Evolution and spermatogenesis

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 365, Issue 1546, 2010, Pages 1465-1480

  White Cooper, Helen ^a   Bausek, Nina ^b  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Evolution; Gene expression; Spermatogenesis

Indexed keywords

EVOLUTIONARY BIOLOGY; FLY; GENE EXPRESSION; GENOME; MOLECULAR ANALYSIS; MOTILITY; NEMATODE; NUMERICAL MODEL; REPRODUCTIVE STRATEGY; RODENT; SEXUAL REPRODUCTION; SPERM;

ANIMALIA; CAENORHABDITIS ELEGANS; MUS;

EID: 77952760955     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2009.0323     Document Type: Review

References (156)

1. Aguinaldo, A., Turbeville, J., Linford, L., Rivera, M., Garey, J., Raff, R. & Lake, J. 1997 Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489-493. (doi:10.1038/387489a0) (Pubitemid 27235464)
2. Anderson, M. & Dixson, A. 2002 Sperm competition: motility and the midpiece in primates. Nature 2002, 496. (doi:10.1038/416496a)
3. Anderson, R., Copeland, T. K., Scholer, H., Heasman, J. & Wylie, C. 2000 The onset of germ cell migration in the mouse embryo. Mech. Dev. 91, 61-68. (doi:10.1016/ S0925-4773(99)00271-3) (Pubitemid 30125905)
4. Andrews, J., Bouffard, G. G., Cheadle, C., Lu, J. N., Becker, K. G. & Oliver, B. 2000 Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis. Gen. Res. 10, 2030-2043. (doi:10.1101/gr.10.12.2030) (Pubitemid 32050827)
5. Arbouzova, N. I. & Zeidler, M. P. 2006 JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development 133, 2605-2616. (doi:10. 1242/dev.02411)
6. Ariz, M., Mainpal, R. & Subramaniam, K. 2009 C. elegans RNA-binding proteins PUF-8 and MEX-3 function redundantly to promote germline stem cell mitosis. Dev. Biol. 326, 295-304. (doi:10.1016/j.ydbio.2008.11.024)
7. Bacetti, B. & Dallai, R. 1977 The first multi-flagellate spermatozoa in the animal kingdom, discovered in Mastotermes danviniensis. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D 285, 785-788.
8. Baccetti, B., Gibbons, B. H. & Gibbons, I. R. 1989 Bidirectional swimming in spermatozoa of tephritid flies. J. Submicrosc. Cytol. Pathol. 21, 619-625.
9. Barroca, V., Lassalle, B., Coureuil, M., Louis, J., Le Page, F., Testart, J., Allemand, I., Riou, L. & Fouchet, P. 2009 Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat. Cell Bio. 11, 190-196. (doi:10.1038/ncb1826)
10. Basto, R., Lau, J., Vinogradova, T., Gardiol, A., Woods, C., Khodjakov, A. & Raff, J. 2006 Flies without centrioles. Cell 125, 1375-1386. (doi:10.1016/j.cell.2006.05.025)
11. Begun, D., Lindfors, H., Kern, A. & Jones, C. 2007 Evidence for de novo evolution of testis-expressed genes in the Drosophila yakuba/Drosophila erecta clade. Genetics 176, 1131-1137. (doi:10.1534/genetics.106.069245) (Pubitemid 46961110)
12. Betran, E., Thornton, K. & Long, M. 2002 Retroposed new genes out of the X in Drosophila. Genome Res. 12, 1854-1859. (doi:10.1101/gr.6049)
13. Blobel, C. 2000 Functional processing of fertilin: evidence for a critical role of proteolysis in sperm maturation and activation. Rev. Reprod. 5, 75-83. (doi:10.1530/ror.0. 0050075) (Pubitemid 30303561)
14. Bonilla, E. & Xu, E. Y. 2008 Identification and characterization of novel mammalian spermatogenic genes conserved from fly to human. Mol. Hum. Reprod. 14, 137-142. (doi:10.1093/molehr/gan002) (Pubitemid 351404886)
15. Boutanaev, A. M., Kalmykova, A. I., Shevelyov, Y. Y. & Nurminsky, D. I. 2002 Large clusters of co-expressed genes in the Drosophila genome. Nature 420, 666-669. (doi:10.1038/nature01216)
16. Braun, R. 2001 Packaging paternal chromosomes with protamine. Nat. Genet. 28, 10-12. (doi:10.1038/88194)
17. Brawley, C. & Matunis, E. 2004 Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science304, 1331-1334. (doi: 10.1126/science. 1097676) (Pubitemid 38697431)
