Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T19:07:43.121Z Has data issue: false hasContentIssue false
  • English
  • Français

Assuring paternity in a promiscuous world: are there lessons for ticks among the insects?

Published online by Cambridge University Press:  19 April 2005

W. R. KAUFMAN
W. R. KAUFMAN
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada, T6G 2E9
Get access Rights & Permissions [Opens in a new window]

Abstract

In this article I begin with a few current ideas on some physiological factors that influence mating choice in insects. Emphasis is placed on those proteins produced by the male reproductive accessory glands which increase female fecundity and reduce her receptivity to subsequent males. Strategies used by late-arriving males to favour their paternity are also mentioned. With a number of insect models as background, I then review what is currently known about several male factors in ticks (a capacitation factor, a male factor, an engorgement factor and a vitellogenesis stimulating factor) and suggest where we might focus our experimental activities in the future.

Keywords

Tick and insect reproductionfecundity enhancing substancesreceptivity inhibiting substancessperm competitionmale accessory gland proteinssperm precedence
Type
Research Article
Information
Parasitology , Volume 129 , Issue S1 , October 2004 , pp. S145 - S160
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ADLAKHA, V. & PILLAI, M. K. K. ( 1975). Involvement of male accessory gland substances in the fertility of mosquitoes. Journal of Insect Physiology 21, 1453–1455.CrossRefGoogle Scholar
AESCHLIMANN, A. A. & GRANDJEAN, O. ( 1973). Observations on fecundity in Ornithodoros moubata Murray (Ixodoidea: Argasidae). Relationships between mating and oviposition. Acarologia 15, 206–217.Google Scholar
ALJAMALI, M., BOWMAN, A. S., DILLWITH, J. W., TUCKER, J. S., YATES, G. W., ESSENBERG, R. C. & SAUER, J. R. ( 2002). Identity and synthesis of prostaglandins in the lone star tick, Amblyomma americanum (L.), as assayed by radio-immunoassay and gas chromatography/mass spectrometry. Insect Biochemistry and Molecular Biology 32, 331–341.Google Scholar
ANDERSON, R. B., SCRIMGEOUR, G. J. & KAUFMAN, W. R. ( 1998). Responses of the tick, Amblyomma hebraeum (Acari: Ixodidae), to carbon dioxide. Experimental and Applied Acarology 22, 667–681.CrossRefGoogle Scholar
AUSTAD, S. N. ( 1982). First male sperm priority in the bowl and doily spider, Frontinella pyramitela (Walckenaer). Evolution 36, 777–785.CrossRefGoogle Scholar
AUSTAD, S. N. ( 1984). Evolution of sperm priority patterns in spiders. In Sperm Competition and the Evolution of Animal Mating Systems (ed. Smith, R. L.), pp. 223–249. Orlando and San Diego, Academic Press.CrossRef
BIRKHEAD, T. R. ( 1998). Cryptic female choice: Criteria for establishing female sperm choice. Evolution 52, 1212–1218.CrossRefGoogle Scholar
BOROVSKY, D. ( 1985). The role of male accessory gland fluid in stimulating vitellogenesis in Aedes taeniorhynchus. Archives of Insect Biochemistry and Physiology 2, 405–413.CrossRefGoogle Scholar
