Evolution of intra-ejaculate sperm interactions: Do sperm cooperate?

Biological Reviews

Volumn 86, Issue 1, 2011, Pages 249-270

  Higginson, Dawn M ^a   Pitnick, Scott ^a  

^a SYRACUSE UNIVERSITY   (United States)

Author keywords

Haploid expression; Motility; Sperm competition; Sperm conjugation; Sperm heteromorphism; Sperm morphological evolution

Indexed keywords

ANIMAL; ARTICLE; EVOLUTION; FEMALE; FERTILIZATION; GENETIC SELECTION; MALE; MATE CHOICE; PHYSIOLOGY; SPERMATOGENESIS; SPERMATOZOON;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; FERTILIZATION; MALE; MATING PREFERENCE, ANIMAL; SELECTION, GENETIC; SPERMATOGENESIS; SPERMATOZOA;

SYNAPSIS;

EID: 78951494373     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/j.1469-185X.2010.00147.x     Document Type: Article

References (243)

1. Abro, A. (1998). Structure and development of sperm bundles in the dragonfly Aeshna juncea L. (Odonata). Journal of Morphology 235, 239-247.
2. Afzelius, B. A. & Dallai, R. (1983). The paired spermatozoa of the marine snail, Turritella communis Lamark (Molluscoa, Mesogastropoda). Journal of Ultrastructure research 85, 311-319.
3. Afzelius, B. A. & Dallai, R. (1987). Conjugated spermatozoa. In New Horizons in Sperm Cell Research (ed. H. Mohri ), pp. 349-355. Japan Science Society, Tokyo.
4. Alberti, G. (1990). Comparative spermatology of Araneae. Acta Zoologica Fenn. 190, 17-34.
5. Alberti, G. (2000). Chelicerata. In Reproductive biology of invertebrates, vol. 9, Part B. Progress in male gamete ultrastructure (ed. B. G. M. Jamieson ), pp. 311-388. John Wiley and Sons, Ltd., New York.
6. Alberti, G. (2005). Double spermatogenesis in Chelicerata. Journal of Morphology 266, 281-297.
7. Alberti, G., Afzelius, B. A. & Lucas, S. M. (1986). Ultrastructure of spermatozoa and spermatogenesis in bird spiders (Theraphosidae, Mygalomorphae, Araneae). Journal of Submicroscopic Cytology 18.
8. Alberti, G. & Colye, R. A. (1991). Ultrastructure of the primary male genital system, spermatozoa and spermiogenesis of Hypochilus pococki (Araneae, Hypochilidae). Journal of Acarchnology 19, 136-149.
9. Alberti, G. & Weinmann, C. (1985). Fine structure of spermatozoa of some labidognath spiders (Filistatidae, Segestriidae, Dysderidae, Oonopidae, Scytodidae, Pholcidae; araneae' Arachnida) with remarks on spermiogenesis. Journal of Morphology 185, 1-35.
10. Amsden, B. (1998). Solute diffusion within hydrogels. Mechanisms and models. Macromolecules 31, 8382-8395.
11. Au, D. W.-t ., Reunov, A. A. & Wu, R. S.-s. (1998). Four lines of spermatid development and dimorphic spermatozoa in the sea urchin Anthocidaris crassispina (Echinodermata, Echinoida). Zoomorphology 118, 159-168.
12. Auerbach, L. (1893). Remarkable behaviour of the spermatozoa of Dytiscus marginalis. Journal of the Royal Microscopical Society, Series 2 13, 622.
13. Baccetti, B. (1972). Insect sperm cells. Advances in Insect Physiology 9, 315-397.
14. Baccetti, B. (1986). Spermatozoa and phylogeny in orthopteroid insects. In Biology of Orthopteroid Insects (ed. B. Baccetti ), pp. 12-112. John Wiley and Sons, New York.
15. Baccetti, B. & Afzelius, B. A. (1976). The biology of the sperm cell. In Monographs in Developmental Biology, vol. 10 (ed. A. Wolsky ). Karger, Basel.
16. Baker, R. R. & Bellis, M. A. (1987). 'Kamikaze' sperm in mammals? Animal Behaviour 36, 936-938.
17. Ballowitz, E. (1895). Die dopplespermatozoen der Dyticiden. Zeitschrift für Wissenschaftliche Zoologie 60, 458-499.
18. Bawa, S. R. (1964). Electron microscope study of spermiogenesis in a fire-brat insect, Thermobia domestica Pack. The Journal of Cell Biology 23, 431-445.
19. Bawa, S. R. (1975). Joined spermatozoa. In The Functional Anatomy of the Spermatozoon (ed. B. A. Afzelius ), pp. 259-266. Pergamon Press, Oxford.
20. Beatty, R. A. & Burgoyne, P. S. (1971). Size classes of the head and flagellum of Drosophila spermatozoa. Cytogenetics 10, 1770189.
21. Beatty, R. A. & Sidhu, N. S. (1969). Polymegaly of spermatozoan length and its genetic control in Drosophila species. Proceedings of the Royal Society of Edinburgh B 71b, 14-29.
22. Bedford, J. M., Rodger, J. C. & Breed, W. G. (1984). Why so many mammalian spermatozoa - a clue from Marsupials? Proceedings of the Royal Society B: Biological Sciences 221, 221-233.
23. Bertkau, P. (1877). Über die übertragungsorgane und die spermatozoen der spinnen. Verhandlungen des Naturhistorischen Vereins preussisher Rheinlande 34, 28-32.
24. Biggers, J. D. & Creed, R. F. S. (1962). Conjugate spermatozoa of the North American opossum. Nature 196, 1112-1113.
25. Birkhead, T. R. & Mèller, A. P. (1998). Sperm Competition and Sexual Selection. Academic Press, London.
26. Birkhead, T. R., Mèller, A. P. & Sutherland, W. J. (1993). Why do females make it so difficult for males to fertilize their eggs? Journal of Theoretical Biology 161, 51-60.