18. Brown, F. D., Prendergast, A. & Swalla, B. J. 2008 Man is but a worm: chordate origins. Genesis 46, 605-613. (doi:10.1002/dvg.20471)
19. Bunt, S. & Hime, G. R. 2004 Ectopic activation of Dpp signalling in the male Drosophila germline inhibits germ cell differentiation. Genesis 39, 84-93. (doi:10.1002/gene. 20030) (Pubitemid 38924655)
20. Byrne, P. G., Simmons, L. W. & Roberts, J. D. 2003 Sperm competition and the evolution of gamete morphology in frogs. Proc. R. Soc. Lond. B 270, 2079-2086. (doi: 10. 1098/rspb.2003.2433)
21. Caceres, L. & Nilson, L. 2005 Production of gurken in the nurse cells is sufficient for axis determination in the Drosophila oocyte. Development 132, 2345-2353. (doi:10.1242/dev.01820) (Pubitemid 40872804)
22. Chang C. C., Lin, G. W., Cook, C. E., Horng, S. B., Lee, H. J. & Huang, T. Y. 2007 Apvasa marks germ-cell migration in the parthenogenetic pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Dev. Genes Evol. 217, 275-287. (doi:10.1007/s00427-007-0142-7)
23. Chen, C. et al. 2005 ERM is required for transcriptional control of the spermatogonial stem cell niche. Nature 436, 1030-1034. (doi:10.1038/nature03894) (Pubitemid 41191687)
24. Chintapalli, V., Wang, J. & Dow, J. 2007 Using FlyAtlas to identify better Drosophila models of human disease. Nat. Genet. 39, 715-720. (doi:10.1038/ng2049) (Pubitemid 46848596)
25. Choi, E. et al. 2007 Integrative characterization of germ cell-specific genes from mouse spermatocyte unigene library. BMC Genomics 8, 256. (doi:10.1186/1471-2164-8-256)
26. Cinquin, O. 2009 Purpose and regulation of stem cells: a systems-biology view from the Caenorhabditis elegans germ line. J. Pathol. 217, 186-198. (doi:10.1002/path. 2481)
27. Coffman, C. R., Strohm, R. C., Oakley, F. D., Yamada, Y., Przychodzin, D. & Boswell, R. E. 2002 Identification of X-linked genes required for migration and programmed cell death of Drosophila melanogaster germ cells. Genetics 162, 273-284.
28. Cooper, K. W. 1950 Normal spermatogenesis in Drosophila. In Biology of Drosophila (ed. M. Demerec), pp. 1-61. London, UK: Chapman and Hall.
29. Correia, J. N., Conner, S. J. & Kirkman-Brown, J. C. 2007 Non-genomic steroid actions in human spermatozoa. Persistent tickling from a laden environment. Semin. Reprod. Med. 25, 208-219. (doi:10.1055/s-2007-973433)
30. Cox, D. N., Chao, A., Baker, J., Chang, L., Qiao, D. & Lin, H. 1998 A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12, 3715-3727. (doi:10.1101/gad.12.23.3715) (Pubitemid 29019652)
31. Cox, D. N., Chao, A. & Lin, H. 2000 piwi encodes a nucleoplasms factor whose activity modulates the number and division rate of germline stem cells. Development 127, 503-514. (Pubitemid 30093398)
32. Dawe, H. R., Farr, H., Portman, N., Shaw, M. K. & Gull, K. 2005 The Parkin co-regulated gene product, PACRG, is an evolutionarily conserved axonemal protein that functions in outer-doublet microtubule morphogenesis. J. Cell Sci. 118, 5421-5430. (doi:10.1242/jcs.02659) (Pubitemid 43079284)
33. Dorus, S., Busby, S. A., Gerike, U., Shabanowitz, J., Hunt, D. F. & Karr, T. L. 2006 Genomic and functional evolution of the Drosophila melanogaster sperm proteome. Nat. Genetics 38, 1440-1445. (doi:10.1038/ng1915) (Pubitemid 44837568)
34. Dorus, S., Freeman, Z. N., Parker, E. R., Heath, B. D. & Karr, T. L. 2008 Recent origins of sperm genes in Drosophila. Mol. Biol. Evol. 25, 2157-2166. (doi:10.1093/ molbev/msn162)
35. Eddy, E. M. 2002 Male germ cell gene expression. Recent Prog. Horm. Res. 57, 103-128. (doi:10.1210/rp.57.1.103)
36. Extavour, C. G. & Akam, M. 2003 Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130, 5869-5884. (doi:10.1242/dev. 00804) (Pubitemid 38008792)
37. Fraser, L. R., Harrison, R. A. & Herod, J. E. 1990 Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J. Reprod. Fertil 89, 135-148.
