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Extranuclear influences on behavior

Direct Effects of the Cytoplasmic Genome

Chemical Substances Affecting Behavior


Muscidifurax Parasitoid Complex



[ Please refer also to Selected Reviews #1, #2  &  Detailed Research ]



Extranuclear influences on behavior involving cytoplasmic entities are well known among both prokaryotes and eukaryotes (Beale & Knowles 1978, Cosmides & Tooby 1981, Goodenough 1984, Levine 1973, Sager & Ramanis 1963, Sonneborn 1959), but the subsequent incorporation of an extranuclear expression into the nuclear genome apparently have not been found. Extranuclear factors in the form of microorganisms (e.g., viruses, bacteria, spiroplasmas) can alter sex ratios in parasitoids by selectively killing developing males or females (Skinner 1982, 1985; Werren et al. 1981, 1986), may confer resistance to host encapsulation (Krell & Stoltz 1979, Stoltz & Vinson 1977, Stoltz et al. 1976, Vinson & Stoltz 1986), and affect sex ratios in Drosophila (Poulson & Sakaguchi 1961), and are passed on to succeeding generations. Cosmides and Tooby (1981) recently reviewed how cytoplasmic genes control such characters as allocation of reproductive effort in hermaphrodites, sex ratios of offspring (Williamson & Poulson 1979), organism size (Faulkner & Arlett 1964), growth rate, colony size, rate of senescence (Smith & Rubenstein 1973), competitive ability (Preer et al. 1974), drug resistance in bacteria, protozoans, fungi, and mammals (Beale & Knowles 1978), and rates of recombination among nuclear genes (Thoday & Boam 1956). Oishi et al. (1984) explained how two kinds of microorganisms (spiroplasma and virus) may interact to modify expressions of the sex-ratio factor in Drosophila. Stoltz & Vinson (1979) have found viruses in the calyx epithelial cells of endoparasitoids. Fleming & Summers (1986) found them also in the lumen of the oviduct. These viruses were passed from parent to offspring, males being able to transmit viral DNA to females with whom they mated (Stoltz et al. 1986).


The direct effects of the cytoplasmic genome on the nuclear genome has been hypothesized (Cosmides & Tooby 1981), but not demonstrated. However, the extrachromosomal genetic system can be influenced by the chromosomal system (Levine 1973). Microorganisms implicated in inheritance have been known to cause illness and death in male Drosophila (Leventhal 1968).


Chemical substances affect behavior of insects following mating. Reports include a lepidopteran (Webster & Carde 1984), and ichneumon wasp Venturia (Nemeritis) canescens (Gravenhorst) (where heneicosane was involved) (Mudd et al. 1982); and the dipteran Drosophila, involving enzymes (Mane et al. 1983, Richmond & Senior 1981). Prostaglandins, derivatives of certain polyunsaturated fatty acids, alter egg laying behavior in crickets (Stanley-Samuelson & Loher 1986). It has been suggested than an influence on the chemosensory responsiveness of an individual by chemical cues derived from its parents would be hard to distinguish from a genetic effect (Corbet 1985).


Microorganisms involved in the production of thelytoky have been identified molecularly by Stouthamer et al. (1993). They comment that inherited microorganisms are widespread in insects, having been implicated as causes of female parthenogenesis and cytoplasmic incompatibility. Normal sexual reproduction can be restored by treatment with antibiotics. Sequence analysis of the DNA encoding 16S ribosomal RNA shows that cytoplasmic incompatibility bacteria from diverse insect taxa are closely related, sharing 95% sequence similarity. They belong to the alpha subdivision of Proteobacteria. Stouthamer et al. (1993) show that parthenogenesis-associated bacteria from parasitoid Hymenoptera fall into this bacterial group, having up to 99% sequence similarity to some incompatibility microorganisms. Both incompatibility and parthenogenesis microorganisms alter host chromosome behavior during early mitotic division in the egg. Incompatibility bacteria act by interfering with paternal chromosome incorporation in fertilized eggs, while parthenogenesis bacteria prevent segregation of chromosomes in unfertilized eggs. These traits are adaptive for the microorganisms. Judging from their sequence similarities, Stouthamer et al. (1993) concluded that parthenogenesis bacteria and cytoplasmic incompatibility bacteria form a monophyletic group of microorganisms that specialize in manipulating chromosome behavior and insect reproduction.


Research on the genus Muscidifurax  (see Research) has uncovered a polygenic system controlling rates of larval cannibalism and therefore reproductive success. The genes involved are able to cause partial expression of the traits they govern shortly after insemination and before being inherited by the progeny. Extranuclear phases prior to chromosomal inheritance may involve microorganisms and/or enzymes present in hymenopteran seminal fluid. 