BOWMAN, A. S., DILLWITH, J. W. & SAUER, J. R. ( 1996). Tick salivary prostaglandins: Presence, origin and significance. Parasitology Today 12, 388–396.CrossRefGoogle Scholar
BRENNER, R. R. & BERNASCONI, A. ( 1989). Prostaglandin biosynthesis in the gonads of the hematophagus insect Triatoma infestans. Comparative Biochemistry and Physiology 93B, 1–4.CrossRefGoogle Scholar
CHANG, E. S. & KAUFMAN, W. R. ( 2005). Endocrinology of Crustacea and Chelicerata. In Volume 3 (Endocrinology) Comprehensive Insect Science ( ed. Gilbert, L. I., Iatrou, K. & Gill, S. S.), Oxford, Elsevier, pp. 805–842.CrossRef
CHAPMAN, T., NEUBAUM, D. M., WOLFNER, M. F. & PARTRIDGE, L. ( 2000). The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster. Proceedings of the Royal Society of London B 267, 1097–1105.CrossRefGoogle Scholar
CHEN, P. S. & BÜHLER, R. ( 1970). Paragonial substance (sex peptide) and other free ninhydrin-positive components in male and female adults of Drosophila melanogaster. Journal of Insect Physiology 16, 615–627.CrossRefGoogle Scholar
CHEN, P. S., STUMM-ZOLLINGER, E., AIGAKI, T., BALMER, J., BIENZ, M. & BOHLEN, P. ( 1988). A male accessory gland peptide that regulates reproductive behaviour of female D. melanogaster. Cell 54, 291–298.Google Scholar
CONNAT, J.-L., DUCOMMUN, J., DIEHL, P.-A. & AESCHLIMANN, A. A. ( 1986). Some aspects of the control of the gonotrophic cycle in the tick, Ornithodoros moubata (Ixodoidea, Argasidae). In Morphology, Physiology and Behavioural Biology of Ticks (ed. Sauer, J. R. & Hair, J. A.), pp. 194–216. Chichester, UK, Ellis Horwood Publishers.
CRAIG, G. B. Jr. ( 1967). Mosquitoes: Female monogamy induced by male accessory gland substance. Science 156, 1499–1501.CrossRefGoogle Scholar
DAVEY, K. G. ( 1958). The migration of spermatozoa in the female of Rhodnius prolixus Ståhl. Journal of Experimental Biology 35, 694–701.Google Scholar
DAVEY, K. G. ( 1965). Copulation and egg production in Rhodnius prolixus: The role of the spermathecae. Journal of Experimental Biology 42, 373–378.Google Scholar
DAVEY, K. G. ( 1967). Some consequences of copulation in Rhodnius prolixus. Journal of Insect Physiology 13, 1629–1636.CrossRefGoogle Scholar
DESTEPHANO, D. B. & BRADY, U. E. ( 1977). Prostaglandin and prostaglandin synthetase in the cricket Acheta domesticus. Journal of Insect Physiology 23, 905–911.CrossRefGoogle Scholar
DESTEPHANO, D. B., BRADY, U. E. & FARR, C. A. ( 1982). Factors influencing oviposition behaviour in the cricket Acheta domesticus. Annals of the Entomological Society of America 75, 111–114.CrossRefGoogle Scholar
DESTEPHANO, D. B., BRADY, U. E. & LOVINS, R. E. ( 1974). Synthesis of prostaglandins by reproductive tissue of the house cricket, Acheta domesticus. Prostaglandins 6, 71–79.CrossRefGoogle Scholar
DIEHL, P. A., AESCHLIMANN, A. A. & OBENCHAIN, F. D. ( 1982). Tick Reproduction: Oogenesis and Oviposition. In Physiology of Ticks (ed. Obenchain, F. D. & Galun, R.), pp. 277–350. Oxford, Pergamon Press.CrossRef
DUCOMMUN, J. ( 1984). Contribution á la connaissance de la reproduction chez la tique Ornithodoros moubata, Murray, 1877; sensu Walton, 1962 (Ixodoidea: Argasidae). Thesis, University of Neuchâtel, Switzerland, 138 pp.