38. Friedlander, M., Jeshtadi, A. & Reynolds, S. 2001 The structural mechanism of trypsin-induced intrinsic motility in Manduca sexta spermatozoa in vitro. J. Insect Physiol. 47, 245-255. (doi:10.1016/S0022-1910(00) 00109-8) (Pubitemid 32157329)
39. Fukuda, N., Yomogida, K., Okabe, M. & Touhara, K. 2004 Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J. Cell Sci. 117, 5835-5845. (doi:10.1242/jcs.01507) (Pubitemid 40123950)
40. Gage, M. J. & Morrow, E. H. 2003 Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Curr. Biol. 13, 754-757. (doi:10.1016/ S0960-9822(03)00282-3)
41. Gage, M. J., Parker, G. A., Nylin, S. & Wiklund, C. 2002 Sexual selection and speciation in mammals, butterflies and spiders. Proc. R. Soc. Lond. B 269, 2309-2316. (doi: 10.1098/rspb.2002.2154) (Pubitemid 35397511)
42. Gaino, E. & Mazzini, M. 1991 Aflagellate sperm in three species of Leptophlebiidae (Ephemeroptera). Int. J. Insect Morphol. Embryol. 20, 119-125.
43. Gangaraju, V. K. & Lin, H. 2009 MicroRNAs: key regulators of stem cells. Nat. Rev. Mol. Cell Biol. 10, 116-125. (doi:10.1038/nrm2621)
44. Garcia-Gonzalez, F. & Simmons, L. W. 2007 Shorter sperm confer higher competitive fertilization success. Evolution 61, 816-824. (doi:10.1111/j.1558- 5646.2007.00084.x) (Pubitemid 46537660)
45. Gomendio, M. & Roldan, E. R. 2008 Implications of diversity in sperm size and function for sperm competition and fertility. Int. J. Dev. Biol. 52, 439-447. (doi:10.1387/ijdb. 082595mg)
46. Gou, G. & Zheng, G. 2004 Hypotheses for the functions of intercellular bridges in male germ cell development and its cellular mechanisms. J. Theor. Biol. 229, 139-146. (Pubitemid 38721257)
47. Haerty, W. et al. 2007 Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177, 1321-1335. (doi:10.1534/genetics. 107.078865) (Pubitemid 350277035)
48. Handel, M., Park, C. & Kot, M. 1994 Genetic control of sex-chromosome inactivation during male meiosis. Cytogen. Genome Res. 66, 83-88. (doi: 10.1159/ 000133672) (Pubitemid 24042835)
49. Hansbrough, J. R. & Garbers, D. L. 1981 Speract. Purification and characterization of a peptide associated with eggs that activates spermatozoa. J. Biol. Chem. 256, 1447-1452.
50. Hansen, D., Wilson-Berry, L., Dang, T. & Schedl, T. 2004 Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131, 93-104. (doi:10.1242/dev.00916) (Pubitemid 38111418)
51. Henderson, S. T., Gao, D., Lambie, E. J. & Kimble, J. 1994 lag2 may encode a signaling ligand for the GLP-1 and LEN-12 receptors of C. elegans. Development 120, 2913-2924. (Pubitemid 24312059)
52. Hense, W., Baines, J. F. & Parsch, J. 2007 X chromosome inactivation during Drosophila spermatogenesis. PLoS Biol. 5, e273. (doi:10.1371/journal. pbio.0050273)
53. Hill, D., Shakes, D., Ward, S. & Strome, S. 1989 A spermsupplied product essential for initiation of normal embryogenesis in Caenorhabditis elegans is encoded by the paternal-effect embryonic-lethal gene, spe-11. Dev. Biol. 136, 154-166. (doi:10.1016/0012-1606(89)90138-3) (Pubitemid 19262693)
54. Hou, S. X., Zheng, Z., Chen, X. & Perrimon, N. 2002 The Jak/STAT pathway in model organisms: emerging roles in cell movement. Dev. Cell 3, 765-778. (doi:10.1016/ S1 534-5807(02)00376-3) (Pubitemid 35460778)
55. Huckins, C. 1978 Spermatogonial intercellular bridges in whole-mounted seminiferous tubules from normal and irradiated rodent testes. Am. J. Anat. 153, 97-121. (doi:10.1002/aja.1001530107) (Pubitemid 9019148)
56. Inaba, K. 2007 Molecular basis of sperm flagellar axonemes: structural and evolutionary aspects. Ann. N. Y. Acad. Sci. 1101, 506-526. (doi:10.1196/annals.1389.017) (Pubitemid 47092706)
57. Ishijima, S., Ishijima, S. A. & Afzelius, B. A. 1994 Movement of Myzostomum spermatozoa: calcium ion regulation of swimming direction. Cell Motil. Cytoskel. 28, 135-142. (doi:10.1002/cm.970280205) (Pubitemid 24176931)
58. Jamieson, B. G. M., Dallai, R. & Afzelius, B. A. 1999 Insects their spermatozoa and phylogeny. Enfield, NH: Science Publishers Inc.
