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0300-3256187 $3.00 .OO Pergamon Journals Ltd. 1987 The N o r w e g i a n A c a d e m y of Science a n d Letters

Zoologica S c r i p t a , VoI. 16, N o . 2 , pp. 111-116, 1987 Printed in G r e a t Britain

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Phylogeneticrelationships between the families Capsalidae and Dionchidae (Platyhelminthes, Monogenea, Monopisthocotylea) indicated by the comparative ultrastructural study of spermiogenesis JEAN-LOU JUSTINE and XAVIER MATTE1 Accepted 23 June 1986

Justine, J.-L. & Mattei, X . 1987. Phylogenetic relationships between the families Capsalidae and Dionchidae (Platyhelminthes, Monogenea, Monopisthocotylea) indicated by the comparative ultrastructural study of spermiogenesis.-Zool. Scr. 16: 11 1-1 16. Comparative ultrastructural observations were carried out on the spermiogenesis of the capsalid Caballerocotyla manteri Price and the dionchid Dionchus remorae MacCallum. At the beginning of spermiogenesis the zones of differentiation (ZD) jut out in all directions. A large mitochondrion shaped like a perforated bead, and through which the elongated nucleus passes, is found facing each Z D . Later the Z D become parallel and are embedded within the common cytoplasmic mass. Cortical longitudinal microtubules are present in the Z D at the outset of spermiogenesis, but they later disappear. The spermatozoon is long and filiform. It shows two parallel axonemes of the “1” flatworm pattern, the nucleus and mitochondrion, and no cortical microtubule. The 9 ultrastructure of spermiogenesis and spermatozoon is remarkably similar in the two species studied, as in other capsalids previously described. Two characteristics, the perforated bead shape of the spermatid mitochondrion and the progressive disappearance of the microtubules of the Z D , may be considered as synapomorphies which indicate close phylogenctic relationships between the families Dionchidae and Capsalidae. This interpretation coincides with Llewellyn’s (1971) scheme of the evolution of the monogeneans.

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Jean- Lou Justine, Laborutoire des Vers, Museum National d’Histoire Naturelle, 61 rue Buffon, F-75231 Paris CCdex 0.5, France. Xavier Mattei, Dkpurtement de Biologie Animale, Facult& des Sciences, Dakar, Stnigal, West Africa.

Introduction

Material and methods

Comparative spermatology has been shown to be a useful tool for elucidating the phylogenetic interrelationships of monogeneans. It was used in a phylogeny proposed for the Monogenea (Justine et al. 1985a) and to elucidate the relationships between the closely related families Loimoidae and Monocotylidae (Justine & Mattei 1985). The present paper deals with a comparison of the ultrastructure of spermiogenesis between a capsalid, Caballerocotyla manteri (Price, 1951) Price, 1960, and a dionchid, Dionchus remorae MacCallum, 1916. The first ultrastructural observations on a capsalid spermatozoon were those of Tuzet & Ktari (1971) and Ktari (1971), on Trochopus pini (van Beneden & Hesse, 1863). Spermiogenesis has been described in detail in the capsalid Megalocotyle grandiloba (Paperna & Kohn, 1964) by Justine & Mattei ( 1 9 8 3 ~ )and Justine (1983). Observations on the related species M . hexacantha (Parona & Perugia, 1889) revealed a similar process (Justine 1985). Spermatozoa of Caballerocotyla manteri and Dionchus rernorae have been briefly described (Justine etal. 1985a), but not spermiogenesis.

