Insect sperm motility

Biological Reviews

Volumn 83, Issue 2, 2008, Pages 191-208

  Werner, Michael ^a   Simmons, Leigh W ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Bidirectional swimming; Double helical movement; Energy metabolism; Insect sperm structure; Low Reynolds number; Seminal fluids; Sperm activation

Indexed keywords

CELL STRUCTURE; FERTILIZATION; INSECT; NONHUMAN; REVIEW; SEXUAL SELECTION; SPERM COMPETITION; SPERMATOZOON MOTILITY;

ANIMALS; INSECTS; MALE; REPRODUCTION; SELECTION (GENETICS); SPERM COUNT; SPERM MOTILITY; SPERM TAIL; SPERMATOZOA;

HEXAPODA;

EID: 42649092892     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/j.1469-185X.2008.00039.x     Document Type: Review

References (182)

1. Afzelius, B. A 1959). Electron microscopy of the sperm tail. Results obtained with a new fixative. Journal of Biophysical and Biochemical Cytology 5, 269 278.
2. Aigaki, T., Kasuga, H. Osanai, M 1987). A specific endopeptidase, BAEE esterase, in the glandula prostatica of the male reproductive system of the silkworm, Bombyx mori. Insect Biochemistry 17, 323 328.
3. Ainsworth, C 2005). The secret life of sperm. Nature 436, 770 771.
4. Alavi, S. M. H. Cosson, J 2005). Sperm motility in fishes. I. Effects of temperature and pH: a review. Cell Biology International 29, 101 110.
5. Anderson, M. J. Dixson, A. F 2002). Motility and the mid-piece. Nature 416, 496.
6. Anderson, W. A. Personne, P 1970). Recent cytochemical studies on spermatozoa of some invertebrate and vertebrate species. In Comparative Spermatology (ed. B. Baccetti pp. 432 449. Accademia Nazionale dei Lincei, Rome.
7. Baccetti, B 1972). Insect sperm cells. Advances in Insect Physiology 9, 315 397.
8. Baccetti, B. Afzelius, B. A 1976). The Biology of the Sperm Cell. S. Karger, Basel.
9. Baccetti, B., Bernini, F., Bigliardi, E., Burrini, A. G., Dallai, R., Giusti, F., Mazzini, M., Pallini, V., Renieri, T., Rosati, F., Selmi, G. Vegni, M 1975). Motility patterns in sperms with different tail structure. In The Functional Anatomy of the Spermatozoon, vol. 23. Wenner-Gren Center International Symposium Series (ed. B. A. Afzelius pp. 141 150. Pergamon Press, Oxford, New York, Toronto, Sydney.
10. Baccetti, B., Burrini, A. G., Dallai, R., Giusti, F., Mazzini, M., Renieri, T., Rosati, F. Selmi, G 1973a). Structure and function in the spermatozoon of Tenebrio molitor (The Spermatozoon of Arthropoda. XX). Journal of Mechanochemistry and Cell Motility 2, 149 161.
11. Baccetti, B., Burrini, A. G., Dallai, R., Pallini, V 1982). A motile system of singlet microtubules in spermatozoa. Cell Motility 2, 93 101.
12. Baccetti, B., Burrini, A. G., Dallai, R., Pallini, V., Periti, P., Piantelli, F., Rosati, F. Selmi, G 1973b). Structure and function in the spermatozoon of Bacillus rossius - The Spermatozoon of Arthropoda XIX. Journal of Ultrastructure Research 44, 1 73.
13. Baccetti, B. Dallai, R 1976). The Spermatozoon of Arthropoda. XXVII. Uncommon axoneme patterns in different species of the cecidomyid flies. Journal of Ultrastructure Research 55, 50 69.
14. Baccetti, B., Dallai, R., Pallini, V., Rosati, F. Afzelius, B. A 1977). Protein of insect sperm mitochondrial crystals - Crystallomitin. Journal of Cell Biology 73, 594 600.
15. Baccetti, B., Dallai, R. Rosati, F 1970). The spermatozoon of Arthropoda VII. Plecoptera and Trichoptera. Journal of Ultrastructure Research 31, 212 228.
16. Baccetti, B., Gibbons, B. H. Gibbons, I. R 1989). Bidirectional swimming in spermatozoa of tephritid flies. Journal of Submicroscopic Cytology and Pathology 21, 619 626.
17. Baer, B., Schmid-Hempel, P., Hoeg, J. T. Boomsma, J. J 2003). Sperm length, sperm storage and mating system characteristics in bumblebees. Insectes Sociaux 50, 101 108.
