Novelties of conception in insectivorous mammals (Lipotyphla), particularly shrews

Biological Reviews of the Cambridge Philosophical Society

Volumn 79, Issue 4, 2004, Pages 891-909

  Bedford, J Michael ^a   Mock, Orin B ^b   Goodman, Steven M ^c  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b A T STILL UNIVERSITY   (United States)

^c FIELD MUSEUM OF NATURAL HISTORY   (United States)

Author keywords

Cumulus oophorus; Fallopian tube; Fertilisation; Gametes; Golden moles; Hedgehogs; Insectivora; Lipotyphla; Moles; Penis; Reproductive tract; Shrews; Tenrecs

Indexed keywords

CUMULUS OOPHORUS; EVOLUTION; FERTILIZATION; GAMETE; GOLDEN MOLE; HEDGEHOG; HUMAN VERSUS ANIMAL COMPARISON; INSECT GENETICS; INSECTIVORE; LIPOTYPHLA; MAMMAL; MITOCHONDRIAL GENETICS; MOLE RAT; NONHUMAN; PENIS; PHYLOGENY; REPRODUCTION; REVIEW; SPECIES COMPARISON; SPERMATOZOON; TAXONOMY;

ANIMALS; FEMALE; GENITALIA, FEMALE; GENITALIA, MALE; INSECTIVORA; MALE; PHYLOGENY; REPRODUCTION; SHREWS; SPERM-OVUM INTERACTIONS;

ANIMALIA; CHRYSOCHLORIDAE; ELEPHANT; ERINACEIDAE; EUTHERIA; FALLOPIA; INSECTA; INSECTIVORA; MACROSCELIDEA; MAMMALIA; MYOSOREX; MYOSOREX VARIUS; SORICIDAE; TENRECIDAE; VERTEBRATA;

EID: 9644300907     PISSN: 14647931     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1464793104006529     Document Type: Review

References (96)