59. Johnson, J. M., Edwards, S., Shoemaker, D. & Schadt, E. E. 2004 Dark matter in the genome: evidence of widespread transcription detected by microarray tiling experiments. Trends Genet 21, 93-102. (doi:10.1016/j.tig.2004. 12.009) (Pubitemid 40127353)
60. Kalmykova, A. I., Nurminsky, D. I., Ryzhov, D. & Shevelyov, Y. Y. 2005 Regulated chromatin domain comprising cluster of co-expressed genes in Drosophila melanogaster. Nuckic Acids Res. 33, 1435-1444. (doi:10.1093/nar/ gki281)
61. Kawano, N. & Yoshida, M. 2007 Semen-coagulating protein, SVS2, in mouse seminal plasma controls sperm fertility. Biol. Reprod. 76, 353-361. (doi:10.1095/biolreprod.106.056887) (Pubitemid 46311020)
62. Kawase, E., Wong, M. D., Ding, B. C. & Xie, T. 2004 Gbb/ Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131, 1365-1375. (doi:10.1242/ dev.01025) (Pubitemid 38443890)
63. Kiger, A. A., Jones, D. L., Schulz, C., Rogers, M. B. & Fuller, M. T. 2001 Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294, 2542-2545. (doi:10.1126/science.1066707) (Pubitemid 34027293)
64. Kimble, J. & Crittenden, S. 2007 Control of germline stem cells, entry into meiosis, and the sperm/oocyte decision in C. elegans. Annu. Rev. Cell Dev. Biol. 23, 405-433. (doi:10.1146/annurev.cellbio.23.090506.123326)
65. Kimble, J. E. & White, J. G. 1981 On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 81, 208-219. (doi:10.1016/0012-1606(81)90284-0)
66. King, R. C. 1970 Ovarian development in Drosophila melanogaster. New York, NY: Academic Press.
67. Kloc, M. & Etkin, L. 2005 RNA localization mechanisms in oocytes. J. Cell Sci. 118, 269-282. (doi:10.1242/jcs. 01637)
68. Knowles, D. & McLysaght, A. 2009 Recent de novo origin of human protein-coding genes. Genome Res. 19, 1752-1759. (doi:10.1101/gr.095026.109)
69. Kramer,J.,McCarrey,J.,Djakiew,D.&Krawetz,S.1998Differentiation: theselectivepotentiationofchromatindomains.Development125,4749-4755. (Pubitemid29027204)
70. Kusnetsov,S.,Lyanguzowa,M.&Bosch,T. 2001RoleofepithelialcellsandprogrammedcelldeathinHydraspermatogenesis. Zoology104,25-31.(Pubitemid33769155)
71. Lam, N., Chesney, M. A. & Kimble, J. 2006 Wnt signaling and CEH-22/tinman/Nkx2.5 specify a stem cell niche in C. elegans. Curr. Biol. 16, 287-295. (doi:10.1016/j.cub. 2005.12.015) (Pubitemid 43190228)
72. LaMunyon, C. W. & Ward, S. 1995 Sperm precedence in a hermaphroditic nematode (Caenorhabditis elegans) is due to competitive superiority of male sperm. Experientia 51, 817-823. (doi:10.1007/BF01922436)
73. Le Bras, S. & Van Doren, M. 2006 Development of the male germline stem cell niche in Drosophila. Dev. Biol. 294, 92-103.
74. Lefevre Jr, G. & Jonsson, U. B. 1962 Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47, 1719-1736.
75. Lessells, C. M., Snook, R. R. & Hosken, D. J. 2009 The evolutionary origin and maintenance of sperm: selection for a small, motile gamete mating type. In Sperm biology: an evolutionary perspective (eds T. Birkhead, D. Hosken & S. Pitnick), pp. 43-67. New York, NY: Academic Press.
