The evolution of expenditure on testes

Journal of Zoology

Volumn 298, Issue 1, 2016, Pages 3-19

  Parker, G A ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Gonadosomatic index; Mating rate; Relative testes size; Sexual cascade; Sperm allocation; Sperm competition; Sperm demand

Indexed keywords

ANIMALIA;

EID: 84961927520     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/jzo.12297     Document Type: Article

References (141)

1. Alonzo, S.H. & Pizzari, T. (2013). Selection on female remating interval is influenced by male sperm competition strategies and ejaculate characteristics. Phil. Trans. Roy. Soc. B 368, 20120044.
2. Anholeto, L.A., Nunes, P.H., Remédio, R.N., Camargo-Mathias, M.I. (2015). Testes of fed and unfed Amblyomma cajennense ticks (Acari: Ixodidae). First morphological data. Acta Zool. 96, 375-382.
3. Arnqvist, G. & Rowe, L. (2005). Sexual conflict. Princeton: Princeton University Press.
4. Baker, R.R. & Bellis, M.A. (1995). Human sperm competition: copulation, masturbation and infidelity. London: Chapman and Hall.
5. delBarco-Trillo, J. (2011). Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J. Evol. Biol. 24, 1706-1714.
6. Barrett, S.C.H. & Hough, J. (2013). Sexual dimorphism in flowering plants. J. Exp. Bot. 64, 67-82.
7. Benítez-Villalobos, F., Aguilar-Duarte, C. & Avila-Poveda, O.H. (2012). Reproductive biology of Ophiocoma aethiops and O. alexandri (Echinodermata: Ophiuroidea) from Estacahuite Bay, Oaxaca, Mexico. Aquat. Biol. 17, 119-128.
8. Birkhead, T.R. (2008). The wisdom of birds. London: Bloomsbury Publishing.
9. Birkhead, T.R. (2010). How stupid not to have thought of that: post-copulatory sexual selection. J. Zool. 281, 78-93.
10. Birkhead, T.R. & Møller, A.P. (1992). Sperm competition in birds: evolutionary causes and consequences. London: Academic Press.
11. Birkhead, T.R. & Monaghan, P. (2010). Ingenious ideas: the history of behavioral ecology. In Evolutionary behavioral ecology: 3-15. Westneat, D.F. & Fox, C. (Eds). Oxford: Oxford University Press.
12. Bissoondath, C.J. & Wiklund, C. (1995). Protein content of spermatophores in relation to monandry/polyandry in butterflies. Behav. Ecol. Sociobiol. 37, 365-371.
13. Buffon, G.L. (1781). Histoire Naturelle des Oiseaux. Paris: De l'imprimerie royale.
14. Buzatto, B.A., Roberts, J.D. & Simmons, L.W. (2015). Sperm competition and the evolution of precopulatory weapons: increased male density promotes sperm competition and reduces selection on arm strength in a chorusing frog. Evolution (in press). DOI: 10.1111/evo.12766.
15. Byrne, P.G., Roberts, J.D. & Simmons, L.W. (2002). Sperm competition selects for increased testes mass in Australian frogs. J. Evol. Biol. 15, 347-355.
16. Byrne, P.G., Simmons, L.W. & Roberts, J.D. (2003). Sperm competition and the evolution of gamete morphology in frogs. Proc. Roy. Soc. B 270, 2079-2086.
17. Calhim, S. & Birkhead, T.R. (2007). Testes size in birds: quality versus quantity-assumptions, errors, and estimates. Behav. Ecol. 18, 271-275.
18. Charnov, E.L. (1979). Simultaneous hermaphroditism and sexual selection. Proc. Natl Acad. Sci. USA 76, 2480-2484.
19. Charnov, E.L. (1980). Sex allocation and local mate competition in barnacles. Mar. Biol. Lett. 1, 269-272.
20. Charnov, E.L. (1982). The theory of sex allocation. Princeton: Princeton University Press.
21. Charnov, E.L. (1996). Sperm competition and sex allocation in simultaneous hermaphrodites. Evol. Ecol. 10, 457-462.
22. Charnov, E.L., Maynard Smith, J. & Bull, J.J. (1976). Why be an hermaphrodite? Nature 263, 125-126.
23. Choat, J.H. & Robertson, D.R. (1975). Protogynous hermaphroditism of the family Scaridae. In Intersexuality in the animal kingdom: 263-283. Reinboth, R. (Ed). New York: Springer-Verlag.
