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The chemical nature and evolutionary significance of monogenean attachment sclerites

Published online by Cambridge University Press:  06 April 2009

Kathleen M. Lyons
Affiliation:
Department of Zoology and Comparative Physiology, The University, Birmingham*

Extract

The chemical and physical nature of monogenean attachment sclerites has been investigated by chromatography, histochemistry, solubility studies and X-ray diffraction, and these sclerites have been shown to be scleroproteinaceous and not, as the bulk of the literature suggests, chitinous in composition.

Hooks sclerites (i.e. marginal hooks and hamuli), which are the most primitive type of monogenean attachment sclerites and arise early on ontogeny, have been shown to be keratinous; clamp sclerites, accessory bars and the spines arming the pseudohaptors and squamodisks of certain genera which appear to have been acquired later in the phylogeny of the group to supplement the efficiency of the haptoral hooks, contain no cystine sulphur.

While the chemical nature of the non-cystine-containing skeletal structures has not been fully elucidated, clamp substance was found to differ from that of the other scleroproteins with which it was compared, namely sclerotin, vertebrate elastin, reticulin, collagen and keratin. Clamp substance does not appear to be quinonetanned; acid proteins maybe important in the stabilization of this scleroprotein.

Evidence for the occurrence of a variety of S–S bearing scleroproteins throughout the invertebrates has been collated and the problems involved in adequately defining a keratin have been discussed. The implications of the apparent affinity of monogenean hook protein to vertebrate keratins, which in general are intracellular and epidermal derivatives have been considered and some speculations have been made about the possible differences in the development of hook and clamp structures.

Contrary to the prevalent opinion that monogenean sclerites are ‘cuticularizations’, evidence has been presented that these structures are in fact deeply seated and unlikely to be derivations of a superficial cuticle.

The chemical differences elucidated between the median and lateral sclerites of the chimaericolid adhesive organ have encouraged speculation on the evolution of the different types of attachment organ throughout the polyopisthocotylineans.

Outside the Monogenea, studies on the sulphur content of digenean spines and stylets and on the larval hooklets of the ‘cestodarians’ Gyrocotyle, Amphilina and Archigetes, and of eucestodes, have helped to substantiate the view that the cestodes and monogeneans are more closely related to each other than either of these groups is related to the digeneans.

I wish to thank the Director and staff of the Plymouth Laboratory and in particular Mr J. E. Green, for invaluable assistance. I am also indebted to Dr R. W. H. Small for his guidance on X-ray diffraction technique, to Dr J. Morris of the M.R.C. Skin Unit for his advice on the chromatography and to Dr J. Llewellyn for his interest and helpful criticism throughout.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1966

