Maupas_1900

MODES AND FORMS

OF

REPRODUCTION OF NEMATODES

BY

E. MAUPAS

Curator of the National Library of Algiers

Translation from the French: Marie-Anne Félix

INTRODUCTION

Nematodes reproduce and multiply solely by oogenesis. No case of scissiparity nor of blastogenesis is known at present among them1.

For a long time, it was believed that their eggs were always and exclusively the product of the participation of distinct females and males, in other words that dioicy was among them the absolute rule.

This belief was actually the necessary result of the historical development in the study of these animals. For many long years, indeed, researchers have mostly dealt with parasitic species, then with marine species. In both of these groups, of which a large number of representatives are already known, separation of sexes appears to be an almost absolutely constant rule.

As far as marine species are concerned, all authors who made them the subject of their research, Ebhert (1863), Bastian (1865),

1 The singular phenomenon of extroversion of the genital organs of the female of Sphærularia bombi and the hypertrophic development that they undergo following this hernia have nothing in common with gemmiparity, as Schneider believed it to be (Monographie der Nematoden, 1866, p. 322).

MODES AND FORMS OF REPRODUCTION OF NEMATODES. 5

species in the Rhabditis genus can still be distinguished using the females, as long as they are carefully described and studied.

In any case, Schneider made long-term cultures of those species without males and saw them reproduce for many generations. Moreover, in all of them he observed the presence of spermatozoa in the uterus and, by observing larvae reaching the adult stage, he saw the genital gland produce first spermatozoa, then oocytes, the latter being fertilized upon their arrival into the uterus by the spermatozoa that were stored therein. All these Rhabditis were thus unquestionably protandrous autogamous hermaphrodites.

Schneider wonders if these hermaphrodites are able to reproduce themselves indefinitely through autogamous eggs. The fact appears to him improbable and he assumes that they undergo a heterogonic development, analogous to that described by Leuckart and himself in Ascaris nigrovenosa. The hermaphroditic generations must alternate with a dioicious generation, which appears in yet unknown circumstances and which is yet to be discovered 1. We do not share his opinion, and all our observations tend to make us believe that these hermaphrodites perpetuate themselves indefinitely by autogamy.

In addition to these Rhabditis, the German scientist also acknowledged the hermaphroditism of a Dorylaimus (Enoplus liratus) and, as said above, was the first to demonstrate the hermaphroditic condition of the parasitic generation of Ascaris nigrovenosa.

It is to Schneider again that we owe the first observation of a truly parthenogenetic species 2. Unfortunately, he did not describe

1Claus also argues for the necessity of a dioic form that would alternate with the hermaphroditic form. Beobachtungen über die Organization und Fortpflanzung von Leptodera appendiculata, 1869, p. 22.

2Monographie der Nematoden, 1866, p. 321.

nor illustrate this species, and only gave us some details about its genital organs. He saw it multiply without ever encountering males and without seeing the least trace of sperm in its uteri. Bütschli 1 believes that he rediscovered the species of Schneider and described and illustrated it under the name of Rhabditis Schneideri. We know this species, having encountered it several times, and we believe the rediscovery by Bütschli to be perfectly exact.

A few years later, Vernet 2 added to the list of hermaphroditic Rhabditis two species, in which he observed very precisely the early production of spermatozoa, followed by that of the eggs. He gave them the names of Rhabditis terricola 3 and R. Leuckarti.

The following year, Bütschli 4 again found the Rhabditis dolichura of Schneider and provided us with a good description, confirming the state of hermaphroditism that was pointed out by his predecessor. He further described, under the name of R. Clausii, a second species without males, the seminal reservoir of which was however always full of spermatozoa. He dared not commit to describing this species as hermaphroditic, although hermaphroditism is highly probable in this case. But his most interesting discovery is to have found again the parthenogenetic species mentioned by Schneider, which he described well under the name of Rhabditis Schneideri. Like his predecessor, Bütschli observed the complete absence of males and spermatozoa. We can confirm these observations, having verified them several times and,

1Beiträge zur Kenntniss der freilebenden Nematoden, 1873, p. 116.

2Archives des sciences physiques et naturelles. Genève, t. 145, 1872, p. 61-75, pl. I.

3Vernet made a mistake by wanting to assimilate his first Rhabditis to the R. terricola of Dujardin. This latter species, according to its author, is a dioic Rhabditis that is therefore

impossible to confuse with a hermaphroditic species. Therefore, the name terricola cannot be maintained for the hermaphrodite of Vernet, and I propose to dedicate it to the scientist who made it so well known to us, by calling it henceforth Rhabditis Verneti.