EBERHARD, W. G. ( 1998). Female roles in sperm competition. In Sperm Competition and Sexual Selection (ed. Birkhead, T. R. & Møller, A. P.), pp. 91–116. San Diego, Academic Press.CrossRef
ELGAR, M. A. ( 1998). Sperm competition and sexual selection in spiders and other arachnids. In Sperm Competition and Sexual Selection (ed. Birkhead, T. R. & Møller, A. P.), pp. 307–339. San Diego, Academic Press.CrossRef
EL SAID, A., SWIDERSKI, Z., AESCHLIMANN, A. & DIEHL, P. A. ( 1981). Fine structure of spermiogenesis in the tick Amblyomma hebraeum (Acari: Ixodidae): Late stages of differentiation and structure of the mature spermatozoon. Journal of Medical Entomology 18, 464–476.CrossRefGoogle Scholar
EL SHOURA, S. ( 1987). Fine structure of the vasa deferentia, seminal vesicle, ejaculatory duct and accessory gland of male Ornithodoros (Pavloskkyella) erraticus (Acari: Ixodoidea: Argasidae). Journal of Medical Entomology 24, 235–242.CrossRefGoogle Scholar
FELDMAN-MUHSAM, B. ( 1986). Observations on the mating behaviour of ticks. In Morphology, Physiology and Behavioural Biology of Ticks (ed. Sauer, J. R. & Hair, J. A.), pp. 217–232. Chichester, UK, Ellis Horwood Publishers.
FELDMAN-MUHSAM, B. ( 1991). The role of Adleorcystis sp. in the reproduction of argasid ticks. In The Acari: Reproduction, Development and Life-history Strategies (ed. Schuster, R. & Murphy, P. W.), pp. 179–190. London, Chapman & Hall.
FELDMAN-MUHSAM, B., BORUT, S., SALITERNIK-GIVANT, S. & EDEN, C. ( 1973). On the evacuation of sperm from the spermatophore of the tick Ornithodoros savignyi. Journal of Insect Physiology 19, 951–962.CrossRefGoogle Scholar
FINN, C. A. (Ed.) ( 1983). Oxford Reviews of Reproductive Biology, Vol. 5. Oxford, Clarendon Press.
FRIEDEL, T. & GILLOTT, C. ( 1977). Contribution of male-produced proteins to vitellogenesis in Melanoplus sanguinipes. Journal of Insect Physiology 23, 145–151.CrossRefGoogle Scholar
FRIESEN, K. & KAUFMAN, W. R. ( 2002). Quantification of vitellogenesis and its control by 20-hydroxyecdysone in the ixodid tick, Amblyomma hebraeum. Journal of Insect Physiology 48, 773–782.CrossRefGoogle Scholar
FUCHS, M. S., CRAIG, G. B. Jr. & HISS, E. A. ( 1968). The biochemical basis of female monogamy in mosquitoes. I. Extraction of the active principle from Aedes aegypti. Life Sciences 7, 835–839.CrossRefGoogle Scholar
GILLOTT, C. ( 1988). Arthropoda–Insecta. In Reproductive Biology of Invertebrates, Volume III, Accessory Sex Glands (ed. Adiyodi, K. G. & Adiyodi, R. G.), pp. 319–471. Chichester, New York, Brisbane, Toronto, Singapore, John Wiley & Sons.