18. Ball, M. A. Parker, G. A 1997). Sperm competition games: inter and intra species results of a continuous external fertilization model. Journal of theoretical Biology 186, 459 466.
19. Ball, M. A. Parker, G. A 1998). Sperm-competition games: energy dependence and competitor numbers in the continuous-external-fertilization model. Mathematical Medicine and Biology 15, 87 96.
20. Báo, S. N., Lins, U., Farina, M. de Souza, W 1992). Mitochondrial derivatives of Culex quinquefasciatus (Culicidae) spermatozoon: Some new aspects evidenced by cytochemistry and image processing. Journal of Structural Biology 109, 46 51.
21. Bigliardi, E., Baccetti, B., Burrini, A. G. Pallini, V 1970). The spermatozoon of Arthropoda. XII. The distribution of some enzymes in the insect sperm tail. In Comparative Spermatology (ed. B. Baccetti pp. 451 463. Accademia Nazionale dei Lincei, Rome.
22. Birkhead, T. R., Martinez, J. G., Burke, T. Froman D. P 1999). Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proceedings of the Royal Society of London - Series B: Biological Sciences 266, 1759 1764.
23. Bloch Qazi, M. C., Aprille, J. R. Lewis, S 1998). Female role in sperm storage in the red flour beetle, Tribolium castaneum. Comparative Biochemistry and Physiology Part A 120, 641 647.
24. Blum, M. S., Glowska, Z. Taber, S., III. 1962). Chemistry of the drone honey bee reproductive system. II. Carbohydrates in the reproductive organs and semen. Annals of the Entomological Society of America 55, 135 139.
25. Bressac, C., Fleury, A. Lachaise, D 1994). Another way of being anisogamous in Drosophila subgenus species: Giant sperm, one-to-one gamete ratio, and high zygote provisioning. Proceedings of the National Academy of Sciences of the United States of America 91, 10399 10402.
26. Bressac, C., Joly, D., Devaux, J., Serres, C., Feneux, D. Lachaise, D 1991). Comparative kinetics of short and long sperm in sperm dimorphic Drosophila species. Cell Motility and the Cytoskeleton 19, 269 274.
27. Briskie, J. V., Montgomerie, R. Birkhead, T. R 1997). The evolution of sperm size in birds. Evolution 51, 937 945.
28. Brokaw, C. J 1966). Effects of increased viscosity on the movements of some invertebrate spermatozoa. Journal of Experimental Biology 45, 113 139.
29. Brokaw, C. J 1987). Regulation of sperm flagellar motility by calcium and cAMP-dependent phosphorylation. Journal of Cellular Biochemistry 35, 175 184.
30. Byrne, P., Simmons, L. W. Roberts, J. D 2003). Sperm competition and the evolution of gamete morphology in frogs. Proceedings of the Royal Society of London - Series B: Biological Sciences 270, 2079 2086.
31. Cameron, M. L 1965). Some details of ultrastructure in the development of flagellar fibers of the Tenebrio sperm. Canadian Journal of Zoology 43, 1005 1010.
32. Chapman, R. F 1982). The Insects - Structure and Function. Hodder and Stoughton, London, Sydney, Aukland, Toronto.
33. Christen, R., Schackmann, R. W. Shapiro, B. M 1983). Metabolism of sea urchin sperm. Interrelationships between intracellular pH, ATPase activity, and mitochondrial respiration. Journal of Biological Chemistry 258, 5392 5399.
34. Cook, P. A. Wedell, N 1999). Non-fertile sperm delay female remating. Nature 397, 486.
35. Cooper, K. W 1950). Normal spermatogenesis in Drosophila. In Biology of Drosophila (ed. M. Demerec pp. 1 61. Chapman & Hall, Ltd., London.
36. Cosson, J 2004). The ionic and osmotic factors controlling motility of fish spermatozoa. Aquaculture International 12, 69 85.
37. Curtis, S. K. Benner, D. B 1991). Movement of spermatozoa of Megaselia scalaris (Diptera: Brachycera: Cyclorrhapha: Phoridae) in artificial and natural fluids. Journal of Morphology 210, 85 99.
38. Dallai, R 1988). The spermatozoon of Asphondyliidi (Diptera, Cecidomyiidae). Journal of Ultrastructure and Molecular Structure Research 101, 98 107.
39. Dallai, R. Afzelius, B. A 1990a). Microtubular diversity in insect spermatozoa: results obtained with a new fixative. Journal of Structural Biology 103, 164 179.
40. Dallai, R. Afzelius, B. A 1990b). Ultrastructural patterns of the flagellar axoneme in the non-motile part of the mole-cricket sperm. Biology of the Cell 70, 19 26.