27. Birkhead, T. R., Pellatt, E. J., Brekke, P., Yeates, R. & Castillo-Juarez, H. (2005). Genetic effects on sperm design in the zebra finch. Nature 434, 383-387.
28. Boissin, L. (1973). Étude ultrastructurale de la spermiogenès de Meta bourneti Simon (Arachinides, Araneides, Metinae). Comptes rendus de la 2e runion d'archnologie d'expression fancaise, Montpellier, 7-22.
29. Boyd, R. & Richerson, P. J. (1992). Punishment allows the evolution of cooperation (or anything else) in sizable groups. Ethology and Sociobiology 13, 171-195.
30. Braidotti, P., Ferraguti, M. & Fleming, T. P. (1980). Cell junctions between spermatozoa flagella within the spermatozeugmata of Tubifex tubifex (Annelida: Oligochaeta). Journal of Ultrastructure Research 73, 299-309.
31. Braun, R. E., Behringer, R. R., Peschon, J. J., Brinster, R. L. & Palmiter, R. D. (1989). Genentically haploid spermatids are phenotypically diploid. Nature 337, 373-376.
32. Breed, W. G. (2004). The spermatozoon of Eurasian murine rodents: its morphological diversity and evolution. Journal of Morphology 261, 52-69.
33. Breed, W. G. (2005). Evolution of the spermatozoon in muroid rodents. Journal of Morphology 265, 271-290.
34. Breland, O. P. & Simmons, E. (1970). Preliminary studies of the spermatozoa and the male reproductive system of some whirligig beetles (Coleoptera: Gyrinidae). Entomological News 81, 101-110.
35. Buckland-Nicks, J. (1998). Prosobranch parasperm: sterile cells germ cells that promote paternity? Micron 29, 267-280.
36. Buckland-Nicks, J., Bryson, I., Hart, L. & Partridge, L. (1999). Sex and a snail's sperm: on the transport, storage and fate of dimorphic sperm in Littorinidae. Invertebrate Reproduction and Development 36, 145-152.
37. Buckland-Nicks, J., Williams, D., Chia, F.-S. & Fontaine, A. (1982). The fine structure of the polymorphic spermatozoa Fusitriton oregonensis (Mollusca: Gastropoda) with notes on the cytochemistry of the internal secretions. Cell and Tissue Research 227, 235-255.
38. Burness, G. P., Casselman, S. J., Schulte-Hostedde, A. I., Moyes, C. D. & Montgomerie, R. (2004). Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behavioral Ecology and Sociobiology 56, 65-70.
39. Buss, L. W. (1987).The evolution of individuality. Princeton University Press, Princeton, New Jersey.
40. Calhim, S., Immler, S. & Birkhead, T. R. (2007). Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PloS One 2, e413.
41. Chapman, R. F. (1998).The insects: structure and function. Cambridge University Press, Cambridge.
42. Chawanji, A. S., Hodgson, A. N. & Villet, M. H. (2005). Sperm morphology in four species of African platypleurine cicadas (Hemiptera: Cicadomorpha: Cicadidae). Tissue & Cell 37, 257-267.
43. Chawanji, A. S., Hodgson, A. N. & Villet, M. H. (2006). Sperm morphology in five species of cicadettine cicadas (Hemiptera: Cicadomorpha: Cicadidae). Tissue & Cell 38, 373-388.
44. Chawanji, A. S., Hodgson, A. N., Villet, M. H., Sanborn, A. F. & Phillips, P. K. (2007). Spermiogenesis in three species of cicadas (Hemiptera: Cicadidae). Acta Zoologica 88, 337-348.
45. Clark, A. G., Dermitzakis, E. T. & Civetta, A. (2000). Nontransitivity of sperm precedence in Drosophila. Evolution 54, 1030-1035.
46. Cohen, J. (1967). Correlation between chiasma frequency and sperm redundancy. Nature 215, 862-863.
47. Cohen, J. (1973). Cross-overs, sperm redundancy and their close association. Heredity 31, 408-413.
48. Cohen, J. (1975).Gamete redundancy - wastage or selection? In Gamete Competition in Plants and Animals (ed. D. L. Mulcahy ), pp. 99-112, Amsterdam.
49. Cooke, H. J. & Saunders, P. T. K. (2002). Mouse models of male infertility. Nature Reviews Genetics 3, 790-801.
50. Cornwallis, C. K. & Birkhead, T. R. (2007). Changes in sperm quality and numbers in response to experimental manipulation of male social status and female attractiveness. The American Naturalist 170, 758-770.
51. Cruz-Landim, C. D. & Ferreira, A. (1977). Spermatophore formation in Conocephalus saltator (Saussure). (Orthoptera: Conocephalidae). International Journal of Insect Morphology and Embryology 6, 97-104.
52. Dadoune, J.-P., Siffroi, J.-P. & Alfonsi, M.-F. (2004). Transcription in haploid male germ-cells. International Journal of Cytology 237, 1-55.
53. Dallai, R. & Afzelius, B. A. (1985). Membrane specializations in the paired spermatozoa of dytiscid water beetles. Tissue & Cell 17, 561-572.
54. Dallai, R. & Afzelius, B. A. (1987). Sperm ultrastructure in the water beetles (Insecta, Coleoptera). Bollettino di Zoologia 54, 301-306.
55. Dallai, R., Carapelli, A., Nardi, F., Fanciulli, P. P., Lupetti, P., Afzelius, B. A. & Frati, F. (2004). Sperm structure and spermiogenesis in Coletinia sp. (Nicoletiidae, Zygentoma, Insecta) with a comparative analysis of sperm structure in Zygentoma. Tissue & Cell 36, 233-244.