GILLOTT, C. ( 1996). Male insect accessory glands: Functions and control of secretory activity. Invertebrate Reproduction and Development 30, 199–205.CrossRefGoogle Scholar
GILLOTT, C. ( 2003). Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annual Reveiw of Entomology 48, 163–184.CrossRefGoogle Scholar
GLADNEY, W. J. & DRUMMOND, R. O. ( 1971). Spermatophore transfer of lone star ticks off the host. Annals of the Entomological Society of America 64, 379–381.Google Scholar
GREGSON, J. D. ( 1944). The influence of fertility on the feeding rate of the female of the Wood Tick, Dermacentor andersoni Stiles. Entomological Society of Ontario 74, 46–47.Google Scholar
HARRIS, R. A. & KAUFMAN, W. R. ( 1981). Hormonal control of salivary gland degeneration in the ixodod tick Amblyomma hebraeum. Journal of Insect Physiology 27, 241–248.CrossRefGoogle Scholar
HARRIS, R. A. & KAUFMAN, W. R. ( 1984). Neural involvement in the control of salivary gland degeneration in the ixodid tick Amblyomma hebraeum. Journal of Experimental Biology 109, 281–290.Google Scholar
HARRIS, R. A. & KAUFMAN, W. R. ( 1985). Ecdysteroids: Possible candidates for the hormone which triggers salivary gland degeneration in the ixodid tick Amblyomma hebraeum. Experientia 41, 740–742.CrossRefGoogle Scholar
HARTMANN, R. & LOHER, W. ( 1996). Control mechanisms of the behavior ‘secondary defense’ in the grasshopper Gomphocerus rufus L. (Gomphocerinae: Orthoptera). Journal of Comparative Physiology A 178, 329–336.Google Scholar
HARTMANN, R. & LOHER, W. ( 1999). Post-mating effects in the grasshopper, Gomphocerus rufus L. mediated by the spermatheca. Journal of Comparative Physiology A 184, 325–332.CrossRefGoogle Scholar
HISS, E. A. & FUCHS, M. S. ( 1972). The effect of matrone on oviposition in the mosquito, Aedes aegypti. Journal of Insect Physiology 18, 2217–2225.CrossRefGoogle Scholar
HORROBIN, D. F. ( 1978). Prostaglandins: Physiology, Pharmacology and Clinical Significance. Montreal, Eden Press.
JOHNS, R., SONENSHINE, D. E. & HYNES, W. L. ( 1998). Control of bacterial infections in the hard tick, Dermacentor variabilis (Acari: Ixodidae): Evidence for the existence of antimicrobial proteins in tick hemolymph. Journal of Medical Entomology 35, 458–464.CrossRefGoogle Scholar
JOHNS, R., SONENSHINE, D. E. & HYNES, W. L. ( 2001). Identification of a defensin from the hemolymph of the American dog tick, Dermacentor variabilis. Insect Biochemistry and Molecular Biology 31, 857–865.CrossRefGoogle Scholar
KALB, J. M., DiBENEDETTO, A. J. & WOLFNER, M. F. ( 1993). Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proceedings of the National Academy of Sciences, USA 90, 8093–8097.CrossRefGoogle Scholar
KAUFMAN, W. R. ( 1976). The influence of various factors on fluid secretion by in vitro salivary glands of ixodid ticks. Journal of Experimental Biology 64, 727–742.Google Scholar
KAUFMAN, W. R. ( 1983). The function of tick salivary glands. Current Topics in Vector Research 1, 215–247.Google Scholar
KAUFMAN, W. R. ( 1991). Correlation between haemolymph ecdysteroid titre, salivary gland degeneration and ovarian development in the ixodid tick, Amblyomma hebraeum Koch. Journal of Insect Physiology 37, 95–99.CrossRefGoogle Scholar
KAUFMAN, W. R. ( 1997). Arthropoda–Chelicerata. In Reproductive Biology of Invertebrates ( series editors: Adiyodi, K. G. & Adiyodi, R.) Vol. 8, Part A, Progress in Reproductive Endocrinology (ed. Adams, T. S.), pp. 211–245. Oxford & IBH Publishing Co. Pvt. Ltd., New Delhi, India, and Wiley, NY.
