In spite of known dissimilarities, in
modes of fission, nuclear composition, stages
at which meiosis occurs, types of sexual
phenomena exhibited, detailed cytoarchitectural differences, etc., the basic similarities between ciliates and flagellates has
been spotlighted by the advent of electron
microscopy (for a simple but significant example: flagella and blepharoplasts, cilia
and kinetosomes: couplets no longer separable) . Other convincing bits of evidence
exist for linkages and affinities between
and among flagellates and most other (nonciliate) protozoan groups, discussion of
which is beyond the scope of the present
paper. Thus, including the Ciliophora as a
legitimate assemblage within the phylum
Protozoa does seem a supportable, if conservative, view; admittedly, it may seem
debatable to others. An open mind is certainly necessary here.
Some taxonomic "house-cleaning" within
the Protozoa has been and will continue to
be necessary as our knowledge increases.
The opalinids, for example, are surely best
excluded from their long-held position
among the ciliates (Corliss, 1955; Honigberg
et al., 1964; Kozloff, 1972), though their
uniqueness suggests an isolated position on
the phylogenetic tree rather than the neat
role of a "missing link" of some kind between "regular" flagellates and the ciliates.
Other high-level enigmatic groups (not to
mention hundreds at lower levels) also con-
745
tinue to baffle and plague the conscientious
taxonomist (Corliss, 1960): principal ones
among these are the cnidosporidians, mentioned briefly above, minute parasitic forms
with highly unusual life cycles; the dinoflagellates, with some remarkably unique
features; the mycetozoa, some subgroups of
which surely have very close affinities with
fungi; the foraminifera, their fossil record
notwithstanding, with their curious dual
nuclear apparatus during a stage in the life
cycle; and the radiolarians (also with fossils, but again of no value outside the
group), with their beautiful, complex skeletons, incomparable central capsules, and
highly polyploid nuclei.
Kozloff (1960, 1972) holds some fascinating and iconoclastic views concerning the
"relatedness" of the various major protozoan groups known today; unfortunately,
his thought-provoking ideas have not yet
been published anywhere in any detail. In
the very recent chapter of his in the new
"Parker and Haswell" he has employed
purely vernacular names for the groups
in a kind of protest against the implied stability of formal, latinized names
and as a way of indicating our woeful lack
of solid knowledge concerning the phylogeny of forms which he believes probably
represent not one but several separate and
independent phyla. Interestingly enough,
Sandon (1963, 1966) hints at going even
farther in defying convention and tradition.
WHO WERE ANCESTRAL TO THE PROTOZOA?
There seems to be a great gap between
the Protozoa, no matter what their exact
composition as a phylum and their position
within the kingdom Protista, and the much
more primitive membership of the kingdom
Monera (see Copeland, 1956; Dodson, 1971;
Margulis, 1970; Whittaker, 1959, 1969; and
references therein, and disregard minor nomenclatural discrepancies). Unfortunately,
studies and speculation are most often
based solely on information obtainable
from extant forms. (Think, if it is not
too discouraging, of the many phyla, possibly other kingdoms, of pre-multicellular groups which may have arisen and fal-
746
JOHN O. CORLISS
len, never to be detected, in aeons of the
dim past!) But it would be comforting to
be able to identify an ancestral group or
groups, even if hypothetical, particularly
if it seems reasonable to retain the Protozoa on the main line of organic evolution.
Hope is to be found in the stimulating
writing of Margulis (1970), who has dynamically rejuvenated and refined the hypothesis of origin of eukaryotic organisms
by "amalgamations" of certain prokaryotic
forms: that is, by a series of selected symbioses which are predicted to have occurred
late in the long Precambrian Era. (Early
thinkers along such lines included Wallin,
1927; recent volumes of mainly biochemical
contributions to this subject: Charles
and Knight, 1970; Reinert and Ursprung,
1971). The idea of incorporation of "protomitochondria" and "protoplastids" in this
fashion is intellectually appealing, even
without any living or fossil evidence of truly
missing-link forms. Such an arrival of the
"protoflagellum"—and thus of the ultimate
flagellum-centriole complex as it is so
widely and well-known today—is, however,
much harder to accept. Other minor problems with the hypothesis, or with parts of
it, exist; but as nearly universally agreed,
the scholarly monograph by Margulis has
heuristic value and is causing scores of upset
"evolutionary microbiologists" to scurry
back to the (principally, alas) biochemical
laboratory in search of critical data which
will significantly support or refute one or
more of the bold propositions she propounds or endorses. Further direct consideration of her book would be out of place
here, but it should really be starred in the
bibliography. One of the most critical reexaminations of her ideas (and of those of
several others on the same subject), incidentally, appeared in the journal Science
as this paper was going to press (see Raff
and Mahler, 1972).