41. Dallai, R. Afzelius, B. A 1993). Development of the accessory tubules of insect sperm flagella. Journal of Submicroscopic Cytology and Pathology 25, 499 504.
42. Dallai, R., Lupetti, P. Mencarelli, C 2006). Unusual axonemes of hexapod spermatozoa. In International Review of Cytology: A Survey of Cell Biology, vol. 254 (ed. K. W. Jeon pp. 45 99. Elsevier, San Diego.
43. Dallai, R. Mazzini, M 1980). Characteristics of the motile spermatozoa in 5 species of gall-midges (Diptera: Cecidomyiidae). International Journal of Insect Morphology and Embryology 9, 383 393.
44. Dallai, R., Xué, L. Yin, W 1992). Flagellate spermatozoa of Protura (Insecta, Apterygota) are motile. International Journal of Insect Morphology and Embryology 21, 137 148.
45. Davey, K. G 1965a). Reproduction in the Insects. Annals of the Entomological Society of Quebec 10, 13 25.
46. Davey, K. G 1965b). Reproduction in the Insects. Oliver and Boyd, Edinburgh, London.
47. Davis, N. T 1965). Studies of the reproductive Physiology of Cimicidae (Hemiptera) - II. Artificial insemination and the function of the seminal fluid. Journal of Insect Physiology 11, 355 366.
48. Degrugillier, M. E. Leopold, R. A 1976). Ultrastructure of sperm penetration of house fly eggs. Journal of Ultrastructure Research 56, 312 325.
49. Fauci, L. F. Dillon, R 2006). Biofluidmechanics of reproduction. Annual Review of Fluid Mechanics 38, 371 394.
50. Franzén, Å 1956). On spermiogenesis, morphology of the spermatozoon, and biology of fertilization among invertebrates. Zoologiska Bidrag från Uppsala 33, 355 482.
51. Friedländer, M., Jeshtadi, A. Reynolds, S. E 2001). The structural mechanism of trypsin-induced intrinsic motility in Manduca sexta spermatozoa in vitro Journal of Insect Physiology 47, 245 255.
52. Frola, J. Norman, C 1964). Studies of morphology and Motility of Byrsotria fumigata spermatozoa. Proceedings of the West Virginia Academy of Science 36, 53 58.
53. Froman, D. P., Pizzari, T., Feltman, A. J., Castillo-Juarez, H. Birkhead, T. R 2002). Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proceedings of the Royal Society of London - Series B: Biological Sciences 269, 607 612.
54. Gack, C. Peschke, K 1994). Spermathecal morphology, sperm transfer and a novel mechanism of sperm displacement in the rove beetle, Aleochara curtula (Coleoptera; Staphylinidae). Zoomorphology 114, 227 237.
55. Gage, M. J. G 1994). Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society of London B, Biological Sciences 258, 247 245.
56. Gage, M. J. G. Freckleton, R. P 2003). Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proceedings of the Royal Society of London - Series B: Biological Sciences 270, 625 632.
57. Gage, M. J. G., Macfarlane, C. P., Yeates, S., Ward, R. G., Searle, J. B. Parker, G. A 2004). Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Current Biology 14, 44 47.
58. Gage, M. J. G. Morrow, E. H 2003). Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Current Biology 13, 754 757.
59. García-González, F. Simmons, L. W 2007). Shorter sperm confer higher competitive fertilization success. Evolution 61, 816 824.
60. Gardner, L. C., O'Toole, E., Peronne, C. A., Giddings, T. Porter, M. E 1994). Components of a "dynein regulatory complex" are located at the junction between the radial spokes and the dynein arms in Chlamydomonas flagella. Journal of Cell Biology 127, 1311 1325.
61. Gibbons, I. R 1981). Cilia and flagella of eukaryotes. Journal of Cell Biology 91, 107s 124s.
62. Gibbons, I. R., Fronk, E 1972). Some properties of bound and soluble dynein from sea urchin sperm flagella. Journal of Cell Biology 54, 365 381.
63. Ginger, M. L 2005). Post-genomic views of a 'unique' metabolism in the eukaryotic flagellum. Biochemical Society Transactions 33, 975 976.
64. Gomendio, M., Martin-Coello, J., Crespo, C., Magaña, C. Roldan, E. R. S 2006). Sperm competition enhances functional capacity of mammalian spermatozoa. Proceedings of the National Academy of Sciences of the United States of America 103
65. Gray, J. Hancock, G. J 1955). The propulsion of sea-urchin spermatozoa. Journal of Experimental Biology 32, 802 814.
66. Gschwentner, R. Tadler, A 2000). Functional anatomy of the spermatheca and its duct in the seed bug Lygaeus simulans (Heteroptera: Lygaeidae). European Journal of Entomology 97, 305 312.
