Female Monopolization and Paternity Assurance in South American Crickets (Orthoptera, Grylloidea): Mating Plugs, Extra Claspers and Forced Copulation
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Volume 47(20):245-257, 2007 Female monopolization and paternity assurance in South American crickets (Orthoptera, Grylloidea): mating plugs, extra claspers and forced copulation Francisco de A.G. de Mello1 ABSTRACT This paper describes the first three cases in which male crickets monopolize females by means of mating plugs. The origin of the plugs vary among the cases (i.e., they are not homologous). Female monogamy is assured by the permanent presence of the plug attached to their genitalia after first mating, while males are potentially polygamous. The presence of an additional clasping structure and the occurrence of forced copulation are also described. Key-words: Crickets, Grylloidea, Mate monopolization, Mating plug, Mating system Paternity assurance, Rape behavior, Forced copulation, Rape. INTRODUCTioN surface with citral from his mandibular glands during copulation. That supposedly makes her smell like a A brief account on male insect and arachnid male, since the same substance is used by males to ploys to sexually monopolize females mark the vegetation of their territory (Frankie et al., 1980). Male animals of many taxonomical groups show Some female insects become sexually unrecep- adaptations that avoid or reduce the chances that sper- tive for at least a certain period after copulation. matozoa from rival males succeed in fertilizing the ova That is, for instance, what occurs with the dipter- of females with whom they copulate. These paternity- ans Aedes aegypti (Craig, 1967), Musca domestica directed strategies may have chemical, behavioral, or (Riemann et al., 1967; Riemann & Thorson, 1969), structural natures. Drosophila melanogaster (Burnett et al., 1973), D. fu- Male beetles of the genus Tenebrio mark females, nebris (Baumann, 1974a, b) and Hylemya brassicae during copulation, with an anti-aphrodisiacal phero- (Swailes, 1971). In most of the cases, loss of female mone which is transferred via genital apparatus; that sexual receptivity is promoted by stimuli caused by substance acts by repelling other males (Happ, 1969). secretions from the male’s accessory glands which are Gilbert (1976) describes a parallel case in the butter- transferred to the female during insemination (Leop- fly Heliconius erato but there special structures have old, 1976; Gillott & Friedel, 1977), but in Drosoph- evolved for the transfer and spread of the pheromone. ila, mating inhibition is thought to be accomplished Males of the bee Centris adani mark the female body mainly by the presence of sperm in the spermathe- 1. Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de Botucatu, 18618-000, Botucatu, São Paulo, Brasil. E-mail: [email protected] 246 Mello, F. de A.G. de: Female Reproductive Monopolization by Male Crickets cae (Burnett et al., 1973; Manning, 1967; Merle, tain period of time. Male hymenopterans like those 1968). of the honey bee, Apis mellifera, and of harvester ants Behavioral means by which males can reduce the of the genus Pogonomyrmex plug the female genitalia chances for a female to re-mate with a rival include with a portion of their bodies, more specifically with such maneuvers as: concealment of the partner or the copulatory apparatus that is lost upon the end of potential partner from competitors; reduction of the copulation. In these cases the wound causes them to conspicuousness of courtship displays; exhibition of die after having mated (Alcock, 1989; Hölldobler, some kind of female guarding (i.e., with or without 1976; Markl et al., 1977; Michener, 1974; Thornhill body contact), among other strategies (Thornhill & & Alcock, 1983). The minute male of the ceratopogo- Alcock, 1983). nid Johannseniella nitida blocks the female’s genitalia Several species of Drosophila exhibit what is by introducing himself inside of it (Downes, 1978; called the “insemination reaction”. This phenom- Goetghebuer, 1914). enon is an enlargement of the vagina produced by Honey bee drones also transfer glandular secre- the male’s ejaculate (Patterson, 1946) which, in intra- tions (mucopolysaccharides) that coagulate within the specific matings, appears to prevent the female from female and block her genitalia (Blum et al., 1962). re-mating for a certain period and thus securing him Similar cases were reported by Boldyrev (1913) for paternity of offspring (Patterson, 1947). Alonso- locusts. Leopold (1976) mentions that secretion- Pimentel et al. (1994) have argued that, in Drosophila, derived plugs are produced by accessory glands, such more than one type of phenomena have been consid- types of plugs have been found in a number of ani- ered under the name of insemination reaction