56. Dallai, R., Frati, F., Lupetti, P. & Adis, J. (2003). Sperm ultrastructure of Mantophasma zephyra (Insecta, Mantophasmatodea). Zoomorphology 122, 67-76.
57. Dallai, R., Lupetti, P., Carapelli, A., Frati, F. & Afzelius, B. A. (2002). Sperm structure and spermiogenesis in Atelura formicaria Heyden (Zygentoma, Insecta). Acta Zoologica 83, 245-262.
58. Dallai, R., Lupetti, P., Frati, F., Nardi, F. & Afzelius, B. A. (2001). Binucleate and biflagellate spermatozoa in Tricholepidion gertschi Wygodzynsky (Insecta, Zygentoma). Tissue & Cell 33, 606-613.
59. Dallai, R., Lupetti, P. & Mencarelli, C. (2006). Unusual axonemes of hexapod spermatozoa. Int. Rev. Cytol. 254, 45-99.
60. Dallai, R., Ryuichiro, M., Uchifune, T., Lupetti, P. & Frati, F. (2005). The sperm structure of Galloisiana yuasai (Insecta, Grylloblattodea) and implications for the phylogenetic position of Gyrlloblattodea. Zoomorphology 124, 205-212.
61. Davey, K. G. (1960).The evolution of spermatophores in insects. Proceedings of the Royal Entomological Society of London 35, 107-113.
62. Dawkins, R. (1976). The selfish gene. Oxford University Press, Oxford.
63. Dewsbury, D. A. (1985). Interactions between males and their sperm during multi-male copulatory episodes of deer mice (Peromyscus maniculatus). Animal Behaviour 33, 1266-1274.
64. Dobler, R. & Hosken, D. J. (2009). Response to selection and realized heritability of sperm length in the yellow dung fly ( Scatophaga stercoraria ). Heredity.
65. Dorus, S. & Karr, T. L. (2009).Sperm proteomics and genomics. In Sperm biology, an evolutionary perspective (ed. T. R. Birkhead, D. J. Hosken and S. Pitnick ), pp. 433-459. Elsevier, London.
66. Downing, A. L. & Burns, J. R. (1995). Testis morphology and spermatozeugma formation in 3 genera of viviparous halfbeaks - Nomorhamphus, Dermogenys and Hemirhamphodon (Teleostei, Hemiramphidae). Journal of Morphology 225, 329-343.
67. Dresdner, R. D. & Katz, D. F. (1981). Relationships of mammalian sperm motility and morphology to hydrodynamic aspects of cell function. Biology of Reproduction 25, 920-930.
68. Dusenbery, D. B. (2000). Selection for high gamete encounter rates explains the success of male and female mating types. Journal of Theoretical Biology 202, 1-10.
69. Eberhard, W. G. (1996). Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton, NJ.
70. Eddy, E. M. (2002). Male germ cell gene expression. Recent Progress in Hormone Research 57, 103-128.
71. Erickson, R. P. (1990). Post-meiotic gene expression. Trends in Genetics 6, 264-269.
72. Fain-Maurel, F.-A. (1966). Aquisitions récentes sur les spermatogenèses atypiques. Année Biologique, sér 4-5, 513-564.
73. Fawcett, D. W. (1975). The mammalian spermatozoon. Developmental Biology 44, 394-436.
74. Fawcett, D. W. & Hollenberg, R. (1963). Changes in the acrosome of guinea pig spermatozoa during passage through the epididymis. Zeitschrift für Mikroskopische Anatomie 60, 276-292.
75. Ferraguti, M. (2000). Euclitellata. In Reproductive biology of invertebrates, vol. IX. Part B. Progress in male gamete ultrastructure and phylogeny (ed. B. G. M. Jamieson ), pp. 125-182. John Wiley & Sons, Ltd, New York.
76. Ferraguti, M., Bernardini, G., Melone, G. & Dallai, R. (1988). Structure and function of the metachronal wave in Tubifex tubifex spermatozeugmata (Annelida, Oligochaeta). Journal of Ultrastructure and Molecular Structure Research 99, 79-95.
77. Ferraguti, M., Grassi, G. & Erséus, C. (1989). Different models of tubificid spermatozeugmata. Hydrobiologia 180, 73-82.
78. Firman, R. C. & Simmons, L. W. (2009). Sperm competition and the evolution of the sperm hook in house mice. Journal of Evolutionary Biology 22, 2505-2511.
79. Fishelson, L., Gon, O., Holdengreber, V. & Delarea, Y. (2007). Comparative spermatogenesis, spermatocytogenesis, and spermatozeugmata formation in males of viviparous species of Clinid fishes (Teleostei: Clinidae, Blennioidei). The Anatomical Record 290, 311-323.
80. Fisher, H. S., & Hoekstra, H. E. (2010). Competition drives cooperation among closely related sperm of deer mice. Nature 463, 801-803.
81. Fitzpatrick, J. L., Montgomerie, R., Desjardins, J. K., Stiver, K. A., Kolm, N. & Balshine, S. (2009). Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proceedings of the National Academy of Science 106, 1128-1132.
82. Frank, S. A. (2003). Repression of competition and the evolution of cooperation. Evolution 57, 693-705.
83. Fretter, V. (1953).The transference of sperm from male to female prosobranch, with reference also, to the pyramidellids. Proceedings of the Linnean Society of London 164, 217-224.
84. Friedländer, M. (1997). Control of the eupyrene-apyrene sperm dimorphism in Lepidoptera. Journal of Insect Physiology 43, 1085-1092.
85. Friend, D. S. & Fawcett, D. W. (1974). Membrane differentiations in freeze-fractured mammalian sperm. Journal of Cell Biology 63, 641-664.
86. Fuller, M. T. (1993). Spermatogenesis. In The development of Drosophila melanogaster, vol. Vol. I (ed. M. Bate and A. M. Arias ), pp. 71-147. Cold Spring Harbor Laboratory Press.