Material. The monogeneans Caballerocotyla rnanteri and Dionchus rernorae were collected live from the gills of the teleost fishes Euthynnus alletteratus (Rafinesque, 1810) and Echeneis naucrates Linnaeus, 1758, respectively, caught near Dakar, Senegal. Light microscopy. Living worms were gently squashed between a slide and a cover glass, in order to recover the spermatozoa. Living spermatozoa were observed between a slide and a cover glass in a drop of sea water, with a phase contrast microscope. The length of the spermatozoa was measured for Dionchus on living sperm, with a phase contrast microscope equipped with an eyepiece micrometer, and for Caballerocotyla on presemed material [Aquamount (Gurr) with a small quantity of osmium tetroxide] with a Nomarski interference microscope equipped with a camera lucida. Electron microscopy. The method used in electron microscopy has been previously described (Justine & Mattei 1985).

Observations

Light microscopy In both species spermatozoa are long and filiform. Spermatozoa of Caballerocotyla have a mean length of 70 p m

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Zoologica Scrip ta 16

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J . -L. Justine and X . Mattei

Figs. 1-2. Outset of spermiogenesis in Dionchus remorse.-1. The common cytoplasmic mass ( C C M ) of the 64 fused spermatids shows protuberances which jut out in all directions. Each protuberance contains a large mitochondrion ( M ) shaped like a perforated bead, through which the elongated nucleus ( N )passes. Each nucleus penetrates in a long zone of differentiation ( Z D ) .9000X .-2. Magnification of a part of Fig. 1. The zone of differentiation contains two axonemes, one of which ( A )is visible here, with its centriole (C). The nucleus ( N ) migrates in the zone of differentiation. AM early arching membranes. 40,OOOX.

(ranging from 55 to 80 pm); living spermatozoa exhibit slow movements of undulation. Spermatozoa of Dionchus are about 150 p m long; no movement was noted in living spermatozoa.

Electron microscopy At the beginning of spermiogenesis in both species the common cytoplasmic mass of the spermatids is round in shape and shows protuberances on its surface. A large mitochondrion faces each protuberance; the mitochondrion is spherical in shape, about 2 p m in diameter, and is perforated by a cylindrical hole about 200 nm in diameter, into which a filiform nucleus penetrates. This large mitochondrion is thus shaped as a perforated bead (Fig. 1). Each nucleus, after passing through the mitochondrial bead, penetrates into a long process, the zone of Zoologica Scripta 16

differentiation, which juts out of the common cytoplasmic mass (Fig. 2). This stage is illustrated here only for Dionchus (Figs. 1-2). After structural changes which affect the common cytoplasmic mass the 64 zones of differentiation of each mass become parallel and are embedded within the mass. Each zone of differentiation, the distal extremity of which lengthens and extends outside the mass, has its proximal part encircled within an empty cylindrical space or ‘cytoplasmic canal’. A t this stage the zone of differentiation shows in transverse section two axonemes, the nucleus and a mitochondrial cord coming from the mitochondrial bead. Cortical longitudinal microtubules are present under the cell membrane (Fig. 3a, Cuballerocotylu; Fig. 3b, Dionchus). Longitudinal sections show that the basal extremity of the zone of differentiation has arching membranes. Elements of smooth endoplasmic reticulum in the

Spermiogenesis and phylogeny of monogeneans common cytoplasmic mass are placed along the arching membranes and the cytoplasmic canal. The mitochondria1 cord moves through the zone of differentiation. Cortical microtubules progressively disappear (Fig. 4a, Caballerocotyla; Fig. 4b, Dionchus). In both species spermiogenesis produces bundles of 64 spermatozoa. The mature spermatozoon shows in transverse section two axonemes of the 9 + “1”flatworm pattern, and the nucleus and mitochondrion, both filiform. No cortical microtubules are found (Fig. Sa, Caballerocotyla; Fig. Sb, Dionchus). Longitudinal sections show that the mitochondrion is apparently continuous. Mitochondria1 cristae are irregularly arranged (Fig. 6a, Caballerocotyla ; Fig. 6b, Dionchus). Discussion

Ultrastructural aspects During spermiogenesis the common cytoplasmic mass of the spermatids shows deep structural changes: the zones of differentiation jut out in all directions at the beginning, but are all parallel and embedded in the mass at the end. The early stage has been illustrated in the present paper only in Dionchus, but the same structure is seen in Caballerocotyla and in another capsalid, Megalocotyle (Justine & Mattei 1 9 8 3 ~ ) Such . important structural changes of the common cytoplasmic mass are often found in monopisthocotylean monogeneans (see Justine & Mattei 1983a, 1983b, 1984), although they are poorly understood. The number of 64 elements in each bundle of spermatozoa, noted in both species, is a feature commonly found in the monogeneans (see Justine & Mattei 1983~).

