The Biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). II. Duration of Biparental and Parthenogenetic Reproductive Abilities Author(s): B. W. Betz Source: Journal of the Kansas Entomological Society, Vol. 56, No. 3 (Jul., 1983), pp. 420-426 Published by: Allen Press on behalf of Kansas (Central States) Entomological Society Stable URL: http://www.jstor.org/stable/25084429 . Accessed: 21/06/2014 01:39 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact
[email protected]. . Kansas (Central States) Entomological Society and Allen Press are collaborating with JSTOR to digitize, preserve and extend access to Journal of the Kansas Entomological Society. http://www.jstor.org This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/action/showPublisher?publisherCode=acg http://www.jstor.org/action/showPublisher?publisherCode=kes http://www.jstor.org/stable/25084429?origin=JSTOR-pdf http://www.jstor.org/page/info/about/policies/terms.jsp http://www.jstor.org/page/info/about/policies/terms.jsp JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 56(3), 1983, pp. 420-426 The Biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). II. Duration of Biparental and Parthenogenetic Reproductive Abilities B. W. Betz 1000 North Lake Shore Drive, Chicago, Illinois 60611 abstract: Female receptivity to mating in Trichadenotecnum al exanderae Sommerman is found to be restricted to the period between an initial teneral state and the onset of oviposition. Females are only able to mate once. Unmated females are able to reproduce by partheno genesis (thelytoky), but mated females apparently never reproduce by parthenogenesis. Non-teneral males are able to mate at any time and are capable of mating repeatedly. Biparental reproduction in populations of T alexanderae may be promoted by the males' long survivorship, long duration of mating receptivity, and repeated mating ability. Other pro moting factors may include a sex-attractant pheromone produced by females and a patchy distribution of populations. A restriction of mating receptivity must be considered when tests for hybridization are used to determine the reproductive mode of females of a uniparental-biparental species complex. Trichadenotecnum alexanderae is a relatively common psocid in eastern United States (Betz, 1983a). The species inhabits trees and rock outcroppings providing its principal food source, pleurococcine algae. Formerly, T. alexanderae was con fused morphologically with three other species, all obligatorily parthenogenetic, which I have identified and described as T. castum, T. merum, and T. innuptum (Betz, 1983a). Trichadenotecnum alexanderae is a biparental species but is capable of facul tative parthenogenesis (thelytoky) (Betz, 1983a). The mode of reproduction through which females of T. alexanderae produce viable progeny is important in the population biology ofthe species. Females reproducing by parthenogenesis rather than by biparental reproduction lay fewer eggs which have an overall decreased fertility (Betz, unpubl. data). The ability to change to biparental reproduction after reproducing by parthenogenesis could increase the production of progeny. Facultative parthenogenesis can result in progeny when females remain un mated but also could contribute to the production of additional progeny if mated females deplete their supply of stored sperm. Such a depletion of stored sperm during the ovipositional stage apparently does occur in mated females oiPsoquilla marginepunctata (Hagen). Mated females of this species undergo a period of decreasing fecundity during the ovipositional stage, although the ovipositional rate during this period can be increased if females are allowed to mate again (Broadhead, 1961). In this paper I investigate the possibility of switching reproductive modes in females of T alexanderae. The results show that females are unable to change Accepted for publication 17 January 1983. This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp VOLUME 56, NUMBER 3 421 from parthenogenesis to biparental reproduction, or vice versa, once oviposition has begun. This paper is part of a series (cf. Betz, 1983b, c, d) presenting the life history of T. alexanderae. Aspects of the population biology of the species will be pre sented in future papers. Materials and Methods Specimens of T. alexanderae were obtained along the Sangamon River at Lake of the Woods, Champaign County, Illinois. They were collected from tree trunks with an aspirator and kept with pieces of bark in cotton-stoppered test tubes. Cultures were transported to the laboratory over ice-water in a cooler. Laboratory cultures were kept in cotton-stoppered test tubes. Each tube was supplied with food in the form of pleurococcine algae on bark. Culture tubes were stored in closed, glass desiccator jars over a saturated potassium chloride (KC1) solution to maintain a relative humidity of 80 ? 