Abstract
The fine structure of bivalents in metaphase I spermatocytes of two Lepidoptera species, Orgyia thyellina Butler (n = 11) and O. antiqua (L.) (n = 14) (Lymantriidae), and a Trichoptera species, Limnephilus decipiens (Kolenatý) (n = 10) (Limnephilidae) were studied using a series of ultrathin sections and transmission electron microscopy. The bulk of species in both orders possess a haploid chromosome number of about 30. Thus, the experimental species have relatively small chromosome numbers. This study showed that metaphase I bivalents in both Lepidoptera species are polykinetic; attachment of kinetochore microtubules is found scattered throughout the entire poleward chromosomal surface. The microtubules were inserted in material of medium electron density. A pair of distinct kinetochore plates, consisting of material of about the same electron density as the chromatin, was detected at each poleward chromosomal surface in metaphase I bivalents of the caddis-fly, L. decipiens. The observations suggest that DNA elements responsible for the organization of the kinetochores are dispersed throughout the chromosomes in the two Lepidoptera species, whereas they are narrowly clustered in the Trichoptera. Thus, karyotype evolution in the closely related Lepidoptera and the Trichoptera involved widely differing mechanisms.
Similar content being viewed by others
Article PDF
References
Ault, J G, and Lyttle, T W. 1988. A transmissible dicentric chromosome in Drosophila melanogaster. Chromosoma 97, 71–79.
Choo, K H, Vissel, B, Nagy, A, Earle, E, and Kalitsis, P. 1991. A survey of the genomic distribution of alpha satellite DNA on all the human chromosomes, and derivation of a new consensus sequence. Nucl Acids Res, 19, 1179–1182.
Cretschmar, M. 1928. Das Verhalten der Chromosome bei der Spermatogenese von Orgyia thyellina Btl. und antiqua L., sowie eines ihrer Bastarde. Z Zellforsch Mikrosk Anat, 7, 291–399.
Earnshaw, W C, and Migeon, B R. 1985. Three related centromere proteins are absent from the inactive centromere of a stable isodicentric chromosome. Chromosoma 92, 290–296.
Friedländer, M. 1983. Phylogenetic branching of Trichoptera and Lepidoptera: An ultrastructural analysis on comparative spermatology. J Ultrastruct Res, 83, 141–147.
Gassner, G, and Klemetson, D J. 1974. A transmission electron microscope examination of Hemipteran and Lepidopteran gonial centromeres. Can J Genet Cytol, 16, 457–464.
Goodpasture, C. 1975. High-resolution chromosome analysis in Lepidoptera. Ann Entomol Soc Am, 69, 537–544.
Hamon, C, and Chauvin, G. 1992. Ultrastructural analysis of spermatozoa of Korscheltellus lupulinus L. (Lepidoptera: Hepialidae) and Micropterix calthella L. (Lepidoptera: Micropterigidae). Int J Insect Morphol Embryol, 21, 149–160.
Holm, P B, and Rasmussen, S W. 1980. Chromosome pairing, recombination nodules and chiasma formation in diploid Bombyx males. Carlsberg Res Comm, 45, 483–548.
Kiauta, B. 1971. The chromosome condition in the spermatogenesis of the caddis-fly Goera pilosa (Fabricius, 1775) (Trichoptera, Integripalpia, Limnephiloidea: Goeridae) from the God dal Fuorn in the Swiss National Park, with considerations on the phylogenetic position of the family. Ergeb Wiss Untersuch Schweiz Natl-Park, 9, 174–185.
Klingstedt, H. 1931. Digametie beim Weibchen der Trichoptere Limnophilus decipiens Kol. nebst Erörterungen zur Theorie der Geschlechtsvererbung. Acta Zool Fenn, 10, 1–64.
Kobayashi, Y, and Ando, H. 1988. Phylogenese relationships among the lepidopteran and trichopteran suborders (Insecta) from the embryological standpoint. Z Zool Syst Evolut-forsch, 26, 186–210.
Kristensen, N P. 1991. Phylogeny of extant Hexapods. In: Naumann, I. D., Carne, P. B., Lawrence, J. F., Nielsen, E. S., Spradbery, J. P., Taylor, R. W. et al. (eds) The Insects of Australia, 2nd edn, 1, pp. 125–140. Melbourne University Press, Carlton, Victoria, Australia.
Lankhorst, L. 1970. A note on the periodicity of cell divisions in the gonads of Trichoptera, with a review of the main cytotaxonomic data on the caddis-fly species so far studied. Genen Phaenen, 14, 9–14.
Le Lannic, J. 1975. Contribution à l'étude du développment et de la maturation de l'appareil reproducteur de Limnephilus rhombicus L. Bull Soc Zool Fr, 100, 539–550.