Biology of fertilization Spermatozoon morphology may be related to phylogeny and to the biology of fertilization (see Baccetti & Afzelius 1976). An exceptional characteristic of fertilization, the presence of spermatophores, has been reported in some capsalids: in Entobdella diadema by Llewellyn & Euzet (1964) and in E. soleae by Kearn (1970). One could try to relate this characteristic to spermatozoon morphology, but spermatophores are not known in capsalids other than Entobdella (whose spermatozoon ultrastructure is unfortunately unknown), are not known in dionchids, and on the contrary have been reported in other monopisthocotylean monogeneans with a different sperm pattern (see Justine & Mattei 1984; Justine 198.5). Ultrastructural observations revealed that the process of fertilization in Dionchus is grossly similar to that found in other parasitic Platyhelminthes, with a special feature, the fact that spermatozoq and fertilized female germ cells are found in the ovary (Justine & Mattei 1986). Similarly, Kearn (1970, 1985) noted motile spermatozoa in the ovary of the capsalid E. soleae. Bychowski (1957) reported the presence of a ‘receptaculum seminis’ in the ovary of the capsalid Benedenia derzhavini (Layman). Rakotofiringa and Lambert (personnal communication) examined Dionchus remorae and D. rachycentris Hargis, 1955 and also found spermatozoa in the ovary. Thus, it seems that the capsalids

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and dionchids share a common anatomical feature, the fusion of the seminal receptacle with the ovary. It is possible that this anatomical feature is correlated with a particular biology of fertilization, and maybe with the ultrastructure of the spermatozoon.

Phylogeny The structure of the spermatozoon is now known in four species of capsalids: Trochopuspini (Tuzet & Ktari 1971), Megalocotyle grandiloba (Justine & Mattei 1983a), M . hexacantha (Justine 1985) and Caballerocotyla manteri. This structure is remarkably similar in all four cases, thus suggesting that this family is monophyletic. In a review of monogenean and digenean spermiogenesis, Justine (198s) found that polyopisthocotylean monogeneans and digeneans share a common process, called ‘classical’ spermiogenesis. This ‘classical’spermiogenesis is clearly plesiomorphic. Spermiogenesis in the monopisthocotyleans, including the capsalids and dionchids, is generally simplified when compared to the ‘classical’ spermiogenesis. This simplification involves the lack of several elements normally found in the polyopisthocotyleans: centriole-like bodies, striated roots and free flagella which fuse with a median cytoplasmic process. These simplifications may be considered as derived characters that separate monopisthocotylean monogeneans from the polyopisthocotyleans. Spermatozoa of monogeneans may be classified into four patterns based on the number of axonemes and the presence of cortical microtubules. Pattern 1 or ‘standard pattern’ is the more complete one, and has two axonemes and cortical microtubules. This pattern 1 comes from the ‘classical’ spermiogenesis. Patterns 2, 3 and 4 are simplified. This classification of sperm patterns was used to propose a phylogeny of the monogeneans (Justine et al. 1 9 8 5 ~ )Since . this work, we have found in the polyopisthocotylean monogenean Diplozoon an aflagellate spermatozoon, which adds a fifth, aberrant pattern to this classification. This aberrant morphology appears to be an autapomorphy correlated with the exceptional biology of fertilization of Diplozoon (the two members of a pair are permanently fused) and has no phylogenetical significance (Justine et al. 1985b,c). Dionchids and capsalids share pattern 2, presence of two axonemes and absence of cortical microtubules in the mature spermatozoon. If the ultrastructure of the mature spermatozoon alone is considered, three other cases, Euzetrema (Fournier 1980), Gyrodactylus (Kritsky 1976) and Udonella (Justine et al. 1985a), should be included in sperm pattern 2. The ultrastructure of spermiogenesis is only partly known in these three cases and it is possible that the resemblance of mature spermatozoa comes from different spermiogenesis processes, through a phenomenon of convergence. In contrast, the present paper shows that spermiogenesis is very similar in dionchids and capsalids. The two characteristics of spermiogenesis shared by these two families and unknown in other monogeneans, i.e. (a) perforated bead-like mitochondrion and (b) progressive disappearance of the microtubules in the zone of differentiation, may be considered as synapomorphies uniting the two families Capsalidae and Dionchidae. In the case of Zoologica Scripta 16

