Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-18T10:53:35.401Z Has data issue: false hasContentIssue false
  • English
  • Français

Progenesis in digenean trematodes: a taxonomic and synthetic overview of species reproducing in their second intermediate hosts

Published online by Cambridge University Press:  03 February 2005

F. LEFEBVRE  and
R. POULIN
F. LEFEBVRE
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56 Dunedin, New Zealand
R. POULIN
Affiliation:
Department of Zoology, University of Otago, P.O. Box 56 Dunedin, New Zealand
Get access Rights & Permissions [Opens in a new window]

Abstract

Precocious egg production, i.e. progenesis, has been documented for a number of species in scattered reports throughout the trematode literature. The last 2 extensive studies on the subject date from Buttner in the early 1950s (in French) and from Tang in the early 1980s (in Chinese). Overall, 43 species were then known for their ability to produce eggs at the metacercarial stage while still in the second intermediate host. Here, we update the list, and document the existence of progenesis in a total of 79 digenean trematode species, for which we provide information on the taxonomy of the hosts, the facultative or obligate character of progenesis, relevant references, as well as some other pertinent biological information. We then review the subject by asking 7 questions of fundamental evolutionary importance. These include: What favours progenetic development? What are the associated costs and benefits? How are progenetic eggs released from the host? While exposing the various opinions of previous authors, we attempt to give a synthetic overview and stress on the importance of the metacercarial cyst wall (whether it is present, and if so its thickness) in the evolution and the adoption of a progenetic life-cycle.

Keywords

Digenealife-cyclemetacercariaereproductive strategiesself-fertilizationegg production
Type
Review Article
Information
Parasitology , Volume 130 , Issue 6 , June 2005 , pp. 587 - 605
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ADAMSON, M. L. ( 1986). Modes of transmission and evolution of life histories in zooparasitic nematodes. Canadian Journal of Zoology 64, 1375–1384.CrossRefGoogle Scholar
ANDERSON, R. C. ( 1988). Nematodes transmission patterns. Canadian Journal of Zoology 74, 30–45.CrossRefGoogle Scholar
ANDERSON, R. C. & BARTLETT, C. M. ( 1993). The significance of precocity in the transmission of the nematode parasites of vertebrates. Canadian Journal of Zoology 71, 1917–1922.CrossRefGoogle Scholar
BAER, J. G. & JOYEUX, C. ( 1961). Classe des trématodes (Trematoda Rudolphi). In Traité de Zoologie (ed. Grassé, P. P.), pp. 561–692. Masson, Paris.
BAYANOV, M. G. ( 1975). The progenesis of the trematode Prosotocus confusus (Looss, 1894), an amphibian parasite. Parazitologiya 9, 122–126.Google Scholar
BRAY, R. A. ( 1987). A revision of the family Zoogonidae Odhner, 1902 (Platyhelminthes: Digenea): subfamily Lepidophyllinae and comments on some aspects of biology. Systematic Parasitology 9, 83–123.CrossRefGoogle Scholar
BRAY, R. A. & GIBSON, D. I. ( 1980). The Fellodistomidae (Digenea) of fishes from the northeast Atlantic. Bulletin of the British Museum, Zoology Series 37, 199–293.Google Scholar
BROWN, F. J. ( 1933). On the excretory system and life history of Lecithodendrium chilostomum (Mehl.) and other bat trematodes, with a note on the life history of Dicrocoelium dendriticum (Rudolphi). Parasitology 25, 317–328.Google Scholar
BUSH, A. O. & KENNEDY, C. R. ( 1994). Host fragmentation and helminth parasites: hedging your bets against extinction. International Journal for Parasitology 24, 1333–1343.CrossRefGoogle Scholar
BUTTNER, A. ( 1950 a). La progénèse chez les trématodes digénétiques. Sa signification. Ses manifestations. Contributions à l'étude de son déterminisme. Annales de Parasitologie Humaine et Comparée 25, 376–434.Google Scholar
BUTTNER, A. ( 1950 b). Première démonstration expérimentale d'un cycle abrégé chez les trématodes digénétiques. Cas du Plagiorchis brumpti A. Buttner, 1950. Annales de Parasitologie Humaine et Comparée 25, 21–26.Google Scholar
BUTTNER, A. ( 1951 a). La progénèse chez les trématodes digénétiques. Technique et recherches personnelles. Annales de Parasitologie Humaine et Comparée 26, 19–66.Google Scholar
BUTTNER, A. ( 1951 b). La progénèse chez les trématodes digénétiques. Recherches personnelles sur deux espèces progénétiques déjà connues: Ratzia joyeuxi (E. Brumpt, 1922) et Pleurogenes medians (Olsson, 1876). Annales de Parasitologie Humaine et Comparée 26, 138–189.Google Scholar
BUTTNER, A. ( 1951 c). La progénèse chez les trématodes digénétiques. Etude de quelques métacercaires à évolution inconnue et de certaines formes de développement voisines de la progénèse. Conclusions générales. Annales de Parasitologie Humaine et Comparée 26, 279–322.Google Scholar
BUTTNER, A. ( 1953). Valeur évolutive de la progénèse chez les trématodes digénétiques. Thapar Commemoration Volume, Lucknow, 13–24.