KAUFMAN, S. E., KAUFMAN, W. R. & PHILLIPS, J. E. ( 1981). Fluid balance in the argasid tick, Ornithodorus moubata, fed on modified blood meals. Journal of Experimental Biology 93, 225–242.Google Scholar
KAUFMAN, S. E., KAUFMAN, W. R. & PHILLIPS, J. E. ( 1982). Mechanism and characteristics of coxal fluid execretion in the argasid tick Ornithodorus moubata. Journal of Experimental Biology 98, 343–352.Google Scholar
KAUFMAN, W. R. & LOMAS, L. O. ( 1996). ‘Male Factors’ in ticks: Their role in feeding and egg development. Invertebrate Reproduction and Development 30, 191–198.CrossRefGoogle Scholar
KEIRANS, J. E., CLIFFORD, C. M., HOOGSTRAAL, H. & EASTON, E. R. ( 1976). Discovery of Nuttalliella namaqua Bedford (Acarina: Ixodoidea: Nutalliellidae) in Tanzania and redescription of the female based on scanning electron microscopy. Annals of the Entomological Society of America 69, 926–932.CrossRefGoogle Scholar
KHALIL, G. M. ( 1970). Biochemical and physiological studies of certain ticks (Ixodoidea). Gonad development and gametogenesis in Hyolomma (H.) anatolicum excavatum Koch (Ixodidae). Journal of Parasitology 56, 596–610.Google Scholar
KIZEWSKI, A. E., MATUSCHKA, F.-R. & SPIELMAN, A. ( 2001). Mating strategies and spermiogenesis in ixodid ticks. Annual Review of Entomology 46, 167–182.CrossRefGoogle Scholar
KLOWDEN, M. J. ( 1999). The check is in the male: Male mosquitoes affect female physiology and behavior. Journal of the American Mosquito Control Association 15, 213–220.Google Scholar
KLOWDEN, M. J. ( 2001). Sexual receptivity in Anopheles gambiae mosquitoes: Absence of control by male accessory gland substances. Journal of Insect Physiology 47, 661–666.CrossRefGoogle Scholar
KLOWDEN, M. J. & CHAMBERS, G. M. ( 1991). Male accessory gland substances activate egg development in nutritionally stressed Aedes aegypti mosquitoes. Journal of Insect Physiology 37, 721–726.CrossRefGoogle Scholar
KRIGER, F. L. & DAVEY, K. G. ( 1982). Ovarian motility in mated Rhodnius prolixus requires an intact cerebral neurosecretory system. General and Comparative Endocrinology 48, 130–134.CrossRefGoogle Scholar
KRIGER, F. L. & DAVEY, K. G. ( 1983). Ovulation in Rhodnius prolixus Stål is induced by an extract of neurosecretory cells. Canadian Journal of Zoology 61, 684–686.CrossRefGoogle Scholar
KUSTER, J. E. & DAVEY, K. G. ( 1986). Mode of action of cerebral neurosecretory cells on the function of the spermatheca in Rhodnius prolixus. International Journal of Invertebrate Reproduction and Development 10, 59–69.CrossRefGoogle Scholar
LANGE, A. B. ( 1984). The transfer of prostaglandin-synthesizing activity during mating in Locusta migratoria. Insect Biochemistry 14, 551–556.CrossRefGoogle Scholar
LEAHY, M. G. & LOWE, M. L. ( 1967). Purification of the male factor increasing egg deposition in D. melanogaster. Life Sciences 6, 151–156.Google Scholar
LEES, A. D. & BEAMENT, J. W. L. ( 1948). An egg-waxing organ in ticks. Quarterly Journal of Microscopical Science 89, 291–232.Google Scholar
LOHER, W., GANJIAN, I., KUBO, I., STANLEY-SAMUELSON, D. & TOBE, S. S. ( 1981). Prostaglandins: Their role in egg-laying of the cricket Teleogryllus commodus. Proceedings of the National Academy of Sciences, USA 78, 7835–7838.CrossRefGoogle Scholar
LOMAS, L. O. & KAUFMAN, W. R. ( 1992 a). The influence of a factor from the male genital tract on salivary gland degeneration in the female ixodid tick Amblyomma hebraeum. Journal of Insect Physiology 38, 595–601.Google Scholar
LOMAS, L. O. & KAUFMAN, W. R. ( 1992 b). An indirect mechanism by which a protein from the male gonad hastens salivary gland degeneration in the female ixodid tick Amblyomma hebraeum. Archives of Insect Biochemistry and Physiology 21, 169–178.Google Scholar
LOMAS, L. O. & KAUFMAN, W. R. ( 1999). What is the meaning of ‘critical weight’ to female ixodid ticks?: A ‘grand unification theory’! In Acarology IX, Volume 2, Symposia ( ed. Needham, G. R., Mitchell, R., Horn, D. J. & Welbourn, W. C.), pp. 481–485. Columbus, Ohio, The Ohio Biological Survey.