67. Hayashi, F 1998). Sperm co-operation in the Fishfly, Parachauliodes japonicus. Functional Ecology 12, 347 350.
68. Heming-van Battum, K. E. Heming, B. S 1986). Structure, function and evolution of the reproductive system in females of Hebrus pusillus and H. ruficeps (Hemiptera, Gerromorpha, Hebridae). Journal of Morphology 190, 121 167.
69. Hosken, D. J 1997). Sperm competition in bats. Proceedings of the Royal Society of London - Series B: Biological Sciences 264, 385 392.
70. Hosken, D. J. Ward, P. I 2000). Copula in yellow dung flies (Scathophaga stercoraria): investigating sperm competition models by histological observation. Journal of Insect Physiology 46, 1355 1363.
71. Hughes, M. Davey, K. G 1969). The activity of spermatozoa of Periplaneta. Journal of Insect Physiology 15, 1607 1616.
72. Hünefeld, F. Beutel, R. G 2005). The sperm pumps of Strepsiptera and Antliophora (Hexapoda). Journal of Zoological Systematics and Evolutionary Research 43, 297 306.
73. Ishida, S., Yamashita, Y. Teshirogi, W 1991). Analytical studies of the ultrastructure and movement of the spermatozoa of freshwater triclades. Hydrobiologica 227, 95 104.
74. Ishijima, S., Ishijima, S. A. Afzelius, B. A 1994). Movement of Myzostomum spermatozoa: Calcium ion regulation of swimming direction. Cell Motility and the Cytoskeleton 28, 135 142.
75. Ishijima, S., Ishijima, S. A. Afzelius, B. A 1999). Movement of Turritella spermatozoa: Direction of propagation and chirality of flagellar bends. Cell Motility and the Cytoskeleton 44, 85 95.
76. Ito, S 1966). Movement and structure of louse spermatozoa. Journal of Cell Biology 31, 128A.
77. Jamieson, B. G. M 1987). The Ultrastructure and Phylogeny of Insect Spermatozoa. Cambridge University Press, Cambridge, London, New York, New Rochelle, Melbourne, Sydney.
78. Jamieson, B. G. M., Ausio, J. Justine, J.-L. (1995). Advances in Spermatozoal Phylogeny and Taxonomy. In Mémoires du Muséum National d'Histoire Naturelle, vol. 166. Muséum National d'Histoire Naturelle Paris, Paris.
79. Jamieson, B. G. M., Dallai, R. Afzelius, B. A 1999). Insects: Their Spermatozoa and Phylogeny. Science Publishers, Inc., Enfield, New Hampshire, USA.
80. Kamp, G., Büsselmann, G. Lauterwein, J 1996). Spermatozoa: models for studying regulatory aspects of energy metabolism. Experientia 52, 487 494.
81. Karr, T. L 1996). Paternal investment and intracellular sperm-egg interactions during and following fertilization in Drosophila. In Current Topics in Developmental Biology, vol. 34. Current Topics in Developmental Biology (ed. R. A. Pedersen and G. P. Schatten pp. 89 115. Academic Press, San Diego.
82. Karr, T. L. Pitnick, S 1996). The ins and outs of fertilization. Nature 379, 405 406.
83. Katsuno, S 1978). Studies on eupyrene and apyrene spermatozoa in the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae) VII. The motility of sperm bundles and spermatozoa in the reproductive organs of males and females. Applied Entomology and Zoology 13, 91 96.
84. Keskes, L., Giroux-Widemann, V., Serres, C., Pignot-Paintrand, I., Jouannet, P. Feneux, D 1998). The reactivation of demembranated human spermatozoa lacking outer dynein arms is independent of pH. Molecular Reproduction and Development 49, 416 425.
85. King, P. E 1962). The structure and action of the spermatheca in Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). Proceedings of the Royal Entomological Society of London A 37, 73 75.
86. Koeniger, G 1970). Die Bedeutung der Tracheenhülle und der Anhangsdrüse der Spermatheka für die Befruchtungsfähigkeit der Spermatozoen in der Bienenkönigin. Apidologie 1, 55 71.
87. LaChance, L. E., Proshold, F. I. Ruud, R. L 1978). Pink bollworm: effects of male irradiation and ejaculate sequence on female ovipositional response and sperm radiosensitivity. Journal of Economic Entomology 71, 361 365.
88. Landa, V 1961). Use of an artificial spermatophore in the study of activation of spermatozoa and development of the spermatophores in the cockchafer. Nature 190, 935 936.