BUTTNER, A. ( 1955). Les distomes progénétiques sont-ils des pré-adultes ou des adultes véritables? Valeur évolutive de la progénèse chez les Digenea. Comptes Rendus des Séances de la Société de Biologie 149, 267–272.Google Scholar
CABLE, R. M. ( 1965). Thereby hangs a tail. Journal of Parasitology 51, 3–12.CrossRefGoogle Scholar
CAIRA, J. N. & SCUDDER, G. G. E. ( 1985). Pseudoallocreadium alloneotenicum (Wootton, 1957) Yamaguti, 1971 (Digenea: Allocreadiidae) from Psychoglypha alascensis Banks (Trichoptera: Limnephilidae) in Vancouver, British Columbia. Journal of Parasitology 71, 524.CrossRefGoogle Scholar
CAMP, J. W. ( 1989). Population biology of Allocreadium lobatum (Trematoda: Allocreadiidae) in Semotilus atromaculatus. American Midland Naturalist 122, 236–241.CrossRefGoogle Scholar
CAMP, J. W. ( 1992). Occurrence of Allocreadium neotenicum in aquatic hosts from Northern Indiana. American Midland Naturalist 128, 203–208.CrossRefGoogle Scholar
CARNEY, J. P. & BROOKS, D. R. ( 1991). Phylogenetic analysis of Alloglossidium Simer, 1929 (Digenea: Plagiorchiiformes: Macroderoididae) with discussion of the origin of truncated life cycle patterns in the genus. Journal of Parasitology 77, 890–900.CrossRefGoogle Scholar
CAVENY, B. A. & ETGES, F. J. ( 1971). Life history studies of Microphallus opacus (Trematoda: Microphallidae). Journal of Parasitology 57, 1215–1221.CrossRefGoogle Scholar
CHABAUD, A. G. & BIGUET, J. ( 1954). Etude d'un trématode hémiuroïde à métacercaire progénétique. Annales de Parasitologie Humaine et Comparée 29, 527–545.CrossRefGoogle Scholar
CHENG, T. C. ( 1957). A study of the metacercarial cyst and metacercaria of Crepidostomum cornutum (Trematoda: Allocreadiidae), with notes on the similarity of the larval forms of the genus. Proceedings of the Helminthological Society of Washington 24, 107–109.Google Scholar
CHUBRIK, C. M. ( 1952). On the life cycle of the fish trematode Prosorhynchus squamatus Odhner, 1905. Compte Rendu de l'Académie des Sciences de l'URSS 85, 2.Google Scholar
COMBES, C. ( 1967). Biologie des Polystomatidae (Monogenea): existence et démonstration expérimentale des possibilités de cycle interne directe. Bulletin de la Société Zoologique de France 92, 129–133.Google Scholar
COOPER, A. R. ( 1915). Trematodes from marine and freshwater fishes, including one species of ectoparasitic turbellarian. Transactions of the Royal Society of Canada 9, 181–199.Google Scholar
CORKUM, K. C. & BECKERDITE, F. W. ( 1975). Observations on the life history of Alloglossidium macrobdellensis (Trematoda: Macroderoididae) from Macrobdella ditetra (Hirudinea: Hirudinidae). American Midland Naturalist 93, 484–491.CrossRefGoogle Scholar
CORKUM, K. C. & TURNER, H. M. ( 1977). Alloglossoides cardicola gen. et sp. n. (Trematoda: Macroderoididae) from a Louisiana crayfish. Proceedings of the Helminthological Society of Washington 44, 176–178.Google Scholar
CRIBB, T. H., BRAY, R. A., OLSON, P. D. & LITTLEWOOD, D. T. J. ( 2003). Life cycle evolution in the Digenea: a new perspective from phylogeny. Advances in Parasitology 24, 197–254.CrossRefGoogle Scholar
DAWES, B. ( 1946). The Trematoda, with Special Reference to British and other European Forms. Cambridge University Press, Cambridge.
DEBLOCK, S. ( 1975). Contribution à l'étude des Microphallidae Travassos, 1920 (Trematoda). XXXI. De la condensation des cycles évolutifs chez les Microphallidés, à propos de Maritrema oocysta (Lebour, 1907). Annales de Parasitologie Humaine et Comparée 50, 579–589.Google Scholar
DEGIUSTI, D. L. ( 1962). Ecological and life history notes on the trematode Allocreadium lobatum (Wallin, 1909) and its occurrence as a progenetic form in amphipods. Journal of Parasitology 48, 22.Google Scholar
DISSANAIKE, A. S. & FERNANDO, C. H. ( 1960). Paratelphusa ceylonensis C. H. Fern., second intermediate host of Pleurogenoides sitapurii (Srivastava). Journal of Parasitology 46, 889–890.Google Scholar
DOGIEL, V. A. ( 1964). General Parasitology. Oliver & Boyd, Edinburgh.