24. Cohen, J. (1973). Cross-overs, sperm redundancy and their close association. Heredity 31, 408-413.
25. Coleman, S.W. & Jones, A.G. (2011). Patterns of multiple paternity and maternity in fishes. Biol. J. Linn. Soc. 103, 735-760.
26. Cordes, N., Albrecht, F., Engqvist, L., Schmoll, T., Baier, M., Müller, C. & Reinhold, K. (2015). Larval food composition affects courtship song and sperm expenditure in a lekking moth. Ecol. Ent. 40, 34-41.
27. Crudgington, H.S., Fellows, S., Badcock, N.S. & Snook, R.R. (2009). Experimental manipulation of sexual selection promotes greater male mating capacity but does not alter sperm investment. Evolution 63, 926-938.
28. Darwin, C. (1871/1874). The descent of man selection in relation to sex. London: John Murray.
29. Dixson, A.F. (2009). Sexual selection and the origins of human mating systems. Oxford: Oxford University Press.
30. Düsing, C. (1884). Die Regulierung des Geschlechtsverhältnisses bei der Vermehrung der Menschen, Tiere und Pflanzen. Jean: Fischer.
31. Edwards, A.W.F. (2000). Carl Düsing (1884) on the regulation of the sex-ratio. Theor. Pop. Biol. 58, 255-257.
32. Emerson, S.B. (1997). Testis size variation in frogs: testing the alternatives. Behav. Ecol. Sociobiol. 41, 227-236.
33. Engqvist, L. & Reinhold, K. (2005). Pitfalls in experiments testing predictions from sperm competition theory. J. Evol. Biol. 18, 116-123.
34. Evans, J.P. & Simmons, L.W. (2008). The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good- and sexy-sperm? Genetica 134, 5-19.
35. Ferrandiz-Rovira, M., Lemaître, J.-F., Lardy, S., López, B.C. & Cohas, A. (2014). Do pre- and post-copulatory sexually selected traits covary in large herbivores? BMC Evol. Biol. 14, 79.
36. Firman, R.C., Garcia-Gonzalez, F., Thyer, E., Wheeler, S., Yamin, Z., Yuan, M. & Simmons, L.W. (2015). Evolutionary change in testes tissue composition among experimental populations of house mice. Evolution 69, 848-855.
37. Fischer, E.A. (1981). Sexual allocation in a simultaneously hermaphroditic coral reef fish. Am. Nat. 117, 64-82.
38. Fisher, R.A. (1930). The genetical theory of natural selection. Oxford: Clarendon Press.
39. Fisher, D.O., Dickman, C.R., Jones, M.E. & Blomberg, S.P. (2013). Sperm competition drives the evolution of suicidal reproduction in mammals. Proc. Natl Acad. Sci. USA 110, 17910-17914.
40. Fitzpatrick, J.L., Simmons, L.W. & Evans, J.P. (2012a). Complex patterns of multivariate selection on the ejaculate of a broadcast spawning marine invertebrate. Evolution 66, 2451-2460.
41. Fitzpatrick, J.L., Almbro, M., Gonzalez-Voyer, A., Kolm, N. & Simmons, L.W. (2012b). Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66, 3595-3604.
42. Flatt, T. & Heyland, A. (2011). Mechanisms of life history evolution: the genetics and physiology of life history evolution. Oxford: Oxford University Press.
43. Fromhage, L., McNamara, J. & Houston, A.I. (2008). Sperm allocation strategies and female resistance: a unifying perspective. Am. Nat. 172, 25-33.
44. Gage, M.J.G. (1995). Continuous variation in reproductive strategy as an adaptive response to population density in the moth Plodia interpunctella. Proc. Roy. Soc. Lond. B 261, 25-30.
45. Haldane, J.B.S. (1932). The causes of evolution. London: Longmans: Green & Co..
46. Hamilton, W.D. (1967). Extraordinary sex ratios. Science 156, 477-488.
47. Harcourt, A.H., Harvey, P.H., Larson, S.G. & Short, R.V. (1981). Testis weight, body weight and breeding system in primates. Nature 293, 55-57.