The ciliate Protozoa are classified as
eukaryotic cells, along with members of the
other groups included in the Protista (one
of thefivekingdoms of organisms, following
the recent scheme of Whittaker, 1969). The
Monera embrace all of the prokaryotic
forms. No one suggests that the ciliates
themselves sprang full-blown from prokaryotic ancestry. But other groups of Protozoa
(notably the flagellates, including certain
algae) which are commonly believed (e.g.,
see Pringsheim, 1963) to be directly ancestral to the ciliates very likely did have their
origins in early prokaryotic assemblages
of the remote Precambrian past: there
seems to be widespread, even universal,
agreement on this latter point.
There is another school of thought, however, with respect to origin of ciliates: it
holds that they may have been derived from
some multicellular or multisyncytial group
of "lower" invertebrate Metazoa represented most closely among extant animals by various turbellarian flatworms. Interestingly enough, this little publicized
viewpoint would exactly reverse the arrowhead in the phylogenetic line ciliates—>
turbellarians proposed long ago and revived
by Hadzi (1953) and others for the origin of
Eumetazoa from Protozoa, as discussed in
a subsequent section of this paper. Call for
Occam's razor?!?
CONCEPTS OF MONOPHYLY AND POLYPHYLY
One of the most perplexing unanswei'ed,
and often unanswerable, questions of phylogeny, applicable to several of the sections
of this paper and thus appropriate for brief
discussion at this point, is whether or not an
assemblage of organisms "higher" (i.e.,
more recent in origin) on the evolutionary
scale arose from essentially a single predecessor or predecessor-group (immediately
ancestral taxon of the same or lower rank),
via one or more lineages, or from a number
of quite diverse predecessors (polyphyly) of
the same rank and perhaps at approximately the same time in history. (Simpson,
1961, should be consulted for an excellent
and detailed exposition of these often misunderstood concepts.) The matter is of great
importance to taxonomy simply because a
polyphyletic situation of the kind just described must be repaired in the classification
scheme; that is, a single group of organisms
cannot have been derived from several other
taxa of the same rank. Such a polyphyletic
assemblage must be broken apart into several groups, until each, in accordance with
PRESIDENTIAL ADDRESS
Simpson's precise but not too restrictive
definitions, is monophyletic: derived from
a single common ancestor or ancestral
group. (Or repair can be made in some
other way, shuffling ranks and/or lineages
in some appropriate and acceptable
manner.)
It is important to note, however, that
polyphyly is still legitimate in another context, that is, to describe a situation in which
different ranks or taxa are involved. A convenient example from Simpson (1961) will
quickly make the distinction clear: at the
class level, the Mammalia arose monophyletically from the Reptilia, although five
independent lineages are postulated to have
been involved in the evolutionary process.
But at the family level, if all families are
lumped together and considered simultaneously, the origin of the mammals may
be viewed as being polyphyletic. Nonetheless, at the level of each mammalian family,
considered separately, the origin was, again,
monophyletic: the progenitors of any single
family were derived solely from an immediately ancestral taxon of the same, or lower,
rank through one or more lineages.
The primary problem is to recognize a
polyphyletic situation of the kind described
first above. Curiously enough, many taxonomists of the "lower" organisms do not seem
to have trouble doing this; unfortunately,
they often seem to ignore the second challenge, the need to correct or adjust the classification scheme to such a phylogenetic
conclusion.
