Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality

Reproduction

Volumn 141, Issue 5, 2011, Pages 595-605

  Lüpold, Stefan ^a   Wistuba, Joachim ^b   Damm, Oliver S ^b   Rivers, James W ^c   Birkhead, Tim R ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^c OREGON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL TYPE; CONTROLLED STUDY; FOWL; GERM CELL; MALE; MATING SYSTEM; MORPHOLOGY; NONHUMAN; PRIORITY JOURNAL; SERTOLI CELL; SPERM COMPETITION; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; SPERMATOZOON COUNT; TESTIS SIZE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL SHAPE; CELL SIZE; FERTILIZATION; MALE; PASSERIFORMES; SPECIES SPECIFICITY; SPERM COUNT; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

AVES; ICTERIDAE;

EID: 79955829351     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-10-0501     Document Type: Article

References (75)

1. Aire TA 2007 Spermatogenesis and testicular cycles. In Reproductive Biology and Phylogeny of Birds, pp 279-347. Ed. BGM Jamieson. Enfield, New Hampshire: Science Publishers.
2. Aire TA, Olowo-Okorun MO & Ayeni JS 1980 The seminiferous epithelium in the guinea fowl (Numida meleagris). Cell and Tissue Research 205 319-325. (doi:10.1007/BF00234690)
3. Amann RP & Lambiase JT Jr 1969 The male rabbit. III. Determination of daily sperm production by means of testicular homogenates. Journal of Animal Science 28 369-374.
4. Balshine S, Leach BJ, Neat F, Werner NY & Montgomerie R 2001 Sperm size of African cichlids in relation to sperm competition. Behavioral Ecology 12 726-731. (doi:10.1093/beheco/12.6.726)
5. Berndtson WE 1977 Methods for quantifying mammalian spermatogenesis: a review. Journal of Animal Science 44 818-833.
6. Birkhead TR, Martínez JG, Burke T & Froman DP 1999 Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proceedings of the Royal Society of London. Series B 266 1759-1764. (doi:10.1098/rspb.1999.0843)
7. Bozkurt HH, Aktaş A, Ulkay MB & Firat UB 2007 Sertoli cell proliferation during the post hatching period in domestic fowl. Journal of Veterinary Science 8 219-222. (doi:10.4142/jvs.2007.8.3.219)
8. Briskie JV & Montgomerie R 1992 Sperm size and sperm competition in birds. Proceedings of the Royal Society of London. Series B 247 89-95. (doi:10.1098/rspb.1992.0013)
9. Briskie JV, Montgomerie R & Birkhead TR 1997 The evolution of sperm size in birds. Evolution 51 937-945. (doi:10.2307/2411167)
10. Byrne PG, Simmons LW & Roberts JD 2003 Sperm competition and the evolution of gamete morphology in frogs. Proceedings of the Royal Society of London. Series B 270 2079-2086. (doi:10.1098/rspb.2003.2433)
11. Calhim S, Immler S & Birkhead TR 2007 Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS ONE 2 e413 (doi: 410.1371/journal.pone.0000413). (doi:10.1371/journal.pone.0000413)
12. Clermont Y 1958 Structure de l'épithélium séminal et mode de renouvellement des spermatogonies chez le canard. Archives d'Anatomie Microscopique et de Morphologie Expérimentale 44 47-66.
13. Clermont Y & Perey B 1957 Quantitative study of the cell population of the seminiferous tubules in immature rats. American Journal of Anatomy 100 241-267. (doi:10.1002/aja.1001000205)
14. Courot M, Hochereau-de Reviers M-T & Ortavant R 1970 Spermatogenesis. In The Testis, pp 339-432. Eds AD Johnson, WR Gomes & NL Vandemark. New York: Academic Press.
15. Ehmcke J, Wistuba J & Schlatt S 2006 Spermatogonia: physiology, pathology and clinical relevance. Human Reproduction Update 12 275-282. (doi:10.1093/humupd/dmk001)
16. Fawcett DW 1975 Ultrastructure and function of the Sertoli cell. In Handbook of Physiology, pp 21-55. Eds DW Hamilton & RO Greep. Washington, DC: American Physiological Society.