LOMAS, L. O., TURNER, P. C. & REES, H. H. ( 1997). A novel neuropeptide–endocrine interaction controlling ecdysteroid production in ixodid ticks. Proceedings of the Royal Society of London B 264, 589–596.CrossRefGoogle Scholar
LUNG, O., KUO, M. F. & WOLFNER, M. F. ( 2001 a). Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochemistry and Molecular Biology 31, 543–551.Google Scholar
LUNG, O., KUO, M. F. & WOLFNER, M. F. ( 2001 b). Drosophila males transfer antibacterial proteins from their accessory gland and ejaculatory duct to their mates. Journal of Insect Physiology 47, 617–622.Google Scholar
LUNG, O., TRAM, U., FINNERTY, C. M., EIPPER-MAINS, M. A., KALB, J. M. & WOLFNER, M. F. ( 2002). The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression. Genetics 160, 211–224.Google Scholar
MAO, H. & KAUFMAN, W. R. ( 1999). Profile of the ecdysteroid hormone and its receptor in the salivary gland of the adult female tick, Amblyomma hebraeum. Insect Biochemistry and Molecular Biology 29, 33–42.CrossRefGoogle Scholar
MEDEIROS, M. N., OLIVEIRA, D. N. P., PAIVA-SILVA, G. O., SILVA-NETO, M. A. C., ROMEIRO, A., BOZZA, M., MASUDA, H. & MACHADO, E. A. ( 2002). The role of eicosanoids on Rhodnius heme-binding protein (RHBP) endocytosis by Rhodnius prolixus ovaries. Insect Biochemistry and Molecular Biology 32, 537–545.CrossRefGoogle Scholar
MORTIMER, D. ( 1983). Sperm transfer in the human female reproductive tract. In Oxford Reviews of Reproductive Biology, Vol. 5 (ed. Finn, C. A.), pp. 30–61. Oxford, Clarendon Press.
OLIVER, J. H. Jr., POUND, J. M. & ANDREWS, R. H. ( 1984). Induction of egg maturation and oviposition in the tick, Ornithodoros parkeri (Acari: Argasidae). Journal of Parasitology 70, 337–342.CrossRefGoogle Scholar
PAPPAS, P. J. & OLIVER, J. H. Jr. ( 1971). Mating necessary for complete feeding of female Dermacentor variabilis (Acari: Ixodidae). Journal of the Georgia Entomological Society 6, 122–124.Google Scholar
PAPPAS, P. J. & OLIVER, J. H. Jr. ( 1972). Reproduction in ticks (Acari:Ixodoidea). 2. Analysis of the stimulus for rapid and complete feeding of female Dermacentor variabilis (Say). Journal of Medical Entomology 9, 47–50.Google Scholar
PARKER, G. A. ( 1998). Sperm competition and the evolution of ejaculates: Towards a theory base. In Sperm Competition and Sexual Selection (ed. Birkhead, T. R. & Møller, A. P.), pp. 3–54. San Diego and London, Academic Press.CrossRef
POTTERAT, O., HOSTETTMANN, K., HÖLTZEL, A., JUNG, G., DIEHL, P. A. & PETRINI, O. ( 1997). Boophiline, an antimicrobial sterol amide from the cattle tick Boophilus microplus. Helvetica Chimica Acta 80, 2066–2072.CrossRefGoogle Scholar
POYSER, N. L. ( 1987) Prostaglandins and ovarian function. In Eicosanoids and Reproduction (ed. Hillier, K.), pp. 1–29. Lancaster, England, MTP Press Ltd.
