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The Maupas Medal : Nodes on the Ciliatology Net
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Emile Maupas (1844-1916) ...and the Maupas MedaI
Essay: The Continuing Story
Flashback: Nanney's Review of Graham Bell's Sex and Death in Protozoa
Maupas Update
From Emile Maupas: "Prince de Protozoologistes" (First Page of biography by Edmond Sergent, 1955. Archives de L’Institut Pasteur D’Algerie 33:152-164.) English Translation: Emile Maupas: Prince of Protozoologists

The title is not mine. On the 11th of April, 1948, Professor Enrique Beltran, professor of Biology at the University of Mexico, asked how he could obtain a photograph of the ‘gran protozoologo frances, que alguin califico como el principe de los protozoologicos'. Professor Beltran requested a good photograph of Maupas and also of the medal commemorating his work which his friends had struck in 1913, after having requested subscriptions from all parts of the world.

Earlier, in 1909, in similar terms, Dr. E. Roux, Director of the Institute Pasteur in Paris, spoke of Maupas to Alfred Giard, his colleague at the Academy of Sciences, Professor at the Sarbonne and Head of the School of French Zoology at the time. Why, he asked Giard, has Maupas not been formally honored. He is the greatest zoologist living today. The Governor General, C. Jonnart, alerted, immediately undertook to decorate Maupas with the Legion of Honor.

How paradoxical it seems! This master naturalist began his career in literature. Born in 1842 in Calvados, in the village of Vaudry, some 60 kilometers from Caen, he studied humanities at the communal college of Vire, and entered the School of Chartres. >> Maupas Bibliography

Essay: The Continuing Story

During his lifetime, Emile Maupas was well-known, not only as a meticulous microscopist, but as a thoughtful and independent interpreter of the events he observed. He described, for example, the nuclear divisions and movements that occurred during conjugation in strains of paramecium, and disagreed with the description published simultaneously by Richard Hertwig, the noted German cytologist. The discrepancy in their accounts involved the fates of the macronuclear anlagen produced after synkaryon formation. in exconjugant cells. Hertwig reported that the macronuclei were separated at the first cell division. Maupas, on the other hand, claimed that the macronuclear anlagen fused into a single new macronuclear anlagen.

Later, when Tracy Sonneborn (1937) discovered mating types in paramecium and learned to control conjugation, the fates of macronuclear anlagen became an important issue in mating type epigenetics. In some species of paramecium Sonneborn (1947) found that mating types were distributed randomly among the division products of exconjugants, which according to his own observations contained separate new macronuclei. He called the first division products of exconjugants (and exautogamonts) “karyonides”, and concluded that newly established new macronuclei, though genetically identical, underwent random epigenetic alterations. These epigenetic modifications, he argued later (Sonneborn 1957), provided the possibility of inbreeding among the progeny of a single conjugating pair. He considered karyonidal mating type inheritance an adjunct adaptation to an inbreeding ecogenetic strategy.

` In a careful analysis of the early cytological descriptions, Sonneborn noted that Hertwig isolated conjugating pairs of paramecium into fresh culture medium before undertaking cytological examination. Maupas, aware of the high frequency of death at conjugation in natural populations, and suspecting that placing pairs in fresh medium might contribute to their distress, always kept his conjugants in the original medium. Hertwig, in effect, observed the post-fertilization events in fed cells, while Maupas described conjugation in starved cells. Sonneborn (1947) confirmed this inference by observing macronuclear fusion in starved conjugants.

Nanney (1953), in a follow-up experiment, used the phenomenon of macronuclear fusion to confirm the macronuclear site of mating type fixation, as well as a plausible explanation for the vegetative “selfers” that occur in some strains of paramecium. He starved exconjugants of a strain of (now) P. primeaurela that had never produced selfing karyonides. After several days he observed fused macronuclei, and first fission products often produced selfing “karyonides”. This experience led to a similar explanation for the normal selfing karyonides of tetrahymena. The quantitative analysis of the assortment kinetics of the tetrahymena selfers (Allen and Nanney, 1958; Schensted, 1958, Nanney 1964), led to the first - and a remarkably robust - estimate of the number of assorting genetic units in a ciliate macronucleus.

