Functional variation of sperm morphology in sticklebacks

Behavioral Ecology and Sociobiology

Volumn 68, Issue 4, 2014, Pages 617-627

  Bakker, Theo C M ^a   Hollmann, Michael ^a   Mehlis, Marion ^a   Zbinden, Marc ^a,b  

^a UNIVERSITY OF BONN   (Germany)

^b Schweizerische Nationalfonds SNF   (Switzerland)

Author keywords

Fertilisation rate; Flagellum length; Gasterosteus aculeatus; Midpiece volume; Ratio of head to tail length; Sperm morphology

Indexed keywords

BIOLOGICAL PRODUCTION; BODY SHAPE; BODY SIZE; FERTILIZATION (REPRODUCTION); FISH; FUNCTIONAL CHANGE; POPULATION GENETICS; SCANNING ELECTRON MICROSCOPY; SPERM;

GASTEROSTEUS ACULEATUS;

EID: 84896100603     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-013-1676-5     Document Type: Article

References (80)

1. Anderson MJ, Dixson AF (2002) Motility and the midpiece in primates. Nature 416: 496.
2. Anderson MJ, Dixson AS, Dixson AF (2006) Mammalian sperm and oviducts are sexually selected: evidence for co-evolution. J Zool 270: 682-686.
3. Bakker TCM, Zbinden M, Frommen JG, Weiss A, Largiadèr CR (2006) Slow fertilization of stickleback eggs: the result of sexual conflict? BMC Ecol 6: 7.
4. Ball MA, Parker GA (1996) Sperm competition games: external fertilization and "adaptive" infertility. J Theor Biol 180: 141-150.
5. Ball MA, Parker GA (1997) Sperm competition games: inter- and intraspecies results of a continuous external fertilization model. J Theor Biol 186: 459-466.
6. Balshine S, Leach BJ, Neat F, Werner NY, Montgomerie R (2001) Sperm size of African cichlids in relation to sperm competition. Behav Ecol 12: 726-731.
7. Barber I, Arnott SA (2000) Split-clutch IVF: a technique to examine indirect fitness consequences of mate preferences in sticklebacks. Behaviour 137: 1129-1140.
8. Barber I, Arnott SA, Braithwaite VA, Andrew J, Huntingford FA (2001) Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc R Soc Lond B 268: 71-76.
9. Becker WA (1992) Manual of quantitative genetics, 5th edn. Academic, Pullman.
10. Bell MA, Foster SA (eds) (1994) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford.
11. Birkhead TR, Hosken DJ, Pitnick S (eds) (2009) Sperm biology: an evolutionary perspective. Academic, Amsterdam.
12. Briskie JV, Montgomerie R (1992) Sperm size and sperm competition in birds. Proc R Soc Lond B 247: 89-95.
13. Burness G, Casselman SJ, Schulte-Hostedde AI, Moyes CD, Montgomerie R (2004) Sperm swimming speed and energetics vary with sperm competition risk in bluegill (Lepomis macrochirus). Behav Ecol Sociobiol 56: 65-70.
14. Butts IAE, Johnson K, Wilson CC, Pitcher TE (2013) Ovarian fluid enhances sperm velocity based on relatedness in lake trout, Salvelinus namaycush. Theriogenology 78: 2105-2109.
15. Candolin U, Vlieger L (2013) Should attractive males sneak: the trade-off between current and future offspring. PLoS ONE 8: e57992.
16. de Fraipont M, FitzGerald GJ, Guderley H (1993) Age-related differences in reproductive tactics in the three-spined stickleback, Gasterosteus aculeatus. Anim Behav 46: 961-968.
17. Dean MD, Nachman MW (2009) Faster fertilization rate in conspecific versus heterospecific matings in house mice. Evolution 63: 20-28.
18. Dziminski MA, Roberts JD, Beveridge M, Simmons LW (2009) Sperm competitiveness in frogs: slow and steady wins the race. Proc R Soc Lond B 276: 3955-3961.
19. Elgee KE, Evans JP, Ramnarine IW, Rush SA, Pitcher TE (2010) Geographic variation in sperm traits reflects predation risk and natural rates of multiple paternity in the guppy. J Evol Biol 23: 1331-1338.
20. Elofsson H, McAllister BG, Kime DE, Mayer I, Borg B (2003) Long lasting stickleback sperm; is ovarian fluid a key to success in fresh water? J Fish Biol 63: 240-253.
21. Evans JP (2011) Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies. Heredity 106: 869-875.
22. Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Longman, Harlow.
23. Fauvel C, Savoye O, Dreanno C, Cosson J, Suquet M (1999) Characteristics of sperm of captive seabass in relation to its fertilization potential. J Fish Biol 54: 356-369.
24. Firman RC, Simmons LW (2009) Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64: 1245-1256.