87. Gage, M. J. G., Macfarlane, C. P., Yeates, S., Schackleton, R. & Parker, G. A. (2002). Relationships between sperm morphometry and sperm motility in Atlantic salmon. Journal of Fish Biology 61, 1528-1539.
88. Gaino, E., Burlando, B., Zunino, L., Pansini, M. & Buffa, P. (1984). Origin of male gametes in Spongia officinalis (Porifera, Demospongiae). International Journal of Invertebrate Reproduction 7, 83-93.
89. Gao, J.-j., Watabe, H.-a., Aotsuka, T., Pang, J.-f. & Zhang, Y.-p. (2007). Molecular phylogeny of the Drosophila obscura species group, with emphasis on the Old World species. BMC Evolutionary Biology 7, 87.
90. Gray, J. (1930). The mechanism of ciliary movement. VI. Photographic and stroboscopic analysis of ciliary movement. Proceedings of the Royal Society of London B 107, 313-332.
91. Grier, H. J. (1984). Testis structure and formation of spermatophores in the atherinimorph teleost Heraichtyhys setnai. Copeia, 833-839.
92. Hackstein, J. H. P., Beck, H., Hochstenbach, R., Kremer, H. & Zacharias, H. (1990). Spermatogensis in Drosophila hydei: a genetic survey. Roux's Archives of developmental biology 199, 251-280.
93. Haig, D. & Bergstrom, C. T. (1995). Multiple mating, sperm competition and meiotic drive. Journal of Evolutionary Biology 8, 265-282.
94. Hamilton, W. D. (1964). The genetical evolution of social behaviour. I. Journal of Theoretical Biology 7, 1-16.
95. Hanson, J., Randall, J. T. & Bayley, S. T. (1952). The microstructure of the spermatozoa of the snail Viviparus. Experimental Cell Research 3, 65-78.
96. Harcourt, A. H. (1988). Deformed sperm are probably not adaptive. Animal Behaviour 37, 863-864.
97. Harcourt, A. H. (1991). Do mammals produce adaptive non-fertilizing sperm? In Comparative Spermatology 20 Years After, vol. 75 (ed. B. Baccetti ), pp. 765-770. Raven Press, New York.
98. Hauschteck-Jungen, E. & Maurer, B. (1976). Sperm dysfunction in sex ratio males of Drosophila subobscura. Genetica 46, 459-477.
99. Hayakawa, Y. (2007). Parasperm: morphological and functional studies on nonfertile sperm. Icthyological Research 54, 111-130.
100. Hayakawa, Y., Komaru, A. & Munehara, H. (2002). Ultrastructural observations of eu- and paraspermiogenesis in the cottid fish Hemilepidotus gilberti (Teleostei: Scorpaeniformes: Cottidae). Journal of Morphology 253, 243-254.
101. Hayashi, F. (1996). Insemination through an externally attached spermatophore: Bundled sperm and post-copulatory mate guarding by male fishflies (Megaloptera: Corydalidae). Journal of Insect Physiology 42, 859-866.
102. Hayashi, F. (1997). A trypsin-degradable protein agglutinates fishfly sperm-bundles. International Journal of Insect Morphology and Embryology 26, 63-66.
103. Hayashi, F. (1998). Sperm co-operation in the fishfly, Parachauliodes japonicus. Functional Ecology 12, 347-350.
104. Hayashi, F. & Kamimura, Y. (2002a). Sperm-bundles of Cicadomorpha insects (Homoptera). Natural Environmental Science Research 15, 9-15.
105. Hayashi, F. & Kamimura, Y. (2002b). The potential for incorporation of male derived proteins into developing eggs in the leafhopper Bothrogonia ferruginea. Journal of Insect Physiology 48, 153-159.
106. Healy, J. M. & Jamieson, B. G. M. (1981). An ultrastructural examination of developing and mature paraspermatozoa in Pyrazus ebeninus (Mollusca, Gastropoda, Potamididae). Zoomorphology 98, 101-119.
107. Healy, J. M. & Jamieson, B. G. M. (1993). Euspermatozoa, paraspermatozoa and spermatozeugmata of Littoraria (Palustorina) articulata (Prosobranchia: Caenogastropoda) with special reference to the Pseudotrich. Acta Zoologica 74, 321-330.
108. Heath, E., Meritt, D. A. & Jeyendran, R. S. (1987). Rouleaux formation by spermatozoa in the naked-tail armadillo, Cabassosus unicinctus. Journal of Reproductive Fertility 79, 153-159.
109. Hecht, N. B. (1998). Molecular mechanisms of male germ cell differentiation. BioEssays 20, 555-561.
110. Hodgson, A. N. (1997). Paraspermatogenesis in gastropod molluscs. Invertebrate Reproduction and Development 31, 31-38.
111. Hoekstra, R. F. (1984). Evolution of gamete motility differences. II. Interaction with the evolution of anisogamy. Journal of Theoretical Biology 107, 71-83.
112. Holman, L. & Snook, R. R. (2006). Spermicide, cryptic female choice and the evolution of sperm form and function. Journal of Evolutionary Biology 19, 1660-1670.
113. Humphries, S., Evans, J. P. & Simmons, L. W. (2008). Sperm competition: linking form to function. BMC Evolutionary Biology 8, 319.
114. Hunter, F. M. & Birkhead, T. R. (2002). Sperm viability and sperm competition in insects. Current Biology 12, 121-123.
115. Immler, S. (2008). Sperm competition and sperm cooperation: the potential role of diploid and haploid expression. Reproduction 135, 275-283.
116. Immler, S., Calhim, S. & Birkhead, T. R. (2008). Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62, 1538-1543.
117. Immler, S., Moore, H. D. M., Breed, W. G. & Birkhead, T. R. (2007). By hook or by crook? Morphometry, competition and cooperation in rodent sperm. PloS One 2, e170.