5%. The temperature regimen for rearing was 23.3?: 18.0?C light: dark, and the photoperiod was 15 h:9 h light: dark. Illumination was 4300 lumens/m2, supplied by incandescent and fluorescent lamps. Because the other species of the T alexanderae complex are obligatorily par thenogenetic and often occur sympatrically with the biparental species, I began a laboratory culture of T. alexanderae from the locality with females mated in the laboratory to assure the identity of the culture as the biparental species. Several breeding pairs were used to begin a culture, an attempt to represent the genetic diversity of the original field population. I also examined anatomical details of the original breeding pairs to verify that they were T. alexanderae. Only bark obtained from the original field locality was used in cultures; bark was examined for eggs before it was placed in a culture. Duration of mating accessibility in males and females of T. alexanderae was determined by the following procedure. Males and females from cultures were isolated as late stage nymphs and reared in four-dram shell vials containing one piece of bark each. At various times after molting to adult form, isolated males and females were brought together by the following method. The cotton stopper on each vial was removed, the open ends of pairs of vials were apposed, and the vials were tilted carefully until the piece of bark contained in one vial contacted the bark in the other. The open ends of pairs of vials were kept together until each observation was completed. Vials were not moved during observation of the insects. I examined the possibility that mated females were also able to reproduce by parthenogenesis. The kind of parthenogenesis in T alexanderae is thelytoky; only female progeny are produced. If mated females begin to produce some female progeny by parthenogenesis, then the sex ratio of the progeny should change to favor females. Female progeny produced by parthenogenesis would probably be most evident near the end of the parental females' lives, when their supply of stored sperm might become depleted and their mode of reproduction might change to parthenogenesis to continue the production of progeny. Mated females were isolated in shell vials when they were 12 days old, slightly older than the mean of female survivorship as adults (Betz, unpubl. data). Each female was transferred to a new vial daily, and the progeny from the ovipositions in each vial were reared to adulthood to determine their sex. This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp 422 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY Males Females teneral teneral adult adult mating ^- receptive - mating mating _ receptive ? mating occurs ? to mating * delayed occurs ** to mating -*- delayed (one . day) j_ unreceptive | to mating (age dependent) oviposition Fig. 1. Summary of the changes in mating ability of males and females of Trichadenotecnum alexanderae. Results duration of mating ability: Factors influencing the mating ability of males and females of T alexanderae are summarized in Fig. 1. Receptivity of females to males was related to their age and length of time prior to oviposition (Table 1). Female receptivity was restricted to a period of a few days after the teneral state and before the onset of oviposition. Females younger than two days old (as adults) never mated in these experiments. Males courted these young females only if older, receptive females were present (N = 5). Male courting behavior always caused young females to flee. Biparental females were teneral for 1.5-2.5 days. Most (95.5%) two-day-old fe males mated readily, but one which did not mate on the second day mated on the following day. Once females had mated, they never acquiesced to courting males (N = 7). While males sometimes disturbed a mating pair, they immediately lost interest in females that had mated. Males occasionally courted recently mated Table 1. Age-specific mating receptivity of virgin females (N = 60) to males (2-3 day adults) of Trichadenotecnum alexanderae. Age when females were tested Number of females (days after molting) tested : receptive % receptive 1 5:0 0 2 22:21 95.5 3 5:4 80 4 6:3 50 5 10:1 10 6 11:2 18.2 7 1:0 0 This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp VOLUME 56, NUMBER 3 423 Table 2. Daily numbers of male and female progeny produced by mated females of Trichadeno tecnum alexanderae up to death of parental females. Age of females (number of days after molting) Number of male and female progeny from mated females Female 1 Female 3 Female 4 Female 5 13 14 15 16 17 18 19 20 21 22 23 24 Total 1 1 6 3 1 3 0 1 1 2 2 4 3 1 0 0 2 3 0 1 3 4 0 0 0 1 13 16 8 10 13 22 0 3 2 4 2 4 9 1 8 4 3 5 45 1 5 3 3 1 2 8 3 