The spermatozoon of eurasian murine rodents: Its morphological diversity and evolution

Journal of Morphology

Volumn 261, Issue 1, 2004, Pages 52-69

  Breed, William G ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Morphology; Murine rodents; Sperm head

Indexed keywords

ANIMAL; ARTICLE; ASIA; COMPARATIVE STUDY; EUROPE; EVOLUTION; HISTOLOGY; MALE; PHYLOGENY; RODENT; SCANNING ELECTRON MICROSCOPY; SPERMATOZOON; SPERMATOZOON TAIL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; ASIA; EUROPE; EVOLUTION; MALE; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; PHYLOGENY; RODENTIA; SPERM HEAD; SPERM TAIL;

APODEMUS; BANDICOTA; MAMMALIA; MICROMYS; MURINAE; RODENTIA; TOKUDAIA;

EID: 3142613683     PISSN: 03622525     EISSN: None     Source Type: Journal    
DOI: 10.1002/jmor.10228     Document Type: Article

References (65)

1. Aplin KP, Chesser T, Ten Have J. 2003. Evolutionary biology of the genus Rattus: profile of an archetypal rodent pest. In: Singleton GR, Hinds LA, Krebs CJ, Spratt DM, editors. Rats, mice and people: rodent biology and management. Canberra: Australian Centre for International Agricultural Research Monograph No 96. p 487-498.
2. Baskevich MI, Lavrenchenko LA. 1995. On the morphology of spermatozoa in some African murines (Rodentia, Muridae): the taxonomic and phylogenetic aspects. J Zool Syst Evol Res 33:9-16.
3. Bedford JM. 1996. What marsupial gametes disclose about gamete function in eutherian mammals. Reprod Fertil Dev 8:569-580.
4. Bedford JM, Hoskins DD. 1990. The spermatozoon: morphology, physiology, and biochemistry. In: Lamming GE, editor. Marshall's physiology of reproduction. The male reproductive system, vol. 2. London: Churchill Livingstone. p 379-568.
5. Bishop MWH, Austin CR. 1957. Mammalian spermatozoa. Endeavour 16:137-150.
6. Bishop MWH, Walton A. 1960. Spermatogenesis and the structure of mammalian spermatozoa. In: Parkes AS, editor. Marshall's physiology of reproduction, vol. 1, 3rd ed. London: Longmans. p 1-129.
7. Breed WG. 1984. Sperm head structure in the Hydromyinae (Rodentia: Muridae): a further evolutionary development of the subacrosomal space in mammals. Gamete Res 10:31-44.
8. Breed WG. 1993. Novel organization of the spermatozoon in two species of murid rodents from southern Asia. J Reprod Fertil 99:149-158.
9. Breed WG. 1995a. Spermatozoa of murid rodents from Africa: morphological diversity and evolutionary trends. J Zool (Lond) 237:625-651.
10. Breed WG. 1995b. Variation in sperm head morphology of muroid rodents of Africa: phylogenetic implications. In: Jamieson BMG, Ausio J, Justine J-L, editors. Advances in spermatozoal phylogeny and taxonomy. Mem Mus Natn Hist Nat 166:409-420.
11. Breed WG. 1997. Evolution of the spermatozoon in Australasian rodents. Aust J Zool 45:459-478.
12. Breed WG. 1998. Interspecific variation in structural organization of the spermatozoon in the Asian Bandicoot rats, Bandicota species. Acta Zool 79:277-284.
13. Breed WG. 2002. Variation in sperm form in rats and mice (subfamily Murinae). In: Van der Horst G, Franken D, Bornman R, DeJager T, Dyer S, editors. Proceedings of the 9th International Symposium on Spermatology. Bologna, Italy: Monduzzi. p 269-274.
14. Breed WG, Aplin K. 1994. Sperm morphology of murid rodents from New Guinea and the Solomon Islands: phylogenetic implications. Aust J Zool 43:17-30.
15. Breed WG, Leigh CM. 1991. Distribution of filamentous actin in and around spermatids and in spermatozoa of Australian conilurine rodents. Mol Reprod Dev30:369-384.
16. Breed WG, Musser GG. 1991. Sulawesi and Philippine rodents (Muridae); a survey of spermatozoal morphology and its significance for phylogenetic inference. Am Mus Novit 3003:1-15.
17. Breed WG, Sarafis V. 1979. On the phylogenetic significance of spermatozoal morphology and male reproductive tract anatomy in Australian rodents. Trans R Soc SA 103:127-139.