76. Levine, M., Jones, C., Kern, A., Lindfors, H. & Begun, D. 2006 Novel genes derived from non-coding DNA in Drosophila melanogaster are frequently X-linked and show testis-biased expression. Proc. Natl Acad. Sci. USA 103, 9935-9939. (doi:10.1073/pnas.0509809103) (Pubitemid 43993601)
77. Lewis,J.,Song,Y.,deJong,M.,Bagha,S.&Ausio,J. 2003Awalkthroughvertebrateandinvertebrateprotamines.Chromosoma111,473-482.(doi: 10.1007/s00412-002-0226-0)(Pubitemid36705629)
78. Lewis, J. D., de Jong, M. E., Bagha, S. M., Tang, A., Gilly, W. F. & Ausio, J. 2004a All roads lead to arginine: the squid protamine gene. J. Mol. Evol. 58, 673-680. (doi: 10.1007/S00239-004-2589-8) (Pubitemid 38781700)
79. Lewis, J. D., Saperas, N., Song, Y., Zamora, M. J., Chiva, M. & Ausio, J. 20046 Histone H1 and the origin of protamines. Proc. Natl Acad. Sci. USA 101, 4148-4152. (doi:10.1073/ pnas.0308721101)
80. Li, L. & Neaves, W. B. 2006 Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 66, 4553-4557. (doi:10.1158/0008-5472.CAN-05- 3986)
81. Li, J. & Wu, C. 2005 New symbiotic hypothesis on the origin of eukaryotic flagella. Naturwissenschaften 92, 305-309. (doi: 10.1007/s00114-005- 0635-z) (Pubitemid 41187665)
82. Li, L. & Xie, T. 2005 Stem cell niche: structure and function. Annu. Rev. Cell Dev. Biol. 21, 605-631. (doi:10. 1146/annurev.cellbio.21.012704. 131525) (Pubitemid 41740648)
83. Li, M., Hong, N., Xu, H., Yi, M., Li, C., Gui, J. & Hong, Y. 2009 Medaka vasa is required for migration but not survival of primordial germ cells. Mech. Dev.
84. Manton, I. 1953 Number of fibrils in the cilia of green algae. Nature 111, 485-486. (doi:10.1038/171485b0)
85. Manton, I. 1970 Plant spermatozoids. In Comparative spermatology (ed. B. Baccetti), pp. 143-158. Rome, Italy: Academia Nazionale Dei Lincei.
86. Mattei, X. 1991 Spermatozoon ultrastructure and its systematic implictions in fishes. Can. J. Zool. 69, 3038-3055. (doi: 10.1139/z91-428)
87. Mattei, X., Mattei, C., Reizer, C. & Chevalier, J.-L. 1972 Ultrastructure des spermatozoids aflagelles des Mormyres (poisson teleosteens). J. Microsc. 15, 67-78.
88. Maxwell, W. M., de Graaf, S. P., Ghaoui Rel, H. & Evans, G. 2007 Seminal plasma effects on sperm handling and female fertility. Soc. Reprod. Fertil. Suppl. 64, 13-38.
89. Michiels,F.,Gasch,A.,Kaltschmidt,B.&Renkawitz-Pohl,R. 1989A14bppromoterelementdirectsthetestisspecificityoftheDrosophilab2- tubulingene.EMBOJ.8,1559-1565.(Pubitemid19274383)
90. Miller, M., Cutter, A., Yamamoto, I., Ward, S. & Greenstein, D. 2004 Clustered organization of reproductive genes in the C. elegans genome. Curr. Biol. 14, 1284-1290. (doi:10.1016/j.cub.2004.07.025) (Pubitemid 38991817)
91. Morrow, E. H. 2004 How the sperm lost its tail: the evolution of aflagellate sperm. Biol. Rev. Comb. Phil. Soc. 79, 795-814.
92. Mottier-Pavie, V. & Megraw, T. L. 2009 Drosophila Bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol. Biol. Cell.
93. Mueller, J., Mahadevaiah, S., Park, P., Warburton, P., Page, D. & Turner, J. 2008 The mouse X chromsome is enriched for multicopy testis genes showing postmeiotic expression. Nat. Genet. 40, 794-799. (doi: 10. 1038/ng.126) (Pubitemid 351748859)
94. Newton, W. D. 1980 Ultrastructural analysis of the motile apparatus of the aflagellate spermatozoon of macrostomum tubum. J. Ultrastruct. Res. 73, 318-330. (doi:10. 1016/S0022-5320(80)90091-X)
95. Nielsen, M., Caserta, J., Kidd, S. & Phillips, C. 2006 Functional constraint underlies 60 million year stasis of dipteran testis-specific beta-tubulin. Evol. Dev. 8, 23-29.
96. Nixon, B., MacIntyre, D. A., Mitchell, L. A., Gibbs, G. M., O'Bryan, M. & Aitken, R. J. 2006 The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biol. Reprod. 74, 275-287. (doi:10.1095/biolreprod.105. 044644) (Pubitemid 43122278)
97. Normark, B. B. 2009 Unusual gametic and genetic systems. In Sperm biology: an evolutionary perspective (eds T. R. Birkhead, D. J. Hosken & S. Pitnick), pp. 507-538. New York, NY: Academic Press.