The ability to change expression of a quantitative character immediately after mating, either positively or negatively, challenges accepted views of polygenic loci, and it may be that such loci are not in fact inherited, but rather another group of genes which have the capability to switch on or off the loci. Such genes may influence DNA methylation of the loci controlling oviposition behavior, as shown for other organisms (). All polygenic loci may be perpetually present for a given quantitative trait in all individuals of both Muscidifurax raptorellus races, but they are either activated or inactivated by substances under the control of another group of genes (Legner 1993  ).


Allowing natural selection for nonlethal undesirable and desirable characteristics to begin to act in the parental generation theoretically accelerates evolution in the Muscidifurax system. Traits, which are detrimental to the population, might thus be more prone to elimination and beneficial ones may be expressed in the mother before the appearance of her active progeny. If a similar genetic system occurs more generally in Hymenoptera, it might account partially for the rapid evolution thought to occur in certain groups of Hymenoptera. The ability of male Hymenoptera to activate heritable behavior in females with whom they mate has practical significance in biological control. Greater importance may be placed on liberated males during mass release strategies that seek to accelerate and increase the magnitude of parasitism, because it is possible to convey certain desirable strain characteristics directly to unmated females already resident in the environment. This subject will be treated in greater detail in a subsequent section on arrhenotoky.


            Studies with new field isolates of a Peruvian strain in 1995 by Richard Stouthamer et al. (unpublished) have shown a greater involvement of larval cannibalism and much complexity in this species' reproduction.  Indeed survival mechanisms in parasitoids include many behaviors; among which increased cannibalism by more aggressive larvae may be triggered during times of host scarcity. An account may be found in <aggress.htm>. [Please refer also to Related Research ]


Exercise 10.1. How may you distinguish behavior that is regulated by extranuclear factors from that regulated by genetic factors?

Exercise 10.2. Name the kinds of organisms that have been implicated in triggering extranuclear responses in animals.

Exercise 10.3. Could extranuclear factors be used to control behavior in insects?


REFERENCES:       [Additional references may be found at  MELVYL Library ]

Ayala, F. J. & J. A. Kiger, Jr. 1984. Modern Genetics, 2nd ed. The Benjamin/Cummings Publ. Co., Inc. Menlo Park, CA. 923 p.

Beale, G. & J. Knowles. 1978. Extranuclear Genetics. Edward Arnold, London. 142 p.

Bellows, T. S., Jr. & T. W. Fisher, (eds) 1999. Handbook of Biological Control: Principles and Applications. Academic Press, San Diego, CA. 1046 p.

Bownes, M. & L. Partridge. 1987. Transfer of molecules from ejaculate to females in Drosophila melanogaster and Drosophila pseudoobscura. J. Insect Physiol. 33: 941-47. Bull, J. J. 1983. Evolution of Sex Determining Mechanisms. The Benjamin/Cummings Publ. Co., Inc., Menlo Park, CA. 316 p.

Cosmides, L. M. & J. Tooby. 1981. Cytoplasmatic inheritance and intragenomic conflict. J. Theor. Biol. 89: 83-129.

Corbet, S. A. 1985. Insect chemosensory responses: a chemical legacy hypothesis. Ecol. Ent. 10: 143-53.

264.   Etzel, L. K. & E. F. Legner.  1999.  Culture and Colonization.  In:  T. W. Fisher & T. S. Bellows, Jr. (eds.), Chapter 15, p. 125-197, Handbook of Biological Control:  Principles and Applications.  Academic Press, San Diego, CA  1046 p.

Faulkner, B. M. & C. F. Arlett. 1964. The "minute" cytoplasmic variant of Aspergillus nidulans. Heredity 19: 63-73.

Fleming, J. G. W. & M. D. Summers. 1986. Campoletis sonorensis endoparasitic wasps contain forms of C. sonorensis virus DNA suggestive of integrated and extrachromosomal polydnavirus DNAs. J. Virol. 57: 552-62.

Goodenough, U. 1984. Genetics, 3d. ed. Saunders College Publ., Philadelphia/New York. 894 p.

Gordh, G. 1975. Some evolutionary trends in the Chalcidoidea (Hymenoptera) with particular reference to host preference. J. New York Ent. Soc. 83: 279-80.

Gordh, G. 1979. Catalog of Hymenoptera in America north of Mexico. Smithsonian Inst. Press, Vol. I, pp. 743-48.

Gwynne, D. T. 1984. Courtship feeding increases female reproductive success in bush crickets. Nature 307: 361-63.

Krell, P. J. & D. B. Stoltz. 1979. Unusual baculovirus of the parasitoid wasp Apanteles melanoscelus: isolation and preliminary characterization. J. Virol. 29: 1118-30.