With respect to the Protozoa, it is entirely
possible that many of the diverse groups of
this phylum (as generally recognized today)
did indeed arise from distinct, widely separated ancestral groups. Depending, of
course, on the ranks of the taxa involved,
there might be no close phylogenetic affinities or straight-line ancestral-descendant relationships among many of them. Their
classification together into one supergroup might simply represent "taxonomic
convenience," perhaps accompanied by the
"justification" that there are certain properties held in common, even if brought
about through convergence following aeons
of living in similar habitats, possessing
747
basically similar body plans (all "prisonniers de leur unicellularite": Faur6-Fremiet, 1953), and the like. But as soon as critical data do become available demonstrating the existence of tremendous differences
among protistan forms currently lumped
together, then failure to repair the polyphyletic situation by taxonomic removal of
the "offending" forms to separate highlevel taxa will be as criminal as it would
be today to persist in classifying whales
with fishes, the Tasmanian wolf with dogs,
or Li?niilns with crabs.
WHO DESCENDED FROM THE PROTOZOA?
Depending in part on conclusions reached
in reply to previous questions in this series,
no one or everyone may have descended
from one (or more) group (s) of the Protozoa. Perhaps more pertinently the central
question here should be: how could it have
come about?
There are several theories as to how organisms might have bridged the gap from
unicellularity to multicellularity. I shall
mention only those related to origin
of animal (i.e., eumetazoan) groups,
because there seems to be no doubt of the
relatively smooth evolution of "higher"
plants from algal (or phytoflagellate, if you
will) ancestry. A degree of over-simplification is dictated by space available, and
miscellaneous groups cannot even be mentioned here.
Essentially disregarded by everyone, but
perhaps worthy of passing attention, is the
possibility that holozoic multinucleate
amoeboid plasmodial forms, already really
syncytial in nature, became compartmentalized by appearance of complete internal
"cell" membranes, divided up their physiological tasks, developed "ectoderm" and
"endoderm" layers, etc. to become primitive, or pro-metazoan forms, eventually leading to ancestors of multicellular groups still
with us today. "From amoeba to man"
might be a more direct line than usually
visualized!
Long appealing have been various colonial theories, the original Haeckelian one
involving Volvox-like progenitors, neat aggregations of unicellular individuals formed
748
JOHN O. CORLISS
into hollow spheres poised for gastrulation
and an appointment with destiny. Modern
modifications suggest other kinds of colonial
organization than that represented by
Volvox itself (though still involving "lower"
algae orflagellates),with subsequent arising
of germ layers, further division of labor
among the cells and developing tissues, etc.
(see Hanson, 1958, and Hyman, 1940, for
review, critical comments, and references to
the pertinent literature). Problems of getting rid of plastids, cellulose, and (some)
flagella and acquiring mouths, digestive
tracts, etc. are never fully explained. Nevertheless, the basic idea remains the most
attractive one for many biologists today.
The early eumetazoan group thus derived
would presumably be the common ancestor
of certain present-day cnidarians and of
members of the flatworm phylum as well.
What is now widely known as the Hadzi
theory of origin of turbellarian-like metazoa
(alleged by his school to be the "lowest" or
first group of eumetazoan multicellular animals) from ciliate Protozoa is nearly as old
as the colonial theory, but has been revived,
and has been the cause of considerable comment, only relatively recently (see Hadzi,
1953, 1958, 1963; Hanson, 1958, 1963; Steinbock, 1963; and valuable references therein).
Primitive polyenergid ciliate-like organisms
could presumably have become compartmentalized (perhaps in the manner suggested briefly for amoeboid forms, above)
and, by such a cellularization process of
originally syncytial cytoplasm, have given
rise to primitive multicellular forms which,
in turn, would serve as the direct ancestors
of certain of the acoelous Turbellaria with
us today. Cnidarians would have come
along later. To me there appear to be
many drawbacks to acceptance of Hadzi's
hypothesis, in spite of its extension and
noble
defense
by Hanson
(1958,
1963), who has rigorously applied Remanian criteria of homology (Remane,
1956) in his analysis. Incidentally, proponents of the idea like to insist that ciliates, of long ago and still today, would have
to be considered acellular to fit the picture.