DOLLFUS, R. P. ( 1924). Polyxénie et progénèse de la larve métacercaire de Pleurogenes medians (Olsson). Comptes Rendus hebdomadaires des Séances de l'Académie des Sciences, Paris 179, 305–308.Google Scholar
DOLLFUS, R. P. ( 1927). Sur une métacercaire progénétique d'hémiuride (Trém. Digen.). Bulletin Biologique de la France et de la Belgique 61, 49–58.Google Scholar
DOLLFUS, R. P. ( 1929). Existe-t-il des cycles évolutifs abrégés chez les trématodes digénétiques? Le cas de Ratzia parva (Stossich, 1904). Annales de Parasitologie Humaine et Comparée 7, 196–203.CrossRefGoogle Scholar
DOLLFUS, R. P. ( 1938). Cycle évolutif d'un trématode du genre Coitocaecum W. Nicoll. Progénèse de la larve métacercaire chez des amphipodes. Comptes Rendus de l'Académie des Sciences, Paris 207, 431.Google Scholar
DOLLFUS, R. P. ( 1954). Métacercaire progénétique de Derogenes (Trematoda; Hemiuroidea) chez un copépode parasite de poisson. Vie et Milieu 5, 565–568.Google Scholar
DOLLFUS, R. P. ( 1958). Recherches expérimentales sur Nicolla gallica (R.-Ph. Dollfus, 1941) R.-Ph. Dollfus 1958, sa cercaire cotylicerque et sa métacercaire progénétique. Observations sur la famille des Coitocaecidae Y. Ozaki 1928, s.f. Coitocaecinae F. Poche 1926 Trematoda Podocotyloidea et sur les cercaires cotylicerques d'eau douce et marines. Annales de Parasitologie Humaine et Comparée 33, 595–622.Google Scholar
DOLLFUS, R. P., CHABAUD, A. G. & GOLVAN, Y. J. ( 1957). Helminthes de la région de Banyuls. V. Nouveau distome Aphalloides coelomica n. gen. n. sp. de la cavité générale d'un Gobius d'eau saumâtre. Annales de Parasitologie Humaine et Comparée 32, 28–40.Google Scholar
ERWIN, B. E. & HALTON, D. W. ( 1983). Fine structural observations on spermatogenesis in a progenetic trematode, Bucephaloides gracilescens. International Journal for Parasitology 13, 413–426.CrossRefGoogle Scholar
EWALD, P. W. ( 1995). The evolution of virulence: a unifying link between parasitology and ecology. Journal of Parasitology 81, 659–669.CrossRefGoogle Scholar
FAGERHOLM, H. P. & BUTTERWORTH, E. ( 1988). Ascarophis sp. (Nematoda: Spirurida) attaining sexual maturity in Gammarus spp. (Crustacea). Systematic Parasitology 12, 123–129.Google Scholar
FISH, T. D. & VANDE VUSSE, F. J. ( 1976). Hirudicolotrema richardsoni gen. et sp. n. (Trematoda: Macroderoididae) from Minnesota hirudinid leeches. Journal of Parasitology 62, 899–900.Google Scholar
FONT, W. F. ( 1980). The effect of progenesis on the evolution of Alloglossidium (Trematoda, Plagiorchiida, Macroderoididae). Acta Parasitologica Polonica 27, 173–183.Google Scholar
FONT, W. F. ( 1994). Alloglossidium greeri n. sp. (Digenea: Macroderoididae) from the Cajun dwarf crayfish, Cambarellus schufeldti, in Louisiana, U.S.A. Transactions of the American Microscopical Society 113, 86–89.Google Scholar
FONT, W. F. & CORKUM, K. C. ( 1975). Alloglossidium renale n. sp. (Digenea: Macroderoididae) from a fresh-water shrimp and A. progeneticum n. comb. Transactions of the American Microscopical Society 94, 421–424.Google Scholar
FONT, W. F. & CORKUM, K. C. ( 1976). Ecological relationship of Alloglossidium renale (Trematoda: Macroderoididae) and its definitive host, the freshwater shrimp, Palaemonetes kadiakensis, in Louisiana. American Midland Naturalist 96, 473–478.CrossRefGoogle Scholar
FUHRMANN, O. ( 1928). Zweite Klasse des Cladus Plathelminthes. Trematoda. In Handbuch der Zoologie (ed. Kükenthal, W. & Krumbach, T.), pp. 1–140. De Gruyter, Berlin, Leipzig.
GALAKTIONOV, K. V. & DOBROVOLSKIJ, A. A. ( 2003). The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmission, and Evolution of Digenetic Trematodes. Kluwer Academic Publishers, Boston. [Translated from Russian.]CrossRef
GEORGE-NASCIMENTO, M., BALBOA, L., ALDANA, M. & OLMOS, V. ( 1998). Las lapas Fissurella spp. (Mollusca: Archaeogastropoda) y el pejesapo Sicyases sanguineus (Pisces: Gobiesocidae) son huéspedes secuenciales de Proctoeces lintoni (Digenea: Fellodistomidae) en Chile. Revista Chilena de Historia Natural 71, 169–176.Google Scholar
GIARD, A. ( 1887). Sur la progenèse. Bulletin Scientifique de la France et de la Belgique 18, 25.Google Scholar
GIBSON, D. I., JONES, A. & BRAY, R. A. ( 2002). Keys to the Trematoda. Vol. I. CABI Publishing, Wallingford and New York.
GINETSINSKAYA, T. A. ( 1988). Trematodes, their Life Cycles, Biology and Evolution. Amerind Publishing, New Delhi. [Translated from Russian.]