17. Felsenstein J 1985 Phylogenies and the comparative method. American Naturalist 125 1-15. (doi:10.1086/284325)
18. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N & Balshine S 2009 Female promiscuity promotes the evolution of faster sperm in cichlid fishes. PNAS 106 1128-1132. (doi:10.1073/pnas.0809990106)
19. França LR & Godinho CL 2003 Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus). Biology of Reproduction 68 1554-1561. (doi:10.1095/biolreprod.102. 010652)
20. França LR & Russell LD 1998 The testis of domestic animals. In Male Reproduction. A Multidisciplinary Overview, pp 197-219. Eds F Martínez & J Regadera. Madrid: Churchill Livingsone.
21. França LR, Ogawa T, Avarbockm MR, Brinster RL & Russell LD 1998 Germ cell genotype control cell cycle during spermatogenesis in the rat. Biology of Reproduction 59 1371-1377. (doi:10.1095/biolreprod59.6.1371)
22. Freckleton RP, Harvey PH & Pagel M 2002 Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160 712-726. (doi:10.1086/343873)
23. Gage MJG 1994 Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society of London. Series B 258 247-254. (doi:10.1098/rspb.1994.0169)
24. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB & Parker GA 2004 Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Current Biology 14 44-47. (doi:10.1016/j.cub.2003.12.028)
25. Gondos B & Berndtson WE 1993 Postnatal and pubertal development of Sertoli cells. In The Sertoli Cell, pp 115-154. Eds LD Russell & MD Griswold. Clearwater, FL: Cache River Press.
26. Griswold MD 1993 Protein secretion by Sertoli cells. In The Sertoli Cell, pp 195-200. Eds LD Russell & MD Griswold. Clearwater, FL: Cache River Press.
27. Gundersen HJ & Jensen EB 1987 The efficiency of systematic sampling in stereology and its prediction. Journal of Microscopy 147 229-263.
28. Harvey PH & Pagel MD 1991 The Comparative Method in Evolutionary Biology, Oxford, UK: Oxford University Press.
29. Hess RA & de Franca LR 2008 Spermatogenesis and cycle of the seminiferous epithelium. In Molecular Mechanisms in Spermatogenesis, pp 1-15. Ed. CY Cheng. New York: Springer.
30. Honaramooz A, Li M-W, Penedo MCT, Meyers S & Dobrinski I 2004 Accelerated maturation of primate testis by xenografting into mice. Biology of Reproduction 70 1500-1503. (doi:10.1095/biolreprod.103.025536)
31. Immler S & Birkhead TR 2007 Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proceedings of the Royal Society of London. Series B 274 561-568. (doi:10.1098/rspb.2006.3752)
32. Immler S, Calhim S & Birkhead TR 2008 Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62 1538-1543. (doi:10.1111/j.1558-5646.2008.00393.x)
33. Immler S, Pitnick S, Parker GA, Durrant K, Lüpold S, Calhim S & Birkhead TR 2011 Resolving variation in the reproductive tradeoff between sperm size and number. PNAS 108 5325-5330. (doi:10.1073/pnas.1009059108)
34. Jamieson BGM 2007 Avian spermatozoa: structure and phylogeny. In Reproductive Biology and Phylogeny of Birds, pp 349-511. Ed. BGM Jamieson. Enfield, New Hampshire: Science Publishers.
35. Jaramillo A & Burke P 1999 New World Blackbirds: the Icterids, London: Helm.
36. Johnson L, Varner DD, Tatum ME & Scrutchfield WL 1991 Season but not age affects Sertoli cell number in adult stallions. Biology of Reproduction 45 404-410. (doi:10.1095/biolreprod45.3.404)
37. Jones RC & Lin M 1993 Spermatogenesis in birds. Oxford Reviews of Reproductive Biology 15 233-264.
38. Kleven O, Laskemoen T, Fossøy F, Robertson RJ & Lifjeld JT 2008 Intraspecific variation in sperm length is negatively related to sperm competition in passerine birds. Evolution 62 494-499. (doi:10.1111/j.1558-5646. 2007.00287.x)