89. LeCato, L. G. Pienkowski, R. L 1973). Insemination and sperm storage in the alfalfa weevil, Hypera postica (Gyllenhal) (Coleoptera: Curculionidae). International Journal of Insect Morphology and Embryology 2, 257 263.
90. Lefevre, G., Jr. Johnsson, U. B 1962). Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47, 1719 1736.
91. Linley, J. R 1979). Activity and motility of spermatozoa of Culicoides melleus (Diptera: Ceratopogonidae). Entomologia Experimentalis et Applicata 26, 85 96.
92. Linley, J. R 1981a). Ejaculation and spermatophore formation in Culicoides melleus (Coq.) (Diptera: Ceratopogonidae). Canadian Journal of Zoology 59, 332 346.
93. Linley, J. R 1981b). Emptying of the spermatophore and spermathecal filling in Culicoides melleus (Coq.) (Diptera: Ceratopogonidae). Canadian Journal of Zoology 59, 347 356.
94. Linley, J. R. Simmons, K. R 1981). Sperm motility and spermathecal filling in lower diptera. International Journal of Invertebrate Reproduction 4, 137 146.
95. Lowe, C. P 2003). Dynamics of filaments: modelling the dynamics of driven microfilaments. Philosophical Transactions of the Royal Society of London - Series B: Biological Sciences 358, 1543 1550.
96. Lupetti, P., Mencarelli, C., Rosetto, M., Heuser, J. E. Dallai, R 1998). Structural and molecular characterization of dynein in a gall-midge insect having motile sperm with only the outer arm. Cell Motility and the Cytoskeleton 39, 303 317.
97. Malo, A. F., Gomendio, M., Garde, J., Lang-Lenton, B., Soler, A. J. Roldan, E. R. S 2006). Sperm design and sperm function. Biology Letters 2, 246 249.
98. Mencarelli, C., Lupetti, P., Rosetto, M., Mercati, D., Heuser, J. D. Dallai, R 2001). Molecular structure of dynein and motility of a giant sperm axoneme provided with only the outer dynein arm. Cell Motility and the Cytoskeleton 50, 129 146.
99. Miller, G. T. Pitnick, S 2002). Sperm-female coevolution in Drosophila. Science 298, 1230 1233.
100. Minder, A. M., Hosken, D. J. Ward, P. I 2005). Co-evolution of male and female reproductive characters across the Scathophagidae (Diptera). Journal of Evolutionary Biology 18, 60 69.
101. Mojica, J. M. Bruck, D. L 1996). Sperm bundle coiling: transporting long sperm bundles in Drosophila dunni dunni. Journal of Insect Physiology 42, 303 307.
102. Moore, H. D. M. Taggart, D. A 1995). Sperm pairing in the opossum increases the efficiency of sperm movement in a viscous environment. Biology of Reproduction 52, 947 953.
103. Morrow, E. H 2004). How the sperm lost its tail: the evolution of aflagellate sperm. Biological Reviews 79, 795 814.
104. Morrow, E. H. Gage, M. J. G 2000). The evolution of sperm length in moths. Proceedings of the Royal Society of London - Series B: Biological Sciences 267, 307 313.
105. Nakajima, A., Morita, M., Takemura, A., Kamimura, S. Okuno, M 2005). Increase in intracellular pH induces phosphorylation of axonemal proteins for activation of flagellar motility in starfish sperm. Journal of Experimental Biology 208, 4411 4418.
106. Okelo, O 1979). Mechanisms of sperm release from the receptaculum seminis of Schistocerca vaga Scudder (Orthoptera: Acrididae). International Journal of Invertebrate Reproduction 1, 121 131.
107. Omura, S 1936). Studies on the reproductive system of the male of Bombyx mori. I. Structure of the testis and the intratesticular behaviour of the spermatozoa. Journal of the Faculty of Agriculture Hokkaido Imperial University 38, 151 181.
108. Omura, S 1938a). Structure and function of the female genital system of Bombyx mori with special reference to the mechanism of fertilization. Journal of the Faculty of Agriculture Hokkaido Imperial University 40, 111 128.
109. Omura, S 1938b). Studies on the reproductive system of the male of Bombyx mori. II. Post-testicular organs and post-testicular behaviour of the spermatozoa. Journal of the Faculty of Agriculture Hokkaido Imperial University 40, 129 170.
110. Osanai, M., Aigaki, T. Kasuga, H 1987a). Energy metabolism in the spermatophore of the silkmoth, Bombyx mori, associated with accumulation of alanine derived from arginine. Insect Biochemistry 17, 71 75.