GOULD, S. J. ( 1977). Ontogeny and Phylogeny. Belknap Press of Harvard University Press, Cambridge.
GRABDA-KAZUBSKA, B. ( 1969). Studies on abbreviation of the life cycle in Opisthioglyphe ranae (Frölich, 1791) and O. rastellus (Olsson, 1876) (Trematoda: Plagiorchiidae). Acta Parasitologica Polonica 16, 249–269.Google Scholar
GRABDA-KAZUBSKA, B. ( 1975). A study on the trematode Genus Paralepoderma Dollfus, 1950 (Trematoda, Plagiorchiidae). Acta Parasitologica Polonica 23, 463–484.Google Scholar
GRABDA-KAZUBSKA, B. ( 1976). Abbreviation of the life cycles in plagiochid trematodes. General remarks. Acta Parasitologica Polonica 24, 125–141.Google Scholar
GREER, G. J. & CORKUM, K. C. ( 1980). Notes on the biology of three trematodes (Digenea: Cryptogonimidae). Proceedings of the Helminthological Society of Washington 47, 47–51.Google Scholar
GUIDELLI, G. M., ISAAC, A. & TAKEMOTO, R. M. ( 2003). Endoparasite infracommunities of Hemisorubim platyrhynchos (Valenciennes, 1840) (Pisces: Pimelodidae) of the Baía River, upper Paraná River floodplain, Brazil: specific composition and ecological aspects. Brazilian Journal of Biology 63, 261–268.CrossRefGoogle Scholar
HALL, J. E. ( 1960). Some lecithodendriid metacercariae from Indiana and Michigan. Journal of Parasitology 46, 309–315.CrossRefGoogle Scholar
HALTON, D. W. & JOHNSTON, B. R. ( 1982). Functional morphology of the metacercarial cyst of Bucephaloides gracilescens (Trematoda: Bucephalidae). Parasitology 85, 45–52.CrossRefGoogle Scholar
HICKMAN, V. V. ( 1934). On Coitocaecum anaspidis sp. nov., a trematode exhibiting progenesis in the fresh-water crustacean Anaspides tasmaniae Thomson. Parasitology 26, 121–128.Google Scholar
HINE, P. M. ( 1978). Distribution of some parasites of freshwater eels in New Zealand. New Zealand Journal of Marine and Freshwater Research 12, 179–187.CrossRefGoogle Scholar
HOLTON, A. L. ( 1983). Observations on the life history of Deretrema minutum Manter, 1954 (Digenea: Zooginidae) in freshwater crustacean and fish hosts from Canterbury. New Zealand Journal of Marine and Freshwater Research 17, 373–376.CrossRefGoogle Scholar
HOLTON, A. L. ( 1984 a). Progenesis as a means of abbreviating life histories in two New Zealand trematodes, Coitocaecum parvum Crowcroft, 1945 and Stegodexamene anguillae MacFarlane, 1951. Mauri Ora 11, 63–70.Google Scholar
HOLTON, A. L. ( 1984 b). A redescription of Coitocaecum parvum Crowcroft, 1945 (Digenea: Allocreadiidae) from crustacean and fish hosts in Canterbury, previously misidentified as Coitocaecum anaspidis Hickman, 1934. New Zealand Journal of Zoology 11, 1–8.Google Scholar
HUNNINEN, A. V. & CABLE, R. N. ( 1941). Studies on the life history of Anisoporus manteri Hunninen et Cable 1940 (Trematoda: Allocreadiidae). Biological Bulletin 80, 415–428.CrossRefGoogle Scholar
HUNNINEN, A. V. & CABLE, R. N. ( 1943). The life cycle of Podocotyle atomon (Rudolphi) (Trematoda: Opecoelidae). Transactions of the American Microscopical Society 62, 57–68.CrossRefGoogle Scholar
HUNTER, W. S. & VERNBERG, W. B. ( 1953). Early stages in the life cycle of the trematode Gynaecotyla adunca (Linton, 1905). Transactions of the American Microscopical Society 72, 163–170.CrossRefGoogle Scholar
JACKSON, C. J., MARCOGLIESE, D. J. & BURT, M. D. B. ( 1997). Precociously developed Ascarophis sp. (Nematoda, Spirurata) and Hemiurus levinseni (Digenea, Hemiuridae) in their crustacean intermediate hosts. Acta Parasitologica 42, 31–35.Google Scholar
JAMIESON, B. G. M. ( 1966). Larval stages of the progenetic trematode Parahemiurus bennettae Jamieson, 1966 (Digenea, Hemiuridae) and evolutionary origin of cercariae. Proceedings of the Royal Society of Queensland 77, 81–93.Google Scholar
JANARDANAN, K. P., RAMANANDAN, S. K. & USHA, N. V. ( 1987). On the progenetic metacercaria of Pleurogenoides ovatus Rao, 1977 (Trematoda: Pleurogenitinae) from the freshwater crab, Paratelphusa hydrodromous (Herbst), with observations on its in vitro excystment. Zoologischer Anzeiger 219, 313–320.Google Scholar
JARLING, C. & KAPP, H. ( 1985). Infestation of Atlantic chaetognaths with helminths and ciliates. Diseases of Aquatic Organisms 1, 23–28.CrossRefGoogle Scholar
JOHNSTON, B. R. & HALTON, D. W. ( 1981). Excystation in vitro of Bucephaloides gracilescens metacercaria (Trematoda: Bucephalidae). Zeitschrift für Parasitenkunde 65, 71–78.CrossRefGoogle Scholar
JOYEUX, C., NOYER, R. & BAER, J. G. ( 1930). L'activité génitale des métacercaires progénétiques. Bulletin de la Société de Pathologie Exotique 23, 967–977.Google Scholar
KECHEMIR, N. ( 1978). Démonstration expérimentale d'un cycle biologique à quatre hôtes obligatoires chez les Trématodes Hémiurides. Annales de Parasitologie Humaine et Comparée 53, 75–92.CrossRefGoogle Scholar
