Abstract
Cytogenetics and gene flow were studied in microbe-associated parthenogenetic (thelytokous) forms of three species of the genus Trichogramma (T. pretiosum, T. deion and T. nr. deion). The chromosome behaviour in newly laid eggs indicated that the mechanism allowing restoration of diploidy in unfertilized thelytokous eggs was a segregation failure of the two sets of chromosomes in the first mitotic anaphase. This results in a nucleus containing two sets of identical chromosomes. The mechanism is known as gamete duplication and results in complete homozygosity. This was confirmed by investigation of the segregation pattern of allozymes in the offspring of heterozygous thelytokous females. Contrary to the generally assumed genetic isolation of thelytokous lines, thelytokous females of these species can mate and will use the sperm to fertilize some of their eggs. These fertilized eggs give rise to females whose genome consists of one set of chromosomes from each parent. Egg fertilization and the resulting syngamy of the sperm and egg pronucleus apparently precludes the gamete duplication that would have taken place if the egg had remained unfertilized. Most field populations of Trichogramma contain both parthenogenetic (thelytokous) and sexual (arrhenotokous) forms. In the two field populations that we studied there was evidence for high levels of gene flow from the sexual (arrhenotokous) fraction to the parthenogenetic (thelytokous) fraction of the population. The implications of the cytogenetic mechanism of parthenogenesis, i.e. gamete duplication, for the mechanism of sex determination in Hymenoptera are discussed.
Similar content being viewed by others
Article PDF
References
Aeschlimann, J P. 1986. Distribution and effectiveness of Anaphes diana, a parasitoid of Sitona spp. eggs in the Mediterranean region. Entomophaga, 31, 163–172.
Babi, A, and Pintureau, B. 1983. Effet de masse et superparasitisme: Influence sur l'appartion des intersexues chez Trichogramma oleae. Bull ent Soc Mulhouse, 1983, 53–55.
Benson, R B. 1950. An introduction to the natural history of British sawflies. Trans Soc Br Entomol, 10, 48–142.
Bowen, W R, and Stern, V M. 1966. Effect of temperature on the production of males and sexual mosaics in a uniparental race of Trichogramma semifumatum (Hymenoptera: Trichogrammatidae). Ann Entomol Soc Am, 59, 823–834.
Carter, W. 1937. Importation and laboratory breeding of two chalcid parasites of Pseudococcus brevipes. J Econ Entomol, 30, 370–372.
Cook, J M. 1993a. Experimental tests of sex determination in Goniozus nephantidis. Heredity, 71, 130–137.
Cook, J M. 1993b. Sex determination in the Hymenoptera: a review of models and evidence. Heredity, 71, 421–435.
Cooper, K W. 1959. A bilaterally gynandromorphic Hyodynerus, and a summary of cytologic origins of such mosaic Hymenoptera. Biology of Eumine wasps VI. Bull Fl St Mus Biological Sci, 5, 25–40.
Crozier, R H. 1971. Heterozygosity and sex determination in haplo-diploidy. Am Nat, 105, 399–412.
Day, W H, and Hedlund, R C. 1988. Biological comparisons between arrhenotokous and thelytokous biotypes of Mesochorus nigriceps. Entomophaga, 33, 201–210.
Flanders, S E. 1945. The bisexuality of uniparental hymenoptera, a function of the environment. Am Nat, 79, 122–141.
Flanders, S E. 1950. Races of apomictic parasitic hymenoptera introduced into California. J Econ Entomol, 43, 719–720.
Flanders, S E. 1965. On the sexuality and sex ratios of hymenopterous populations. Am Nat, 94, 489–494.
Kazmer, D J. 1991. Isoelectric focusing procedures for the analysis of allozymic variation in minute arthopods. Ann Entomol Soc Am, 84, 332–339.
Kazmer, D J. 1992. The Evolution of Reproductive Strategies in Trichogramma and its Relationship to Biological Control. Ph.D. Thesis, University of California, Riverside.
Laraichi, M. 1978. L'effect de hautes temperatures sur le taux sexuel de Ooencyrtus fecundus (Hym: Encyrtidae). Entomol Exp Appl, 23, 237–242.
Legner, E F. 1985. Effects of scheduled high temperature on male production in thelytokous Muscidifurax uniraptor. Can Entomol, 117, 383–389.
Legner, E F. 1987. Transfer of thelytoky to arrhenotokous Muscidifurax raptor Girault and Sanders (Hymenoptera: Pteromalidae). Can Entomol, 119, 265–271.
Luck, R F, Stouthamer, R, and Nunney, L. 1992. Sex determination and sex ratio patterns in parasitic hymenoptera. In: Wrench D. L. and Ebbert, M. A. (eds) Evolution and Diversity of Sex Ratio in Haplodiploid Insects and Mites, pp. 442–476. Chapman & Hall, New York.
Mackay, M R. 1955. Cytology and parthenogenesis of the wheat stem sawfly, Cephus cinctus Nort. Can J Zool, 33, 161–174.
Muller, H J. 1964. The relation of recombination to mutational advance. Mutat Res, 1, 2–9.