Nanney’s more embarrassing intersection with Maupas had come a little earlier. When he left Indiana in 1951, hoping to escape the “crowded” culture of paramecium genetics, he encountered A. M. (Del) Elliott at the University of Michigan, who had studied the nutrition and physiology of ciliated protozoa for many years. Nanney learned that tetrahymena had much simpler nutritional requirements than paramecium, but had never been studied genetically, for the simple reason that tetrahymena had no sex. A quick cytological examination of lab strains seemed to explain the problem; they were all without micronuclei. A hurried dash to local ponds and streams brought in many new strains, and these had micronuclei, and mated avidly when deprived of food. (Elliott and Nanney, 1952; Nanney, 1953).

In preparing to publish the nuclear events at conjugation, Nanney sent a draft of the manuscript to Tracy Sonneborn for comment. Sonneborn’s advice was to check Emile Maupas; these drawings looked awfully familiar. Indeed, Maupas’ drawings could have been used to replace those Nanney had prepared. Here the disconnect was semantic, or taxonomic if one doesn’t worry about offending colleagues. The word tetrahymena was coined by Furgason (1940) to define a group of small ubiquitous ciliates that could be distinguished in silver stains (Chatton and Lwoff, 1936) by a distinctive set of oral membranelles. Before Furgason’s analysis, the small ciliates went under a variety of names, that were unstable in the absence of a firm morphological reference. We cannot be sure, in fact, which of the cytological sequences described by Maupas refers to which of the “modern” tetrahymenas. The basic patterns are remarkable conserved.

Maupas’ largest impact, however, came not directly from his microscopical work, but from his involvement in the theoretical tempests at the turn of the century. While observing his laboratory cultures, Maupas came to believe that unicellular organisms have a finite life cycle, that they are not capable of indefinite replication, but pass from immaturity to maturity, and from maturity to senescence and death, unless the program is interrupted by a sexual episode that starts a new program. This concept of the “maupasian life cycle” engaged a lot of attention. Many investigators denied the validity of the concept, and claimed that protozoa were in fact immortal. Even some of the early workers on paramecium denied a natural limit on the somatic cycle. The most famous of the investigators bent on contradicting Maupas was L. L. Woodruff (1932) at Yale University, who periodically displayed the records of his “Methuselah” strain of paramecium, whose division rate would occasionally falter, but whose ability to divide recovered and continued year after year.

As with other classical puzzles, Sonneborn found an explanation. During the periodic slowing of growth in the Methuselah strain, some peculiar reorganization events - first called endomixis - were reported. When this process was eventually analyzed carefully, Sonneborn (1939) found that the reorganization was in fact “autogamy”, a sexual process involving meiosis and fertilization. He further showed that the prevention of autogamy for a time (by continuous feeding) resulted in death when sexual processes were again allowed. Paramecium is not capable of indefinite vegetative growth. Paramecium, when analyzed with appropriate genetic controls has a programmed life cycle, with intervals of immaturity and adolescence followed by sexual maturity, competence for autogamy, and eventually senility and death.

Maupas’ interpretation of the programmed ciliate life seemed finally to have been vindicated. Its acceptance on a broader biological terrain was, however, disputed. Studies on protozoa were always subliminally treated as proxies for studies on real animals. The development of tissue cultures and cellular explants brought Ross G. Harrison fame and prizes, because the work brought hopes and portended dramatic advances in health care and organ replacements. The validity of the ciliate studies was denied because they contradicted the accepted wisdom concerning the behavior of explanted vertebrate cells in culture. Human cells were believed to be potentially immortal. If ciliates showed programmed cell death, the phenomena were irrelevant, or the experimenters were mistaken. Only when finally Leonard Hayflick (1967) established the finitude of life span in vertebrate cell cultures, was it possible to accept the Maupasian life cycle in ciliates. But the acceptance of the vertebrate parallel came too late to revive the protist studies. And a new word was coined to designate the phenomenon apoptosis. >>Bibliography

Nanney’s review of Graham Bell’s Sex and Death in Protozoa, J. Euk. Microbiol. 43: 159-160.