KHALIL, G. M. & CABLE, R. M. ( 1968). Germinal development in Philophthalmus megalurus (Cort, 1914) (Trematoda: Digenea). Zeitschrift für Parasitenkunde 31, 211–231.CrossRefGoogle Scholar
KØIE, M. ( 1981). On the morphology and life-history of Podocotyle reflexa (Creplin, 1825) Odhner, 1905, and a comparison of its developmental stages with those of P. atomon (Rudolphi, 1802) Odhner, 1905 (Trematoda, Opecoelidae). Ophelia 20, 17–43.Google Scholar
KOMAKI, Y. ( 1970). On the parasitic organisms of krill, Euphausia similis, from Suruga Bay. Journal of Oceanography Society of Japan 26, 283–295.CrossRefGoogle Scholar
KOMIYA, K. & TAJIMI, T. ( 1941). Metacercariae from Chinese Pseudorasbora parva Temm. et Schleg. with special reference to their excretory system. Journal of Shanghai Sciences Institute (N. S.) 1, 69–196.Google Scholar
LACKIE, A. M. ( 1975). The activation of infective stages of endoparasites of vertebrates. Biological Reviews 50, 285–323.CrossRefGoogle Scholar
LEFEBVRE, F. & POULIN, R. ( 2005 a). Life history constraints on the evolution of abbreviated life cycle in parasitic trematodes. Journal of Helminthology (in the Press).Google Scholar
LEFEBVRE, F. & POULIN, R. ( 2005 b). Alternative reproductive strategies in the progenetic trematode Coitocaecum parvum: comparison of selfing and mating worms. Journal of Parasitology (in the Press).Google Scholar
LLUCH, J., NAVARRO, P. & ROCA, V. ( 1985). Presencia en España de Ratzia parva (Stossich, 1904) Poche 1926 (Digenea, Opisthorchiidae) parasito de anfibios y reptiles. Miscellanea Zoologica 9, 25–29.Google Scholar
LOTZ, J. M. & CORKUM, K. C. ( 1983). Studies on the life history of Sogandaritrema progeneticus (Digenea: Microphallidae). Journal of Parasitology 69, 918–921.CrossRefGoogle Scholar
MacFARLANE, W. V. ( 1939). Life cycle of Coitocaecum anaspidis Hickman, a New Zealand digenetic trematode. Parasitology 31, 172–184.CrossRefGoogle Scholar
MacFARLANE, W. V. ( 1945). The life cycle of the heterophyid trematode, Telogaster opisthorchis n. g., n. sp. Proceedings of the Royal Society of New Zealand 75, 218–230.Google Scholar
MacFARLANE, W. V. ( 1951). The life cycle of Stegodexamene anguillae n. g., n. sp., an allocreadid trematode from New Zealand. Parasitology 41, 1–10.Google Scholar
MacINTOSH, A. ( 1935). A progenetic metacercaria of a Clinostomum in a West-Indian land snail. Proceedings of the Helminthological Society of Washington 2, 79–80.Google Scholar
MacMULLEN, D. B. ( 1938). Observations on precocious metacercarial development in the trematode superfamily Plagiorchioidea. Journal of Parasitology 24, 273–280.CrossRefGoogle Scholar
MACY, R. W. & BASCH, P. F. ( 1972). Orthetrotrema monostomum gen. et sp. n., a progenetic trematode (Dicrocoeliidae) from dragonflies in Malaysia. Journal of Parasitology 58, 515–518.Google Scholar
MADHAVI, R. & SWARNAKUMARI, V. G. M. ( 1995). The morphology, life-cycle and systematic position of Orthetrotrema monostomum Macy & Basch, 1972, a progenetic trematode. Systematic Parasitology 32, 225–232.CrossRefGoogle Scholar
MAILLARD, C. ( 1973). Mise en évidence du cycle évolutif abrégé d'Aphalloïdes coelomicola Dollfus, Chabaud, et Golvan, 1957 (Trematoda). Notion d'hôte historique. Comptes Rendus de l'Académie des Sciences, Paris 277, 317–320.Google Scholar
MANTER, H. W. ( 1954). Some digenetic trematodes from fishes of New Zealand. Transactions of the Royal Society of New Zealand 82, 475–568.Google Scholar
MARCOGLIESE, D. J. ( 1996). Evidence for specificity of Steganoderma formosum for its second intermediate host in the Northwest Atlantic. Journal of Helminthology 70, 215–218.CrossRefGoogle Scholar
MARKOWSKI, G. ( 1936). Über die Trematodenfauna der baltischen Mollusken aus der Umgebung der halbinsel Hel. Bulletin de l'Académie Polonaise des Sciences et Lettres, Sciences Mathématiques et Naturelles, B 2, 311.Google Scholar
MARTORELLI, S. R. ( 1989). Estudios parasitológicos en biotopos lénticos de la República Argentina V: Desarrollo del ciclo biológico monoxeno de la metacercaria progenética de Genarchella genarchella Travassos, 1928 (Digenea, Hemiuridae) parásita de Littoridina parachappei (Mollusca, Hydrobiidae). Revista del Museo de la Plata, Buenos Aires 14, 109–117.Google Scholar
MATTHEWS, R. A. ( 1973). The life-cycle of Prosorhynchus crucibulum (Rudolphi, 1819) Odhner, 1905, and a comparison of its cercaria with that of Prosorhynchus squamatus Odhner, 1905. Parasitology 66, 133–164.CrossRefGoogle Scholar
MATTHEWS, R. A. ( 1974). The life cycle of Bucephaloides gracilescens (Rudolphi, 1819) Hopkins 1954 (Digenea: Gasterostomata). Parasitology 68, 1–12.CrossRefGoogle Scholar
MAYNARD-SMITH, J. ( 1998). Evolutionary Genetics, 2nd Edn. Cambridge University Press, Cambridge.