1. ALLANSON, M. (1934). The reproductive processes of certain mammals. VII - Seasonal variation in the reproductive organs of the male hedgehog. Philosophical Transactions of the Royal Society, London B 223, 277-303.
2. ARNASON, U., ADEGOKE, J. A., BODIN, K., BORN, E. W., ESA, Y. B., GULLBERG, A., NILSSON, M., SHORT, R. V., XU, X. & JANKE, A. (2002). Mammalian mitogenic relationships and the root of the eutherian tree. Proceedings of the National Academy of Sciences, U.S.A. 99, 8151-8156.
3. ASDELL, S. A. (1966). Evolutionary trends in physiology of reproduction. In Comparative Biology of Reproduction in Mammals (ed. I. W. Rowlands). Symposia of the geological Society of London 15, pp. 1-13. Academic Press, London.
4. ASHER, R. J. (1999). A morphological basis for assessing the phylogeny of the "Tenrecoidea" (Mammalia, Lipotyphla). Cladistics 15, 231-251.
5. ASHER, R. J. (2003). Phylogenetics of the Tenrecidae (Mammalia): a response to Douady et al., 2002. Molecular Phylogenetics and Evolution 26, 328-330.
6. BEDFORD, J. M. (1974). Biology of primate spermatozoa. In Contributions to Primatology 3. (ed. W. P. Euckett), pp. 97-141. S. Karger, Basel.
7. BEDFORD, J. M. (2004). The enigmas of mammalian gamete form and function. Biological Reviews 79, 429-460.
8. BEDFORD, J. M., BERNARD, R. T. F. & BAXTER, R. M. (1998). The 'hybrid' character of the gametes and reproductive tracts of the African shrew, Myosorex varius, supports its classification in the Crocidosoricinae. Journal of Reproduction and Fertility 112, 165-173.
9. BEDFORD, J. M., BERRIOS, M. & DRYDEN, G. L. (1982). Biology of the scrotum. IV. Testis location and temperature sensitivity. The Journal of Experimental Zoology 224, 379-388.
10. BEDFORD, J. M., COOPER, G. W., PHILLIPS, D. M. & DRYDEN, G. L. (1994). Distinctive features of the gametes and reproductive tracts of the Asian Musk Shrew, Suncus murinus. Biology of Reproduction 50, 820-834.
11. BEDFORD, J. M., MOCK, O. B., NAGDAS, S. K., WINFREY, V. P. & OLSON, G. E. (1999). Reproductive features of the eastern mole (Scalopus aquaticus) and star nose mole (Condylura cristata). Journal of Reproduction and Fertility 117, 345-353.
12. BEDFORD, J. M., MOCK, O. B., NAGDAS, S. K., WINFREY, V. P. & OLSON, G. E. (2000). Reproductive characteristics of the African pygmy hedgehog. Atelerix albiventris. Journal of Reproduction and Fertility 120, 143-150.
13. BEDFORD, J. M., MOCK, O. B. & PHILLIPS, D. M. (1997 a). Unusual ampullary sperm crypts, and behavior and role of the cumulus oophorus, in the oviduct of the Least Shrew, Cryptotis parva. Biology of Reproduction 56, 1255-1267.
14. BEDFORD, J. M., MŌRI, T. & ODA, S. (1997A). Ovulation induction and gamete transport in the female tract of the musk shrew, Suncus murinus. Journal of Reproduction and Fertility 110, 115-125.
15. BEDFORD, J. M., MŌRI, T. & ODA, S. (1997 c). The unusual state of the cumulus oophorus and of sperm behavior within it, in the musk shrew, Suncus murinus. Journal of Reproduction and Fertility 110, 127-134.
16. BEDFORD, J. M., PHILLIPS, D. M. & MOVER-LEV, H. (1997 d). Novel sperm crypts and behavior of gametes in the Fallopian tube of the white-toothed shrew, Crocidura russula monacha. The Journal of Experimental Zoology 277, 262-273.
17. BEDFORD, J. M., RODGER, J. C. & BREED, W. G. (1984). Why so many mammalian spermatozoa - a clue from marsupials. Proceedings of the Royal Society of London B 221, 221-233.
18. BLUNTSCHLI, H. (1938). Le développement primaire et l'implantation chez un Centetine (Hemicentetes). Comptes Rendu Séances Association Anatomique 33, 39-46.
19. BUTLER, P. M. (1988). Phylogeny of the insectivores. In The Phylogeny and Classification of the Tetrapods. Vol. 2. Mammals (ed. M. J. Benton), pp. 117-141. Clarendon Press, Oxford.
20. CARTER, A. M. (2001). Evolution ofthe placenta and fetal membranes seen in the light of molecular phylogenetics. Placenta 22, 800-807.
21. CASTLE, P. E. (2002). Could multiple low-affinity bonds mediate primary sperm-zona pellucida binding? Reproduction 124, 29-32.
22. COOPER, G. W. & BEDFORD, J. M. (1976). Asymmetry of spermiation and sperm surface charge patterns over the giant acrosome in the musk shrew, Suncus murinus. Journal of Cell Biology 69, 415-428.
23. DANNELID, E. (1991). The genus Sorex (Mammalia, Soricidae) - distribution and evolutionary aspects of Eurasian species. Mammal Review 21, 1-20.