Bell, Graham. 1988. Sex and Death in Protozoa. The History of an Obsession. Cambridge University Press, Cambridge. ISBN 361419. 199 pp. $59.95, cloth.

Bell’s book is the result of a foray of a brave population biologist, normally employed in the context of higher organisms, into the badlands of the eukarvotic protists. The book deals with a traditional theme in protozoological research, dating back over a century to the concerns of the French librarian Emile Maupas, i.e. the ciliate life cycle.

According to Bell. “The problem (of a closed life cycle in ciliates) was never resolved: after fifty years it was simply abandoned.” (p. 5) The “fusty old Maupasian controversy” has been given another look and evaluated with new tools, leading to new conclusions, to wit: “The existence of a life-cycle in asexual protists therefore represents a serious challenge to current evolutionary theory. I have interpreted the later stages of this process as being caused by the irreversible accumulation of deleterious mutations in isolate lines.” (p. 131)

“Protozoan senescence is the nonadaptive consequence of an irreversible accumulation of deleterious mutations under the (Mullerian) Ratchet. The ciliate life history evolves as a con-sequence of senescence, with the period of immaturity repre-senting a compromise between senescent decline favouring ear-lier maturity, and the expense of nuclear reorganization favouring later maturity. These are three quite distinct processes, and few if any useful parallels can be drawn between them.” (p. 134)

There it is. The ciliate life cycle, from Maupas on, “‘as a misunderstanding, the consequence of an “obsession.” Isolated ciliate lineages certainly die off, but only as a consequence of steady mutational erosion, by damages that cannot be removed by recombinational dispersion. The death is not programmatic nor is it a consequence of ecogenetic adaptations.

The “misunderstanding” concerning clonal life histories is disposed of by the formal analysis of selected data, leading to the conclusion: . . . where adequate data are available the se-nescence of a series (of isolation lines) does not usually involve the sudden death or total sterility of an increasing proportion of its lines. Rather, there is a gradual decrease in vitality in all lines.” (p. 105)

The destruction of the clonal life cycle as a species adaptation reduces the noise within Bell’s own unified evolutionary theory [I]. Whether it reduces the noise within ciliatology is more problematic. Sonneborn’s 1954 critical examination of the issues in Paramecium [2] led to the conclusion that postsexual vegetative functions were initially vigorous, but that after a species specific interval they declined in a progressive way to extinction. This is the conclusion reached by both myself [3] and Smith-Sonneborn [4]. We accepted the reality of adaptive clonal life histories, and focused primarily on mechanisms of control. Data documenting the Sonnebornian view on Tetrahymena [5] and on Paramecium [6] are cited by Bell (p. 166) but are treated in a different context.

In any case, I am glad that Bell has written this book. At least I think that I am glad. My judgement turns on whether the book preempts or promotes the book I hoped he had written when I first saw his title. I know that it isn’t fair to evaluate an author’s work by comparison with a book he did not attempt to write. But I am concerned that Bell’s book may be perceived not as a preface to a larger work but as an obituary for an obsolete perception. His take-home message is not that ciliate phenonena require consideration, but that the work of ciliatologists is safely ignored.

My impression is that the conclusions in Bell’s book are based on inadequate understanding of the data and of the genetics and natural economy of protists. I suspect that his search for sim-plification has done violence to genuine understanding. (I hesitate to be critical of the efforts of a disciplinary outsider, for the last thing protistologists need at this juncture is an exercise In territorial imperative. And even if Bell is mistaken in his evaluation of the phenomena, one must applaud his use of the comparative method as an approach to more generalizable knowledge.)