39. LaMunyon CW & Ward S 1998 Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proceedings of the Royal Society of London. Series B 265 1997-2000. (doi:10.1098/rspb.1998.0531)
40. Lin M, Jones RC & Blackshaw AW 1990 The cycle of the seminiferous epithelium in the Japanese quail (Coturnix coturnix japonica) and estimation of its duration. Journal of Reproduction and Fertility 88 481-490. (doi:10.1530/jrf.0.0880481)
41. Luetjens CM, Weinbauer GF & Wistuba J 2005 Primate spermatogenesis: new insights into comparative testicular organisation, spermatogenic efficiency and endocrine control. Biological Reviews 80 475-488. (doi:10.1017/ S1464793105006755)
42. Lüpold S, Calhim S, Immler S & Birkhead TR 2009a Sperm morphology and sperm velocity in passerine birds. Proceedings of the Royal Society of London. Series B 276 1175-1181. (doi:10.1098/rspb.2008.1645)
43. Lüpold S, Linz GM & Birkhead TR 2009b Sperm design and variation in the New World Blackbirds (Icteridae). Behavioral Ecology and Sociobiology 63 899-909. (doi:10.1007/s00265-009-0733-6)
44. Lüpold S, Linz GM, Rivers JW, Westneat DF & Birkhead TR 2009c Sperm competition selects beyond relative testes size in birds. Evolution 63 391-402. (doi:10.1111/j.1558-5646.2008.00571.x)
45. Martin PA, Reimers TJ, Lodge JR & Dziuk PJ 1974 Effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. Journal of Reproduction and Fertility 39 251-258. (doi:10.1530/jrf.0.0390251)
46. Meachem SJ, Stanton PG & Schlatt S 2005 Follicle-stimulating hormone regulates both Sertoli cell and spermatogonial populations in the adult photoinhibited Djungarian hamster testis. Biology of Reproduction 72 1187-1193. (doi:10.1095/biolreprod.104.039321)
47. Miller GT & Pitnick S 2002 Sperm-female coevolution in Drosophila. Science 298 1230-1233. (doi:10.1126/science.1076968)
48. Nagy F 1972 Cell division kinetics and DNA synthesis in the immature Sertoli cells of the rat testis. Journal of Reproduction and Fertility 38 389-395. (doi:10.1530/jrf.0.0280389)
49. Nakagawa S & Cuthill IC 2007 Effect size, confidence interval and statistical significance: a practical guide for biologists. Biological Reviews 82 591-605. (doi:10.1111/j.1469-185X.2007.00027.x)
50. Noirault J, Brillard JP & Bakst MR 2006 Spermatogenesis in the turkey (Meleagris gallopavo): quantitative approach in immature and adult males subjected to various photoperiods. Theriogenology 65 845-859. (doi:10.1016/j.theriogenology.2005.01.012)
51. Oppliger A, Hosken DJ & Ribi G 1998 Snail sperm production characteristics vary with sperm competition risk. Proceedings of the Royal Society of London. Series B 265 1527-1534. (doi:10.1098/rspb.1998.0468)
52. Pagel M 1999 Inferring the historical patterns of biological evolution. Nature 401 877-884. (doi:10.1038/44766)
53. Parker GA 1970 Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45 526-567. (doi:10.1111/j.1469-185X.1970.tb01176. x)
54. 2. Journal of Theoretical Biology 264 1003-1023. (doi:10.1016/j.jtbi.2010.03.003)
55. Pattarini JM, Starmer WT, Bjork A & Pitnick S 2006 Mechanisms underlying the sperm quality advantage in Drosophila melanogaster. Evolution 60 2064-2080. (doi:10.1554/06-142.1)
56. Pitnick S 1996 Investment in testes and the cost of making long sperm in Drosophila. American Naturalist 148 57-80. (doi:10.1086/285911)
57. Ramm SA & Stockley P 2010 Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biology Letters 6 219-221. (doi:10.1098/rsbl.2009.0635)