It is not entirely clear why such would have
to be the case.
In a stimulating discussion of the phylogeny of groups belonging to certain extant
"lower" metazoan phyla, Greenberg (1960)
draws a conclusion that represents a kind
of refreshing compromise with respect to
the possible protozoan ancestry of these
groups and with respect to which multicellular groups may have arisen first.
He concludes, using symmetry as one
of his criteria, that "the origin of the Cnidaria and Platyhelminthes is to be found
in separate groups of Protozoa."
It seems to me an inescapable conclusion
that multicellular forms can have arisen
only from unicellular forms, and then by
only one or the other (or perhaps both:
back to problems of polyphyly!) of two
pathways: via aggregations of originally
separate cells (present-day colonial species
of Protista indicate that at least some degree of this is not impossible of achievement) or compartmentalization of some sort
of single cell (more difficult to find persisting examples of this, although certain syncytial or coenocytic situations are suggestive).
Hanson (1958) has neatly termed these two
modes "integration of a protistan colony"
and "cellularization of a protistan individual."
Space does not permit treatment here of
the "aberrant" groups of multicellular organisms which, nevertheless, should not be
excluded from our thinking in considering
further the problems so briefly posed above:
for example, the Fungi, the Parazoa (Porifera), the wholly fossil Archeocyatha, the
so-called Mesozoa, and Grell's (1971a, b)
tremendously exciting placozoa, established
for Trichoplax adhaerens.
CLASSIFICATIONS REFLECT PHYLOGENY?
This topic is interjected, very briefly,
because of the sincere desire of many phylogeneticists, on the one hand, to influence the
arrangement of taxonomic categories of organisms and of many systematists, on the
other hand, to use evolutionary considerations in construction of their schemes.
(This need not lead to circular reasoning,
as some seem to claim.) Entire books have
been written on the subject (a recent ex-
PRESIDENTIAL ADDRESS
ample: Hennig, 1966), and I have no intention of getting embroiled or enmeshed
in the seemingly endless, most philosophical, often abstrusely logical arguments of
which came first, or what is meant exactly by a "natural" classification, or
how "phenetic" treatments may or may
not represent the only truly "objective"
approach in comparison with "cladistic" and "phyletic" methods, etc., etc.
(see the well-developed arguments, special
aspects of the controversies involved, biased
views, historical approaches, etc. in either
such worthy selected references as the following or in works cited therein: Dougherty
etal., 1963; Hennig, 1966; Hull, 1967, 1970;
Mayr, 1965a, b, 1969; Michener, 1970; Remane, 1956; Rensch, 1959; Schlee, 1969;
Sibley, 1969; Simpson, 1961; Sneath, 1969;
Sokal and Camin, 1965; Sokal and Sneath,
1963; Wagner, 1969).
A good classification, along with other
attributes, must be convenient and predictive (Mayr, 1969). If a taxonomist's labors
are to be .useful he must be at least somewhat pragmatic in his outlook, although
classification-making itself is an inductive
process. Darlington (1971) has recently
stressed a need for "a return to reality" in
"modern practical taxonomy," and Mayr
(1971) has lashed out at inefficiency in
methods of taxonomic research, with constructive suggestions for improvement.
Many working biologists depend on a
reasonable scheme of classification to provide them with a framework onto which
they can hang at least tentatively the organism or group of organisms they study. The
classifier who is a perfectionist is apt to
become completely immobilized by frustration: how does one set about creating
the ideal hierarchial arrangement of great
groups of diverse biological entities? He
has to either make lavish use of question marks (if his scheme is presented as a "phlylogenetic tree"); or include
numerous "Anhangen" or "incertae sedis"
appendixes to each major grouping; or resort to purely vernacular names, a neat
escape from the decision of what levels of
rank to use (and it even avoids the minor
problem of deciding for or against uniform
749
endings on names of equivalent ranks: Corliss, 1962a).