25. Firman RC, Simmons LW (2010) Sperm midpiece length predicts sperm swimming velocity in house mice. Biol Lett 6: 513-516.
26. Fitzpatrick JL, Desjardins JK, Milligan N, Montgomerie R, Balshine S (2007) Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid. Biol Reprod 77: 280-284.
27. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci U S A 106: 1128-1132.
28. Fitzpatrick JL, Garcia-Gonzalez F, Evans JP (2010) Linking sperm length and velocity: the importance of intramale variation. Biol Lett 6: 797-799.
29. Fitzpatrick JL, Simmons LW, Evans JP (2012) Complex patterns of multivariate selection on the ejaculate of a broadcast spawning marine invertebrate. Evolution 66: 2451-2460.
30. Gage MJG, Macfarlane C, Yeates S, Shackleton R, Parker GA (2002) Relationships between sperm morphometry and sperm motility in the Atlantic salmon. J Fish Biol 61: 1528-1539.
31. Gasparini C, Pilastro A (2011) Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc R Soc Lond B 278: 2495-2501.
32. Gomendio M, Roldan ERS (1991) Sperm competition influences sperm size in mammals. Proc R Soc Lond B 243: 181-186.
33. Helfenstein F, Podevin M, Richner H (2010) Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behav Ecol Sociobiol 64: 557-565.
34. Higginson DM, Miller KB, Segraves KA, Pitnick S (2012) Female reproductive tract form drives the evolution of complex sperm morphology. Proc Natl Acad Sci U S A 109: 4538-4543.
35. Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8: 319.
36. Jamieson BGM (1991) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, Cambridge.
37. Jamieson BGM (2009) Ultrastructure of spermatozoa: Acanthopterygii continued: Percomorpha. In: Jamieson BGM (ed) Reproductive biology and phylogeny of fishes (agnathans and bony fishes), part A. Science Publishers, Enfield, pp 503-684.
38. Johnson DW, Monro K, Marshall DJ (2012) The maintenance of sperm variability: context-dependent selection on sperm morphology in a broadcast spawning invertebrate. Evolution 67: 1383-1395.
39. Karr TL, Swanson WJ, Snook RR (2009) The evolutionary significance of variation in sperm-egg interactions. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, Amsterdam, pp 305-365.
40. Katz DF, Drobins EZ (1990) Analysis and interpretation of the forces generated by spermatozoa. In: Bavister BD, Cummins J, Roldan ERS (eds) Fertilization in mammals. Serono Symposia, Norwell, pp 125-137.
41. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT (2009) Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63: 2466-2473.
42. Kraak SBM, Bakker TCM, Mundwiler B (1999) Correlates of the duration of the egg collecting phase in the three-spined stickleback. J Fish Biol 54: 1038-1049.
43. Largiadèr CR, Fries V, Bakker TCM (2001) Genetic analysis of sneaking and egg-thievery in a natural population of the three-spined stickleback (Gasterosteus aculeatus L.). Heredity 86: 459-468.
44. Laskemoen T, Kleven O, Fossøy F, Robertson RJ, Rudolfsen G, Lifjeld JT (2010) Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolour. Behav Ecol Sociobiol 64: 1473-1483.
45. Laskemoen T, Albrecht T, Bonisoli-Alquati A, Cepak J, de Lope F et al (2013) Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations. Behav Ecol Sociobiol 67: 301-309.
46. Lemke MJ, Chiva M, Coyle B, Kulak D, MacKay M, Kasinsky H (1999) Variability of sperm nuclear basic proteins in the three-spined stickleback and related species of Gasterosteoidei. Comp Biochem Physiol B 122: 339-353.
47. Levitan DR (2000) Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegates. Proc R Soc Lond B 267: 531-534.
48. Lifjeld JT, Laskemoen T, Kleven O, Albrecht T, Robertson RJ (2010) Sperm length variation as a predictor of extrapair paternity in passerine birds. PLoS ONE 5: e13456.
49. Lifjeld JT, Laskemoen T, Kleven O, Pedersen ATM, Lampe HM, Rudolfsen G, Schmoll T, Slagsvold T (2012) No evidence for pre-copulatory sexual selection on sperm length in a passerine bird. PLoS ONE 7: e32611.
50. Lüpold S, Calhim S, Immler S, Birkhead TR (2009) Sperm morphology and sperm velocity in passerine birds. Proc R Soc Lond B 276: 1175-1181.
51. Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ, Roldan ERS (2006) Sperm design and sperm function. Biol Lett 2: 246-249.
52. Mattei X (1991) Spermatozoon ultrastructure and its systematic implications in fishes. Can J Zool 69: 3038-3055.
53. Mehlis M, Frommen JG, Rahn AK, Bakker TCM (2012) Inbreeding in three-spined sticklebacks (Gasterosteus aculeatus L.): effects on testis and sperm traits. Biol J Linn Soc 107: 510-520.
54. Mehlis M, Hilke LK, Bakker TCM (2013) Attractive males have faster sperm in three-spined sticklebacks Gasterosteus aculeatus. Curr Zool 59: 761-768.
55. Montgomerie R, Fitzpatrick JL (2009) Testes, sperm, and sperm competition. In: Jamieson BGM (ed) Reproductive biology and phylogeny of fishes (agnathans and bony fishes), part B. Science Publishers, Enfield, pp 1-53.
56. Moore PJ, Harris WE, Montrose VT, Levin D, Moore AJ (2004) Constraints on evolution and postcopulatory sexual selection: trade-offs among ejaculate characteristics. Evolution 58: 1773-1780.
57. Mortimer D (1994) Practical laboratory andrology. Oxford University Press, Oxford.
58. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev Camb Philos Soc 45: 525-567.
59. Parker GA (1993) Sperm competition games: sperm size and sperm number under adult control. Proc R Soc Lond B 253: 245-254.
60. Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, San Diego, pp 3-54.
61. Pinheiro JC, Bates D, DebRoy S, Sarkar D (2009) nlme: linear and nonlinear mixed effects models. R Packag 3: 1-93.
62. Pitnick S, Hosken DJ, Birkhead TR (2009a) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, Amsterdam, pp 69-149.
63. Pitnick S, Wolfner MF, Suarez SS (2009b) Ejaculate-female and sperm-female interactions. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, Amsterdam, pp 247-304.
64. Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, Amsterdam, pp 207-245.
65. Pizzari T, Worley K, Burke T, Froman DP (2008) Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol Biol 8: 332.
66. Rice WD, Gaines SD (1994) Extending nondirectional heterogeneity tests to evaluate simply ordered alternative hypotheses. Proc Natl Acad Sci U S A 91: 225-226.
67. Rick IP, Mehlis M, Eßer E, Bakker TCM (2013) The influence of ambient UV light on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus). Oecologia (published online, doi: 10. 1007/s00442-013-2773-x).
68. Simpson JL, Humphries S, Evans JP, Simmons LW, Fitzpatrick JL (2013) Relationship between sperm length and speed differ among three internally and three externally fertilizing species. Evolution. doi: 10. 1111/evo. 12199.
69. Skinner AMJ, Watt PJ (2007) Phenotypic correlates of spermatozoon quality in the guppy, Poecilia reticulata. Behav Ecol 18: 47-52.
70. Smith CC, Ryan MJ (2010) Evolution of sperm quality but not quantity in the internally fertilized fish Xiphophorus nigrensis. J Evol Biol 23: 1759-1771.
71. Snook RR (2005) Sperm in competition: not playing by the numbers. Trends Ecol Evol 20: 46-53.
72. Stockley P, Gage MJG, Parker GA, Møller AP (1996) Female reproductive biology and the coevolution of ejaculate characteristics in fish. Proc R Soc Lond B 263: 451-458.
73. Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149: 933-954.
74. Swarup H (1958) Stages in the development of the stickleback Gasterosteus aculeatus (L.). J Embryol Exp Morphol 6: 373-383.
75. Tourmente M, Gomendio M, Roldan ERS (2011) Sperm competition and the evolution of sperm design in mammals. BMC Evol Biol 11: 12.
76. Tuset VM, Dietrich GJ, Wojtczak M, Słowinska M, de Monserrat J, Ciereszko A (2008) Relationships between morphology, motility and fertilization capacity in rainbow trout (Oncorhynchus mykiss) spermatozoa. J Appl Ichthyol 24: 393-397.
77. Urbach D, Folstad I, Rudolfsen G (2005) Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus). Behav Ecol Sociobiol 57: 438-444.
78. Wootton RJ (1976) The biology of the sticklebacks. Academic, London.
79. Wootton RJ (1984) A functional biology of sticklebacks. Croom Helm, London.
80. Zbinden M, Largiadèr CR, Bakker TCM (2001) Sperm allocation in the three-spined stickleback. J Fish Biol 59: 1287-1297.