5 3 3 3 40 1 1 1 2 3 1 6 0 2 1 0 3 21 0 5 2 3 5 1 6 2 2 0 0 1 27 females if they occurred with receptive females (N = 3). However, mated females always fled. Receptivity of females increased as the teneral state was lost. A daily decline in receptivity later followed in females that had not mated or oviposited, except in the six-day age cohort (Table 1). A chi-square test was performed on the data in Table 1. The results of the mating tests for the age one-day females were not included in the analysis because the mating ability of the one-day and the two-day females was significantly dif ferent (x2 = 5.05, d.f. = 1, P < 0.05), indicating that the younger females were teneral. The relative number of females that were receptive to mating differed significantly among the age two- through seven-day cohorts (x2 = 18.21, d.f. = 5, P < 0.01); the daily decline in mating receptivity was related to the age of the females. Most of the females failing to mate in the experiments began ovipositing within a few days after the test. The female that did not oviposit died prematurely. Females became gravid about two days after attaining adult form. Gravidity increased in the next few days of adulthood, and unmated females eventually laid eggs. Isolated females that had oviposited or were extremely gravid no longer elicited a courting response from introduced males. If receptive females were present in a culture vial with gravid or ovipositional females, males often at tempted to court both. Usually the gravid females ran away; females which had oviposited always fled. Only three (12.0%) unmated, gravid females acquiesced when courted, but the distention of their abdomens prevented the courting males from establishing genitalic contact. Successful mating was not observed in these females after the first attempt failed. The female of one of the pairs consented to another mounting attempt, but this also was unsuccessful. In one pair, the female fled when the male courted again, and in another pair, the male no longer courted. The duration of mating ability in males of T. alexanderae contrasts with the This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp 424 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY short period of receptivity in females. Most males were able to mate about 1.5 days after molting, and all were able to mate after two days (N = 15). Males were thus able to mate at a slightly earlier age after molting than females. After the initial teneral period, adult males were able to mate at any time. The refractory period between matings appeared to be about one day, so males could potentially have mated once daily after the first day of adulthood. ABSENCE OF PARTHENOGENETIC REPRODUCTION IN MATED FEMALES! Table 2 pre sents the number of male and female progeny produced daily by isolated, mated females of T. alexanderae (N = 7). Sex ratios of progeny from these females indicated that the relative number of female progeny produced by each parental female did not differ significantly among parents (x2 = 2.45, d.f. = 6, P < 0.10). Male progeny were produced by the mated females over the entire period of observation. Chi-square tests on the relative daily numbers of female progeny for each parental female, excluding the days in which progeny were not produced, show that no significant changes occurred (at P < 0.10) in the sex ratios of progeny over the life of an individual female. Mated females were probably not reproducing by parthenogenesis during the period of observation, although it would not be possible to detect an occasional female offspring produced by parthenogenesis. Discussion The cessation of mating receptivity is related to the onset of oviposition in females of T. alexanderae. Between these two events, females apparently change from a biparental to a parthenogenetic type of reproduction. The mechanism of reproduction accounting for this switch is unknown but the change appears to be permanent during the lives of females. Because of the short duration of female receptivity, and the reduction of the number and fertility of eggs in females reproducing by parthenogenesis, biparental reproduction is probably being promoted in some way in populations of the species. Factors that may be important in facilitating biparental reproduction are the long period of males' receptivity and their ability to mate repeatedly. Also, males have an adult survivorship significantly longer than that of females, allowing them to mate with the next non-overlapping female generation; such matings have been effected experimentally (Betz, unpubl. data). Receptive females apparently produce a sex-attractant pheromone, although it only elicits responses in males within about 1 cm of females (Betz, 1983c). Additionally, populations of T. alexanderae are highly localized within