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J . -L. Justine and X . Mattei

Zoologicu Scriptu 16

Spermiogenesis and phylogeny of monogeneans

1 15

point (b) it should be emphasized that in other monoge- Baer, J . G. & Euzet. L. 1961. Classe des Monogi.ncs. I n Trait@de Zoologie (ed. P. P. GrassC) 4:243-325. Masson, Paris neans microtubules never exist in the spermatid (sperm Beverley-Burton. M. 1984. Monogenea and Turbellaria. In Guide to the pattern 4) or, on the contrary, exist in the spermatid and parasites of fishes of Canada (eds. L. Margolis & Z . Kabata): 5-209.-Can. Spec. Puhl. A s h . aquut. Sci. 74 Purl 1. persist in the spermatozoon (sperm patterns 1 and 3 ) . B. E. 1957. (Monogenetic tremcrtoile.\. therr ,systematics and There is no consensus on the phylogenetic positions of Bychowski, phylogeny). Izdanie Akademic Nauk SSSR, Moscow (in Russian). dionchids and capsalids in classifications, which are gener1961. English edition translated by AIBS, Washington. DC (ed. W . J. Hargis), VIMS Translation Series No. I , Washington. ally based upon the morphology of the haptor of the A . 1980. Les Monogi.nes d’Aniphibicns. Approchc ultrastruclarvae and of the adults. According to Sproston (1946) Fournier, turale des modifications adaptativcs iiu cours du cycle et dcs relations and Baer & Euzet (1961) the Dionchinae are a subfamily phyletiques. These d’Etat, UniversitC de Perpignan. France. of the family Monocotylidae, and thus are separated from Justine, J.-L. 1983. A new look at Monogcnca and Digcnea spermatdzoa. In The sperm cell (ed. J . Andre): 450453. Martinus the Capsalidae. Bychowski (1957) upgrades the DionNijhoff. The Hague. chidae to the family level and places them close to the Justine, J.-L. 1985. Etudc ultrastructuralc comparCc de la spermiogenese des Digkncs et dcs Monog6ncs (Plathclminthes). RelaCapsalidae. Llewellyn (1970; updated and illustrated by tions entre la morphologic du spcrrnatozoidc. la biologic de la Beverley-Burton 1984) claimed that the Capsalidae and fecondation et la phylogCnie. T h Dionchidae are closely related and imagined a ‘protoet Techniques du Languedoc (Mc dionchid’ at the origin of these two families. This latter Justine, J.-L., Lamhert, A . & Mattei. X . 1985tr. Spermatozoon ultrastructure and phylogenetic relationships in the Monogenea interpretation is thus corroborated by the comparative (Platyhelminthes).-In/. J . Parasit. I Y : 601-608. study of spermiogenesis presented here, and we even may Justine, J.-L., Le Brun, N . & Mattci, X . 198Sh.First report ofaflagcllate spermatozoon in a parasitic Platyhelminthe. found i n the rnonogehypothesize that this proto-dionchid had spermatozoa nean Diplozoon gracile (Polyopisthocotylea, Diplozoidac).