24. DEANESELY, R. (1934). The reproductive processes of certain mammals VI. The reproductive cycle of the female hedgehog. Philosophical Transactions of the Royal Society B 223, 239-276.
25. DEKEL, N. & PHILLIPS, D.M. (1979). Maturation of rat cumulus oophorus - a scanning electron microscope study. Biology of Reproduction 21, 9-18.
26. DOBSON, G. E. (1882). A Monograph of the Insectivora. Systematic and Anatomical. J. van Voorst, London.
27. DOUADY, C. J., CHATELIER, P. I., MADSEN, O., DE JONG, W. W., CATZEFLIS, F., SPRINGER, M. S. & STANHOPE, M. J. (2002). Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as a sister group to shrews. Molecular Phylogenetics and Evolution 25, 200-209.
28. DOUADY, C. J., SCALLY, M., SPRINGER, M. S. & STANHOPE, M. J. (2004). "Lipotyphlan" phylogeny based on the growth hormone receptor gene: a reanalysis. Molecular Phylogenetics and Evolution 30, 778-788.
29. DRYDEN, G. L. (1969). Reproduction in Suncus murinus. Journal of Reproduction and Fertility Supplement 6, 377-396.
30. EADIE, W. R. (1948). The male accessory reproductive glands of Condylura with notes on a unique prostatic secretion. Anatomical Record 101, 59-71.
31. ECKSTEIN, P. & ZUCKERMAN, S. (1956). Morphology ofthe reproductive tract. In Marshall's Physiology of Reproduction. Vol. I. Part One (ed. A. S. Parkes), pp. 41-153. Longmans, London.
32. EISENBERG, J. E. (1981). The Mammalian Radiations. The University of Chicago Press, Chicago.
33. EPPIG, J. J. (1979). FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature London 281, 483-484.
34. FAWCETT, D.W. & PHILLIPS, D.M. (1969). Observations on the release of spermatozoa and on changes in the head during passage through the epididymis. Journal of Reproduction and Fertility Supplement 6, 405-418.
35. FORESMAN, K. R. & BADYAEV, A. V. (2004). Development instability and the environment: why are some species better indicators of stress than others? In International Colloquium on the Biology of the Soricidae II (eds. J. F. Merritt, S. Churchfield, R. Hutterer and B. I. Sheftel). Pittsburgh: Carnegie Museum of Natural History Special Publication - in press.
36. GOODMAN, S. M., GANZHORN, J. U. & RAKOTONDRAVONY, D. (2003). Introduction to the mammals. In Natural History of Madagascar (eds. S. M. Goodman and J. P. Benstead), pp. 1159-1186. The University of Chicago Press, Chicago, IL.
37. GREEN, J. A. & DRYDEN, G. L. (1976). Ultrastructure of epididymal spermatozoa of the Asiatic Musk Shrew, Suncus murinus. Biology of Reproduction 14, 327-331.
38. HAYSSEN, V., VAN TIENHOVEN, A. & VAN TIENHOVEN, A. (1993). Asdell's Patterns of Mammalian Reproduction: A Compendium of Species-Specific Data. Cornell University Press, Ithaca, NY.
39. HEIM DE BALSAC, H. & LAMOTTE, M. (1957). Evolution et phylogénie des Soricidés africains - II. Mammalia 21, 16-46.
40. HUNTER, R. H. F. (1995a). Ovarian endocrine control of sperm progression in the Fallopian tubes. Oxford Reviews of Reproductive Biology 17, 85-124.
41. HUNTER, R. H. F. (19956). Significance of the epithelial crypts at the bovine uterotubal junction in the preovulatory phase of sperm regulation. Acta Vetennaria Scandinavica 36, 413-421.
42. HUTTERER, R. (1993). Order Insectivora. In Mammal Species of the World: A Taxonomic and Geographic Reference (eds. D. E. Wilson and D. M. Reeder), pp. 69-130. Smithsonian Institution Press. Washington, D.C.
43. KANEKO, T., IIDA, H., BEDFORD, J. M. & MORI, T. (2001). Spermatozoa of the shrew, Suncus murinus, undergo the acrosome reaction and then selectively kill cells in penetrating the cumulus oophorus. Biology of Reproduction 65, 544-553.
44. KANEKO, T., IIDA, H., BEDFORD, J. M., ODA, S. & MŌRI, T. (2003). Mating-induced cumulus-oocyte maturation in the shrew, Suncus murinus. Reproduction 126, 817-826.
45. KOWALSKA-DYRCZ, A. (1966). A comparative study of the male genital tract in some species of shrews. Acta Theriologica 11, 71-127.
46. KRETZOI, M. (1965). Drepanosorex - neu definiert. Vertebrata Hungarica 7, 117-129.
47. LUCKETT, W. P. (1980). The use of reproductive and developmental features in assessing tupaiid affinities. In Comparative Biology and Evolutionary Relationships of Tree Shrews (ed. W. P. Luckett), pp. 245-266. Plenum Press, New York.
48. LUCKETT, W. P. (1993). Uses and limitations of mammalian fetal membranes and placenta for phylogenetic reconstruction. The Journal of Experimental Zoology 266, 514-527.