118. 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.
119. Jamieson, B. G. M. (1987). The ultrastructure and phylogeny of insect spermatozoa. Cambridge University Press, Cambridge.
120. Jamieson, B. G. M., Dallai, R. & Afzelius, B. A. (1999). Insects: their spermatozoa and phylogeny. Science Publishers, Inc., Enfield.
121. Jans, P., Benz, G. & Friedländer, M. (1984). Apyrene-spermatogenesis-inducing factor is present in the haemolymph of male and female pupae of the codling moth. Journal of Insect Physiology 30, 495-497.
122. Jespersen, Å., Kosuge, T. & Lützen, J. (2001). Sperm dimorphism and spermatozeugmata in the commensal bivavle Pseudopythina macrophthalmensis (Galeommatoidea, Kelliidae). Zoomorphology 120, 177-189.
123. Johnston, S. D., Smith, B., Pyne, M., Stenzel, D. & Holt, W. V. (2007). One-sided ejaculation of echidna sperm bundles. The American Naturalist 170, E162-E164.
124. Joly, D., Cariou, M. L. & Lachaise, D. (1991). Can sperm competition explain sperm polymorphism in Drosophila teissieri? Evolución Biológica 5, 25-44.
125. Joseph, S. B. & Kirkpatrick, M. (2004). Haploid selection in animals. Trends in Ecology and Evolution 19, 592-597.
126. Kawamura, N., Sahara, K. & Fugo, H. (2003). Glucose and ecdysteroid increase apyrene sperm production in in vitro cultivation of spermatocysts of Bombyx mori. Journal of Insect Physiology 49, 25-30.
127. Keller, L. (2002). Marsupial sperm pairing: a case of 'sticky' green beards? Trends in Ecology and Evolution 17, 113.
128. Keller, L & Reeve, H. K. (1995). Why do females mate with multiple males? The sexually selected sperm hypothesis. Advances in the Study of Behavior 24, 291-315.
129. Kim, E., Waters, S. H., Hake, L. E. & Hecht, N. B. (1989). Identification and developmental expression of smooth muscle gamma-actin in post-meiotic male germ cells of mice. Molecular and Cellular Biology 9, 1875-1881.
130. Kleene, K. C. (2001). A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mechanisms of Development 106, 3-23.
131. Kubo-Irie, M., Irie, M., Nakazawa, T. & Mohri, H. (2003). Ultrastructure and function of long and short sperm in Cicadidae (Hemiptera). Journal of Insect Physiology 49, 983-991.
132. Kura, T. & Nakashima, Y. (2000). Conditions for the evolution of soldier sperm classes. Evolution 54, 72-80.
133. Kurokawa, H. & Hihara, F. (1976). Number of first spermatocytes in relation to phylogeny of Drosophila (Diptera: Drosophilidae). International Journal of Insect Morphology and Embryology 5, 51-63.
134. LaMunyon, C. W. & Ward, S. (1999). Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proceedings of the Royal Society B: Biological Sciences 266, 263-267.
135. Lee, P. E. & Wilkes, A. (1965). Polymorphic spermatozoa in the hymenopterous wasp Dahlbominus. Science 147, 1445-1446.
136. Lehmann, L. & Keller, L. (2006). The evolution of cooperation and altruism - a general framework and a classification of models. Journal of Evolutionary Biology 19, 1365-1376.
137. L'Hernault, S. (2006). Spermatogenesis. In Wormbook (ed. T. C. E. R. Community ), pp. 1-14.
138. Lighthill, J. (1976). Flagellar hydrodynamics. SIAM Review 18, 161-230.
139. Lino-Neto, J., Dolder, H., Mancini, K., Mercati, D. & Dallai, R. (2008). The short spermatodesm of Arge pagana (Hymenoptera: Symphyta). Tissue & Cell 40, 185-193.
140. Lucas, A. (1971). Les gametes des mollusques. Haliotis 1, 185-214.
141. Lyon, M. F. (2003). Transmission ratio distortion in mice. Annual Review of Genetics 37, 393-408.
142. Lyttle, T. W. (1991). Segregation distorters. Annual Review of Genetics 25, 511-557.
143. Mable, B. K. & Otto, S. P. (1998). The evolution of life cycles with haploid and diploid phases. BioEssays 20, 453-462.
144. Machin, K. E. (1963). The control and synchronization of flagellar movement. Proceedings of the Royal Society of London B 158, 88-104.
145. Mackie, J. B. & Walker, M. H. (1974). A study of the conjugate sperm of the dytiscid water beetles Dytiscus marginalis and Colymbetes fuscus. Cell Tissue Research 148, 505-519.
146. Marotta, R., Melone, G., Bright, M. & Ferraguti, M. (2005). Spermatozoa and sperm aggregates in the Vestimentiferan Lamellibrachia luymesi compared with those Riftia pachyptila (Polychaeta: Siboglinidae: Vestimentifera). Biological Bulletin 209, 215-266.
147. Martan, J. & Shepherd, B. A. (1973). Spermatozoa in rouleaux in the female guinea pig genital tract. The Anatomical Record 175, 625-630.
148. Maynard Smith, J. & Szathmáry, E. (1995).The major transitions in evolution. W. H. Freeman and Company Limited, New York, NY.
149. Michalik, P. (2007). Spermatozoa and spermiogenesis of Liphistius cf. phuketensis (Mesothelae, Araneae, Arachnida) with notes on phylogenetic implications. Arthropod Structure & Development 36, 327-335.
150. Michalik, P., Dallai, R., Giusti, F. & Alberti, G. (2004). The ultrastructure of the peculia synspermia of some Dysderidae (Araneae, Arachnida). Tissue & Cell 36, 447-460.