48. Hayward, A. & Gillooly, J.F. (2011). The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6, e16557.
49. Heath, D.J. (1977). Simultaneous hermaphroditism: cost and benefit. J. Theor. Biol. 64, 363-373.
50. Heinroth, O. (1911). Beitrag zur Biologie, namentlich Ethologie und Psychologie der Anatiden. Verh. V. Internat. Ornith. Kongresses, Berlin 1910, 589-702.
51. Henshaw, J.M., Marshall, D.J., Jennions, M.D. & Kokko, H. (2014). Local gamete competition explains sex allocation and fertilization strategies in the sea. Am. Nat. 184, E32-E49.
52. Janicke, T., Marie-Orleach, L., De Mulder, K., Berezikov, E., Ladurner, P., Vizoso, D.B. & Schärer, L. (2013). Sex allocation adjustment to mating group size in a simultaneous hermaphrodite. Evolution 67, 3233-3242.
53. Janicke, T., David, P. & Chapuis, E. (2015). Environment-dependent sexual selection: Bateman's parameters under varying levels of food availability. Am. Nat. 185, 756-768.
54. Jenner, E. (1824). Some observations on the migration of birds. Phil. Trans. Roy. Soc. 42, 11-44.
55. Karlsson, B. (1995). Resource allocation and mating strategies in butterflies. Evolution 49, 955-961.
56. Kelly, C.D. & Jennions, M.D. (2011). Sexual selection and sperm quantity: meta- analyses of strategic ejaculation. Biol. Rev. 86, 863-884.
57. !Kenagy, G.J. & Trombulak, S.C. (1986). Size and function of mammalian testes in relation to body size. J. Mammal. 67, 1-22.
58. Klemme, I., Soulsbury, C.D. & Henttonen, H. (2015). Contrasting effects of large density changes on relative testes size in fluctuating populations of sympatric vole species. Proc. Roy. Soc. B 281, 20141291.
59. Kvarnemo, C. & Simmons, L.W. (2004). Testes investment and spawning mode in pipefishes and seahorses (Syngnathidae). Biol. J. Linn. Soc. 83, 369-376.
60. Kvarnemo, C. & Simmons, L.W. (2013). Polyandry as a mediator of sexual selection before and after mating. Phil. Trans. Roy. Soc. B 2013, 20120042.
61. Lehtonen, J. & Kokko, H. (2011). Two roads to two sexes: unifying gamete competition and gamete limitation in a single model of anisogamy evolution. Behav. Ecol. Sociobiol. 65, 445-459.
62. Lehtonen, J. & Parker, G.A. (2014). Gamete competition, gamete limitation and the evolution of the two sexes. Mol. Human Reprod. 20, 1161-1168.
63. Lemen, C. (1980). Allocation of reproductive effort to the male and female strategies in wind-pollinated plants. Oecologia 45, 156-159.
64. Levitan, D.R. & Petersen, C. (1995). Sperm limitation in the sea. Trends Ecol. Evol. 10, 228-231.
65. Lewis, C. & Long, T.A.F. (2005). Courtship and reproduction in Carybdea sivickisi (Cnidaria: Cubozoa). Mar. Biol. 147, 477-483.
66. Linhart, O., Rodina, M. & Kaspar, V. (2015). Common carp (Cyprinus carpio Linneaus, 1758) male fertilization potency with secure number of spermatozoa per ova. J. Appl. Ichthyol. 31(Suppl. 1), 169-173.
67. Lüpold, S., Wistuba, J., Damm, O.S., Rivers, J.W. & Birkhead, T.R. (2011). Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality. Reproduction 141, 595-605.
68. Lüpold, S., Tomkins, J.L., Simmons, L.W. & Fitzpatrick, J.L. (2014). Female monopolization mediates the relationship between pre- and postcopulatory sexual traits. Nature Commun. 5, 1038.
69. Michiels, N.K., Crowley, P.H. & Anthes, N. (2009). Accessory male investment can undermine the evolutionary stability of simultaneous hermaphroditism. Biol. Lett. 5, 709-712.