98. Oatley, J. M. & Brinster, R. L. 2006 Spermatogonial stem cells. Meth. Enzymol. 419, 259-282.
99. Oatley, J. M. & Brinster, R. L. 2008 Regulation of spermatogonial stem cell self-renewal in mammals. Annu. Rev. Cell Dev. Biol. 24, 263-286. (doi:10.1146/annurev.cellbio.24. 110707.175355)
100. Ogawa, T., Ohmura, M. & Ohbo, K. 2005 The niche for spermatogonial stem cells in the mammalian testis. Int. J. Hematol. 82, 381-388. (doi:10.1532/IJH97.05088) (Pubitemid 46638685)
101. Osborne, C. S. et al. 2004 Active genes dynamically colocalize to shared sites of ongoing transcription. Nat. Genet. 36, 1065-1071. (doi:10.1038/ng1423)
102. Parisi, M., Nuttall, R., Naiman, D., Bouffard, G. G., Malley, J., Andrews, J., Eastman, S. & Oliver, B. 2003 Paucity of genes on the Drosophila X chromosome showing malebiased expression. Science 299, 697-700. (doi:10.1126/ science.1079190) (Pubitemid 36159482)
103. Parisi, M. et al. 2004 A survey of ovary-, testis-, and somabiased gene expression in Drosophila melanogaster adults. Genome Biol. 5, R40. (doi:10.1186/gb-2004-5-6-r40)
104. Parker, G. A. & Begon, M. E. 1993 Sperm competition games: sperm size and number under gametic control. Proc. R. Soc. Lond. B 253, 255-262. (doi:10.1098/rspb. 1993.0111)
105. Phillips, D. M. 1970 Insect sperm: their structure and morphogenesis. J. Cell Biol. 44, 243-277. (doi:10.1083/jcb. 44.2.243)
106. Pittoggi, C. et al. 1999 A fraction of mouse sperm chromatin is organized in nucleosomal hypersensitive domains enriched in retroposon DNA. J. Cell Sci. 112, 3537-3548.
107. Quill, T. A., Sugden, S. A., Rossi, K. L., Doolittle, L. K., Hammer, R. E. & Garbers, D. L. 2003 Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc. Natl Acad. Sci. USA 100, 14869-14874. (doi: 10.1073/pnas.2136654100)
108. Ranz, J., Ponce, A., Hard, D. L. & Nurminsky, D. 2003 Origin and evolution of a new gene expressed in the Drosophila sperm axoneme. Genetica 118, 233-244. (doi: 10. 1023/A:1024186516554) (Pubitemid 36821052)
109. Ren, D., Navarro, B., Perez, G., Jackson, A., Hsu, S., Shi, Q., Tilly, J. & Clapham, D. 2001 A sperm ion channel required for sperm motility and male fertility. Nature 413, 603-609. (doi: 10.1038/35098027) (Pubitemid 32964054)
110. Riparbelli, M. G. & Callaini, G. 2007 The Drosophila parkin homologue is required for normal mitochondrial dynamics during spermiogenesis. Dev. Biol. 303, 108-120. (doi:10.1016/j.ydbio.2006.10.038) (Pubitemid 46241091)
111. Riparbelli, M. G., Callaini, G., Mercati, D., Hertel, H. & Dallai, R. 2009 Centrioles to basal bodies in the spermiogenesis of Mastotermes darzviniensis (Insecta, Isoptera). Cell Motil Cytoskel
112. Roldan,E.,Gomendio,M.&Vitullo,A. 1992Theevolutionofeutherianspermatozoaandunderlyingselectiveforces: femaleselectionandspermcompetition.Biol.Rev.Camb.Phil.Soc.67,551-593. (Pubitemid23002661)
113. Sada, A., Suzuki, A., Suzuki, H. & Saga, Y. 2009 The RNAbinding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science 325, 1394-1398. (doi:10.1126/science.1172645)
114. Santos, A. C. & Lehmann, R. 2004 Germ cell specification and migration in Drosophila and beyond. Curr. Biol. 14, R578-R589. (doi:10.1016/j.cub.2004.07.018) (Pubitemid 38190366)
115. Saunders, C., Larman, M., Parrington, J., Cox, L., Royse, J., Blayney, L., Swann, K. & Lai, F. 2002 PLCzeta: a spermspecific trigger of Ca2+ oscillations in eggs and embryo development. Development 129, 3533-3544.
