Spermatozoon ultrastructure and phylogenetic relationships in the monogeneans (platyhelminthes)

Internutional Journalfor Printed in Great Britain.

Parosifology

Vol. 15, No. 6. pp. 601~608.

1985 SC) 1985 Auslrolion

002&7519/85$3.M)+0.00 Per&wmon Press Ltd. Society .for Parasitology

SPERMATOZOON ULTRASTRUCTURE AND PHYLOGENETIC RELATIONSHIPS IN THE MONOGENEANS (PLATYHELMINTHES) JEAN-LOU JUSTINE*+, ALAIN LAMBERT? and XAVIER MATTEI* *Dtpartement de Biologie Animale, Faculte des Sciences, Dakar, Senegal TLaboratoire de Parasitologie Comparee, Universite des Sciences et Techniques du Languedoc, 34060 Montpellier, France (Received 9 July 1984) Abstract-JusTINa J.-L., LAMBERTA. and MATTEI X. 1985. Spermatozoon ultrastructure and phylogenetic relationships in the monogeneans (Platyhelminthes). International Journalfor Parasitology 15: 601408. New observations reported in this study together with bibliographical data allow comparisons of spermatozoon ultrastructure in 28 genera of monogeneans, belonging to 19 families. The authors propose to compare and classify monogenean spermatozoa using two simple ultrastructural characteristics: (a) the number of axonemes, 1 or 2, (b) the presence or absence of cortical microtubules. These traits make it possible to group monogenean spermatozoa in four patterns. Pattern 1 (2 axonemes plus microtubules) is characteristic of the polyopisthocotyleans (9 families). The three other patterns are found in the monopisthocotyleans. Pattern 2 (2 axonemes without microtubules) is found in the Capsalidae and Dionchidae, which seem closely related, and also in the Udonellidae, Gyrodactylidae and Euzetremu. Pattern 3 (1 axoneme plus 1 altered axoneme plus microtubules) is found in the Monocotylidae and Loimoidae. Pattern 4 (1 axoneme without microtubules) is found in the Amphibdellatidae, Ancyrocephalidae, Calceostomatidae and Diplectanidae. A phylogeny of the monogeneans is drawn from the data of comparative spermatology; this scheme coincides in many points with the phylogeny of Lambert (1980) which was based on the study of chaetotaxy and ciliated cells of the oncomiracidium. INDEX KEY WORDS: Comparative spermatology; ultrastructure; Platyhelminthes; phylogeny.

INTRODUCTION UNTIL now, phylogenetic schemes of the monogeneans have been based mainly on the comparative study of the haptor (attachment organ) of larvae or of adults. Three such important systems exist: those of Sproston (1946) updated by Baer & Euzet (1961), Bychowsky (1957), and Llewellyn (1970). Unfortunately, the homologies between the different parts of the larval haptor are difficult to understand, because their embryology is insufficiently known. Furthermore, the haptor is an attachment organ, and thus its morphology depends on the adaptation of the parasite to its habitat; consequently, phenomena of convergence could hide real phylogenetic relationships. Malmberg (1982) insisted on the necessity of using new tools in order to understand better the evolution of monogeneans. Lambert (1980), to establish a phylogeny of the monogeneans, used two new morphological characteristics, the chaetotaxy and ciliated cells of the oncomiracidium. These structures, which are related to the free phase of the life *Present address (to which reprint requests should be sent): Laboratoire des Vers, Museum National d’Histoire Naturelle, 61 rue de Buffon, 75231 Paris Cedex 05, France. 601

Monogenea;

spermatozoon;

spermiogenesis;

cycle, should be less affected by parasitism than the haptor, which is adapted to the habitat. In the present paper, we propose to use a new tool for the understanding of the phyletic relationships in the monogeneans, the ultrastructure of the spermatozoa. In contrast to the attachment organs, sperm ultrastructure theoretically should not be affected by adaptation to the habitat. Interesting and useful relationships between sperm ultrastructure and phylogeny have been shown in several animal phyla (see Afzelius, 1983). Within the Platyhelminthes, several detailed studies of comparative spermatology have been made, on turbellarians (Hendelberg, 1977, 1983) and on cestodes (Euzet, Swiderski & MokhtarMaamouri, 1981). Rees (1979) and Jamieson & Daddow (1982), concerning the Digenea, both expressed the opinion that sperm studies may well be useful for understanding phylogeny. Rohde (1980) also pointed out that detailed studies may well show that a certain pattern of sperm ultrastructure is characteristic of each group of parasitic platyhelminthes and thus useful for establishing phylogenetic relationships although he urged caution because of the limited number of studies and the considerable degree of variability.