70. Møller, A.P. (1989). Ejaculate quality, testes size and sperm production in mammals. Funct. Ecol. 3, 91-96.
71. Montoto, L.G., Arregui, L., Sanchez, N.M., Gomendio, M. & Roldan, E.R.S. (2012). Postnatal testicular development in mouse species with different levels of sperm competition. Reproduction 143, 333-346.
72. Parker, G.A. (1968). The sexual behaviour of the blowfly, Protophormia terrae-novae R.-D. Behaviour 32, 291-308.
73. Parker, G.A. (1970a). Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525-567.
74. Parker, G.A. (1970b). The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. (Diptera: Scatophagidae). V. The female's behaviour at the oviposition site. Behaviour 37, 140-168.
75. Parker, G.A. (1979). Sexual selection and sexual conflict. In Sexual selection and reproductive competition in insects: 123-166. Blum, M.S. & Blum, N.A. (Eds). New York: Academic Press.
76. Parker, G.A. (1982). Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J. Theor. Biol. 96, 281-294.
77. Parker, G.A. (1984). Sperm competition and the evolution of animal mating strategies. In Sperm competition and the evolution of animal mating systems: 1-60. Smith, R.L. (Ed). London: Academic Press.
78. Parker, G.A. (1990). Sperm competition games: sneaks and extra-pair copulations. Proc. Roy. Soc. B 242, 127-133.
79. Parker, G.A. (1992). The evolution of sexual size dimorphism in fish. J. Fish Biol. 41(Suppl. B), 1-20.
80. Parker, G.A. (1998). Sperm competition and the evolution of ejaculates: towards a theory base. In Sperm competition and sexual selection: 3-54. Birkhead, T.R. & Møller, A.P. (Eds). London: Academic Press.
81. Parker, G.A. (2006a). Behavioural ecology: the science of natural history. In Essays on animal behaviour: celebrating 50 years of animal behaviour: 23-56. Lucas, J.R. & Simmons, L.W. (Eds). Burlington: Elsevier.
82. Parker, G.A. (2006b). Sexual conflict over mating and fertilization: an overview. Phil. Trans. Roy. Soc. B 361, 235-259.
83. Parker, G.A. (2011). The origin and maintenance of two sexes (anisogamy), and their gamete sizes by gamete competition. In The evolution of anisogamy: a fundamental phenomenon underlying sexual selection: 17-74. Togashi, T. & Cox, P.A. (Eds). Cambridge: Cambridge University Press.
84. Parker, G.A. (2014). The sexual cascade and the rise of Darwinian sexual selection, sex roles and sexual conflict. Cold Spring Harb. Perspect. Biol. 6, a017509.
85. Parker, G.A. & Ball, M.A. (2005). Sperm competition, mating rate and the evolution of testis and ejaculate sizes: a population model. Biol. Lett. 1, 235-238.
86. Parker, G.A. & Birkhead, T.R. (2013). Polyandry: the history of a revolution. Phil. Trans. Roy. Soc. B 368, 20120335.
87. Parker, G.A. & Lehtonen, J. (2014). Gamete evolution and sperm numbers: sperm competition versus sperm limitation. Proc. Roy. Soc. B 281, 20140836.
88. Parker, G.A. & Pizzari, T. (2010). Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934.
89. Parker, G.A. & Pizzari, T. (2015). Sexual selection: the logical imperative. In Current perspectives on sexual selection: what's left after Darwin: 119-163. Houquet, T. (Ed.). Berlin: Springer.
90. Parker, G.A., Ball, M.A., Stockley, P. & Gage, M.J.G. (1996). Sperm competition games: assessment of sperm competition intensity by group spawners. Proc. Roy. Soc. B 263, 1291-1297.
91. Parker, G.A., Lessells, C.M. & Simmons, L.W. (2013). Sperm competition games: a general model for precopulatory male-male competition. Evolution 67, 95-109.
92. Pilastro, A., Scaggiante, M. & Rasotto, M.B. (2002). Individual adjustment of sperm expenditure accords with sperm competition theory. Proc. Natl Acad. Sci. USA 99, 9913-9915.
93. Pitcher, T.E., Dunn, P.O. & Whittingham, L.A. (2005). Sperm competition and the evolution of testes size in birds. J. Evol. Biol. 18, 557-567.