4 Beiträge zur Kenntniss der freilebenden Nematoden, 1873, p. 115-119.

obtained in a rhabditoid form in cultures. But under this free-living form, all individuals, in an overwhelming majority (1000 females for 1 male), are ordinary females that remain sterile owing to male rarity. In the free-living form of Strongyloides intestinalis already, only one male is found for eight females.

We saw above that Ascaris nigrovenosa was a species with heterogonic development, whose parasitic form is hermaphroditic. This species was later placed in the Angiostomum genus together with four other species: Angiostomum entomelas, rubrovenosum, macrostomum and sanguinolentum. Linstow 1, having continued the study of these latter species, recognized that their development was identical to the first species, with a protandrous autogamous hermaphroditic state in the parasitic form.

Allantonema mirabile, which was so well studied by Leuckart 2, goes through a heterogonic development as well, with a protandrous hermaphroditic parasitic form.

We still have to cite a parasite of Aphodius fimetarius, i.e. Bradynema rigidum, whose protandrous hermaphroditism was elucidated through the work of Zur Strassen 3. However in this case, in contrast to the previous species, the development is direct, as in the free-living hermaphrodites of the Rhabditis genus.

Oerley, in his monograph on the rhabditids 4, enumerates four to five already known species that he acknowledges to be hermaphrodites, and then adds: “The greater part of nematodes have separate sexes, only a few are hermaphrodites, and parthenogenesis has not yet been well proven.”

1Archiv für Naturgeschichte, 1885, t. I, p. 1-23.

2Abhandl. d. mathem.-phys. Cl. Königl. Sächs. Gesellsch. d. Wissensch. t. XIII, 1887, p. 505-704.

3Zeitsch. F. Wiss. Zoologie, t. LIV, 1892, p. 655-747, pl. XXIX-XXXIII.

4Die Rhabditiden und ihre medicinische Bedeutung, 1866, p. 37 and 58.

MODES AND FORMS OF REPRODUCTION OF NEMATODES. 9

In summary, the well-established exceptions to the general rule are still quite few. At this time, one can estimate the number of known species of nematodes to about 1500 to 1600. Among these, only 18 were described as being able to reproduce without the help of distinct males. Of these 18 species, 15 are hermaphroditic and 3 parthenogenetic.

Here is the list thereof, with the names of the authors who first identified the true sexual state of these species.

Protandrous autogamous hermaphroditic species:

Rhabditis dentata, Schneider;

-Verneti, Vernet;

-Leuckarti, Vernet;

-Clausii, Bütschli;

Dorylaimus liratus, Schneider; Angiostomum nigrovenosum, Schneider;

-rubrovenosum,

-entomelas, Linstow;

-macrostomum, Linstow;

-sanguinolentum, Linstow; Allantonema mirabile, Leuckart; Bradynema rigidum, Zur Strassen. Parthenogenetic species:

Rhabditis Schneideri, Schneider, Bütschli;

Strongyloides intestinalis, Rovelli;

-longus, Grassi and Segré.

These eighteen species can be divided in two equal halves between free-living and parasitic life. The nine parasitic species show a heterogonic development: they develop in a cycle of two alternating generations that differ in their form and organization. One of the forms spends its existence in the free-living state and always has two separate sexes; the other form lives as a parasite and is always hermaphroditic or parthenogenetic. The free-living species belong to the genera Rhabditis and Dorylaimus, the parasites to the genera Angiostomum, Allantonema, Bradynema and Strongyloides.

As can be seen in the above list, the Rhabditis genus provides the greatest share of species that reproduce without males. I do not believe that it should be concluded from these data that this peculiarity of organization is unique to this genus. Rhabditis, being easy to keep in methodical and numerous cultures, simply lend themselves better to this type of observations and were therefore the most well studied.

In the face of the well-established facts that we just enumerated in this historical review, it would seem that the notion of a reproduction without males, through hermaphroditic or parthenogenetic females, should have been accepted as a commonplace idea. It was however not so. The hermaphroditism and parthenogenesis of nematodes have entered science only with difficulty and even now are still sometimes dismissed as mistakes.

The very authors that discovered these facts appear to have only given them scarce attention, pointing them out as singular oddities rather than as phenomena of general interest. Schneider, who devoted a short chapter to them and to whom we owe the most numerous and most complete observations, does not even take the