49. LUCKETT, W. P. & HARTENBERGER, J.-L. (1993). Monophyly or polyphyly of the order rodentia: possible conflict between morphological and molecular interpretations. Journal of Mammalian Evolution 1, 127-147.
50. MACPHEE, R. D. E. & NOVACEK, M. J. (1993). Definition and relationships of Lipotyphla. In Mammal Phylogeny, Vol. 2 : Placentals (eds. F. Szalay, M. J. Novacek and M. C. McKenna), pp. 13-31. Springer-Verlag, New York.
51. MADDALENA, T. & BRONNER, G. (1992). Biochemical systematics of the endemic African genus Myosorex Gray, 1838 (Mammalia, Soricidae). Israel Journal of Zoology 38, 245-252.
52. MADSEN, O., SCALLY, M., DOUADY, C. J., DEBRY, R. W., ADKINS, R., AMRINE, H. M., STANHOPE, M. J., DE JONG, W. W. & SPRINGER, M. S. (2001). Parallel adaptive radiations in major clades of placental mammals. Nature London 409, 610-614.
53. MATTHEWS, L. H. (1935). The oestrous cycle and intersexuality in the female mole (Talpa eunpea Linn.). Proceedings of the geological Society of London Series 2 1935, 347-383.
54. MILLIGAN, S. R. (1982). Induced ovulation in mammals. Oxford Reviews of Reproductive Biologv 4, 1-46.
55. MŌRI, T., ARAI, S., SHIRAISHI, S. & UCHIDA, T. A. (1991). Ultrastructural observations on spermatozoa of the Soricidae, with special attention to a sub-family revision of the Japanese water shrew Chimarrogale himalayica. Journal of the Mammalogical Society of Japan 16, 1-12.
56. MOSSMAN, H. & DUKE, K. L. (1973). Comparative Morphology of the Mammalian Ovary. University of Wisconsin Press, Madison, Wisconsin.
57. NICOLL, M. E. (1982). Reproductive Ecology of Tenrec ecaudatus (Insectivora: Tenrecidae) in the Seychelles. Ph.D. thesis, University of Aberdeen, Scotland.
58. NICOLL, M. E. & RACEY, P.A. (1985). Follicular development, ovulation, fertilization and fetal development in tenrecs (Tenrec ecaudatus). Journal of Reproduction and Fertility 74, 47-55.
59. NICOLL, M. E. & RATHBUN, G. B. (1990). African Insectivora and elephant shrews: an action plan for their conservation. International Union for the Conservation of Nature, Gland, Switzerland.
60. NOVACEK, M. J. (1992). Mammalian phylogeny, shaking the tree. Nature London 356, 121-125.
61. OLSON, L. (1999). Systematics, evolution, and biogeography of Madagascar's tenrecs (Mammalia. Lipotyphla). Ph.D. thesis, University of Chicago.
62. OLSON, L. & GOODMAN, S. M. (2003). Phylogeny and biogeography of tenrecs. In The Natural History of Madagascar (eds,. S. M. Goodman and J. P. Benstead), pp. 1235-1242. University of Chicago Press, Chicago, IL.
63. PEARSON, O. P. (1944). Reproduction in the shrew (Blarina brevicauda Say). American Journal of Anatomy 75, 39-93.
64. PHILLIPS, D. M. & BEDFORD, J. M. (1985). Unusual features of sperm ultrastructure in the Musk Shrew Suncus murinus. The Journal of Experimental Zoology 235, 119-126.
65. PHILLIPS, D. M., RASWEILER, J. J. & MURADALI, F. (1997). Giant accordioned sperm acrosomes of the Greater Bulldog Bat, Noctilio leporinus. Molecular Reproduction and Development 448, 90-94.
66. PUCEK, Z. (1964). The structure of the glans penis in Neomys Kaup, 1929, as taxonomic character. Acta Theriologica 9, 374-377.
67. QUEROUL, S., HUTTERER, R., BARRIERE, P., COLYN, M., PETERHANS, J. C. K. & VERHEYEX, E. (2001). Phylogeny and evolution of African shrews (Mammalia: Soricidae) inferred from 16s rRNA sequences. Molecular Phylogenetics and Evolution 20, 185-195.
68. RACEY, P. A. (1978). Seasonal changes in testosterone levels and androgen-dependent organs in male moles (Talpa europaea). Journal of Reproduction and Fertility 52, 195-200.
69. REPENNING, C. A. (1967). Subfamilies and genera of the Soricidae. United States Geological Survey Professional Paper 565, 1-74.
70. REUMER, J. W. F. (1987). Redefinition of the Soricidae and Heterosoricidae (Insectivora, Mammalia) with the description of the Crocidosoricinae. a new family of the Soricidae. Revue de Palaeobiologie 6, 189-192.
71. RICHARDS J. S., RUSSELL, D. L., OCHSNER, S. & ESPEY, L. L. (2002). Ovulation: new dimensions and new regulators of the inflammatory-like response. Annual Reviews of Physiology 64, 69-92.
72. ROBB, G. W., AMANN, R. P. & KILLIAN, G. J. (1978). Daily sperm production and epididymal sperm reserves of pubertal and adult rats. Journal of Reproduction and Fertility 54, 103-107.
73. ROLDAN, E. R. S. & YANAGIMACHI, R. (1989). Cross-fertilization between Syrian and Chinese hamsters. Journal of Experimental Zoology 250, 221-328.