-Anr/l,s with sperm pattern 2. Lambert (1980) proposed a new Parasit, h a m . romp. 60: 761-762. phylogeny of the monogeneans, based mainly on the Justine, J.-L., Le Brun, N . & Mattci. X . 1085~,.The nHagellate spermatozoon o f Diplozoon (Platyhclniinthc: Monogena: Polyopisstudy of the ciliated cells and chaetotaxy of the larvae. thocotylea). A demonstrative case o l relationship between sperm Capsalids are well documented, but the oncomiracidium ultrastructure and biology o f reproduction.-J. Ultrtr.srruc~t.Res. Y2: of Dionchus does not swim and has no ciliated cells (Ktari 47-54. 1971, 1977). Therefore, the comparative study of ciliated Justine, J.-L. & Mattei, X. 1983a. Etudc ultrastructurale cornparkc dc la spermiogenese des Monogenes. I . Megulocoryle (Monopiscells and chaetotaxy cannot be used to elucidate the thocotylca: Capsalidae).-J. Ultrustruct. Re.s. 82: 296-308. relationships between capsalids and dionchids. Llewellyn Justine, J.-L. & Mattei, X . 1 9 x 3 . Comparative ultrastructural study of spermiogenesis in monogeneans (Hatworms). 2. Heterocoryle (1970) placed Euzetrema close to the capsalids, and that (Monopisthocotylea: Monocotylidae).-J. U1tru.struc.t. Res. 84: 213corresponds well with the common presence of sperm 224. pattern 2. In contrast, the positions of the Gyrodactylidae Justine, J.-L. & Mattei, X . 1984. Comparativc ultrastructural study of spermiogenesis in monogeneans (flatworms). 4. Diplecranum and Udonellidae in classifications based on haptor mor(Monopisthocotylea: Diplcctanidae).-J. Ultra.strucr. Rrs. 88: 77phology (Sproston 1946; Bychowski 1957; Llewellyn 91. 1970) or on chaetotaxy of the oncomiracidium (Lambert Justine, J.-L. & Mattei, X. 1985. Ultrastructure dc la \pcrmiogcn du spermatozoi’dc dc Loiniosinu It /.’\on; c t aflinitCs phyldtiqucs des 1980) are not close to those of the dionchids and capsalids; Loimoidae (Plathclminthes, Monogenea, Monopisthocotylca).a detailed study of spermiogenesis would be necessary to Zool. Scr. 14: 169-174. clarify this point. Justine, J.-L., & Mattci, X . 1986. Ultrastructural observations on Acknowledgements We thank Prof. Louis Euzet, who identified the monogeneans and made a critical reading of the manuscript, and D r Sylvkre Rakotofiringa and Dr Alain Lambert, who communicated helpful information. We acknowledge the help of Prof. John McEachran, who made a critical reading of the manuscript and kindly edited the English. The technical assistance of C . Chauve, E. Coly and D . Ngom in Dakar and D. Morineau in Paris is greatly appreciated.

References Baccetti, B. & Afzelius, B. 1976. The biology ofthesperm cell. Karger, Basel.