94. Pitnick, S. (1996). Investment in testes and the cost of making long sperm in Drosophila. Am. Nat. 148, 57-80.
95. Pizzari, T. & Birkhead, T.R. (2002). The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol. Rev. 77, 183-209.
96. Preston, B.T., Stevenson, I.R., Pemberton, J.M., Coltman, D.W. & Wilson, K. (2003). Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc. Roy. Soc. B 270, 633-640.
97. Preston, B.T., Jalme, M.S., Hingrat, Y., Lacroix, F. & Sorci, G. (2011). Sexually extravagant males age more rapidly. Ecol. Lett. 14, 1017-1024.
98. Ralls, K. (1976). Mammals in which females are larger than males. Q. Rev. Biol. 51, 245-276.
99. Ramm, S.A. & Schärer, L.. (2014). The evolutionary ecology of testicular function: size isn't everything. Biol. Rev. 89, 874-888.
100. Ray, J. (1678). Ornithology of Francis Willughby. London: John Martyn.
101. Robertson, D.R. & Choat, J.H. (1974). Protogynous hermaphroditism and social systems in labrid fishes. Proc. Second Int. Symp. Coral Reefs 1, 217-225.
102. Robertson, D.R. & Warner, R.R. (1978). Sexual patterns in the labroid fishes of the Western Caribbean, II: the Parrotfishes (Scaridae). Smithson. Contrib. Zool. 255, 1-26.
103. Roede, M.J. (1972). Color as related to size, sex, and behavior in seven Caribbean labrid fish species (Genera Thalassoma, Halichoeres, and Hemipterinotus). Stud. Fauna Curacao Other Carrib. Isl. 138, 1-264.
104. Russell, L.D., Ren, H.P., Hikim, I.S., Schulze, W. & Hikim, A.P.S. (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. Am. J. Anat. 188, 21-30.
105. Salisbury, G.W., Vandemark, N.L. & Lodge, J.R. (1978). Physiology of reproduction and artificial insemination of cattle. 2nd edn. San Francisco: Freeman & Co.
106. Schaedelin, F.C., Dongen, W.F.D. & Wagner, R.H. (2015). Mate choice and genetic monogamy in a biparental, colonial fish. Behav. Ecol. 26, 782-788.
107. Schärer, L. (2009). Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution 63, 1377-1405.
108. Schärer, L. & Pen, I. (2013). Sex allocation and investment into pre- and post- copulatory traits in simultaneous hermaphrodites: the role of polyandry and local sperm competition. Phil. Trans. Roy. Soc. B 368, 20120052.
109. Schärer, L. & Vizoso, D.B. (2007). Phenotypic plasticity in sperm production rate: there's more to it than testis size. Evol. Ecol. 21, 295-306.
110. Schaus, J.M. & Sakaluk, S.K. (2001). Ejaculate expenditures of male crickets in response to varying risk and intensity of sperm competition: not all species play games. Behav. Ecol. 12, 740-745.
111. Schultz, A.H. (1938). The relative weights of the testes in primates. Anat. Rec. 72, 387-394.
112. Schulze-Hagen, K. & Birkhead, T.R. (2015). The ethology and life history of birds: the forgotten contributions of Oskar, Magdalena and Katharina Heinroth. J. Ornithol. 156, 9-18.
113. Schwartz, D., MacDonald, P.D.M. & Heuchel, V. (1981). On the relationship between the number of spermatozoa and the probability of conception. Reprod. Nutr. Dével. 21, 979-988.
114. Shaw, R.F. & Mohler, J.D. (1953). The selective significance of the sex ratio. Am. Nat. 87, 337-342.
115. Shen, W., Zhang, Z.-Y., Liu, D.-Z. & Wang, D.-H. (2015). Hormones orchestrated pre- and post-copulatory sexual traits in male Mongolian gerbils. Physiol. Behav. 143, 90-96.
116. Short, R.V. (1977). Sexual selection and the descent of man. In Reproduction and evolution: 3-19. Calaby, J.H. & Tyndale-Biscoe, C.H. (Eds). Canberra: Australian Academy of Sciences.
117. Short, R.J. (1979). Sexual selection and its component parts, somatic and genital selection as illustrated by man and the great apes. Adv. Stud. Behav. 9, 131-158.