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References

REFERENCES

Adams, C.W.M. (1957). A dimethylamino-benzaldehyde-nitrite method for the demonstration of tryptophane and related compounds. J. clin. Path. 10, 5662.CrossRefGoogle ScholarPubMed
Beneden, P. J. van & Hesse, C. E. (1863). Recherches sur les bdellodes ou hirudinées et les trématodes marins. Mém. Acad. r. Beige. Cl. Sci. 34, 1152.Google Scholar
Blower, J. E. (1951). A comparative study of the chilopod and diplopod cuticle. Q. Jl microsc. Sci. 92, 141–61.Google Scholar
Brinkmann, A. Jr (1942). On Octobothrium leptogaster F. S. Leukart. Göteborgs K. Vetensk.-o. Vitterhsamh. Handl. 6F Ser. B, 3, 1290.Google Scholar
Brown, C. H. (1950). A review of the methods available for the determination of the types of forces stabilizing structural proteins in animals. Q. Jl microsc. Sci. 91, 331–9.Google ScholarPubMed
Bychowsky, B. E. (1957). Monogenetic Trematodes, their Classification and Phylogeny, 509 pp. Moscow: Leningrad, Academy of Sciences, U.S.S.R.Google Scholar
Chitwood, B. G. & Chitwood, M. B. (1950). An Introduction to Nematology. Baltimore, Md: Monumental Printing Company.Google Scholar
Coupland, A. C. (1960). Studies on the monogenean gill parasites of elasmobranchs, 72 pp. Unpublished thesis in library of the University of Birmingham.Google Scholar
Crompton, D. W. T. (1963). Morphological and histochemical observations in Polymorphus minutus (Goeze, 1782), with special reference to the body wall. Parasitology, 53, 663–85.CrossRefGoogle Scholar
Crusz, H. (1947). The early development of the rostellum of Cysticercus fasciolaris and the chemical nature of its hooks. J. Parasit. 33, 8798.CrossRefGoogle ScholarPubMed
Crusz, H. (1948). Further studies in the development of Cysticercus fasciolaris and C. rusiformis with special reference to the growth and sclerotization of the rostellar hooks. J. Helminth. 22, 179–98.CrossRefGoogle Scholar
Dubinina, M. N. (1960). K morfologii Amphilinidae (Cestodaria) v svyazi c ich polozheniem v sisteme ploskikh chervei. Dokl. (Proc.) Acad. Sci. U.S.S.R. 135, 501–4.Google Scholar
Dulbecco, R. & Volgt, M. (1954). Plaque formation and isolation of pure lines with poliomyelitis viruses. J. exp. Med. 99, 167–82.CrossRefGoogle ScholarPubMed
Gallagher, I. H. C. (1964). The chemical composition of hooks isolated from hydatid scolices. Expl Parasit. 15, 110–17.CrossRefGoogle ScholarPubMed
Goddard, D. R. & Michaelis, L. (1934). A study on keratin. J. biol. Chem. 106, 605–14.CrossRefGoogle Scholar
Goto, S. (1895). Studies on the ectoparasitic trematodes of Japan. J. Coll. Sci. imp. Univ. Tokyo, 8, 1273.Google Scholar
Hackman, R. H. (1953). The chemistry of insect cuticle. I, The water-soluble proteins. Biochem. J. 54, 362–7.CrossRefGoogle ScholarPubMed
Halkin, H. (1901). Recherches sur la maturation, la fécondation et le developpement du Polystomum integerrimum. Archs Biol., Paris, 18, 291363.Google Scholar
Hanumantha Rao, K. (1963). The structure of Mehlis's gland complex and histochemistry of Artyfechinostomum mehrai (Faraqui) Trematoda: Echinostomatidea, from a girl at Andhra Pradesh, India. Parasitology, 53, 15.Google Scholar
Hargis, W. J. Jr (1958). Homologies of the clamp sclerites of Chimaericola leptogaster Leuckart, 1830, Brinkmann, 1942, Chimaericoloidea: Monogenea and related gill parasites of holocephalan fishes. Abstract. J. Parasit. (sect 2B), 44, 43.Google Scholar
Hargis, W. J. & Oustinoff, P. C. (1961). Monogenetic Trematodes, their Classification and Phylogeny. (English translation of Bychowsky, B. E. (1957). Washington: American Institute of Biological Sciences.)Google Scholar
Hyman, L. J. (1951). The Invertebrates, vol. 2. New York: McGraw-Hill Book Co.Google Scholar
Johri, L. N. (1957). A morphological and histochemical study of the egg formation in a cyclo-phyllidean cestode. Parasitology, 47, 21–9.CrossRefGoogle Scholar
Johri, L. N. & Smyth, J. D. (1956). A histochemical approach to the study of helminth morphology. Parasitology, 46, 107–16.CrossRefGoogle Scholar
Kearn, G. C. (1963). The egg, oncomiracidium and larval development of Entobdella soleae a monogenean skin parasite of the common sole. Parasitology, 53, 435–47.CrossRefGoogle Scholar