and, mals other than insects. by judging Patterson’s original concept too simplistic, The spermatophore itself may constitute the they defined the “true insemination reaction” as “a mating plug once it is inside the female’s genital duct, mass of one amorphous material that greatly distends which is the case of the grasshopper Locusta migrato- the vagina of recently mated females”. ria. That species produces a very long and coiled sper- Some male insects are able to, during sexual con- matophore which remains inside the female’s sperma- tact, displace the sperm of other males which is stored theca (Gregory, 1965). Landa (1960) reports a similar inside the female’s spermathecae or bursa copulatrix case in a melolonthid beetle. and, in certain damselflies, the sperm of a precedent Males of certain spiders leave the distal portion male is removed from the female’s storage organ by of the pedipalpal embolus inside the epigynum after means of the penis (Waage, 1979, 1984). In species sperm transfer (Abalos & Baez, 1963; Bonnet, 1930; where spermatozoa of the last male to copulate are Levi, 1969; Levi, 1975), while others cover the epigy- more likely to fertilize a larger amount of eggs, sperm num with membranous scales derived from the palps from precedent males may be packed deeper into the (Jackson, 1980; Levi, 1972; Robinson, 1982). female’s spermatheca by the penis of subsequent ones. That is the case with the dragonfly Sympetrum rubi- cundilum (Waage, 1984). Mating plugs in crickets Alonso-Pimentel et al. (1994) define the term sperm sac as “structures with distinctive materials that Female monopolization mediated by mating stay soft inside the female’s vagina and do not cause plugs has never been reported from Grylloidea. In inordinate distention of the vaginal pouch”. Accord- fact, anyone familiar with male and female cricket ing to those authors, sperm sacs contain a great quan- genital morphology and the way they function during tity of sperm and become cohesive units in contact sperm transfer would probably have trouble trying to with the air; the cohesion of sperm sacs as compact figure out how a plug system could be possible for units could be explained by the presence of a gela- this group of insects. Since cricket phallic complexes tin-like substance. This type of structure was reported are not intromittent nor are the spermatophore bodies from Drosophila mettlery, D. nigrospiracula and D. me- transferred to the internal tract of the female genitalia lanogaster; females of all three species discard the sacs during copulation, a mating plug system for crickets within 24h after mating. can hardly be imagined. In these insects, the sper- Mating plugs, or copulatory plugs, are male-pro- matophore ampulla is always kept outside the female duced substances or structures which are transferred to body during sperm transfer and it will be removed by the female upon copulation and promote the sealing the male or female, depending on the case, as soon as of her genital opening which will, ultimately, prevent the transfer is accomplished- for details see Alexander her from copulating with other males for at least a cer- & Otte (1967). Papéis Avulsos de Zoologia, 47(20), 2007 247 Although male genitalia does have clasping The terminology for the phallic elements structures that will hold female’s copulatory papilla employed here is that of Desutter (1990) with the cor- on position for spermatophore attachment, the con- rections that author proposed on a subsequent paper tact between spermatophore and copulatory papilla is (Desutter-Grandcolas, 2003). always pinpointed and rather brief. The only contact Additional information on methodology, when of the two structures occurs between the neck of the applicable, is given along the text under each case. spermatophore and the opening of the papilla and that lasts only the time necessary for sperm transfer, normally a matter of minutes. In some cases, the male RESULTS will hold the female on position during insemina- tion and afterwards he will remove and eat the empty The case of Adenophallusia naiguatana spermatophore; in other ones he will just attach the (Eneopteridae, Tafaliscinae) spermatophore to her copulatory papilla by means of an specialized structure named “attachment plate” Adenophallusia naiguatana is a Venezuelan and let her go, carrying the structure on the outside cricket belonging to a so far monotypic genus (Mello of her body; after completion of sperm transfer she & Camargo e Mello, 1996). will remove and eat the empty capsule (Alexander & The pseudepiphallus of that species contains a Otte, op. cit.). pair of sac-shaped glandular structures, each of them People interested in the diversity of cricket with an external opening located distally, on the infe- reproductive strategies should check Zuk & Simmons rior face of the