Lockwood, A P M. 1961. ‘Ringer’ solutions and some notes on the physiological basis of their ionic composition. Comp Biochem Physiol, 2, 241–289.
Meves, F. 1903. über oligopyrene und apyrene Spermien und über ihre Entstehung nach Beobachtungen an Paludina und Pygaera. Arch Mikrosk Anat Entwicklungsgesch, 61, 1–84.
Neboiss, A. 1991. Trichoptera. (Caddis-flies, caddises). In: Naumann, I. D., Carne, P. B., Lawrence, J. F., Nielsen, E. S-, Spradbery, J. P., Taylor, R. W. et al. (eds) The Insects of Australia, 2nd edn, 2, pp. 787–816. Melbourne University Press, Carlton, Victoria, Australia.
Nielsen, E S, and Common, I F B. 1991. Lepidoptera (moths and butterflies). In: Naumann, I. D., Carne, P. B., Lawrence, J. F., Nielsen, E. S., Spradbery, J. P., Taylor, R. W. et al. (eds) The Insects of Australia, 2nd edn, 2, pp. 817–915. Melbourne University Press, Carlton, Victoria, Australia.
Novák, K, and Sehnal, F. 1963. The development cycle of some species of the genus Limnephilus (Trichoptera). Acta Soc Entomol Čechoslov, 60, 68–80.
Rieder, C L. 1982. The formation, structure and composition of the mammalian kinetochore and kinetochore fiber. Int Rev Cytol, 79, 1–58.
Robinson, R. 1971. Lepidoptera Genetics. Pergamon Press, Oxford.
Sonnenschein, M, and Häuser, C L. 1990. Presence of only eupyrene spermatozoa in adult males of the genus Micropterix Hübner and its phylogenetic significance (Lepidoptera: Zeugloptera, Micropterigidae). Int I Insect Morphol Embryol, 19, 269–276.
Suomalainen, M. 1966. Achiasmatische Oogonese bei Trichopteren. Chromosoma, 18, 201–207.
Suomalainen, E. 1969. Chromosome evolution in the Lepidoptera. Chromosomes Today, 2, 132–138.
Traut, W. 1976. Pachytene mapping in the female silkworm, Bombyx mori L. (Lepidoptera). Chromosoma, 58, 275–284.
Traut, W, and Mosbacher, G C. 1968. Geschlechtschromatin bei Lepidopteren. Chromosoma, 25, 343–356.
Wandall, A. 1994. A stable dicentric chromosome: Both centromeres develop kinetochores and attach to the spindle in monocentric and dicentric configuration. Chromosoma, 103, 56–62.
White, M J D. 1973. Animal Cytology and Evolution. Cambridge University Press, Cambridge.
Wolf, K W. 1990. Sheathed nuclear division in primary spermatocytes of Orgyia antiqua (Lepidoptera, Insecta). BioSystems, 24, 5–15.
Wolf, K W. 1994. The unique structure of Lepidopteran spindles. Int Rev Cytol, 152, 1–48.
Wolf, K W. 1995. Spindle membranes and spindle architecture in invertebrates. Micron, 26, 69–98.
Wolf, K W. 1996. The structure of condensed chromosomes in mitosis and meiosis of insects. Int J Insect Morphol Embryol, 25, 37–62.
Wolf, K W, and Traut, W. 1991. Cytology of Lepidoptera. VII. The restructuring of eupyrene prophase I spermatocytes and its relationship to meiotic chromosome and spindle organization in Ephestia kuehniella Z. Protoplasma 165, 51–63.
Wolf, K W, Baumgart, K, and Traut, W. 1987. Cytology of Lepidoptera. II. Fine structure of eupyrene and apyrene primary spermatocytes in Orgyia thyellina. Eur J Cell Biol, 44, 51–61.
Wolf, K W, Novák, K, and Marec, F. 1992. Chromosome structure in spermatogenesis of Anabolia furcata (Trichoptera). Genome, 35, 46–52.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wolf, K., Novák, K. & Marec, F. Kinetic organization of metaphase I bivalents in spermatogenesis of Lepidoptera and Trichoptera species with small chromosome numbers. Heredity 79, 135–143 (1997). https://doi.org/10.1038/hdy.1997.136
Received:
Issue Date:
DOI: https://doi.org/10.1038/hdy.1997.136
Keywords
This article is cited by
-
Observation of morphological abnormalities in silkworm pupae after feeding 137CsCl-supplemented diet to evaluate the effects of low dose-rate exposure
Scientific Reports (2020)
-
Evolutionary mechanisms of runaway chromosome number change in Agrodiaetus butterflies
Scientific Reports (2017)
-
Effects of X-rays on Tuta absoluta for use in inherited sterility programmes
Journal of Pest Science (2012)
-
Evolutionary dynamics of rDNA clusters on chromosomes of moths and butterflies (Lepidoptera)
Genetica (2010)