MYERS, B. J. ( 1956). An adult Hemiurus sp. (Trematoda) from Sagitta elegans Verrill. Canadian Journal of Zoology 34, 206–207.Google Scholar
NATH, D. & PANDE, B. P. ( 1970). A mature halipegid fluke from a libellulid dragonfly. Indian Journal of Helminthology 22, 102–106.Google Scholar
NEUMANN, M. P. & VANDE VUSSE, F. J. ( 1976). Two new species of Alloglossidium Simer 1929 (Trematoda: Macroderoididae) from Minnesota leeches. Journal of Parasitology 62, 556–559.CrossRefGoogle Scholar
NOLLEN, P. M. ( 1971). Viability of a self-fertilizing strain of Philophthalmus megalurus (Trematoda: Digenea). Journal of Parasitology 57, 1222–1226.CrossRefGoogle Scholar
NOLLEN, P. M. ( 1978). Studies on the reproductive system of Philophthalmus gralli using autoradiography and transplantation. Journal of Parasitology 64, 613–616.CrossRefGoogle Scholar
NOLLEN, P. M. ( 1983). Patterns of sexual reproduction among parasitic platyhelminths. Parasitology 86, 99–120.CrossRefGoogle Scholar
OKABE, K. & SHIBUE, H. ( 1951). The second intermediate host of Pleurogenes japonicus Yamaguti. Japanese Medical Association Journal 4, 401–410.CrossRefGoogle Scholar
OLIVA, M. E. & HUAQUIN, L. G. ( 2000). Progenesis in Proctoeces lintoni (Fellodistomidae), a parasite of Fissurella crassa (Archaeogastropoda) in a latitudinal gradient in the Pacific coast of South America. Journal of Parasitology 86, 768–772.CrossRefGoogle Scholar
ØRESLAND, V. ( 1986). Parasites of the chaetognath Sagitta setosa in the western English Channel. Marine Biology 92, 87–91.CrossRefGoogle Scholar
PAMPOULIE, C., LAMBERT, A., ROSECCHI, E., CRIVELLI, A. J., BOUCHEREAU, J.-L. & MORAND, S. ( 2000). Host death: a necessary condition for the transmission of Aphalloides coelomicola Dollfus, Chabaud, and Golvan, 1957 (Digenea, Cryptogonimidae). Journal of Parasitology 86, 416–417.CrossRefGoogle Scholar
PEARSON, J. C. ( 1972). A phylogeny of life-cycle patterns of the Digenea. Advances in Parasitology 10, 153–189.CrossRefGoogle Scholar
PÉREZ-PONCE DE LEÓN, G., OSORIO-SARABIA, D. & GARCÍA-PRIETO, L. ( 1992). Helmintofauna del “juile” Rhamdia guatemalensis (Pisces: Pimelodidae), del lago de Catemaco, Veracruz. Revista de la Sociedad Mexicana de Historia Natural 43, 25–31.Google Scholar
PETERS, L. E. ( 1957). An analysis of the trematode genus Allocreadium with the description of Allocreadium neotenicum sp. nov. from water beetles. Journal of Parasitology 43, 136–142.Google Scholar
PODDUBNAYA, L. G., MACKIEWICZ, J. S. & KUPERMAN, B. I. ( 2003). Ultrastructure of Archigetes sieboldi (Cestoda: Caryophyllidea): relationship between progenesis, development and evolution. Folia Parasitologica 50, 275–292.CrossRefGoogle Scholar
POINAR, G. O., SCHWARTZ, S. S. & CAMERON, G. ( 1995). Alloglossidium anomophagis sp. n. (Trematoda: Plagiorchiidae) exhibiting progenesis in water fleas (Anomopoda: Daphniidae). Experientia 51, 388–390.Google Scholar
POULIN, R. ( 2003). Information about transmission opportunities triggers a life history switch in a parasite. Evolution 57, 2899–2903.CrossRefGoogle Scholar
POULIN, R. & CRIBB, T. H. ( 2002). Trematode life cycles: short is sweet? Trends in Parasitology 18, 176–183.Google Scholar
PRÉVOT, G. ( 1974). Recherches sur le cycle biologique et l'écologie de quelques trématodes nouveaux parasites de Larus argentatus michaellis Naumann dans le midi de la France. Ph.D. thesis, Aix-Marseille University.