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Results presented in this paper combined with bibliographical data allow us to compare the ultrastructure of monogenean spermatozoa in 28 genera, belonging to 19 families.

MATERIALS AND METHODS Spermatozoa of the following species are described for the first time. For each parasite, the list gives the name, family, host and geographical location: Microcotyle sp. (Microcotylidae), from Abudefduf analogus (Dakar); Udonella caligorum (Udonellidae), from Caligus minimus, parasitic copepod of Dicentrarchus labrax (S.E. France); Dionchus remorse (Dionchidae), from Echeneis naucrates (Dakar); Cabalierocotyla sp. (Capsalidae), from Euthynnus alletteratus (Dakar); Loimosina wilsoni (Loimoidae), from Sphyrna lewini (Dakar); Furnestinia echeneis (Diplectanidae), from Sparus aurata (SE. France); Lamellodiscus sp. (Diplectanidae), from Diplodus sargus cadenati (Dakar); Calceostoma herculanea (Calceostomatidae), from Umbrina canariensis (Dakar); Amphibdella paronaperugiae (Amphibdellatidae), from Torpedo torpedo (Dakar). The parasites were taken from their hosts and immediately fixed in cold glutaraldehyde in cacodylate buffer as described by Justine & Mattei (1983a).

OBSERVATIONS Spermatozoon

of Microcotyle. Transverse sections

of the sperm body show two axonemes of the 9 + “1” flatworm pattern, the nucleus and the mitochondrion. A continuous row of cortical longitudinal microtubules run beneath the cell membrane (Fig. 1). Spermatozoon of Caballerocotyla, Dionchus, and Udonella. Transverse sections of the sperm body show the two axonemes, the nucleus and mitochondrion, but no cortical microtubules (Figs. 2 and 3).

Spermatozoon of Loimosina. Depending on the level of the transverse sections along the filiform sperm body, one or two axonemes are found. Sections with two axonemes are fewer in number, thus one of the axonemes is much shorter than the other. Cortical microtubules associated with external ornamentations on the membrane are visible on some of the transverse sections (Figs. 4-7). Spermatozoon of Furnestinia, Lamellodiscus and Amphibdella. Transverse sections always show a single axoneme. A mitochondrion and the nucleus, both filiform, accompany the axoneme (Fig. 8).

DISCUSSION Spermatozoa of parasitic Platyhelminthes (Monogenea, Trematoda, Cestoda) almost all exhibit a long and filiform morphology. Transverse sections of the sperm body generally show two axonemes of the 9 + “1” pattern, the nucleus and mitochondrion, and cortical longitudinal microtubules. This pattern is the “standard pattern” on which some alterations are surimposed: Trematodes: almost all digeneans show the “standard pattern” (see Justine & Mattei, 1982a). Only two exceptions are known: schistosomes with an aberrant sperm morphology (Kitajima, Paraense & Correa, 1976) and a single peculiar sperm flagellum (Justine & Mattei, 1981), and a didymozoid, Didymozoon, with two axonemes of the 9 +0 type and no cortical microtubules (Justine & Mattei, 1983d, 1984b). In the Aspidogastrea, the spermatozoon shows the “standard pattern” (Bakker & Diegenbach 1973) with a minor variation, i.e. the presence of several rows of cortical microtubules (Rohde, 1971b).

FIG. 1. Sperm pattern 1: Microcotyfe sp. Transverse sections of the spermatozoa show two axonemes (A) of the flatworm 9 + “ 1” pattern, the mitochondrion (M) and the nucleus (N). Cortical longitudinal microtubules run at the periphery of the cell (arrows). FIGS.2-3. Sperm pattern 2. Dionchus and Caballerocotyla. FIG. 2. Caballerocotyla-Transverse

sections show two axonemes (A), the mitochondrion no cortical microtubules.

FIG. 3. Dionchus. The spermatozoon

(M) and nucleus (N). There are

shows a striking resemblance to that of Caballerocotyla. A, M, N, as in Fig. 2. FIGS.4-7. Sperm pattern 3. Loimosina.