111. Osanai, M., Aigaki, T., Kasuga, H. Yonezawa, Y 1986). Role of arginase transferred from the vesicula seminalis during mating and changes in amino acid pools of the spermatophore after ejaculation in the silkworm, Bombyx mori. Insect Biochemistry 16, 879 885.
112. Osanai, M. Baccetti, B 1993). Two-step acquisition of motility by insect spermatozoa. Experientia (Basel) 49, 593 595.
113. Osanai, M. Kasuga, H 1990). Role of endopeptidase in motility induction in apyrene silkworm spermatozoa; micropore formation in the flagellar membrane. Experientia 46, 261 264.
114. Osanai, M., Kasuga, H. Aigaki, T 1987b). Physiological role of apyrene spermatozoa of Bombyx mori. Experientia (Basel) 43, 593 596.
115. Osanai, M., Kasuga, H. Aigaki, T 1987c). The spermatophore and its structural changes with time in the bursa copulatrix of the silkworm, Bombyx mori. Journal of Morphology 193, 1 11.
116. Osanai, M., Kasuga, H. Aigaki, T 1989). Isolations of eupyrene sperm bundles and apyrene spermatozoa from seminal fluid of the silkmoth, Bombyx mori. Journal of Insect Physiology 35, 401 405.
117. Osanai, M., Kasuga, H. Aigaki, T 1991). Motility-related ultrastructural changes in the flagellar membrane of apyrene spermatozoa of the silkworm Bombyx mori induced by Arg-C endopeptidases. Invertebrate Reproduction and Development 19, 193 202.
118. Parker, G. A 1970). Sperm competition and its evolutionary effect on copula duration in the fly Scatophaga stercoraria. Journal of Insect Physiology 16, 1301 1328.
119. Parker, G. A 1993). Sperm competition games: sperm size and sperm number under adult control. Proceedings of the Royal Society of London - Series B: Biological Sciences 253, 245 254.
120. Parker, G. A. Begon, M 1993). Sperm competition games: sperm size and number under gametic control. Proceedings of the Royal Society of London - Series B: Biological Sciences 253, 255 262.
121. Pattarini, J. M., Starmer, W. T., Bjork, A. Pitnick, S 2006). Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60, 2064 2080.
122. Payne, M. A 1933). The structure of the testis and movement of sperms in Chortophaga viridifasciata as demonstrated by intravitam technique. Journal of Morphology 54, 321 345.
123. Perotti, M. E 1973). The mitochondrial derivative of the spermatozoon of Drosophila before and after fertilization. Journal of Ultrastructure Research 44, 181 198.
124. Phillips, D. M 1970). Insect sperm: Their structure and morphogenesis. Journal of Cell Biology 44, 243 277.
125. Phillips, D. M 1974). Structural variants in invertebrate sperm flagella and their relationship to motility. In Cilia and Flagella (ed. M. A. Sleigh pp. 379 402. Academic Press, London, New York.
126. Pitnick, S., Spicer, G. S. Markow, T. A 1995). How long is a giant sperm? Nature 375, 109.
127. Pratt, S. A 1968). An electron microscope study of Nebenkern formation and differentiation in spermatids of Murgantia histrionica (Hemiptera, Pentatomidae). Journal of Morphology 126, 31 66.
128. Presgraves, D. C., Baker, R. H. Wilkinson, G. S 1999). Coevolution of sperm and female reproductive tract morphology in stalk-eyed flies. Proceedings of the Royal Society of London B, Biological Sciences 266, 1041 1047.
129. Purcell, E. M 1977). Life at low Reynolds number. American Journal of Physics 45, 3 11.
130. Quicke, D. L. J., Ingram, S. N., Baillie, H. S. Gaitens, P. V 1992). Sperm structure and ultrastructure in the Hymenoptera (Insecta). Zoologica Scripta 21, 381 402.
131. Rao, H. V. Davis, N. T 1969). Sperm activation and migration in bed bugs. Journal of Insect Physiology 15, 1815 1832.
132. Reinhardt, K. Siva-Jothy, M. T 2007). Biology of the bed bugs (Cimicidae). Annual Review of Entomology 52, 351 374.
133. Richards, A. G 1963). The rate of sperm locomotion in the cockroach as a function of temperature. Journal of Insect Physiology 9, 545 549.
134. Riddiford, L. M. Ashenhurst, J. B 1973). The switchover from virgin to mated behaviour in female Cercropia moths: the role of the bursa copulatrix. Biological Bulletin 144, 126 171.