151. Michod, R. E. (1999). Darwinian dynamics: evolutionary transitions in fitness and individuality. Princeton University Press, Princeton, New Jersey.
152. Michod, R. E. (2007). Evolution of individuality during transition from unicellular to multicellular life. Proceedings of the National Academy of Science 104, 8613-8618.
153. Michod, R. E. & Roze, D. (2001). Cooperation and conflict in the evolution of multicellularity. Heredity 81, 1-7.
154. Miller, G. T. & Pitnick, S. (2002). Sperm-female coevolution in Drosophila. Science 298, 1230-1233.
155. Miller, K. B. (2001). On the phylogeny of the Dytiscidae (Insecta: Coleoptera) with emphasis on the morphology of the female reproductive system. Insect Systematics & Evolution 31, 45-92.
156. Mèller, A. P. (1989). Ejaculate quality, testes size and sperm production in mammals. Functional Ecology 3, 91-96.
157. Montgomerie, R. & Fitzpatrick, J. L. (2008). Testes, sperm, and sperm competition. In Reproductive biology and phylogeny of fishes (ed. B. G. M. Jamieson ). Science Publishers, Enfield, NH.
158. Moore, H. D. (1996). Gamete biology of the New World marsupial, the grey short-tailed opossum, Monodelphis domestica. Reproduction, Fertility and Development 8, 605-615.
159. Moore, H. D., Dvořáková, K., Jenkins, N. & Breed, W. (2002). Exceptional sperm cooperation in the wood mouse. Nature 418, 174-177.
160. Moore, H. D., Martin, M. & Birkhead, T. R. (1999). No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proceedings of the Royal Society B: Biological Sciences 266, 2343-2350.
161. Moore, T. & Moore, H. D. (2002). Marsupial sperm pairing: A case of 'sticky' green beards? Trends in Ecology and Evolution 17, 112-113.
162. Moore, H. D. & 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.
163. Morrow, E. H. & Gage, M. J. G. (2001). Consistent significant variation between individual males in spermatozoal morphometry. Journal of Zoology, London 254, 147-153.
164. Mossman, J., Slate, J., Humphries, S. & Birkhead, T. R. (2009). Sperm morphology and velocity are genetically codetermined in the zebra finch. Evolution 63, 2730-2737.
165. Nishiwaki, S. (1964). Phylogenetic study on the type of the dimorphic spermatozoa in Prosobranchia. Sci. Rep Tokyo Kyouiku Daigaku Sect. B 11, 237-275.
166. Nowak, M. A. (2005). Five rules for the evolution of cooperation. Science 314, 1560-1563.
167. Nur, U. (1962). Sperms, sperm bundles and fertilization in a mealy bug, Pseudococcus obscurus Essig. (Homoptera: Coccidea). Journal of Morphology 111, 173-199.
168. Okasha, S. (2006). Evolution and the levels of selection. Oxford University Press Inc., New York.
169. Oppliger, A., Ribi, N.-G. & Hosken, D. J. (2003). Sperm length influences fertilization success during sperm competition in the snail Viviparus ater. Molecular Ecology 12, 485-492.
170. Parker, G. A. (1982). Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. Journal of Theoretical Biology 96, 281-294.
171. Parker, G. A. & Begon, M. E. (1993). Sperm competition games: sperm size and number under gametic control. Proceedings of the Royal Society B: Biological Sciences 253, 255-262.
172. Parker, G. A., Immler, S., Pitnick, S. & Birkhead, T. R. (2010). Sperm competition games: sperm size (mass) and number under raffle and displacement, and the evolution of P2. Journal of Theoretical Biology, in press.
173. Pattarini, J. M., Starmer, W. T., Bjork, A. & Pitnick, S. (2006). Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60, 2064-2080.
174. Pfeiffer, T. & Bonhoeffer, S. (2003). An evolutionary scenario for the transition to undifferentiated multicellularity. Proceedings of the National Academy of Science 100, 1095-1098.
175. Phillips, D. M. (1970). Ultrastructure of spermatozoa of the wooly opossum, Caluromys philander. Journal of Ultrastructure Research 33, 381-397.
176. Pitnick, S. (1996). Investment in testes and the cost of making long sperm in Drosophila. The American Naturalist 148, 57-90.
177. Pitnick, S., Dobler, R. & Hosken, D. J. (2009a). Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria. Proceedings of the Royal Society of London B 276, 4029-4034.
178. Pitnick, S., Hosken, D. J. & Birkhead, T. R. (2009b). Sperm Morphological Diversity. In Sperm biology, an evolutionary perspective (ed. T. R. Birkhead, D. J. Hosken and S. Pitnick ), pp. 69-149. Elsevier, London.
179. Pitnick, S., Markow, T. A. & Spicer, G. S. (1995). Delayed male maturity is a cost of producing large sperm in Drosophila. Proceedings of the National Academy of Science 92, 10614-10618.
180. Pitnick, S., Wolfner, M. F. & Suarez, S. S. (2009c). Ejaculate- and sperm-female interactions. In Sperm biology, an evolutionary perspective (ed. T. R. Birkhead, D. J. Hosken and S. Pitnick ), pp. 245-302. Elsevier, London.
181. Pizzari, T. & Foster, K. R. (2008). Sperm sociality: Cooperation, altruism, and spite. PLoS Biology 6, e130.
182. Pizzari, T. & Parker, G. A. (2009). Sperm competition and sperm phenotype. In Sperm biology, an evolutionary perspective (ed. T. R. Birkhead, D. J. Hosken and S. Pitnick ), pp. 205-244. Elsevier, London.
183. 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 B: Biological Sciences 266, 1041-1047.
184. 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.
185. Radwan, J. (1996). Intraspecific variation in sperm competition success in the bulb mite: a role of sperm size. Proceedings of the Royal Society B: Biological Sciences 263, 855-859.