fertilization in Dionchus rernorae (Platyhcliniiitlics, Monogenea, Dionchidae).-Acta Zool. 67: 97-101. Kcarn, G. C. 1970. The production, transfer a n d assimilation of spermatophorcs by Entohdrlla .solme, a nionogcncan skin parusitc of the common sole.-Parasitology 60: 30 I-.? I I . Kearn. G. C. 1985. Observations on egg production in the monogenean Entohdella soleue-Int. J . Para,\//. 1.5: 187-194. Kritsky, D. C. 1976. (Observations on the ultrastructure of spermatozoa and spermiogenesis in the monogenean Gyroi/trc.tylir.\ rrrculiue Ikezaki et Hoffman, 1957).-Truc/? dtrl‘rirvo.s/. iitrrrc.ktiyc, 7 k n t r u l b i d . Pochvennyi Inst. 34: 70-74 (in Russian). Ktari, M.-H. 1971. Recherches sur la reproduction et le dCveloppement Monogenes (Polyopisthocotylca) parasite\ dc poissons e d’Etat, Universite de Montpellier, France. Ktari, M.-H. lY77. Le parasitisme d’E‘c.henei.snuucrutrs L. (Poisson TCIeostecn) par dcux MonogCnes (Monopisthocotylea) du genre Dionchus: D . ugussrzi Goto 1889 et /I remoruc . Mac Calluni 1916.Excertii Parasit. Mem. D r Eduurrlo C‘irhnllero y C’uhdlero (Publncs esp. Inst. Biol. Univ. nac. Autoncinia MCx.).

Figs. 3 4 . Caballerocotylu manteri and Dionchus remorae.-34. Spermiogenesis.-3. Transverse section of the zone of differentiation, which contains two axonemes ( A ) of the 9 + “1” flatworm pattern, the nucleus ( N ) and mitochondrial cord (M), both in migration. Cortical longitudinal ~ Dionchus: one of the zones of differentiation ( Z D 1 ) microtubules ( T ) are found along the cell membrane.-3a. Cabullerocotyla. 6 0 , 0 0 0 .-36. shows numerous microtubules ( T ) ;the other one ( Z D 2 ) ,more mature, shows only one microtubule ( T ) .6 0 , 0 0 0 ~.4. Longitudinal section of the zone of differentiation ( Z D ) embedded within the common cytoplasmic mass. A axoneme; M mitochondria1 cord, coming from the mitochondria1 bead ( M B ) ; CC cytoplasmic canal; curved arrows arching membranes; R endoplasmic r e t i c u l u m . 4 ~ .Caballerocotyla. 4 0 . 0 0 0 ~. 4 b . Dionchus. 36,000 x .-54. Mature spermatozoa.-5. Transverse sections of mature spermatozoa. The spermatozoa never show cortical microtubules. A axonerne; M mitochondrion; N nucleus.-5a. Caballerocotyla. 6 0 , 0 0 0 ~;-5b. Dionchus. 1 2 0 , 0 0 0 ~ .d. Longitudinal section of spermatozoa, The diameter of the mitochondrion seems constant; cristae are irregularly arranged. A a x o n e m e . d a . passing through the mitochondrion (M). Caballerocotyla. 60,OOOX . d b . Dionchus. 60,000X. Zoologica Scripta I 6

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Lambert, A . 1980. Oncomiracidiums et phylogenese des Monogenes (Plathelminthes) 26me partie: Structures argyrophiles des oncomiracidiums et phylogenese des Monogenea.-Annls Parusit. hum. comp. 55: 281-325. Llewellyn, J. 1970. Monogenea.-J. Parasit. 56 (4, Sect. 11, Pt. 3): 493-504. Llewellyn, J . & Euzet, L. 1964. Spermatophores in the monogenean

Zoologica Scripta 16

Entobdella diadema Monticelli from the skin of sting-rays, with a note on the taxonomy of the parasite.-Parasitology 54: 337-344. Sproston, N. G. 1946. A synopsis of the monogenetic trematodes.Trans. zool. SOC.Lond. 25: 185-600. Tuzet, 0. & Ktari, M.-H. 1971. Recherches sur l’ultrastructure du spermatozoide de quelques Monogenes.-Bull. SOC.zool. Fr. 96: 535-540.

Phylogenetic relationships between the families ...

turale des modifications adaptativcs iiu cours du cycle et dcs relations phyletiques. These d'Etat, UniversitC de Perpignan. France. Justine, J.-L. 1983. A new ...

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