FIG. 4. Transverse section of the anterior region of the sperm cell, showing one axoneme (A), the mitochondrion cortical microtubules with associated external ornamentations (arrows). FIG. 5. Region of the sperm cell with two axonemes (Al and A2) and mitochondrion

(M) and

(M).

FIG. 6. A group of spermatozoa in transverse section, cut at the level where the second axoneme (curved arrows) is progressively altered. FIG. 7. Middle region of the sperm cell, showing a single axoneme and the mitochondrion

(M). The nucleus (not shown)

is at the posterior extremity of the cell. FIG. 8. Sperm pattern 4. Furnestinia. Transverse sections of the spermatozoon exhibit one single axoneme (A), the nucleus (N) and mitochondrion (M).

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TABLEI-LIST OF MONOGENEANS Family

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WHOSESPERMATOZOON LJLTRASTRUCTURE IS KNOWN

Genus

Reference

Polystomoides Polystoma Erpocotyle Hexostoma Plectanocotyle Choricotyle Diclidophora Gotocotyla Microcotyle Heteraxine Heteraxinoides Cemocotyle

Rohde, 1971a Bekkouche et al., abstract cited above. Tuzet & Ktari, 197lb Justine & Mattei, 1984a Tuzet & Ktari, 1971b Tuzet & Ktari, 1971b Tuzet & Ktari, 1971b; Halton & Hardcastle, 1976; Rohde, 1980 Tuzet & Ktari, 1971a*, 1971b Justine & Mattei, in press Justine & Mattei, in press Justine & Mattei, in press

Dionchidae

Euzetrema Gyrodactylus Udonella Trochopus Megalocotyle Caballerocotyla Dionchus

Fournier (Unpublished These d’Etat, University of Perpignan, Kritsky, 1976; Present paper Tuzet & Ktari, 197lb Justine & Mattei, 1983a* Present paper Present paper

Pattern 3

Monocotylidae Loimoidae

Heterocotyle Loimosina

Justine & Mattei, 1982b, 1983b* Present paper

Pattern 4

Diplectanidae

Diplectanum Lamellodiscus Fumestinia Amphibdelloides Amphibdella Cleitharticus Calceostoma

Justine Present Present Justine Present Justine Present

Polyopisthocotylea Polystomatidae Pattern 1 Hexobothriidae Hexostomatidae Plectanocotylidae Diclidophoridae Gotocotylidae Microcotylidae Heteraxinidae Cemocotylidae Monopisthocotylea Pattern 2

lncertae sedis Gyrodactylidae Udonellidae Capsalidae

Amphibdellatidae Ancyrocephalidae Calceostomatidae

1980).*

& Mattei, 1982b, 1984~~ paper paper & Mattei, 1983c* paper & Mattei, 1982b paper

*Indicates references which contain data on spermiogenesis.

Cestodes: cortical

the mitochondrion is missing, but microtubules are always present. In most of

the cestodes, one of the two axonemes disappears during spermiogenesis and the spermatozoon is uniflagellate. Interesting relationships between sperm ultrastructure and phylogeny have been found in this group (Euzet et al., 1981). Monogeneans: a wide variety of sperm ultrastructures is present. We sought to use ultrastructural characteristics as criteria for comparing and classifying them. We propose to use only two simple characteristics: (a) the number of axonemes in the mature sperm cell (1 or 2) and (b) the presence or absence of cortical microtubules. These features have been chosen because: they appear on transverse sections of the sperm cells, which are easy to obtain and are often the only views published; they show variation within the group; the homology of these structures between the various species appears satisfactory, consistent with the rules of Rieger &Tyler (1979). Table 1 shows data concerning 28 genera of monogeneans belonging to 19 families. Thanks to the use of the two simple characteristics cited above, four patterns of sperm-

atozoa may be distinguished within the monogeneans. Pattern 1: 2 axonemev plus cortical microtubules. This pattern is found only in the Polyopisthocotylea, in all families of the group. This is the “standard pattern”, also found in many trematodes and in a turbellarian (Hendelberg, 1983). In a Polystomatidae, Bekkouche, Fournier & Peyritre (1974, Proceedings of the Third International Congress of Parasitology, Munich, 1 sec. B4, 416-417) described a minor variation on this pattern, the absence of cortical microtubules along part of the spermatozoon. Tuzet & Ktari (1971b) claimed that Plectanocotyle has two types of spermatozoa, uni and biflagellate, but they probably misinterpreted sections at various levels along the sperm cell. Pattern 2: 2 axonem@ without microtubules. This pattern has been found in the Capsalidae, one species of Dionchidae, Gyrodactylidae and Udonellidae, and in Euzetrema knoepffleri. In the capsalid Megalocotyfe, we have shown that this sperm pattern is brought about by the loss of the cortical microtubules, which are present at the outset of spermiogenesis (Justine, 1983; Justine & Mattei, 1983a).