186. Reger, J. F. & Cooper, D. P. (1968). Studies on the fine structure of spermatids and spermatozoa from the millipede Polydesmus sp. Journal of Ultrastructure Research 23, 60-70.
187. Ribera, I., Vogler, A. P. & Balke, M. (2008). Phylogeny and diversification of diving beetles (Coleoptera: Dytiscidae). Cladistics 23, 1-28.
188. Roldan, E. R. S., Gomendio, M. & Vitullo, A. D. (1992). The evolution of eutherian spermatozoa and underlying selective forces: female selection and sperm competition. Biological Reviews 67, 551-593.
189. Rouse, G. W. (2006). Annelid sperm and spermiogenesis. In Reproductive Biology and Phylogeny of Annelida (ed. G. W. Rouse and F. Pleijel ), pp. 45-76. Science Publishers, Inc., Enfield.
190. Rudolfsen, G., Figenschou, L., Folstad, I., Tveiten, H. & Figenschou, M. (2006). Rapid adjustments of sperm characteristics in relation to social status. Proceedings of the Royal Society of London B 273, 325-332.
191. Sahara, K. & Kawamura, N. (2004). Roles of actin networks in peristaltic squeezing of sperm bundles in Bombyx mori. Journal of Morphology 259, 1-6.
192. Sasakawa, K. (2007). Sperm bundle and reproductive organs of carabid beetles tribe Pterostichini (Coleoptera: Carabidae). Naturwissenschaften 94, 384-391.
193. Sasakawa, K. (2009). Marked sperm dimorphism in the ground beetle Scarites terricola: a novel type of insect sperm polymorphism. Physiological Entomology 34, 387-390.
194. Schärer, L., Da Lage, J.-L. & Joly, D. (2008). Evolution of testicular architecture in Drosophilidae: a role for sperm length. Evolutionary Biology 8, 143.
195. Scheltinga, D. M. & Jamieson, B. G. M. (2003). Spermatogenesis and the mature spermatozoon: Form, function and phylogenetic implications. In Reproductive Biology and Phylogeney of Anura (ed. B. G. M. Jamieson ), pp. 119-251. Science Publishers, Inc., Enfield.
196. Schiff, N., Flemming, A. J. & Quicke, D. L. J. (2001). Spermatodesmata of the sawflies (Hymenoptera: Symphyta): evidence for multiple increases in sperm bundle size. Journal of Hymenoptera Research 10, 119-125.
197. Schrader, F. (1945). Regular occurrence of heteroploidy in a group of Pentatomidae (Hemiptera). Biological Bulletin 88, 63-70.
198. Schrader, F. (1946a). Autosomal elimination and preferential segregation in the harlequin lobes of certain Discocephalini (Hemiptera). Biological Bulletin 90, 265-290.
199. Schrader, F. (1946b). The elimination of chromosomes in the meiotic divisions of Brachystethus rubromaculatus Dallas. Biological Bulletin 90, 19-31.
200. Schrader, F. (1960a). Cytological and evolutionary implications of aberrant chromosome behavior in the harlequin lobe of some Pentatomidae (Heteroptera). Chromosoma 11, 103-128.
201. Schrader, F. (1960b). Evolutionary aspects of aberrant meiosis in some Pentatominae (Heteroptera). Evolution 14, 498-508.
202. Schrader, F. & Leuchtenberger, C. (1951). The cytology and chemical nature of some constituents of the developing sperm. Chromosoma 4, 404-428.
203. Selenka, E. (1887). Studien über Entwicklelungsgeschichte. Ver Heft das Opossum (Didelphys virginiana). C. W. Kriedels, Verlag, Wiesbaden.
204. Shepherd, B. A. & Martan, J. (1979). Morphology and fertility of guinea-pig spermatozoa aged in vivo. Archives of Andrology 2, 53-58.
205. Silberglied, R. E., Shepherd, J. G. & Dickinson, J. L. (1984). Eunuchs: the role of apyrene sperm in Lepidoptera. The American Naturalist 123, 255-265.
206. Sivinski, J. (1984). Sperm in Competition. In Sperm Competition and Evolution of Animal Mating Systems (ed. R. L. Smith ), pp. 85-115. Academic Press, London.
207. Snook, R. R. (2005). Sperm in competition: not playing by the numbers. Trends in Ecology and Evolution 20, 46-53.
208. Snook, R. R. & Karr, T. L. (1998). Only long sperm are fertilization-competent in six sperm-heteromorphic Drosophila species. Current Biology 8, 291-294.
209. Snook, R. R., Markow, T. A. & Karr, T. L. (1994). Functional nonequivalence of sperm in Drosophila pseudoobscura. Proceedings of the National Academy of Science 91, 11222-11226.
210. Sonnenschein, M. & Häuser, C. L. (1990). Presence of only eupyrene spermatozoa in adult males of the genus Micropterix hübner and its phylogenetic significance (Lepidoptera: Zeugloptera, Micropterigidae). International Journal of Insect Morphology and Embryology 19, 269-276.
211. Swallow, J. G. & Wilkinson, G. S. (2002). The long and short of sperm polymorphisms in insects. Biological Reviews 77, 153-182.
212. Taggart, D. A., Johnson, J. L., O'Brien, H. P. & Moore, H. D. M. (1993). Why do spermatozoa of American Marsupials form pairs? A clue from the analysis of sperm-pairing in the epididymis of the Grey Short-Tailed Opossum, Monodelphis domestica. The Anatomical Record 236, 465-478.
213. Takami, Y. & Sota, T. (2007). Sperm competition promotes diversity of sperm bundles in Ohomopterus ground beetles. Naturwissenschaften 94, 543-550.
214. Taylor, D. R. & Ingvarsson, P. K. (2003). Common features of segregation distortion in plants and animals. Genetica 117, 27-35.