suitable localities, possibly resulting from uneven distribution of food, microhabitat, and/or lack of dispersal (Betz, 1983b). Encounters among individuals in a population may increase when the microhab itat is patchy, although dispersal in T. alexanderae may be somewhat limited even on individual trees (Betz, 1983b). Because reproduction in T. alexanderae is facultatively parthenogenetic, the restricted mating ability of this species may not be representative of other species of Psocoptera. Females of some psocid species are capable of mating more than once (Schneider, 1955; Sommerman, 1956;Broadhead, 1961), yet females of other species (cf. Mockford, 1957) are apparently limited to only one mating, as in T alexanderae. The ability of females to mate repeatedly may be important in certain species reproducing biparentally more or less exclusively (as Psoquilla margine punctata apparently does) because maximum fecundity may be maintained in This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp VOLUME 56, NUMBER 3 425 females throughout the ovipositional stage. Also, the onset of oviposition does not affect the mating ability of females of some species (Sommerman, 1943; Broadhead, 1961). However, Eertmoed (1966) noted that a female from a bipa rental population oiPeripsocus quadrifasciatus (Harris) was receptive to a courting male, although she had laid four eggs, but that she repeatedly disrupted his at tempts to copulate. Such courtship activity in an ovipositional female is similar to behavior in T. alexanderae. Many species of Psocoptera consist of some populations with males, apparently reproducing biparentally, and other populations consisting entirely of females, which appear to be uniparental species (Pearman, 1928; Badonnel, 1951; Broad head, 1954; Schneider, 1955; Mockford, 1971; Betz, 1983a). Understanding gene flow relationships between all-female populations and those containing males within species complexes, such as the T alexanderae complex, is expedited by tests for hybridization. However, the brief period of receptivity in T. alexanderae suggests that demonstrating a female's reproductive type requires more than sim ply noting whether mating occurs. If females' receptivity to males is narrowly restricted to the period between teneral and gravid stages, then selecting females for a test for hybridization without knowing the timing of the period of receptivity could cause misinterpretation of the results. Females of biparental populations not responding in such a test would be considered to be reproductively isolated, when, in fact, they might merely have been non-receptive. In most studies of the reproductive biology of Psocoptera the sexes have been brought together without knowledge of the reproductive condition of the insects. Some previous studies may have falsely interpreted the absence of mating in such pairings as evidence of reproductive isolation. Acknowledgments Dr. E. L. Mockford of Illinois State University, P. R. Vilaro, and two anonymous reviewers supplied helpful comments about the manuscript. Production assistance was provided by I. N. Holod and typing by D. D. Pierce. Literature Cited Badonnel, A. 1951. Ordre des Psocopt?res. In P.-P. Grasse (ed.), Trait? de Zoologie, Vol. 10, Fase. 2, pp. 1301-1340. Masson et Cie., Paris. Betz, B. W. 1983a. Systematics of the Trichadenotecnum alexanderae species complex (Psocoptera: Psocidae) based on an investigation of reproductive modes and morphology. Can. Entomol. (In press.) -. 1983b. The biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). I. Habitat, life stages and events. Entomol. News. (In press.) -. 1983c. The biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). III. Analysis of mating behavior. Psyche. (In press.) -. 1983d. The biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). IV. Mechanism of genitalic coupling. J. Kansas Entomol. Soc. 56:427-433. Broadhead, E. 1954. A new parthenogenetic psocid from stored products, with observations on parthenogenesis in other psocids. Entomol. Mon. Mag. 90:10-16. -. 1961. The biology of Psoquilla marginepunctata (Hagen) (Corrodentia, Trogiidae). Trans. Soc. Brit. Ent. 14:223-236. Eertmoed, G. E. 1966. The life history of Peripsocus quadrifasciatus (Psocoptera: Peripsocidae). J. Kansas Entomol. Soc. 39:54-65. Mockford, E. L. 1957. Life history studies on some Florida insects of the genus Archipsocus (Pso coptera). Bull. Fla. State Mus., Biol. Sei. 1:253-274. This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp 426 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY -. 1971. Parthenogenesis in psocids (Insecta: Psocoptera). Amer. Zool. 11:327-339. Pearman, J. V. 1928. Biological observations on British Psocoptera. III. Sex behavior. IV. Miscel laneous. Entomol. Mon. Mag. 64:263-268. Schneider, H. 1955. Vergleichende Untersuchungen ?ber Parth?nogen?se und Entwicklungsrhythmen bei einheimischen Psocopteren. Biol. Zentr. 