RAO, R. ( 1977). On a new species of Pleurogenoides Travassos, 1921 (Lecithodendriidae Odhner, 1910) and P. sitapurii, Srivastava, 1934, from frogs in Hyderabad. Rivista di Parassitologia 38, 23–29.Google Scholar
REILLY, S. M., WILEY, E. O. & MEINHARDT, D. J. ( 1997). An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena. Biological Journal of the Linnean Society 60, 119–143.CrossRefGoogle Scholar
REIMER, L. W. ( 1961). Precocious development of Bunocotyle (a hemiurid) in Hydrobia ventrosa. Wiadomosci Parazytologiczne 7, 843–849.Google Scholar
REIMER, L. W. ( 1973). Das auftreten eines Fischtrematoden der Gattung Asymphylodora Looss, 1899, bei Nereis diversicolor O.F. Müller als Beispiel für einen Alternativzyklus. Zoologischer Anzeiger 191, 187–196.Google Scholar
RIGGS, M. & ULMER, M. J. ( 1983). Host-parasite relationships of helminth parasites of the genus Haemopis. I. Associations at the individual host level. Transactions of the American Microscopical Society 102, 213–226.Google Scholar
ROHDE, K. ( 1994). The origins of parasitism in the Platyhelminthes. International Journal for Parasitology 24, 1099–1115.CrossRefGoogle Scholar
SCHMIDT, G. D. & CHALOUPKA, K. ( 1969). Alloglossidium hirudicola sp. n., a neotenic trematode (Plagiorchiidae) from leeches Haemopis sp. Journal of Parasitology 55, 1185–1186.Google Scholar
SCHOLTZ, T., VARGAS-VASQUEZ, J. & SALGADO-MALDONADO, G. ( 1995). Revision of Genarchella species (Digenea: Derogenidae) parasitizing freshwater fishes in Mexico and Central America. Journal of Natural History 29, 1403–1417.CrossRefGoogle Scholar
SHIMAZU, T. ( 1971). Description of the progenetic metacercaria of Pseudopecoelus japonicus (Allocreadiidae: Trematoda) from Euphausia similis (Euphausiacea: Crustacea) of Suruga Bay. Japanese Journal of Parasitology 20, 83–86.Google Scholar
SHIMAZU, T. ( 1991). Notes on three helminth parasites of Sagitta bedoti (Chaetognatha) from the West Bengal, India. Journal of Nagasaki Prefecture College 46, 1–8.Google Scholar
SINITSIN, D. F. ( 1931). The life history of Plagioporus siliculus and Plagioporus virens, with special reference to the origin of Digenea. Zeitschrift für Wissenschaftliche Zoologie 138, 409–456.Google Scholar
SKRJABIN, K. I. ( 1915). Contribution à la biologie d'un trématode: Lecithodendrium chilostomum (Mehl., 1831). Comptes Rendus des Mémoires de la Société Biologique de Petrograd 78, 751–754.Google Scholar
SMYTH, J. D. ( 1962). Introduction to Animal Parasitology, 1st Edn. English University Press, London.
SMYTHE, A. B. & FONT, W. F. ( 2001). Phylogenetic analysis of Alloglossidium (Digenea: Macroderoididae) and related genera: life-cycle evolution and taxonomic revision. Journal of Parasitology 87, 386–391.CrossRefGoogle Scholar
SOGANDARES-BERNAL, F. ( 1962). Microphallus progeneticus, a new apharyngeate progenetic trematode (Microphallidae) from the dwarf crayfish Cambarellus puer. Tulane Studies in Zoology 9, 319–322.Google Scholar
SOGANDARES-BERNAL, F. ( 1965). Parasites from Louisiana crayfishes. Tulane Studies in Zoology 12, 79–85.Google Scholar
STAFFORD, E. W. ( 1932). Platyhelminths in aquatic insects and crustacea. Journal of Parasitology 18, 131.Google Scholar
STUNKARD, H. W. ( 1959). The morphology and life history of the digenetic trematode Asymphylodora amnicolae n. sp., the possible significance of progenesis for the phylogeny of the Digenea. Biological Bulletin 117, 562–581.Google Scholar
STUNKARD, H. W. ( 1976). Life-cycles, intermediate hosts, and larval stages of Rhipidocotyle transversale Chandler, 1935 and Rhipidocotyle lintoni Hopkins, 1954. Life cycles and systematics of bucephalid trematodes. Biological Bulletin 150, 294–317.Google Scholar
STUNKARD, H. W. & UZMANN, J. R. ( 1959). The life cycle of the digenetic trematode, Proctoeces maculatus (Looss, 1901) Odhner, 1911. (Syn. P. subtenuis (Linton, 1907) Hanson, 1950) and description of Cercaria adranocerca n. sp. Biological Bulletin 116, 184–193.Google Scholar
SUKHDEO, M. V. K. & BANSEMIR, A. D. ( 1996). Critical resources that influence habitat selection decisions by gastrointestinal parasites. International Journal for Parasitology 26, 483–498.CrossRefGoogle Scholar