To clarify what may seem to be cryptic allusions to scientific territories, I have to commit a little undisciplined historiography (hagiography even?) myself. The book I was hoping to read was a book that my mentor, Tracy Sonnebom. was poised to writen the mid l950s. He did prepare a first draft [7]. Tracy Sonneborn was a true neo-Darwinian, a selectionist uncontaminated with the neutralism that was yet to come. He was a champion of the comparative method, and often pronounced when differences were perceived among species, “If a difference exists, there’s a damn good reason for it.” He sought to find adaptationist explanations for the remarkable diversity of life histories among the ciliated protozoa, even among species that seemed indistinguishable upon casual inspection.

Species of ciliated protozoa have different numbers of mating types. They control their mating capacities by mechanisms with radically different effects—e.g. by arrays of alleles at a single locus, by multilocus combinations, by complex methods of macronuclear differentiation with environmental effects on the outcomes, and by the use of parental cytoplasm to control nuclear determination. Associated with evidences of diverse sexual life styles are differences in such things as characteristic species ranges, tendency to resort to endogamous mating, karyotypic uniformity, rate of vegetative reproduction, and length of time between sexual episodes.

In the present context, we note that Sonneborn included in his encylopedic descriptions the striking differences among ciliate species in the total length of the clonal life span. Sonneborn did not merely describe the species diversities, he sought to explain the diversities as an inclusive and coherent neo-selectionist exercise. His thesis was that ciliated protozoa had divided Darwinian space into niches defined along a single inbreeding— outbreeding gradient, the position of a species or a species group being defined by a gradient of “need” for recombinational variety.

This thesis was articulated and argued in one of Sonneborn’s longest, most original, and most neglected publications [7]. Graham Bell does not list this paper in the bibliography of his book, and is uncomfortable with the proposed ecogenetic context of variations in ciliate clonal life cycles. He treats data on ageing and death in ciliates primarily as an opportunity for demonstrating interesting methods in graphic and correlational analysis, and seemingly seeks to diminish if not destroy belief in a bothersome observation. Bell seems to consider the special features of ciliate cytogenetics and life style as irrelevant. I am afraid I have to consider his analysis in much the same terms. Having gone so far in this historical commentary, I need perhaps go a little further, and try to explain the neglect of what I believe to have been an important contribution of a prominent and highly respected biologist.

One can perhaps assign some responsibility to ‘the times.” Molecular genetics was gathering momentum. Research on the material basis of clonal heredity, that had preoccupied Sonneborn and established his authority, was now out of focus and out of fashion. Organisms in which cytoplasmic inheritance had been studied were neglected in favor of the powerful molecular technologies of bacterial and viral genetics.
“The times” also includes prevailing concerns in other bio-logical arenas, and these did not yet include details of life his-tories of unimportant organisms. The “modern synthesis,” the formal union of genetics and evolution, had been completed with the exception of occasional skirmishes with backward disciplines that had yet to get the message. The efflorescence of a new population genetics founded on the consensus had not gathered strength. We did not think much at the time about adaptive strategies, selfish genes, inclusive fitness, and ecogenetics. Sonneborn was either badly out of fashion in his preoccupation with Darwinian themes, or ahead of his time in anticipating interest in perspectives that would flood Evolution and The American Naturalist in another decade.

Perhaps the main reason for the neglect of this work, however, was its failure to be pressed forward by its author. The published paper is a draft, not easy to read and understand, and without Sonneborn’s usual polish. Nevertheless, it contained the sketch of an important thesis that deserved continued investment. I myself repeatedly urged Sonneborn to expound upon the themes, but found him adamantly opposed to any further public presentation. In the 1960s I even tried myself to write the book (Sex and the Single Cell) that he would not undertake. After a few introductory chapters I discovered that I lacked the theoretical and mathematical tools that would be necessary to argue the issues persuasively. Since then I have tried, unsuccessfully thus far, to provoke a student or colleague to write the book on protistan genetic economies. Perhaps Nyberg or Dini will yet do the job that Graham Bell has begun.