116. Schmidt-Rhaesa,A.1997/98PhylogeneticrelationshipsoftheNematomorpha- adiscussionofcurrenthypotheses.Zool.Anzdger236,203-216.(Pubitemid127711310)
117. Seto, A. G., Kingston, R. E. & Lau, N. C. 2007 The coming of age for Piwi proteins. Mol. Cell 26, 603-609. (doi: 10. 1016/j.molcel.2007.05.021)
118. Sheng, X., Posenau, T., Gumulak-Smith, J., Matunis, E., Van Doren, M. & Wawersik, M. 2009 Jak-STAT regulation of male germline stem cell establishment during Drosophila embryogensis. Dev. Biol. 334, 335-344. (doi:10.1016/j.ydbio.2009.07.031)
119. Shevelyov, Y. Y., Lavrov, S., Mikhaylova, L., Nurminsky, I., Kulathainal, R., Egorova, K., Rozovsky, Y. & Nurminsky, D. I. 2009 The B-type lamin is required for somatic repression of testis-specifc gene clusters. Proc. Natl Acad. Sci. USA 106, 3282-3287. (doi:10.1073/pnas. 0811933106)
120. Shi,S.&Stanley,P. 2006EvolutionaryoriginsofNotchsignalinginearlydevelopment.CellCycle5,274-278. (Pubitemid43213497)
121. Shivdasani, A. A. & Ingham, P. W. 2003 Regulation of stem cell maintenance and transit amplifying cell proliferation by tgf-beta signaling in Drosophila spermatogenesis. Curr. Biol. 13, 2065-2072. (doi: 10. 1016/j.cub.2003.10.063)
122. Siddall, N. A., McLaughlin, E. A., Marriner, N. L. & Hime, G. R. 2006 The RNA-binding protein Musashi is required intrinsically to maintain stem cell identity. Proc. Natl Acad. Sci. USA 103, 8402-8407. (doi:10.1073/ pnas.0600906103)
123. Singson, A. 2001 Every sperm is sacred: fertilization in Caenorhabditis elegans. Dev. Biol. 230, 101-109. (doi:10. 1006/dbio.2000.0118)
124. Singson, A. 2006 Sperm activation: time and tide wait for no sperm. Curr. Biol. 16, R160-R162. (doi:10.1016/j.cub. 2006.02.039) (Pubitemid 43343696)
125. Smith, H. 2006 Sperm motility and MSP. WormBook (ed. The C. elegans research community), 1-8. See http://www.wormbook.org
126. Spehr, M., Gisselmann, G., Poplawski, A., Riffell, J. A., Wetzel, C. H., Zimmer, R. K. & Hatt, H. 2003 Identification of a testicular odorant receptor mediating human sperm Chemotaxis. Science 299, 2054-2058. (doi: 10. 1126/science.1080376) (Pubitemid 36383730)
127. Spellman, P. T. & Rubin, G. M. 2002 Evidence for large domains of similarly expressed genes in the Drosophila genome. J. Biol. 1, 5. (doi: 10.1186/1475-4924-1-5)
128. Stanfield, G. M. & Villeneuve, A. M. 2006 Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr. Biol. 16, 252-263. (doi:10.1016/j.cub.2005.12.041)
129. Stockley, P., Gage, M. J., Parker, G. A. & Møller, A. P. 1997 Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149, 933-954. (doi:10.1086/286031) (Pubitemid 27222227)
130. Strome, S. 2005 Specification of the germ line. In WormBook (eds The C. elegans Reasearch Community), pp. 1-10.
131. Sturgill, D., Zhang, Y., Parisi, M. & Oliver, B. 2007 Demasculinization of X chromosomes in the Drosophila genus. Nature 4450, 238-241. (doi:10.1038/nature06330)