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This pattern thus derives from pattern 1 by simplification (loss of the microtubules). Our unpublished observations indicate that spermiogenesis in the dionchid Dionchus closely resembles that of the capsalids Caballerocotyla and Megalocotyle. In contrast, spermiogenesis is poorly known in the other species. It is not certain that the resemblance between the mature spermatozoa justifies the claim that phyletic relationships between the various members of this group exist, since the processes of spermiogenesis might differ. Pattern 3. 1 axoneme plus 1 altered axoneme plus microtubules. This pattern has been. fo&el%nly in a monocotylid and a loimoid. In the &bnocotylid Heterocotyle one of the two axonemes is progressively altered during spermiogenesis (Justine & Mattei, 1983b). A similar phenomenon exists in the loimoid Loimosina (unpublished). This pattern could derive from pattern 1 through the loss of one of the axonemes and a reduced development of the microtubules. It may be considered an intermediate stage between pattern 1 and pattern 4. Pattern 4: 1 axoneme without microtubules. This pattern has been found in the Diplectanidae, the Amphibdellatidae, an ancyrocephahd and a calceostomatid. It seems that only one axoneme exists even in the earlier stages of spermiogenesis (Justine & Mattei, 1983c, 1984c). The use of the two simple characteristics defined above permits us to unite these four families within a group characterized by MONOPISTHOCOTYLEA

FIG. 9.

605

one sperm pattern. However, some differences of detail concerning other ultrastructural characteristics, do exist between the different families. Comparative spermatology and relationships of the monogenans with the other Platyheiminthes Monogeneans are very similar to cestodes and trematodes in their sperm ultrastructure. The polyopisthocotyleans appear to be closer to the trematodes than are the monopisthocotyleans because they have in common the sperm pattern 1 or “standard pattern”. Although uniflagellate spermatozoa exist both in some cestodes and some monopisthocotylean monogeneans, this probably should not be interpreted as an indication of a phyletic link between these groups because spermiogenesis is different in each case (Mokhtar-Maamouri, 1979; Justine & Mattei, 1983b, c, 1984c). A recent study (Williams, 1983) showed that the monogeneans are not linked to the Temnocephala by their sperm ultrastructure; the two sperm axonemes in that group are free and thus the spermatozoon is similar to that of many turbellarians. Comparative spermatology and phyletic relationships within the monogeneans Figure 9 is a scheme of the phyletic relationships within the monogeneans, based on the data of comparative spermatology given in Table 1. For POLYOPISTHOCOTYLEA

Phylogeny of the Monogenea, drawn from the data of comparative spermatology. Numbers l-4 refer to sperm patterns. Representations of the transverse sections of spermatozoa are conventional.

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JEAN-LOU JUSTINE, ALAIN LAMBERTand XAVIER MATTEI MONOPISTHOCOTYLEA

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FOLYOPISTHOCOTYLEA

FIG. 10. Phylogeny of the Monogenea, according to Lambert (1980) elaborated mainly from the study of the chaetotaxy and ciliated cells of the oncomiracidium. This scheme shows remarkable similarities with that of Fig. 9.