SULLIVAN, J. J. & HEARD, R. W. ( 1969). Macroderoides progeneticus n. sp., a progenetic trematode (Digenea: Macroderoididae) from the antennary gland of the crayfish, Procambarus spiculifer (Leconte). Transactions of the American Microscopical Society 88, 304–308.Google Scholar
TAFT, S. J. & KORDIYAK, G. J. ( 1973). Incidence, distribution, and morphology of the Macroderoidid trematode Alloglossidium hirudicola Schmidt and Chaloupka, 1969, from leeches. Proceedings of the Helminthological Society of Washington 40, 183–186.Google Scholar
TANG, Z. ( 1980). Progenetic development of Asymphylodora stenothyrae n. sp. Acta Hydrobiologica Sinica 7, 231–244.Google Scholar
THOMAS, F., BROWN, S. P., SUKHDEO, M. & RENAUD, F. ( 2002). Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387–390.Google Scholar
TIMMERS, S. F. ( 1979). Alloglossidium schmidti sp. n. (Trematoda: Macroderoididae) from hirudinid leeches in Manitoba. Proceedings of the Helminthological Society of Washington 46, 180–184.Google Scholar
TRAVASSOS, L. ( 1931). Note sur l'évolution de l'Ascocotyle angrense (Phagicola). Comptes Rendus des Séances de la Société de Biologie 106, 512.Google Scholar
TURNER, H. M. ( 1999). Distribution and prevalence of Alloglossoides cardicola (Trematoda: Macroderoididae), a parasite of the crayfish Procambarus acutus within the State of Louisiana, U.S.A., and into adjoining States. Journal of the Helminthological Society of Washington 66, 86–88.Google Scholar
USPENSKAYA, A. V. ( 1960). Parasitofaune des crustacés benthiques de la mer des Barents. Annales de Parasitologie Humaine et Comparée 35, 221–242.CrossRefGoogle Scholar
VAES, F. ( 1974). A new type of trematode life-cycle: an invertebrate as final host. Proceedings of the Third International Congress of Parasitology 1, 351.Google Scholar
VANDE VUSSE, F. J. ( 1980). Revision of Alloglossidium Simer, 1929 (Trematoda: Macroderoididae) and description of A. microspinatum sp. n. from a leech. Journal of Parasitology 66, 667–670.Google Scholar
VON SIEBOLD, C. T. E. ( 1835). Helminthologische Beiträge. Archiv für Naturgeschichte, Berlin 1, 45–83.Google Scholar
WANG, C. L. & THOMAS, F. ( 2002). Egg production by metacercariae of Microphallus papillorobustus: a reproductive insurance? Journal of Helminthology 76, 279–281.Google Scholar
WANSON, W. W. & LARSON, O. R. ( 1972). Studies on helminths of North Dakota. V. Life history of Phyllodistomum nocomis Fischthal, 1942 (Trematoda: Gorgoderidae). Journal of Parasitology 58, 1106–1109.Google Scholar
WEST, S. A., LIVELY, C. M. & READ, A. F. ( 1999). A pluralist approach to sex and recombination. Journal of Evolutionary Biology 12, 1003–1012.CrossRefGoogle Scholar
WINSTEAD, J. T. & COUCH, J. A. ( 1981). Proctoeces sp. (Trematoda: Digenea) in the American oyster, Crassostrea virginica. Transactions of the American Microscopical Society 100, 283–321.Google Scholar
WISNIEWSKI, L. W. ( 1932). Uber zwei neue progenitischen Trematoden aus den balkanischen Gammariden. Bulletin de l'Académie Polonaise, Cracovie, B 2, 259–276.Google Scholar
WOOTTON, D. M. ( 1957). Studies on the life history of Allocreadium alloneotenicum sp. nov. (Allocreadiidae – Trematoda). Biological Bulletin 113, 488–498.Google Scholar
WU, K. ( 1938). Progenesis of Phyllodistomum lesteri sp. nov. (Trematoda: Gorgoderidae) in freshwater shrimps. Parasitology 30, 4–19.Google Scholar
YAMAGUTI, S. ( 1958). Systema Helminthum, 1 – Part I. The Digenetic Trematodes of Vertebrates. Interscience Publishers, New York.
YAMAGUTI, S. & NISHIMURA, H. ( 1944). One nematode and two trematode larvae from Caridina denticulata de Hann. Hukuoka Acta Medica 37, 36–41.Google Scholar
YEH, J. & WU, K. ( 1950). Progenesis of Microphallus minus Ouchi (Trematoda: Microphallidae) in freshwater shrimps. Peking Natural History Bulletin 19, 193–208.Google Scholar
YEH, Y. & WU, S. C. ( 1955). Note on a new trematode Genarchopsis shangaiensis (Trematoda: Hemiuridae) and its progenesis in freshwater shrimps around Shangai region. Acta Zoologica Sinica 7, 37–42.Google Scholar