I don’t intend to be meanly critical of Bell’s effort, partly because I suspect that Sonneborn’s uncharacteristic failure to follow through with his own thesis can be attributed to an unsympathetic reception to his incursion into a new field. Ernst Mayr organized the symposium at which Sonnebom presented his ecogenetic hypothesis, and Mayr judged the contribution faulty. He seized upon an awkward neologism as evidence that Sonneborn had no real understanding of the modern synthesis. Just read the entries under ‘Sonneborn” in The Growth of Biological Thought and elsewhere, to identify the pigeonhole among the ignorant to which Sonnebom was assigned.

If the magisterial Mayr didn’t understand that Sonnebom was well ahead of the game, one must not be too harsh on subsequent generations. And if the established and autonomous Sonneborn could be discouraged from exploring new territories because of frowns from the game warden, protectors of disciplinary territories should be cautioned about overly nice criticisms of friendly visitors.

D. L. NANNEY. Ecology, Ethology and Evolution. University of Illinois, Urbana, Illinois 61801.

Received 11-18-92, accepted 11-18-92


I. Bell, G. 1985. Evolutionary and non-evolutionary theories of senescence. Amer. Natural., 124:600—603.
2. Sonneborn, TM. 1954. The relation of autogamy to senescence and rejuvenescence in Paramecium aurelia. J. Protozool. 1:38—53.
3. Nanney, DL. 1974. Aging and Long-term temporal regulation in ciliated protozoa. A critical review. Mech. Aging Devel., 3:81—105.
4. Smith-Sonneborn, J. 1980. Genetics and aging in protozoa. bit. Rev. Cytol.. 73:319—354
5. Weindruck, R.H., and Doerder, F.P. 1974. Age-dependent in’-cronuclear deterioration in Tetrahymena pynjformis. syngen I. Mech. Aging Devel., 4:263—279.
6. Smith-Sonneborn. I. l97l. Age-correlated sensitivity to ultra-violet radiation in Para,neciu,,3. Genet. Res. 46:64—69.
7. Sonneborn, TM. 1957. Breeding systems, reproductive meth-ods, and species problems in protozoa”. in Mayr, E. (ed.), The Species Problem. Amer. Assoc. Adv. Sci.. Wash. D.C. Pp. 155—324.
8. Mayr, E. 1982. The Growth of Biological Thought: Diversity, Evolution and Inheritance. Harvard Univ. Press, Cambridge.

Maupa Update - Aging

"Every generation has to rewrite its history." And in doing so it discovers new heroes, and new villains, new antecedents, and more nuanced judgements. The disciplinary myths that substitute for historical understanding particularly have to be revised, even with some trauma. The materials presented above make Emile Maupas seem to be a unique, if somewhat forgotten, founder of much of significance in modern ciliatology. But even as "big fleas have little fleas", so also do predecessors have predecessors. A recent study by Lustig, listed below, on the biological turmoil at the beginning of the 20th century, makes clearer the contributions of a community of ciliatologists contemporary with and preceding Maupas, particularly Ehrenberg, Englemann, Butschli, R. Hertwig, Dobell, Jennings and Calkins. These materials have to be woven into the fabric of understanding, along with a more sympathetic treatment of Bell’s "Sex and Death" than I was able to muster when I first read his book.

Bell, G. (1982). The Masterpiece of Nature. London:Croom-Helm, Berkeley, University of California Press. (The Red Q ueen)

Bell, G. 1988. Sex and Death in Protozoa: The History of an Obsession. Cambridge Univ. Press, Cambridge.