215. Taylor, G. (1951). Analysis of the swimming of microscopic organisms. Proceedings of the Royal Society A: Mathematical and Physical Sciences 209, 447-461.
216. Temkin, M. H. (1994). Gamete spawning and fertilization in the gymnolaemate bryozoan Membranipora membranacea. Biological Bulletin 187, 143-155.
217. Temkin, M. H. & Bortolami, S. B. (2004). Waveform dynamics of spermatozeugmata during transfer from paternal to maternal individuals of Membranipora membranacea. Biological Bulletin 206, 35-45.
218. Temple-Smith, P. D., & Bedford, J. M. (1980). Sperm maturation and the formation of sperm pairs in the epididiymis of the opossum, Didelphis virginiana. The Journal of Experimental Zoology 214, 161-171.
219. Till-Bottraud, I., Joly, D., LaChaise, D. & Snook, R. R. (2005). Pollen and sperm heteromorphism: convergence across kingdoms? Journal of Evolutionary Biology 18, 1-18.
220. Trivers, R. L. (1971). The evolution of reciprocal altruism. The Quarterly Review of Biology 46, 35-57.
221. Turner, R. M. (2006). Moving to the beat: a review of mammalian sperm motility regulation. Reproduction, Fertility and Development 18, 25-38.
222. Vacquier, V. D. (1998). Evolution of gamete recognition proteins. Science 281, 1995-1998.
223. Véron, N., Bauer, H., Weisse, A. Y., Lüder, G., Werber, M., & Herrmann, B. G. (2009). Retention of gene products in syncytial spermatids promotes non-Mendelian inheritance as revealed by the t complex responder. Genes & Development 23, 2705-2710.
224. Virkki, N. (1969). Sperm bundles and phylogenies. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 101, 13-27.
225. Virkki, N. (1973). Evolution of sperm cell number per bundle in insects. Anales de la Escuela Nacional de Ciencias Bioloigcas (Mexico) 20, 23-34.
226. Viscuso, R., Brundo, M. V. & Sottile, L. (2002). Mode of transfer of spermatozoa in Orthoptera Tettigoniidae. Tissue & Cell 34, 337-348.
227. Viscuso, R., Narcisi, L., Sottile, L. & Barone, N. (1998). Structure of spermatodesms of Orthoptera Tettigonioidea. Tissue & Cell 30, 453-463.
228. von Nordheim, H. (1989). Vergleichende ultrastukturuntersuchungenader eu- und paraspermien von 13 Protodrilus arten (Polychaeta, Annelida) und ihre taxonomische und phylogenetische Bedeutung. Helgoländer wissenschaftliche Meeresuntersuchungen 43, 113-156.
229. von Siebold, C. T. (1836). Fernere beobachtungen über die spermatozoen der tiere. 2. Die spermatozoen der Paludina vivipara. Arch. Anat. Physiol. Wiss. Med 1, 232-255.
230. Ward, P. I. (1998). Intraspecific variation in sperm size characters. Heredity 80, 655-659.
231. Wakimoto, B. T., Lindsley, D. L. & Herrera, C. (2004). Towards a comprehensive genetic analysis of male fertility in Drosophila melanogaster. Genetics 167, 207-216.
232. Weigmann, B. M., Regier, J. C. & Mitter, C. (2002). Combined molecular and morphological evidence on the phylogeny of the lepidopteran lineages. Zoologica Scripta 31.
233. Werner, G. (1976). Entwicklung und bau der doppelspermien bei den Dytisciden Acilius sulcatus L., Dytiscus marginalis L. und Hydaticus transversalis Pont. (Coleoptera). Zoomorphologie 83, 49-87.
234. Werner, G. (1983). The joint seprmatozoa of Dytiscidae. 4th International Symposium on Spermatology, 1982, 167-170.
235. White-Cooper, H., Doggett, K. & Ellis, R. E. (2009). The evolution of spermatogenesis. In Sperm biology, an evolutionary perspective (ed. T. R. Birkhead, D. J. Hosken and S. Pitnick ), pp. 151-182. Elsevier, London.
236. Woolley, D. M., Crockett, R. F., Groom, W. D. I. & Revell, S. G. (2009). A study of synchronisation between the flagella of bull spermatozoa, with related observations. The Journal of Experimental Biology 212, 2215-2223.
237. Woodard, T. M. (1940). The function of the apyrene spermatozoa of Goniobasis laqueata (Say). Journal of Experimental Zoology 85, 103-123.
238. Wu, X.-M., Song, D.-X. & Chen, D.-Y. (1997). Ultrastructure of spermatozoa and spermatogenesis in wolf spider Pardosa astrigera (Araneae: Lycosidae). Acta Zoologica Sinica.
239. Wygodzinsk, P. (1958). Beobachtungen an spermatolophiden und spermatophoren bei Nicoletiidae (Thysanura, Insecta). Zoologischer Anzeiger 161, 280-287.
240. Xu, X., Toselli, P. A., Russell, L. D. & Seldin, D. C. (1999). Globozoopermia in mice lacking the subunit casein α' kinase II catalytic subunit. Nature Genetics 23, 118-121.
241. Yang, Y., Elgeti, J. & Gompper, G. (2008). Cooperation of sperm in two dimensions: synchronization, attraction, and aggregation through hydrodynamic interactions. Physical Review E 78, 061903.
242. Zheng, Y., Deng, X. & Martin-DeLeon, P. A. (2001a). Lack of sharing of Spam1 (Ph-20) among mouse spermatids and transmission ratio distortion. Biology of Reproduction 64, 1740-1738.
243. Zheng, Y., Deng, X., Zhao, Y., Zhang, H. & Martin-DeLeon, P. A. (2001b). Spam1 (PH-20) mutations and sperm dysfunction in mice with the Rb(6.16) or Rb(6.15) translocation Mammalian Genome 12, 822-829.