132. Suarez, S. 2008 Control of hyperactivation in sperm. Hum. Rep. Update 14, 647-657. (doi:10.1093/humupd/ dmn029)
133. Suzuki, N. 1990 Structure and function of sea urchin egg jelly molecules. Zool. Sci. 1, 355-370.
134. Suzuki, N. & Yoshino, K. 1992 The relationship between amino acid sequences of sperm-activating peptides and the taxonomy of echinoids. Comp Biochem. Physiol. B 102, 679-690. (doi:10.1016/0305-0491(92)90064-X)
135. Swanson, W. J. & Vacquier, V. D. 2002 The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3, 137-144. (doi:10.1038/nrg733)
136. Swanson,W.J.,Nielsen,R.&Yang,Q. 2003Pervasiveadaptiveevolutioninmammalianfertilizationproteins.Mol.Biol.Evol.20, 18-20.(Pubitemid36077894)
137. Takahashi, T., McDougall, C., Troscianko, J., Chen, W., Jayaraman-Nagarajan, A., Shimeld, S. & Ferrier, D. 2009 An EST screen from the annelid Pomatoceros lamarckii reveals patterns of gene loss and gain in animals. BMC Evol. Biol. 9, 240. (doi:10.1186/1471-2148-9-240)
138. Tam, P. P. & Zhou, S. X. 1996 The allocation of epiblast cells to ectodermal and germ-line lineages is influenced by the position of the cells in the gastrulating mouse embryo. Dev. Biol. 178, 124-132. (doi:10.1006/dbio. 1996.0203)
139. Tokuyasu, K. T. 1974 Dynamics of spermiogenesis in Drosophila melanogaster. 3. Relation between axoneme and mitochondrial derivatives. Exp. Cell Res. 84, 239-250. (doi: 10.1016/0014-4827(74)90402-9)
140. Tulina, N. & Matunis, E. 2001 Control of stem cell selfrenewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549. (doi: 10.1126/ science.1066700) (Pubitemid 34027294)
141. Turner, J. 2007 Meiotic sex chromsome inactivation. Development 134, 1823-1831. (doi:10.1242/dev.000018)
142. VanSpeybroeck,L.,DeWaele,D.&VandeVijver,G. 2002Theoriesinearlyembryology:closeconnectionsbetweenepigenesis,preformationism, andself-organization.Ann.N.Y.Acad.Sci.981,7-49.(Pubitemid36131116)
143. Wang, P., McCarrey, J., Yang, F. & Page, D. 2001 An abundance of X-linked genes expressed in spermatogonia. Nat. Genet. 27, 422-426. (doi: 10.1038/86927) (Pubitemid 32268424)
144. Ward, S. & Carrel, J. S. 1979 Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev. Biol. 73, 304-321. (doi:10.1016/0012-1606(79)90069-1)
145. Werner, M. & Simmons, L. W. 2008 Insect sperm motility. Biol. Rev. Camb. Phil. Soc. 83, 191-208.
146. White-Cooper, H., Doggett, K. & Ellis, R. E. 2009 The evolution of spermatogenesis. In Sperm biology: an evolutionary perspective (eds T. R. Birkhead, D. J. Hosken & S. S. Pitnick), pp. 151-183. New York, NY: Academic Press.
147. Wu, C.-I. & Xu, E. 2003 Sexual antagonism and X inactivation-the SAXI hypothesis. Trends Genet. 19, 243-247. (doi:10.1016/S0168-9525(03)00058-1) (Pubitemid 36507004)
148. Wylie, C. 1999 Germ cells. Cell 96, 165-174. (doi:10.1016/ S0092-8674(00)80557-7)
149. Xu, M. & Cook, P. 2008 The role of specialized transcription factories in chromsome pairing. Biochim. Biophys. Acta (BBA) 1783, 2155-2160. (doi:10.1016/j.bbamcr.2008. 07.013) (Pubitemid 351717509)
150. Yamashita, Y. M., Fuller, M. T. & Jones, D. L. 2005 Signalling in stem cell niches: lessons from the Drosophila germline. J. Cell Sci. 118, 665-672. (doi:10.1242/jcs. 01680)
151. Yoshida, S., Sukeno, M., Nakagawa, T., Ohbo, K., Nagamatsu, G., Suda, T. & Nabeshima, I. 2006 The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 133, 1495-1505. (doi:10.1242/dev. 02316) (Pubitemid 43732963)
152. Yoshida, S., Sukeno, M. & Nabeshima, Y. 2007 A vasculature-associated niche for undifferentiated spermatogonia in the mouse testis. Science 317, 1722-1726. (doi:10. 1126/science.1144885) (Pubitemid 47461832)
153. Yoshida, M., Kawano, N. & Yoshida, K. 2008 Control of sperm motility and fertility: diverse factors and common mechanisms. Cell Mol. Life Sci. 65, 3446-3457. (doi: 10. 1007/S00018-008-8230-Z)
154. Zhou, Y. & King, M. L. 2004 Sending RNAs into the future: RNA localisation and germ cell fate. IUBMB Life 56, 19-27. (Pubitemid 38209287)
155. Zhu, J., Massey, J. B., Mitchell-Leef, D., Eisner, C. W., Kort, H. I. & Roudebush, W. E. 2006 Platelet-activating factor acetylhydrolase activity affects sperm motility and serves as a decapacitation factor. Fertil. Steril. 85, 391-394. (doi:10.1016/j.fertnstert.2005.07.1303) (Pubitemid 43170912)
156. Zinzen, R., Gairardot, C., Gagneur, J., Braus, M. & Furlong, E. E. M. 2009 Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 462, 65-70. (doi:10.1038/nature08531)