?.....given favorable conditions and protected from shocks, perhaps the cycle of growth and division would continue indefinitely, and thereby prove that natural death was not after all inevitable. Ehrenberg (1838) appears to have been the first to publish this speculation, and by doing so ushered in one of the great debates of biology.
?Ehrenberg’s suggestion was opposed by Englemann (1862, 1876) and Butschli (1876), who found that after a long time in culture ciliate protozoans began to show morphological abnormalities which they interpreted as senescent degeneration akin to that of metazoan cells.
....”These views were memorably opposed by August Weismann (1889, 1891)....”
“....the generality of senescent decline and its reversal by sexual conjugation was not firmly established until the classical work of Maupas (1888, 1889). In his very very extensive experiments he not only laid the te ¸chnical and conceptual foundations for almost all the subsequent work on the subject, but claimed to demonstrate that protozoan cultures pass through a life-cycle comparable to that of metazoans, except, of course, that it is the life-cycle of a clone rather than of an individual.”

Butschli, O. 1876. Studien uber die Entwichlungsvorgange der Eizelle, die Zellteilung und die Conjugation der Infusiorien. Abh. Senchkenberg Naturf. Ges. 10:213-452.

Ehrenberg, C. G. 1838. Die Infusiontiere als Volkomme Organismen. Leipsig.

Engelmann, T. W. 1862. Zur Naturgeschichte der Infusionthiere. Z. Wiss. Zool. 11:1-47.

Engelmann, T. W. 1876. Uber Entwicklung und Fortplanzung der Infusorien. Morph. Jahrbuch. 1:573-634.

Hayflick, L, and Moorhead, P. S. (1961). The serial cultivation of human diploid cell strains. Exp. Cell Res. 25:585-621.

Ishikawa, Y., Suzuki, A., and Takagi, Y. 1998. Factors controlling the length of autogamy-Immaturity in Paramecium tetraurelia. Zoological Science 15:707-712. (“maternal effect”, age of parent on immaturity of progeny)

Lustig, A. J. 2000. Sex, death and evolution in Proto- and Metazoa, 1876-1913. J. Hist. Biol. 33:221-246.

Abstract. In the period 1875-1920, a debate about the generality and applicabiity of evolutionary theory to all organisms was motivated by work on unicellular ciliates like Paramecium because of their peculiar nuclear dualism and life cycles. The French cytologist Emile Maupas and the the German zoologist August Weismann argued in the 1880s about th òe evolutionary origins and functions of sex (which in the ciliates is not linked to reproduction), and death (which appeared to be the inevitable fate of lineages denied sexual conjugation), an argument rooted in the question of whether the ciliates and their processes where (sic) homologous to other cellular organisms.......Where Maupas (contra Weismann) made the ciliates qualitatively the same as all other organisms in order to achieve a coherent evolutionary theory for biology, Jennings and Dobell made them qualitatively different in order to achieve the same end.”

Muller, H. J. 1964. The relation of recombination to mutational advance. Mutation Res. 1:2-9. (Muller’s Ratchet)

Smith-Sonneborn, J. 1981. Genetics and aging in protozoa. Int. Rev. Cytol. 73:319-354.

Smith-Sonneborn, J. 1985. Aging in unicellular organisms. In “HandbooK of the Biology of Aging, 2nd Ed, (C.E. Finch and E.L. Schneid "er, ed.) Van Nostrand Reinhold, New York, 79-104.

Siegel, R.W. 1967. Genetics of ageing and the life cycle in ciliates. Symp. Soc. Exp. Biol. 21:127-148.

Takagi, Y. 1998. Origin of Cellular Lifespan: From a View of Paramecium. Presented at INABIS ‘98 - 5th Internet World Congress in Biomedical Sciences at McMaster University, Canada.

“Until about the middle of this century, the cells of both unicellular and multicellular organisms were thought to have the potential to divide indefinitely. This was disproven by Sonneborn [1] in Paramecium and by Hayflick et al. [2] in normal human cells cultured in vitro; both kinds of cells age with cell division and die after a definite number of cell divisions, called the “Sonneborn limit” for Paramecium cells and “Hayflick limit” for human cells.”