74:273-310. Sommerman, K. M. 1943. Bionomics of Lachesilla nubilis (Aaron) (Corrodentia, Caeciliidae). Can. Entomol. 75:99-105. -. 1956. Two new species of Rhyopsocus (Psocoptera) from the U.S.A., with notes on the bionomics of one household species. J. Wash. Acad. Sei. 46:145-149. This content downloaded from 195.78.109.54 on Sat, 21 Jun 2014 01:39:57 AM All use subject to JSTOR Terms and Conditions http://www.jstor.org/page/info/about/policies/terms.jsp Article Contents p. [420] p. 421 p. 422 p. 423 p. 424 p. 425 p. 426 Issue Table of Contents Journal of the Kansas Entomological Society, Vol. 56, No. 3 (Jul., 1983), pp. 261-456 Front Matter Hessian Fly (Diptera: Cecidomyiidae) in Washington: Distribution, Parasites, and Intensity of Infestations on Irrigated and Nonirrigated Wheat [pp. 261-266] Selenium in Seeds of Astragalus (Leguminosae) and Its Effects on Host Preferences of Bruchid Beetles [pp. 267-272] Seasonal Incidence of Nomuraea rileyi (Farlow) Samson in Larval Populations of Heliothis spp. (Lepidoptera: Noctuidae) in Southeastern Arkansas, 1973-1980 [pp. 273-276] The Relation of Recruitment Rate to Activity Rhythms in the Harvester Ant, Pogonomyrmex barbatus (F. Smith) (Hymenoptera: Formicidae) [pp. 277-285] A New Species of Potamobates from Peru (Hemiptera-Heteroptera: Gerridae) [pp. 286-288] Hemocyte Counts in Susceptible and Resistant Noctuid Larvae Injected with Blastospores of Nomuraea rileyi [pp. 289-296] Recovery of Tetrastichus gallerucae (Hymenoptera: Eulophidae), an Introduced Egg Parasitoid of the Elm Leaf Beetle (Pyrrhalta luteola) (Coleoptera: Chrysomelidae) [pp. 297-298] Chorusing Centers of Periodical Cicadas [pp. 299-304] Biology of Caliroa quercuscoccineae (Dyar) (Hymenoptera: Tenthredinidae) in Central Kentucky I. Observations on the Taxonomy of Principal Life Stages [pp. 305-314] Descriptions of Three New Species of Labocurtidia with a Revised Key to the Species (Cicadellidae: Coelidiinae: Teruliini) [pp. 315-319] Soybean and Mite Interaction: Effects of Cultivar and Plant Growth Stage [pp. 320-326] Nest and Colony Characteristics of Stingless Bees from Panamá (Hymenoptera: Apidae) [pp. 327-355] Studies of Mississippi Fishflies (Megaloptera: Corydalidae: Chauliodinae) [pp. 356-364] New Neotropical Species of Teruliine Leafhoppers (Cicadellidae: Coelidiinae: Teruliini) [pp. 365-370] Descriptions of Two New Species of Perulidia with a Revised Key to the Species (Cicadellidae: Coelidiinae: Teruliini) [pp. 371-374] A New Species of Crepluvia with a Revised Key to the Species (Cicadellidae: Coelidiinae: Teruliini) [pp. 375-376] Morphology of the Male and Female Reproductive Systems of Plathypena scabra (F.) (Lepidoptera: Noctuidae) [pp. 377-386] Correlation of Season and Dominance Status with Activity of Exocrine Glands in Polistes fuscatus (Hymenoptera: Vespidae) [pp. 387-397] The Tallaperla maria Complex of Eastern North America (Plecoptera: Peltoperlidae) [pp. 398-410] The Nymph of Bolotoperla rossi (Frison) (Plecoptera: Taeniopterygidae: Brachypterinae) [pp. 411-414] The Nymph of Somatochlora ensigera (Odonata: Corduliidae) [pp. 415-419] The Biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). II. Duration of Biparental and Parthenogenetic Reproductive Abilities [pp. 420-426] The Biology of Trichadenotecnum alexanderae Sommerman (Psocoptera: Psocidae). IV. Mechanism of Genitalic Coupling [pp. 427-433] Facultative Production of Alates by Greenbug and Corn Leaf Aphid, and Implications in Aphid Population Dynamics (Homoptera: Aphididae) [pp. 434-440] Identity and Classification of Physetopoda, Chaetotilla and Paramyrme (Hymenoptera: Mutillidae) [pp. 441-445] Feeding Tests of Nabis roseipennis (Hemiptera: Nabidae) on Potato Leafhopper, Empoasca fabae (Homoptera: Cicadellidae), and Their Movement into Spring-Planted Alfalfa [pp. 446-450] Fifty-Ninth Annual Meeting, Central States (Kansas) Entomological Society, Columbia, Missouri, 23 April 1983 Simultaneous Functional Responses to Three Prey Species by a Wolf Spider Population [p. 451-451] The Integration of Herbicides and Rhinocyllus conicus Froel. for Musk Thistle Control [pp. 451-452] Comments on Some Morphological Characters of Nymphal Planthoppers (Homoptera: Fulgoroidea) [p. 452-452] Gall-Forming Stages of the Stem Phylloxera, Phylloxera devastatrix Pergande, on Kansas Pecan Trees, with Notes on New State Records of Phylloxeran Species Distribution [pp. 452-453] Evaluation of an Improved Wireworm Sampling Method [p. 453-453] IPM NEWS, a Computerized Information System for Pest Management [pp. 453-454] Pheromones in Cockroach Control [p. 454-454] Natural Enemies of the Stable Fly, Stomoxys calcitrans (L.), and Their Impact in Missouri [pp. 454-456] Back Matter