Supposedly cognizant of the difference
between "key" characters and those of presumed "basic phylogenetic importance" (another disputed concept beyond the present
discussion), the classifier must still rely
heavily on intuition, common sense (and
occasionally courtesy: Corliss, 1972a), and
ought to keep in mind the utilitarian principles alluded to above. He should understand such evolutionary concepts as monophyly and polyphyly (see a preceding section), but parsimony should also be a guiding factor. Since he is very likely to be using
information from others, in any extensive
work involving high-level taxa, he should
recognize the age-old difference, among his
suppliers of data, between lumpers (e.g., all
mammalian carnivores are either cats, dogs,
or bears) and splitters (if two forms differ
slightly they belong to separate genera; if
not at all, to separate species). He should
boldly swing Occam's razor (but with caution, too, for it may be double-edged), while
not being overswayed by similarities which
are superficial or by theories which have
behind them only the weight of classical
tradition or the stentorian voice of an autocratic authoritarian. And it might help if he
followed the rules of nomenclature (Corliss,
1962a, b; ICZN, 1964; Mayr, 1969) when
applicable.
Incidentally, what degree of difference in
characters, what measure of discontinuity,
what gap size of distinctness, should constitute a proper and uniform basis for separation of organisms at the several higher
(supra-familial) taxonomic levels—within
any major group: microorganisms, plants,
or animals? This is an intriguing question
(even if perhaps poorly put here); and it is
one of a general but widely applicable nature, only long neglected and never satisfactorily answered. With the exceptions of
Van Valen's (1969) brilliant quantitative
analysis of the comparability of categories
in different phyla, unfortunately not yet
published, and brief treatments by Michener (1957) and Mayr (1969), phylogeneticists and pheneticists alike have seemed to
avoid even mention of the problem, let
750
JOHN O. CORLISS
alone offer proposals for its possible solution. Guidelines would be of incomparable
value (and those of Mayr, 1969, are helpful), especially in fields concerned with
the taxonomy of minor phyla or of less
well-known groups for which only a fraction of the total number of species very
likely extant in the world have actually
been described and properly named to date.
With respect to a phylogenetically-oriented classification of the Protozoa, the
greatest single difficulty is the lack of a
widely usable fossil record; but close behind
is the dearth of available taxonomic characteristics of differential value. Shockingly
enough, families or even orders may be
separated by only one or two "major" differences, and the significance of these may
sometimes be in doubt. Over-consideration
of the level of organization or of the general
habitat may falsely be holding the membership of certain high-level groups together.
A third discouragement, hard to be appreciated by such people as taxonomic ornithologists, is related to the fact, alluded to earlier,
that only a fraction of the protozoan species
living today have to date been found and
described: transiency of schemes of classification is thus inevitable from this cause
alone. Nevertheless, I should like to make
a plea, conservative though it may be (in
comparison, e.g., with the ideas of Kozloff,
discussed briefly in a preceding section), for
continued use of the celebrated "Honigberg
Report" on the classification of groups of
Protozoa down to the level of suborder
(Honigberg et al., 1964), at least for a few
more years. In spite of faults and growing
weaknesses, its general soundness and relative up-to-dateness, and the welcome degree
of stability which it has given to protozoan
systematics, has made its production a most
worthwhile international project: a revised
scheme might well be brought about by a
similar "committee approach"—and the
time to start it is now.
Because of their close internal unity
(see below) and the convenience of
quite easily identifiable cortical characters,
the ciliates have not seemed to present as
many problems to taxonomists as do the
other subphyla of the Protozoa. A quarter
of a century ago it appeared that FaureFremiet, long the leading systematic ciliatologist of the world until his death in
1971 (see Corliss 19726, for a tribute and
an evaluation of his works), employing
the most modern approaches then possible,
had at last produced a sound and longlasting scheme of classification clearly based
on presumed phylogenetic interrelationships among the major classes and orders
(see Faure-Fremiet, 1950; and the historical
considerations in Corliss, 1956). Yet, before
many years had passed, there were already
growing indications of a need for additional
revision, possibly even drastic overhauling
(e.g., see Canella, 1964, 1971; Jankowski,
1967; Small, 1967): evidence of the "changing world of ciliate systematics" (Corliss,
1969), whether we like it or not! Necessitating revision are new data, especially
those derivable from more and more extensive use of transmission and scanning electron microscopy and from more and more
intensive comparative study of patterns of
morphogenesis, and new ideas, hypotheses,
interpretations, and synthetic approaches.