RIDLEY, M. ( 1988). Mating frequency and fecundity in insects. Biological Reviews 63, 509–549.CrossRefGoogle Scholar
RUEGG, R. P., KRIGER, F. L., DAVEY, K. G. & STEEL, C. G. H. ( 1981). Ovarian ecdysone elicits release of a myotropic ovulation hormone in Rhodnius (Insecta: Hemiptera). International Journal of Invertebrate Reproduction 3, 357–361.CrossRefGoogle Scholar
SAHLI, R., GERMOND, J. E. & DIEHL, P. A. ( 1985). Ornithodoros moubata: Spermateleosis and secretory activity of the sperm. Experimental Parasitology 60, 383–395.CrossRefGoogle Scholar
SAUER, J. R., ESSENBERG, R. C. & BOWMAN, A. S. ( 2000). Salivary glands in ixodid ticks: Control and mechanism of secretion. Journal of Insect Physiology 46, 1069–1078.CrossRefGoogle Scholar
SCHÖL, H., SIEBERZ, J., GÖBEL, E. & GOTHE, R. ( 2001). Morphology and structural organization of Gené's organ in Dermacentor reticulatus (Acari: Ixodidae). Experimental and Applied Acarology 25, 327–352.CrossRefGoogle Scholar
SEIDELMANN, K. & FERENZ, H.-J. ( 2002). Courtship inhibition pheromone in desert locusts, Schistocerca gregaria. Journal of Insect Physiology 48, 991–996.CrossRefGoogle Scholar
SEVALA, V. L., SEVALA, V. M., DAVEY, K. G. & LOUGHTON, B. G. ( 1992). A FMRFamide-like peptide is associated with the myotropic ovulation hormone in Rhodnius prolixus. Archives of Insect Biochemistry and Physiology 20, 193–203.CrossRefGoogle Scholar
SHANBAKY, N. M., EL-SAID, A. & HELMY, N. ( 1990). Changes in neurosecretory cell activity in female Argas (Argas) hermanni (Acari: Argasidae). Journal of Medical Entomology 27, 975–981.CrossRefGoogle Scholar
SHEMESH, M., HADANI, A., SHKLAR, A., SHORE, L. S. & MELEGUIR, F. ( 1979). Prostaglandins in the salivary glands and reproductive organs of Hyalomma anatolicum excavatum Koch (Acari:Ixodidae). Bulletin of Entomological Research 69, 381–385.CrossRefGoogle Scholar
SHEPHERD, J., OLIVER, J. H. Jr. & HALL, J. D. ( 1982). A polypeptide from male accessory glands which triggers maturation of tick spermatozoa. International Journal of Invertebrate Reproduction 5, 129–137.CrossRefGoogle Scholar
SIMMONS, L. W. & SIVA-JOTHY, M. T. ( 1998). Sperm competition in insects: Mechanisms and the potential for selection. In Sperm Competition and Sexual Selection (ed. Birkhead, T. R. & Møller, A. P.), pp. 341–434. San Diego, Academic Press.CrossRef
SNOW, K. R. ( 1969). Egg maturation in Hyalomma anatolicum anatolicum Koch, 1844 (Ixodoidea, Ixodidae). In Proceedings of the 2nd International Congress of Acarology, 1967 ( ed. Owen Evans, G.), pp. 349–355. Budapest, Akademiai Kiodo.
SONENSHINE, D. E. ( 1967). Feeding time and oviposition of Dermacentor variabilis (Acarina: Ixodidae) as affected by delayed mating. Annals of the Entomological Society of America 60, 489–490.CrossRefGoogle Scholar
SONENSHINE, D. E. ( 1991). Biology of Ticks. Vol. 1, Oxford, Oxford University Press.