Kearn, G. C. (1964). The attachment of the monogenean Entobdella soleae to the skin of the common sole. Parasitology, 54, 327–35.CrossRefGoogle Scholar
Krishnan, G. (1953). On the cuticle of the Scorpion Palamneus swammerdami. Q. Jl microsc. Sci. 94, 1121.Google Scholar
Krishnan, G. (1954). The epicuticle of an arachnid Palamneus swammerdami. Q. Jl microsc. Sci. 95, 371–81.Google Scholar
Lee, D. L. (1962). Studies on the function of the pseudosuckers and holdfast organ of Diplostomum phoxini, Faust (Strigeida, Trematoda). Parasitology, 52, 103–12.CrossRefGoogle Scholar
Lison, L. (1936). Histochimie animale, 1st ed.Paris: Gauthier-Villars.Google Scholar
Llewellyn, J. (1957). The mechanism of the attachment of Kuhnia scombri (Kuhn, 1829) (Trematoda: Monogenea) to the gills of its host Scomber scombrus, L., including a note on the taxonomy of the parasite. Parasitology, 47, 30–9.CrossRefGoogle Scholar
Llewellyn, J. (1963). Larvae and larval development of monogeneans. Advances in Parasitology, vol. 1, 287326.CrossRefGoogle ScholarPubMed
Llewellyn, J. (1965). The evolution of parasitive platyhelminths. Symp. Brit. Soc. Parasit. 3, 4778.Google Scholar
Lynch, J. E. (1945). A redescription of the species of Gyrocotyle from the Rat-fish, Hydrolagus colliei (Ray and Bennet), with notes on the morphology and taxonomy of the genus. J. Parasit. 31, 418–46.CrossRefGoogle Scholar
Mercer, E. H. (1961). Keratin and Keratinization. Oxford: Pergamon Press.Google Scholar
Monné, L. (1955). On the histochemical properties of the egg envelopes and external cuticles of some parasitic nematodes. Ark. Zool. 9, 93112.Google Scholar
Monné, L. & Honig, G. (1954 a). On the properties of the egg envelopes of the parasitic nematodes Trichuris and Capillaria. Ark. Zool. 6, 559–62.Google Scholar
Monné, L. & Honig, G. (1954 b). On the embryonic envelopes of Polymorphus botulus and P. minutus (Acanthocephala). Ark. Zool. 7, 257–60.Google Scholar
Neurath, H. & Bailey, K. (1953). The Proteins, vol. 1. New York: Academic Press Inc.Google Scholar
Ogren, R. E. (1957). Morphology and development of oncospheres of the cestode Oochoristica symmetrica Baylis, 1927. J. Parasit. 43, 505–20.CrossRefGoogle ScholarPubMed
Ogren, R. E. (1961). Observations on hook development in the oncoblasts of hexacanth embryos from Hymenolepis diminuta, a tapeworm of mammals. (Cestoda: Cyclophyllidea). Proc. Pa. Acad. Sci. 35, 2331.Google Scholar
Pearse, A. G. E. (1961). Histochemistry, Theoretical and Applied, 2nd ed.London: J. and A. Churchill Ltd.Google Scholar
Prosser, C. L. & Brown, F. A. (1961). Comparative Animal Physiology, 2nd ed.Philadelphia and London: W. B. Saunders Co.Google Scholar
Remley, L. W. (1942). Morphology and life history studies of Microcotyle spinicirrus MacCallum, 1918, a monogenetic trematode parasitic on the gills of Aplodinotus grunniens. Trans. Am. microsc. Soc., 61, 141–55.CrossRefGoogle Scholar
Scheuring, L. (1938). Beitrage zur Kenntnis von Discocotyle sagittatum Dies., pp. 535–50. Grigore Antipa, Hommage a son oeuvre, Bucuresti.Google Scholar
Scott, H. R. & Clayton, B. P. (1953). A comparison of the staining affinities of aldehyde fuchsin and the Schiff reagent. J. Histochem. Cytochem. 1, 336–49.CrossRefGoogle ScholarPubMed
Sewell, M. T. (1955). The histology and histochemistry of the cuticle of a spider Tegenaria domestica L. Ann. ent. Soc. Am. 48, 107–18.CrossRefGoogle Scholar
Smith, I. (1961). Chromatographic and Electrophoretic Techniques, vol. 1. Chromatography. 2nd ed.London: Heinemann.Google Scholar
Smyth, J. D. (1951). Specific staining of egg shell material in Trematodes and Cestodes. Stain Technol. 26, 255–6.CrossRefGoogle ScholarPubMed
Smyth, J. D. & Clegg, J. A. (1959). Eggshell formation in trematodes and cestodes. Expl Parasit. 8, 286323.CrossRefGoogle ScholarPubMed
Sproston, N. G. (1946). A synopsis of monogenetic trematodes. Trans. zool. Soc. Lond. 25, 185600.CrossRefGoogle Scholar
Trim, A. C. H. (1941). The protein of the insect cuticle. Nature, Lond., 147, 115–16.CrossRefGoogle Scholar
Ward, W. H. & Lundgren, H. P. (1954). The formation, composition and properties of keratins. Adv. Protein Chem. 9, 243–97.CrossRefGoogle ScholarPubMed