135. Rikmenspoel, R 1978). The equation of motion for sperm flagella. Biophysical Journal 23, 177 206.
136. Rikmenspoel, R. Jacklet, A. C 1980). Motion characteristics of flagellar fragments of long insect sperm. Biophysical Journal 29, 295 303.
137. Robison, W. G., Jr. 1966). Microtubules in relation to the motility of a sperm syncytium in an armored scale insect. Journal of Cell Biology 29, 251 265.
138. Robison, W. G., Jr. 1972). Microtubular patterns in spermatozoa of coccid insects in relation to bending. Journal of Cell Biology 52, 66 83.
139. Rodríguez, V 1994). Function of the spermathecal muscle in Chelymorpha alternans Boheman (Coleoptera: Chrysomelidae: Cassidinae). Physiological Entomology 19, 198 202.
140. Rosati, F., Selmi, G. Mazzini, M 1976). Comparative observations on the mitochondrial derivatives of insect sperm. Journal of Submicroscopic Cytology 8, 51 67.
141. Rothschild, M. L 1991). Arrangement of sperm within the spermatheca of fleas, with remarks on sperm displacement. Biological Journal of the Linnean Society 43, 313 323.
142. Ruknudin, A. Raghavan, V. V 1988). Initiation, maintenance and energy metabolism of sperm motility in the bed bug, Cimex hemipterus. Journal of Insect Physiology 34, 137 142.
143. Ruttner, F. Koeniger, G 1971). Die Füllung der Spermatheka der Bienenkönigin - Aktive Wanderung oder passiver Transport der Spermatozoen? Zeitschrift für vergleichende Physiologie 72, 411 422.
144. Sasakawa, K 2007). Sperm bundle and reproductive organs of carabid beetles tribe Pterostichini (Coleoptera: Carabidae). Naturwissenschaften 95, 384 391.
145. Satir, P 1965). Studies on cilia. II. Examination of the distal region of the ciliary shaft and the role of the filaments in motility. Journal of Cell Biology 26, 805 834.
146. Satir, P 1968). Studies on cilia. III. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. Journal of Cell Biology 39, 77 94.
147. Shepherd, J. G 1974). Activation of Saturniid moth sperm by a secretion of the male reproductive tract. Journal of Insect Physiology 20, 2107 2122.
148. Shepherd, J. G 1975). A polypeptide sperm activator from male Saturniid moth. Journal of Insect Physiology 21, 9 22.
149. Simmons, L. W 2001). Sperm Competition and its Evolutionary Consequences in the Insects. Princeton University Press, Princeton.
150. Simmons, L. W. Moore, A. J 2008). Evolutionary quantitative genetics of sperm. In Sperm Biology (ed. by T. R. Birkhead, D. J. Hosken S. K. Pitnick). In Press. Elsevier, London.
151. Simmons, L. W., Parker, G. A. Stockley, P 1999). Sperm displacement in the yellow dung fly, Scatophaga stercoraria: an investigation of male and female processes. American Naturalist 153, 302 314.
152. Simmons, L. W., Wernham, J., García-González, F. Kamien, D 2003). Variation in paternity in the field cricket Teleogryllus oceanicus: no detectable influence of sperm numbers or sperm length. Behavioral Ecology 14, 539 545.
153. Sivinski, J 1980). Sexual selection and insect sperm. Florida Entomologist 63, 99 111.
154. Sivinski, J 1984). Sperm in competition. In Sperm Competition and the Evolution of Animal Mating Systems (ed. R. L. Smith pp. 86 115. Academic Press, London.
155. Stockley, P., Gage, M. J. G., Parker, G. A. Møller, A. P 1997). Sperm competition in fishes: The evolution of testis size and ejaculate characteristics. American Naturalist 149, 933 954.
156. Summers, K. E. Gibbons, I. R 1971). Adenosine triphosphate-induced sliding of tubules in trypsin treated sea urchin sperm. Proceedings of the National Academy of Sciences of the United States of America 68, 3092 3096.
157. Summers, K. E. Gibbons, I. R 1973). Effects of trypsin digestion on flagellar structures and their relationship to motility. Journal of Cell Biology 58, 618 629.
158. Swan, M. A 1981). The generation and propagation of double waves in mosquito (Aedes notoscriptus) sperm tails. Gamete Research 4, 241 250.
159. Taylor, H. C. Holwill, M. E. J 1999). Axonemal dynein - a natural molecular motor. Nanotechnology 10, 237 243.
160. Taylor, O. R 1967). Relationship of multiple mating to fertility in Atteva punctella (Lepidoptera: Yponomeutidae). Annals of the Entomological Society of America 60, 583 590.