74. ROUSE, G. W. & ROBSON, S. (1986). An ultrastructural study of megachiropteran (Mammalia: Chiroptera) spermatozoa: implications for chiropteran phylogeny. Journal of Submicroscopic Cytology 18, 137-152.
75. RUBEXSTEIN, N. M., CUNHA, G. R., WANG, Y. Z., CAMPBELL, K. L., CONLEY, A.J., CATANIA, K. C., GLICKMAN, S. E. & PLACE, N.J. (2003). Variation in ovarian morphology in four species of New World moles with a peniform clitoris. Reproduction 126, 713-719.
76. SHOSHANI, J. & MCKENNA, M. C. (1998). Higher taxonomic relationships among extant mammals based on morphology, with selected comparisons of results from molecular data. Molecular Phylogenetics and Evolution 9. 572-584.
77. SIMMONS, N.B. (1993). The importance of methods: archontan phylogeny and cladistic analysis of morphological data. In Primates and their Relatives in Phylogenetic Perspective (ed. R. D. E. MacPhee), pp. 1-61. Plenum Press, New York.
78. SPRINGER, M. S., CLEVE, G. C., MADSEN, O., DE JONG, W. W., WADELL, V. G., AMRINE, H. M. & STANHOPE, M. J. (1997). Endemic African mammals shake the phylogenetic tree. Nature Endemic African 388, 61-64.
79. STANHOPE, M. J., WADDELL, V. G., MADSEN, O., DE JONG, W., HEDGES, S. B., CLEVEN, G. C., KAO, D. & SPRINGER, M. S. (1998). Molecular evidence for multiple origins of Insectivora and for a new order of endemic African insectivore mammals. Proceedings of the National Academy of Sciences U.S.A. 95, 9967-9972.
80. STOCKLEY, P. (1997). No evidence of sperm selection by female common shrews. Proceedings of the Royal Society London B 264, 1497-1500.
81. STOCKLEY, P., SEARLE, J. B., MACDONALD, D. W. & JONES, C. S. (1996). Correlates of reproductive success within alternative mating tactics of the common shrew. Behavioral Ecology 7, 334-340.
82. STRAUSS, F. (1950). Ripe follicles without antra and fertilization within the follicle: a normal situation in a mammal. Anatomical Record 106 251-252.
83. STRAUSS, F. (1966). Weibliche Geschlectsorgane, Volume 8. In Handbuch der Zoologie (eds. J.-G. Helmeke, H. Lengerken, D. Starck and H. Wermuth), pp. 1-96. Walter de Gruyter and Co., Berlin (from Mossman and Duke, 1973).
84. SUAREZ, S. S. (2001). Carbohydrate-mediated formation of the oviductal sperm reservoir in mammals. Cells Tissues Organs 168 105-112.
85. SULTAN, K. M. & BEDFORD, J. M. (1996). Two modifiers of sperm transport within the Fallopian tube of the rat. Journal of Reproduction and Fertility 108, 179-184.
86. TRIPP, H. R. H. (1971). Reproduction in elephant shrews (Macroscelididae) with special reference to ovulation and implantation. Journal of Reproduction and Fertility 26, 149-159.
87. VAN DER HORST, C. J. & GILMAN, J. (1940). Ovulation and corpus luteum formation in Elephantulus. South African Journal of Medical Science 5, 73-91.
88. VAN DIJK, M. A. M., MADSEN, O., CATZEFILS, F. STANHOPE, M. J., DE JONG, W. W. & PAGEL, M. (2001). Protein sequence signatures support the African clade of mammals. Proceedings of the National Academy of Sciences U.S.A. 98, 188-193.
89. VOGEL, P. (1981). Occurrence and interpretation of delayed implantation in insectivores. Journal of Reproduction and Fertility Supplement 29, 51-60.
90. VOSS, R. S. & LINZEY, A. V. (1981). Comparative gross morphology of male accessory glands among Neotropical Muridae (Mammalia: Rodentia) with comments on systematic implications. Miscellaneous Publications Museum of Zoology, University of Michigan, 159.
91. WERDELIN, L. & NILSONNE, A. (1999). The evolution of a scrotum and testicular descent in mammals. Journal of Theoretical Biology 196, 61-72.
92. WHITWORTH, D. J., LIGHT, P., RACEY, P.A. & GLICKMAN, S. E. (1999). Testis-like steroidogenesis in the ovotestis of the European mole, Talpa europaea. Biology of Reproduction 60, 413-418.
93. WOODALL, F.F. (1987). An ultrastructural study of the spermatozoa of elephant shrews (Mammalia; Macroscelidae) and its phylogenetic implications. Journal of Submicroscopic Cytology 23, 47-58.
94. YANAGIMACHI, R., KAMIGUCHI, Y., SUGAWARA, S. & MIKAMO, K. (1983). Gametes and fertilization in the Chinese hamster. Gamete Research 8, 97-117.
95. YATES, T. L. (1984). Insectivores, elephant shrews, tree shrews and dermopterans. In Orders and Families of Recent Mammals of the World (eds. S. Anderson and J. K. Jones), pp. 117-144. Wiley, New York.
96. ZAJACZEK, S. (1946). Untersuchungen über das endocrine system des igels (Erinaceus). Bulletin International de l'Academie Polonaise des Sciences et des Lettres, Classes des Sciences Mathematiques et Naturelles, series B 1939, 379-403.