IS THERE UNITY AMONG THE CILIATES?
Interestingly enough, the answer to this
particular phylogenetic question seems to
be a resounding one in the affirmative, from
all quarters. To the envy of students of
other major protozoan groups, the ciliates
appear to be a compact assemblage
of basically interrelated forms (Corliss,
1960, 1961), an assumption strengthened
rather than weakened by such critical modern approaches as the use of electronmicroscopy.
In spite of the unity among these Protozoa ("once a ciliate, always an infraciliature": Corliss, 1961), there is no such
organism as a "typical ciliate," a concept
to be avoided by taxonomists, experimentalists, and textbook writers alike.
Many problems are still present, of
course! How the ordinal taxa (if ever a
decision can be made as to their number
and what they are) are interrelated and how
they should best be arranged in a scheme
of classification remain unresolved questions
751
PRESIDENTIAL ADDRESS
concerning their phylogeny. In preceding
sections I have mentioned some of the riddles surrounding the ancestry of the group
as a whole and its possible descendants.
Yet even within the assemblage it is far
from clear as to what groups came first (or,
better, what extant groups most resemble
what were probably the first ciliates), which
are most highly evolved, and what characteristics are most trustworthy for making
deductions concerning affinities and phylogenetic lines.
Since the very existence of their macronuclei make the ciliate Protozoa unique in
the whole biotic world, some studies of them
have been undertaken from the point of
view of throwing light on the origin of
nuclear dualism and, simultaneously, logically enough, on the evolution of ciliates
themselves. Discussion of this intriguing
approach, not well publicized even among
protozoologists, is beyond the scope of the
present paper. Suffice it to mention that
certain "lower" marine gymnostome ciliates,
especially forms inhabiting the sands of
intertidal zones, appear to be the most primitive in their nuclear set-up and thus also,
in my opinion, the most likely candidates,
among surviving groups, for closest relatives
to the original "proto-ciliate." For a very
comprehensive review of the macronucleus
in general and for references to its evolution, see the recent excellent paper by
Raikov (1969), a young man who, himself,
is already an acknowledged and highly respected leader in the field of origin and
evolution of nuclear dualism in ciliates.
Extended discussion of the possible phylogenetic pathways in the evolution of the
Ciliophora is not appropriate here, though
even the more recent of the older ideas (e.g.,
see Corliss, 1956) are already demanding updating and revision (Corliss, 1969; and unpublished notes of mine). As mentioned in
preceding sections, new data, new interpretations, new hypotheses, and even old warnings and words of caution are responsible
for a new new look at these fascinating
creatures.
Continued study of the ciliate Protozoa
may, directly or indirectly, throw general
illumination on some of the unresolved
problems of animal and even plant phylogeny. At least, the possible contributions
of this research to such matters should not
be overlooked. Keeping an open mind,
however, is the requisite of key importance,
difficult though this may sometimes be of
achievement, in investigations undertaken
in this intriguing area of biological inquiry,
as in all others.
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POSTSCRIPT
I wish to thank Editor Joseph T. Bagnara and Thomas J. Griffiths Sons, Inc.
(the printer) for so kindly allowing numerous minor emendations and several
additions to this paper at proof-reading time, changes which I hope have made
the work potentially more useful and understandable to the general reader as
well as to the specialist in problems of protistan phylogeny and evolution.
Space permitting, I should also like to take this opportunity to mention
very briefly that major symposia and roundtable discussions on subjects not
dissimilar to many of those touched on in this address are scheduled for two
important international meetings taking place next year. These are the First
International Congress of Systematic and Evolutionary Biology, convening at
Boulder, Colorado, 4-12 August 1973; and the Fourth International Congress
of Protozoology, meeting in Clermont-Ferrand, France, 2-10 September 1973.
J. O.C.