161. Thibout, E 1975). Analyse des causes de l'inhibition de la receptivite sexualle et de l'influence d'une eventualle seconde copulation sur la reproduction chez la Teigne du poireau, Acrolepia assectella (Lepidoptera: Plutellidae). Entomologica Experimentalis et Applicata 18, 105 116.
162. Tokuyasu, K. T 1974). Dynamics of spermiogenesis in Drosophila melanogaster - III. Relation between axoneme and mitochondrial derivatives. Experimental Cell Research 84, 239 250.
163. Tschudi-Rein, K. Benz, G 1990). Mechanisms of sperm transfer in female Pieris brassicae (Lepidoptera: Pieridae). Annals of the Entomological Society of America 83, 1158 1164.
164. Turner, R. M 2006). Moving to the beat: a review of mammalian sperm motility regulation. Reproduction, Fertility and Development 18, 25 38.
165. Verma, L. R. Shuel, R. W 1973). Respiratory metabolism of the semen of the honey-bee, Apis mellifera. Journal of Insect Physiology 19, 97 103.
166. Villavaso, E. J 1975a). Functions of the spermathecal muscle of the boll weevil, Anthonomus grandis. Journal of Insect Physiology 21, 1275 1278.
167. Villavaso, E. J 1975b). The role of the spermathecal gland of the boll weevil, Anthonomus grandis. Journal of Insect Physiology 21, 1457 1462.
168. Viscuso, R., Brundo, M. V. Sottile, L 2002). Mode of transfer of spermatozoa in Orthoptera Tettigoniidae. Tissue and Cell 34, 337 348.
169. Vladic, T. V. Järvi, T 2001). Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proceedings of the Royal Society of London - Series B: Biological Sciences 268, 2375 2381.
170. Watnick, T. J., Jin, Y., Matunis, E. Kernan, M. J. M., C 2003). A flagellar polycystin-2 homolog required for male fertility in Drosophila. Current Biology 13, 2179 2184.
171. Watson, P. A 1991). Function follows form: generation of intracellular signals by cell deformation. Journal of the Federation of American Societies for Experimental Biology 5, 2013 2019.
172. Werner, M 2002). Ultrastruktur und Motilität der Spermien von Aleochara-Arten (Coleoptera, Staphylinidae). PhD thesis, Albert-Ludwigs- Universität Freiburg i.Br., Germany.
173. Werner, M., Böminghaus, A., Zissler, D. Peschke, K 2001). Comparison of sperm structure and motility between Aleochara tristis and A. clavicornis (Coleoptera, Staphylinidae). Zoology 104 (Suppl. IV 44.
174. Werner, M., Gack, C., Speck, T. Peschke, K 2007). Queue up, please! Spermathecal filling in the rove beetle Drusilla canaliculata (Coleoptera, Staphylinidae). Naturwissenschaften 94, 837 841.
175. Werner, M., Speck, T., Zissler, D. Peschke, K 2000). Spermienbewegung beim Kurzflügelkäfer Aleochara bilineata (Coleoptera, Staphylinidae). In Biona-report, vol. 14 (ed. A. Wisser and W. Nachtigall pp. 45 50. Akademie der Wissenschaften, Mainz.
176. Werner, M., Tscheulin, T., Speck, T., Zissler, D. Peschke, K 2002). Ultrastructure and motility pattern of the spermatozoa of Aleochara curtula (Coleoptera, Staphylinidae). Arthropod Structure and Development 31, 243 254.
177. Werner, M., Zissler, D. Peschke, K 1999). Structure and energy pathways of spermatozoa of the rove beetle Aleochara bilineata (Coleoptera, Staphylinidae). Tissue and Cell 31, 413 420.
178. West-Eberhard, M. J 1983). Sexual selection, social competition, and speciation. Quarterly Review of Biology 58, 155 183.
179. West-Eberhard, M. J 1984). Sexual selection, competitive communication and species-specific signals in insects. In Insect Communication (ed. T. Lewis pp. 283 324. Academic Press, London.
180. Wilkes, A 1965). Sperm transfer and utilization by the arrhenotokous wasp Dahlbominus fuscipennis (Zett.) (Hymenoptera: Eulophidae). The Canadian Entomologist 97, 647 657.
181. Woolsey, J. Ingermann, R. L 2003). Acquisition of the potential for sperm motility in steelhead (Oncorhynchus mykiss): effect of pH on dynein ATPase. Fish Physiology and Biochemistry 29, 47 56.
182. Zhang, H. Mitchell, D. R 2004). Cpc1, a Chlamydomonas central pair protein with an adenylate kinase domain Journal of Cell Science 117, 4179 4188.