comparison, Fig. 10 reproduces the phyletic scheme of Lambert (1980), which was drawn mainly from the study of chaetotaxy and ciliated cells of the oncomiracidia. Our new phyletic scheme shows a clear separation between the Monopisthocotylea and the Polyopisthocotylea. The Polyopisthocotylea appear to be very homogeneous with 12 genera showing a similar sperm pattern (pattern 1). However, the Polystomatidae show a minor variation (Bekkouche et al., abstract cited above; Fournier, thesis cited above). This detail confirms the peculiar situation of this family within the Polyopisthocotylea. In contrast to the Polyopisthocotylea, the Monopisthocotylea seem to be heterogeneous and may be divided into three groups, corresponding to sperm patterns 2, 3 and 4. Capsalidae, Dionchidae, Udonellidae, Gyrodactylidae and Euzetrema are Monopisthocotylea with sperm pattern 2. Two subgroupings may be distinguished in that group. The first subgrouping is made up of the Capsalidae and Dionchidae. Spermiogenesis in these two families shows a very similar pattern (Justine, 1983; Justine & Mattei, 1983a, unpublished. This differs from the opinion of Ktari (1977)who considers that the Dionchidae are Monocotylidae from a selacian host that have secondarily migrated to a teleost host. For Llewellyn (1970), the Dionchidae are closely related to the Capsalidae and the data of comparative spermatology perfectly agree

with this interpretation. The second subgrouping is made up of the Udonellidae, Gyrodactylidae and Euzetrema. In this subgrouping, spermiogenesis is not well known, and resemblance between mature sperm cells is not sufficient evidence of close phyletic relationships. According to the data of comparative spermatology, the Gyrodactylidae clearly seem to belong to the Monopisthocotylea, in agreement with the classical opinion (Baer & Euzet, 1961) recently confirmed by Harris (1983), but in opposition to Lambert’s hypothesis (1980). The Udonellidae aJso seem to be linked to the Monopisthocotylea; sperm structure does not allow their separation from the Monogenea as proposed by lvanov (1952). Llewellyn (1970) related Euzetrema to the Capsalidae, and this agrees well with the data of spermatology. Monocotylidae and Loimoidae are Monopisthocotylea with sperm pattern 3. These two families are joined in a single one in some classifications (Baer & Euzet, 1961), so it is not surprising to find them together here. Monocotylidae are often considered close to the Capsalidae; this is not confirmed by comparative spermatology. Amphibdellatidae, Ancyrocephalidae, Calceostomatidae and Diplectanidae are Monopisthocotylea with sperm pattern 4. The last three families are joined within the Dactylogyridea because of their larval chaetotaxy (Lambert, 1980); the Amphibdellatidae also are close to them in the classical

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spermatology

phylogenies (Baer & Euzet, 1961; Llewellyn, 1970). There is a pronounced coincidence here between comparative spermatology and Lambert’s phylogeny, because it is only in these four families that uniflagellate spermatozoa have been found. Lambert (1980) found a strong relationship between Dactylogyridea and Monocotylidae; this may be accepted if one considers that these animals have in common a tendency toward realization of a uniflagellate spermatozoon, partial in the Loimoidae and Monocotylidae, and total in the Dactylogyridea (Ancyrocephalidae, Calceostomatidae and Diplectanidae). Throughout this study, we have considered sperm pattern 1, or “standard pattern”, as the primitive pattern from which patterns 2, 3 and 4 are derived by simplification. Indeed, Franzen (1970) claims that the flatworm spermatozoon is primatively biflagellate. In this perspective, the Polyopisthocotylea appear more primitive than the Monopisthocotylea. It is known that phyletic relationships within Monogenea may be understood very differently depending on whether one admits a regressive or progressive evolution of the haptor (Malmberg, 1982); this seems also to be true for comparative spermatology. One of the clearest conclusions based on comparative spermatology is that Monopisthocotylea and Polyopisthocotylea are clearly separated. Concerning the polyopisthocotyleans, the strong homogeneity in their sperm ultrastructure means that spermatology is of little help in understanding their phylogeny. For the monopisthocotyleans, the classification which best coincides with the conclusions of comparative spermatology is that of Lambert (1980). Comparative spermatology thus may be considered as a useful new tool for the understanding of monogenean phylogeny; of course, this tool should not be used alone but in association with other criteria of phyletic value. Acknowledgements-We

thank Professor Louis Euzet (University of Montpellier, France) for his help in identifying the specimens and his valuable suggestions and critical reading of the manuscript; we acknowledge the assistance of Dr. John Pankratz (Cornell University) in translating the text into English. The technical assistance of Christian Chauve, Edouard Coly, Sylvie Euzet and Doudou Ngom is greatly appreciated.

Note added in proof--Since

submission of this paper, a study of the spermatozoon of Gotocotyla has been published (Justine & Mattei, Journal of Ultrastructure Research 90: 163-171, 1985). Data reported in that article agree with the conclusions of the present paper.

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