118. Short, R.J. (1997). The testis: the witness of the mating system, the site of mutation and the engine of desire. Acta Paediatr Suppl. 422, 3-7.
119. Simmons, L.W. (2001). Sperm competition and its evolutionary consequences in the insects. Princeton: Princeton University Press.
120. Simmons, L.W. & Emlen, D.J. (2006). Evolutionary trade-off between weapons and testes. Proc. Natl Acad. Sci. USA 103, 16346-16351.
121. Simmons, L.W. & Fitzpatrick, J.L. (2012). Sperm wars and the evolution of male fertility. Reproduction 144, 519-534.
122. Simmons, L.W. & Parker, G.A. (1992). Individual variation in sperm competition success of yellow dung flies, Scatophaga stercoraria. Evolution 46, 366-375.
123. Simmons, L.W., Firman, R., Rhodes, G. & Peters, M. (2004). Human sperm competition: testis size, sperm production and rates of extrapair copulations. Anim. Behav. 68, 297-302.
124. Simmons, L.W., Emlen, D.J. & Tomkins, J.L. (2007a). Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles. Evolution 61, 2684-2692.
125. Simmons, L.W., Denholm, A., Jackson, C., Levy, E. & Madon, E. (2007b). Male crickets adjust ejaculate quality with both risk and intensity of sperm competition. Biol. Lett. 3, 520-522.
126. Smith, R.L. (1998). Foreword. In Sperm competition and sexual selection: xv-xxiii. Birkhead, T.R. & Møller, A.P. (Eds). London: Academic Press.
127. Smith, C.C. & Fretwell, S.D. (1974). The optimal balance between size and number of offspring. Am. Nat. 108, 499-506.
128. Stockley, P., Gage, M.J.G., Parker, G.A. & Møller, A.P. (1997). Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am. Nat. 149, 933-954.
129. Svärd, L. & Wiklund, C. (1989). Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behav. Ecol. Sociobiol. 24, 395-402.
130. Tazzyman, S.J., Pizzari, T., Seymour, R.M. & Pomiankowski, A. (2009). The evolution of continuous variation in ejaculate expenditure strategy. Am. Nat. 174, E71-E82.
131. Tiemann, H., Sötje, I., Johnston, B.D., Flood, P.R. & Båmstedt, U. (2009). Documentation of potential courtship-behaviour in Periphylla periphylla (Cnidaria: Scyphozoa). J. Mar. Biol. Assoc. U.K. 89, 63-66.
132. Tomkins, J.L. & Simmons, L.W. (2002). Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Anim. Behav. 63, 1009-1016.
133. Vahed, K. & Parker, D.J. (2012). The evolution of large testes: sperm competition or male mating rate? Ethology 118, 107-117.
134. Vahed, K., Parker, D.J. & Gilbert, J.D.J. (2011). Larger testes are associated with a higher level of polyandry, but a smaller ejaculate volume, across bushcricket species (Tettigoniidae). Biol. Lett. 7, 261-264.
135. Van Look, K.J., Dzyuba, B., Cliffe, A., Koldewey, H.J. & Holt, W.V. (2007). Dimorphic sperm and the unlikely route to fertilisation in the yellow sea- horse. J. Exp. Biol. 210, 432-437.
136. Warner, R.R. & Robertson, D.R. (1978). Sexual patterns in the labroid fishes of the Western Caribbean, I: the Wrasses (Labridae). Smithson. Contrib. Zool. 254, 1-27.
137. Weismann, A. (1893). The germ plasm. A theory of heredity. Charles Scribner's Sons. Electronic Scholarly Publishing. Available at: http://www.esp.org/books/weismann/germ-plasm/facsimile/.
138. Werner, B. (1973). Spermatozeugmen und Paarungsverhalten bei Tripedalia cystophora (Cubomedusae). Mar. Biol. 18, 212-217.
139. West, S.A. (2009). Sex allocation. Princeton: Princeton University Press.
140. Williams, P.D., Day, T. & Cameron, E. (2005). The evolution of sperm-allocation strategies and the degree of sperm competition. Evolution 59, 492-499.
141. Yund, P.O. (2000). How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol. Evol. 15, 10-13.