18. Breed WG, Taylor J. 2000. Body mass, testes mass, and sperm size in murine rodents. J Mammal 81:758-768.
19. Breed WG, Yong HS. 1986. Sperm morphology of murid rodents from Malaysia and its possible phylogenetic significance. Am Mus Novit 2856:1-12.
20. Breed WG, Idriss D, Oko RJ. 2000. Protein composition of the ventral processes on the sperm head of Australian hydromyine rodents. Biol Reprod 63:629-634.
21. Chevret P, Denys C, Jaeger J-J, Michaeux J, Catzeflis FM. 1993. Molecular evidence that the spiny mouse (Acomys) is more closely related to gerbils (Gerbillinae) than to true mice (Murinae). Proc Natl Acad Sci USA 90:3433-3436.
22. Clermont Y, Einberg E, Le Blond CP, Wagner S. 1955. The perforatorium - an extension of the nuclear membrane of the rat spermatozoa. Anat Rec 121:1-12.
23. Cummins JM, Woodall PF. 1985. On mammalian sperm dimensions. J Reprod Fertil 75:153-175.
24. Denys C, Michaux J, Petter F, Aguilar JP, Jaeger J-J. 1992. Molar morphology as a clue to the phylogenetic relationship of Acomys to the Murinae. Israel J Zool 38:253-262.
25. Dooher GB, Bennett D 1977. Spermiogenesis and spermatozoa in sterile mice carrying different lethal T/t locus haplotypes: a transmission and scanning electron microscopic study. Biol Rep 17:268-288.
26. Downing KF, Musser GG, Park LE. 1998. The first fossil record of small mammals from Sulawesi, Indonesia: the large murid, Paruromys dominator, from the late (?)Pliocene walanae formation. In: Tomida Y, Flynn LJ, Jacobs LL, editors. Advances in vertebrate palaeontology and geochronology. Tokyo: National Science Museum Monograph 14. p 105-121.
27. Dubois J-YF, Catzeflis FM, Bernstein JJ. 1999. The phylogenetic position of "Acomyinae" (Rodentia, Mammalia) as a sister group of a Murinae + Gerbillinae clade: evidence from the ribonuclease gene. Mol Phylogenet Evol 13:181-192.
28. Eddy EM, O'Brien DA. 1994. The spermatozoon. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York: Raven Press. p 29-77.
29. Fawcett DW. 1970. A comparative view of sperm ultrastructure. Biol Reprod (Suppl) 2:90-127.
30. Fawcett DW. 1975. The mammalian spermatozoon. Dev Biol 44:394-436.
31. Fawcett DW, Anderson WA, Phillips PM. 1971. Morphogenetic factors influencing the shape of the sperm head. Dev Biol 28:220-251.
32. Flaherty SP, Breed WG. 1983. The sperm head of the plains mouse Pseudomys australis: ultrastructure and effects of chemical agents. Gamete Res 8:231-244.
33. Friend GF. 1936. The sperms of British Muridae. Q J Microsc Sci 78:419-443.
34. Furano AV, Haywood BE, Chevret P, Catzeflis F, Usdin K. 1994. Amplification of the ancient murine Lx family of long interspersed repeated DNA occurred during the murine radiation. J Mol Evol 38:18-27.
35. Gadi IK, Sharma T. 1983. Cytogenetic relationships in Rattus, Cremnomys, Millardia, Nesokia and Bandicota (Rodentia: Muridae). Genetica 61:21-40.
36. Gordon DH, Watson CRB. 1986. Identification of cryptic species of rodents Mastomys, Aethomys and Saccostomus in the Kruger National Park. S Afr J Zool 21:95-99.
37. Jacobs LL. 1978. Fossil rodents (Rhizomyidae and Muridae) from Neogene Siwalik deposits, Pakistan. Mus N Arizona Bull 52:1-103.
38. Jaeger J-J, Tong H, Denys L. 1986. Age de la divergence Mus-Rattus: comparison des données paléontologiques et moléculaires. CR Acad Sci (Paris) 302:917-922.
39. Lalli M, Clermont Y. 1981. Structural changes of the head components of the rat spermatid during spermiogenesis. Am J Anat 160:419-434.
40. Martin Y, Gerlach G, Schlöttever C, Meyer A. 2000. Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Mol Phylogenet Evol 16:37-47.
41. Michaux J, Catzeflis F. 2000. The bushlike radiation of muroid rodents is exemplified by the molecular phylogeny of the LCAT nuclear gene. Mol Phylogenet Evol 17:280-293.