228.   Legner, E. F.  1986.  Breeding superior parasitoids of Diptera using a novel extranuclear inheritance mechanism.  Proc. Calif. Mosq. & Vector Contr. Assoc., Inc. 44:  156-159.


233.   Legner, E. F.  1987.  Inheritance of gregarious and solitary oviposition in Muscidifurax raptorellus Kogan & Legner (Hymenoptera: Pteromalidae).  Canad. Entomol. 119(9):  791-808.


259.   Legner, E. F.  1993.  Theory for quantitative inheritance of behavior in a protelean parasitoid, Muscidifurax raptorellus (Hymenoptera: Pteromalidae).  European J. Ent. 90:  11-21.

Leslie, T. F. 1984. A "sex-ratio" condition in Oncopeltus fasciatus. J. Heredity 75: 260-64.

Levanthal, E. 1968. The sex ratio in Drosophila bifasciata; its experimental transmission. J. Inv. Path. 11: 170-83.

Levine, L. 1973. Biology of the Gene. The C.V. Mosby Co., St. Louis. 358 p.

Malogolowkin, C. 1959. Temperature effects on maternally inherited "sex-ratio" condition. Amer. Nat. 93: 365-68.

Mane, S. D., L. Tompkins & R. C. Richmond. 1983. Male esterase 6 catalyzes the synthesis of a sex pheromone in Drosophila melanogaster females. Science 222: 419-21.

Mudd, A. R., C. Fisher & M. C. Smith. 1982. Volatile hydrocarbons in the Dufour's gland of the parasite Nemeritis canescens (Grav.) (Hymenoptera: Ichneumonidae). J. Chem. Ecol. 8: 1035-42.

Oishi, K., D. F. Poulsen & D. L. Williamson. 1984. Virus-mediated change in clumping properties of Drosophila SR spiroplasmas. Curr. Microbiology 10: 153-58.

Poulson, D. F. & B. Sakaguchi. 1961. Nature of the "sex ratio" agent in Drosophila. Science 133: 1489-90.

Preer, J. R., L. B. Preer & A. Jurand. 1974. Kappa and other endosymbionts in Paramecium aurelia. Bact. Rev. 38: 113-63.

Richmond, R. C. & A. Senior. 1981. Esterase 6 (EC of Drosophila melanogaster: kinetics of transfer to females, decay in females and male recovery. J. Insect Physiol. 27: 849-54.

Sager, R. & Z. Ramanis. 1963. The particulate nature of nonchromosomal genes in Chlamydomonas. Proc. Nat. Acad. Sci. U. S. A. 50: 260-68.

Skinner, S. W. 1982. Maternally inherited sex ratio in the parasitoid wasp Nasonia vitripennis. Science 215: 1133-34.

Skinner, S. W. 1985. Son-killer: a third extrachromosomal factor affecting the sex-ratio. Genetics 109: 745-59.

Smith, J. R. & I. Rubenstein. 1973. The development of 'senescence' in Podospora anserina. J. Gen. Microbiol. 76: 283-96.

Sonneborn, T. M. 1959. Kappa and related particles in Paramecium. Adv. Virus Res. 6: 229-356.

Stanley-Samuelson, D. W. & W. Loher. 1986. Prostaglandins in insect reproduction. Ann. Ent. Soc. Amer. 79: 841-53.

Steele, R. H. 1986. Courtship feeding in Drosophila subobscura I. The nutritional significance of courtship feeding. Anim. Behav. 34: 1987-98.

Stoltz, D. B. & S. B. Vinson. 1977. Baculovirus-like particles in the reproductive tracts of female parasitoid wasp II: The genus Apanteles. Canad. J. Microbiol. 23: 28-37.

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Stoltz, D. B., S. B. Vinson & E. A. Mackinnon. 1976. Baculovirus-like particles in the reproductive tracts of female parasitoid wasps. Canad. J. Microbiol. 22: 1013-23.

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Stouthamer, R., J. A. J. Breeuwer, R. F. Luck & J. H. Werren. 1993. Molecular identification of microorganisms associated with parthenogenesis. Nature 361: 66-8.

2003.  Stouthamer, Richard,, Patrycja Strlppentow, Ingrld Langhout and E. Fred Legner.  2003.  Genetics of solitary and gregarious  emergence in the parasitoid wasp Muscidifurax raptorellus:  paternal modification of larval aggression. (in process)

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Vinson, S. B. & D. B. Stoltz. 1986. Cross-protection experiments with two parasitoid (Hymenoptera: Ichneumonidae) viruses. Ann. Ent. Soc. Amer. 79: 216-18.

Webster, R. P. & R. T. Carde. 1984. The effects of mating, exogenous juvenile hormone and a juvenile hormone analogue on pheromone titre, calling and oviposition in the omnivorous leafroller moth (Platynota stultana). J. Insect Physiol. 30: 113-18.

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