Orphanides, G M, and Gonzalez, D. 1970. Identity of a uniparental race of Trichogramma pretiosum. Ann Entomol Soc Am, 63, 1784–1786.
Peacock, A D, and Sanderson, A R. 1939. The cytology of the thelytokous parthenogenetic sawfly Thrinax maculata. Trans R Soc Edinb, 59, 647–660.
Pinto, J D, and Stouthamer, R. 1994. Systematics of the Trichogrammatidae with emphasis on Trichogramma. In: Wajnberg, E. and Hassan, S. A. (eds) Biological Control with Egg Parasitoids. CAB International, Wallingford, U.K. (in press).
Pinto, J D, Stouthamer, R, Platner, G R, and Oatman, E R. 1991. Variation in reproductive compatibility in Trichogramma and its taxonomic significance. Ann Entomol Soc Am, 84, 37–46.
Rössler, Y, and Debach, P. 1973a. Genetic variability in the thelytokous form of Aphytis mytilaspidis. Hilgardia, 42, 149–175.
Rössler, Y, and Debach, P. 1973b. The biosystematic relations between a thelytokous and arrhenotokous form of Aphytis mytilaspidis. I. The reproductive relations. Entomophaga, 17, 391–423.
Sanderson, A R. 1988. Cytological investigations of parthenogenesis in gall wasps. Genetica, 77, 189–216.
Smith, S G. 1941. A new form of spruce sawfly identified by means of its cytology and parthenogenesis. Sci Agr, 21, 245–305.
Smith, S G. 1955. Cytogenetics of obligatory parthenogenesis. Can Entomol 87, 131–135.
Snell, G D. 1935. The determination of sex in Habrobracon. Proc Natl Acad Sci USA, 21, 446–453.
Speicher, B R. 1937. Oogenesis in a thelytokous wasp, Nemeritus canescens (Grav.). J Morph, 61, 453–471.
Stille, B, and Dävring, L. 1980. Meiosis and reproductive strategy in the parthenogenetic gall wasp Diplolepis rosae. Heriditas, 92, 353–362.
Stouthamer, R. 1991. Effectiveness of several antibiotics in reverting thelytoky to arrhenotoky in Trichogramma spp. Les Colloques de l'INRA, 56, 119–122.
Stouthamer, R. 1993. The use of sexual versus asexual wasps in biological control. Entomophaga, 38, 3–6.
Stouthamer, R, Breeuwer, J A J, Luck, R F, and Werren, J H. 1993. Molecular identification of microorganisms associated with parthogenesis. Nature, 361, 66–69.
Stouthamer, R, Luck, R F, and Hamilton, W D. 1990a. Antibiotics cause parthenogenetic Trichogramma to revert to sex. Proc Natl Acad Sci USA, 87, 2424–2427.
Stouthamer, R, Luck, R F, and Werren, J H. 1992. Genetics of sex determination and the improvement of biological control using parasitoids. Environ Entomol, 21, 427–435.
Stouthamer, R, Pinto, J D, Platner, G R, and Luck, R F. 1990b. Taxonomic status of thelytokous forms of Trichogramma. Ann Entomol Soc Am, 83, 475–581.
Stouthamer, R, and Werren, J H. 1993. Microbes associated with parthenogenesis in wasps of the genus Trichogramma. J Inv Pathol, 61, 6–9.
Thomsom, M. 1927. Studien über die parthenogenese bei einigen Cocciden und Aleurodiden. Zeit für Zellforschung undmikr Anatomie, 5, 1–116.
Tucker, K W. 1958. Automictic parthenogenesis in the honey bee. Genetics, 43, 299–316.
Vargas, P, and Cabello, T. 1985. A new species of Trichogramma, parasitoid of Heliothis eggs in cotton crops in the SW of Spain. Entomophaga, 30, 225–230.
Verma, S, and Rüttner, F. 1983. Cytological analysis of the thelytokous parthenogenesis in the cape honeybee. Apidologie, 14, 41–57.
Whiting, A R. 1961. Genetics of Habrobracon. Adv Genet, 10, 295–348.
White, M J D. 1984. Chromosomal mechanisms in animal reproduction. Boll Zool, 51, 1–23.
Wilson, F. 1962. Sex determination and gynandromorph production in aberrant and normal strains of Ooencyrtus submetallicus (Hym.: Encyrtidae). Aust J Zool, 10, 349–359.
Wilson, F, and Woolcock, L T. 1960. Temperature determination of sex in a parthenogenetic parasite, Ooencyrtus submetallicus. Aust J Zool, 8, 153–169.
Young, D K. 1990. Distribution of Pelectinus polyturator in Wisconsin, with speculations regarding geographical parthenogenesis. The Great Lakes Entomologist, 23, 1–4.
Zchori-Fein, E, Rousch, R T, and Hunter, M S. 1992. Male production induced by antibiotic treatment in Encarsia formosa, an asexual species. Experientia, 48, 102–105.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Stouthamer, R., Kazmer, D. Cytogenetics of microbe-associated parthenogenesis and its consequences for gene flow in Trichogramma wasps. Heredity 73, 317–327 (1994). https://doi.org/10.1038/hdy.1994.139
Received:
Issue Date:
DOI: https://doi.org/10.1038/hdy.1994.139