58. de Reviers M 1988 Appareil génital mâle et production des spermatozoïdes. In Reproduction des Volailles et Production d'Oeufs, pp 141-181. Ed. B Sauveur. Paris: INRA.
59. Roosen-Rungen EC 1973 Germinal-cell loss in normal metazoan spermatogenesis. Journal of Reproduction and Fertility 35 339-348. (doi:10.1530/jrf.0.0350339)
60. Rosiepen G, Weinbauer GF, Schlatt S, Behre HM & Nieschlag E 1994 Duration of the cycle of the seminiferous epithelium, estimated by the 5-bromodeoxyuridine technique, in laboratory and feral rats. Journal of Reproduction and Fertility 100 299-306. (doi:10.1530/jrf.0.1000299)
61. Russell LD & Peterson RN 1984 Determination of the elongate spermatid Sertoli cell ratio in various mammals. Journal of Reproduction and Fertility 70 635-641. (doi:10.1530/jrf.0.0700635)
62. Russell LD, Ren HP, Hikim IS, Schulze W & Hikim APS 1990 A comparative study in twelve mammalian species of volume densities, volumes, and numerical densities of selected testis components, emphasizing those related to the Sertoli cell. American Journal of Anatomy 188 21-30. (doi:10.1002/aja. 1001880104)
63. Segatelli TM, França LR, Pinheiro PFF, Almeida CCD, Martinez M & Martinez FE 2004 Spermatogenic cycle length and spermatogenic efficiency in the gerbil (Meriones unguiculatus). Journal of Andrology 25 872-880. (Pubitemid 39425590)
64. Sharpe RM 1994 Regulation of spermatogenesis. In The Physiology of Reproduction, pp 1363-1394. Eds E Knobil & JD Neill. New York: Raven Press.
65. Snook RR 2005 Sperm in competition: not playing by the numbers. Trends in Ecology & Evolution 20 46-53. (doi:10.1016/j.tree.2004.10.011)
66. Sterio DC 1984 The unbiased estimation of number and sizes of arbitrary particles using the dissector. Journal of Microscopy 134 127-136. (Pubitemid 14121386)
67. Webster MS 1992 Sexual dimorphism, mating system and body size in New World Blackbirds (Icterinae). Evolution 46 1621-1641. (doi:10.2307/2410020)
68. Weinbauer GF, Aslam H, Krishnamurty H, Brinkworth MH, Einspanier A & Hodges JK 2001 Quantitative analysis of spermatogenesis and apoptosis in the common Marmoset (Callithrix jacchus) reveals high rates of spermatogonial turnover and high spermatogenic efficiency. Biology of Reproduction 64 120-126. (doi:10.1095/biolreprod64.1.120)
69. Wing TY & Christensen AK 1982 Morphometric studies on rat seminiferous tubules. American Journal of Anatomy 165 13-25. (doi:10.1002/aja.1001650103)
70. Wistuba J, Schrod A, Greve B, Hodges JK, Aslam H, Weinbauer GF & Luetjens CM 2003 Organization of seminiferous epithelium in primates: relationship to spermatogenic efficiency, phylogeny, and mating system. Biology of Reproduction 69 582-591. (doi:10.1095/biolreprod.103.015925)
71. Wistuba J, Stuckenborg JB & Luetjens CM 2007 Mammalian spermatogenesis. Functional Development and Embryology 1 99-117.
72. Wolfson A 1954 Sperm storage at lower-than-body temperature outside the body cavity in some passerine birds. Science 120 68-71. (doi:10.1126/science. 120.3106.68)
73. Yamamoto S, Tamate H & Itikawa O 1967 Morphological studies on the sexual maturation in the male Japanese quail (Coturnix coturnix japonica). II. The germ cell types and cellular associations during spermatogenesis. Tohoku Journal of Agricultural Research 18 27-37.
74. Zeng W, Avelar GF, Rathi R, França LR & Dobrinski I 2006 The length of the spermatogenic cycle is conserved in porcine and ovine testis xenografts. Journal of Andrology 27 527-533. (doi:10.2164/jandrol.05143)
75. Zhengwei Y, McLachlan RI, Bremner WJ & Wredford NG 1997 Quantitative (stereological) study of normal spermatogenesis in the adult monkey (Macaca fascicularis). Journal of Andrology 18 681-687. (Pubitemid 28098782)