42. Michaux J, Reyes A, Catzeflis F. 2001. Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Mol Biol Evol 18:2017-2031.
43. Michaux JR, Chevret P, Filippucci M-G, Macholan M. 2002. Phylogeny of the genus Apodemus with special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol Phylogenet Evol 23:123-136.
44. Moore H, Dvorakova K, Jenkins N, Breed W. 2002. Exceptional sperm cooperation in the wood mouse. Nature 418:174-177.
45. Musser GG, Brothers EM. 1994. Identification of bandicoot rats from Thailand (Bandicota, Muridae, Rodentia). Am Mus Novit 3110:1-55.
46. Musser GG, Carleton MD. 1993. Family Muridae. In: Wilson DE, Reeder DM, editors. Mammal species of the world, 2nd ed. Washington, DC: Smithsonian Institution Press. p 510-755.
47. Musser GG, Newcomb C. 1983. Malaysian murids and the giant rat of Sumatra. Bull Am Mus Nat Hist 174:327-598.
48. Oko R, Clermont Y. 1988. Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol Reprod 39:673-687.
49. Oko R, Moussakova L, Clermont Y. 1990. Regional differences in composition of the perforatorium and outer periacrosomal layer of the rat spermatozoon as revealed by immunocytochemistry. Am J Anat 188:641-673.
50. Pascale E, Valle E, Furano AV. 1990. Amplification of an ancestral mammalian L1 family of long interspersed repeated DNA occurred just before the murine radiation. Proc Natl Acad Sci USA 87:9481-9485.
51. Piko L. 1969. Gamete structure and sperm entry in mammals. In: Metz CB, Monroy A, editors. Fertilization. New York: Academic Press. p 325-403.
52. Radtke M, Niethammer J. 1984. Zur Stellung der Pestratte (Nesokia indica) im System der Murinae. Saug Mitt 32:13-16.
53. Retzius G. 1909. Spermien der Nagetiere. Biol Untersuchungen NF 14:133-162.
54. Robinson M, Catzeflis F, Briolay J, Mouchiroud D. 1997. Molecular phylogeny of rodents, with special emphasis on murids: evidence from nuclear gene LCAT. Mol Phylogenet Evol 8:423-434.
55. Roldan ERS, Gomendio M, Vitullo AD. 1992. The evolution of eutherian spermatozoa and underlying selective forces: female selection and sperm competition. Biol Rev 67:551-593.
56. Ruedas LA, Kirsch JAW. 1997. Systematics of Maxomys Sody, 1936 (Rodentia: Muridae: Murinae): DNA/DNA hybridization studies of some Borneo-Javan species and allied Sundaic and Australo-Papuan genera. Biol J Linn Soc 61:385-408.
57. Serizawa K, Suzuki H, Tsuchiya K. 2000. A phylogenetic view on species radiation in Apodemus inferred from variation of nuclear and mitochondrial genes. Biochem Genet 38:27-39.
58. Stefanini M, Oura C, Zamboni L. 1969. Ultrastructure of fertilization in the mouse. 2. Penetration of sperm into the ovum. J Submicrosc Cytol 1:1-23.
59. Suzuki H, Tsuchiya K, Takezaki N. 2000. A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata. Mol Phylogenet Evol 15:15-24.
60. Verneau O, Catzeflis F, Furano AV. 1997. Determination of the evolutionary relationships in Rattus sensa lato (Rodentia: Muridae) using L1 (LINE-1) amplification events. J Mol Evol 45:424-436.
61. Visser DS, Robinson TJ. 1987. Systematic implications of spermatozoan and bacular morphology for the South African Aethomys. Mammalia 51:447-454.
62. Watts CHS, Baverstock PR. 1994. Evolution in some Southeast Asian Murinae (Rodentia), as assessed by microcomplement fixation of albumin, and their relationship to Australian Murines. Aust J Zool 42:711-722.
63. Watts CHS, Baverstock PR. 1995. Evolution of the Murinae (Rodentia) as assessed by microcomplement fixation of albumen. Aust J Zool 43:105-118.
64. Yanagimachi R. 1994. Mammalian fertilization. In: Knobil E, Neill JD, editors. The physiology of reproduction, 2nd ed. New York: Raven Press. p 189-317.
65. Yang BG, Jeong HD, Koh HS. 1991. Sperm morphology of two species of the genus Apodemus (Rodentia, Mammalia) in Korea. Korean J Zool 34:59-63.