STERNBERG, S., PELEG, B. A. & GALUN, R. ( 1973). Effect of irradiation on mating competitiveness of the male tick, Argas persicus (Oken). Journal of Medical Entomology 10, 137–142.CrossRefGoogle Scholar
THOMAS, R. W. & ZEH, D. W. ( 1984). Sperm transfer and utilization strategies in arachnids: Ecological and morphological constraints. In Sperm Competition and the Evolution of Animal Mating Systems (ed. Smith, R. L.), pp. 179–221. Orlando, Academic Press.CrossRef
TRAM, U. & WOLFNER, M. F. ( 1999). Male seminal fluid proteins are essential for sperm storage in Drosophila melanogaster. Genetics 153, 837–844.Google Scholar
VAHED, K. ( 1998). The function of nuptial feeding in insects: A review of empirical studies. Biological Reviews 73, 43–78.CrossRefGoogle Scholar
VAN DER GOES VAN NATERS-YASUI, A., TAYLOR, D., SHONO, T. & YAMAKAWA, M. ( 2000). Purification and partial amino acid sequence of antibacterial peptides from the hemolymph of the soft tick, Ornithodoros moubata, (Acari: Argasidae). In Proceedings of the 3rd International Conference ‘Ticks and Tick-Borne Pathogens: Into the 21st Century’ (ed. Kazimirová, M., Labuda, M. & Nuttall, P. A.), pp. 189–194. Bratislava, Slovakia, Institute of Zoology, Slovak Academy of Sciences.
WAKAYAMA, E. J., DILLWITH, J. W. & BLOMQUIST, G. J. ( 1986). Occurrence and metabolism of prostaglandins in the housefly, Musca domestica (L.). Insect Biochemistry 16, 895–902.CrossRefGoogle Scholar
WANG, H., PAESEN, G. C., NUTTALL, P. A. & BARBOUR, A. G. ( 1998). Male ticks help their mates to feed. Nature 391, 753–754.CrossRefGoogle Scholar
WEISS, B. L. & KAUFMAN, W. R. ( 2001). The relationship between ‘critical weight’ and 20-hydroxyecdysone in the female ixodid tick, Amblyomma hebraeum. Journal of Insect Physiology 47, 1261–1267.CrossRefGoogle Scholar
WEISS, B. L. & KAUFMAN, W. R. ( 2004). Two feeding-induced proteins from the male gonad trigger engorgement of the female tick, Amblyomma hebraeum. Proceedings of the National Academy of Science, USA 101, 5874–5879.CrossRefGoogle Scholar
WEISS, B. L., STEPCZYNSKI, J. M., WONG, P. & KAUFMAN, W. R. ( 2002). Identification and characterization of genes differentially expressed in the testis/vas deferens of the fed male tick, Amblyomma hebraeum. Insect Biochemistry and Molecular Biology 32, 785–793.CrossRefGoogle Scholar
WOLFNER, M. F. ( 1997). Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochemistry and Molecular Biology 27, 179–192.CrossRefGoogle Scholar
WOLFNER, M. F. ( 2002). The gifts that keep on giving: Physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88, 85–93.CrossRefGoogle Scholar
WOLFNER, M. F., HARADA, H. A., BERTRAM, M. J., STELICK, T. J., KRAUS, K. W., KALB, J. M., LUNG, Y. O., NEUBAUM, D. M., PARK, M. & TRAM, U. ( 1997). New genes for male accessory gland proteins in Drosophila melanogaster. Insect Biochemistry and Molecular Biology 10, 825–834.CrossRefGoogle Scholar
YAMAJA SETTY, B. N. & RAMAIAH, T. R. ( 1979). Isolation and identification of prostaglandins from the reproductive organs of male silkmoth, Bombyx mori L. Insect Biochemistry 9, 613–617.CrossRefGoogle Scholar
YAMAJA SETTY, B. N. & RAMAIAH, T. R. ( 1980). Effect of prostaglandins and inhibitors of prostaglandin biosynthesis on oviposition in the silkmoth, Bombyx mori. Indian Journal of Experimental Biology 18, 539–541.Google Scholar
YUVAL, B. & SPIELMAN, A. ( 1990). Sperm precedence in the deer tick Ixodes dammini. Physiological Entomology 15, 123–128.CrossRefGoogle Scholar