Abstract
Thus far, I have provided evidence in mammals, birds, and reptiles that mammals may adaptively skew sex ratios of offspring and that mechanisms exist by which this may occur. In fishes, there is virtually no evidence showing parental manipulation of sex ratios, perhaps because many fish species exhibit a higher level of plasticity within their sex-determining systems. We now know that fish exhibit the most diverse range of sex-determining systems, ranging from strict gonochorists to hermaphrodites, some with clear genetic mechanisms of sex determination and others with little or no clear genetic influence. In some cases, individuals maintain ovarian and testicular tissue simultaneously through adulthood, choosing whether to produce sperm or eggs in a given attempt. In this chapter, I introduce the many systems of sex determination found in fish species, highlight the environmental and social influences shown to influence piscine sex ratios, and discuss potential adaptive mechanisms of sex allocation in these systems.
Finding Nemo lied to your kids!
How Finding Nemo should have started if it were biologically accurate:
Father and mother clownfish are tending to their clutch of eggs at their sea anemone when the mother is eaten by a barracuda. Nemo hatches as an undifferentiated hermaphrodite (as all clownfish are born) while his father transforms into a female now that his female mate is dead. Since Nemo is the only other clownfish around, he becomes a male and mates with his father (who is now a female). Should his father die, Nemo would change into a female and mate with another male. Although a much different storyline, it still sounds like a crazy adventure!
Patrick Cooney, in Fun Fish Fodder
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References
Abucay JS, Mair GC, Skibinski DO, Beardmore JA (1999) Environmental sex determination: the effect of temperature and salinity on sex ratio in Oreochromis niloticus L. Aquaculture 173(1):219–234
Alavi S, Cosson J (2005) Sperm motility in fishes. I. Effects of temperature and pH: a review. Cell Biol Int 29(2):101–110
Anthes N, Putz A, Michiels NK (2006) Sex role preferences, gender conflict and sperm trading in simultaneous hermaphrodites: a new framework. Anim Behav 72(1):1–12
Avise J, Mank J (2009) Evolutionary perspectives on hermaphroditism in fishes. Sex Dev 3(2–3):152–163
Axelrod R, Dion D (1988) The further evolution of cooperation. Science 242(4884):1385–1390
Chan S, Yeung W (1983) Sex control and sex reversal in fish under natural conditions. Fish Physiol 9:171–222
Charnov EL (1980) Sex allocation and local mate competition in barnacles. Marine Biol Lett 2:53–57
Charnov EL (1996) Sperm competition and sex allocation in simultaneous hermaphrodites. Evol Ecol 10(5):457–462
Charnov EL, Bull J (1977) When is sex environmentally determined? Nature 266:828–830
Cole KS (1997) Gonadal development and sexual allocation in mangrove killifish, Rivulus marmoratus (Pisces: Atherinomorpha). Copeia 1997(3):596–600
Connor RC (1992) Egg-trading in simultaneous hermaphrodites: an alternative to Tit-for-Tat. J Evol Biol 5(3):523–528
Conover DO (2004) Temperature-dependent sex determination in fishes. In: Valenzuela N, Lance V (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, pp 11–20
Conover DO, Heins SW (1987) The environmental and genetic components of sex ratio in Menidia menidia (Pisces: Atherinidae). Copeia 1987(3):732–743
Conover DO, Kynard BE (1981) Environmental sex determination: interaction of temperature and genotype in a fish. Science 213:31
Conover DO, Ross MR (1982) Patterns in seasonal abundance, growth and biomass of the Atlantic silverside, Menidia menidia, in a New England estuary. Estuar Coasts 5(4):275–286
Conover DO, Van Voorhees DA (1990) Evolution of a balanced sex ratio by frequency-dependent selection in a fish. Science 250(4987):1556
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208(3):191–364
Fischer EA (1980) The relationship between mating system and simultaneous hermaphroditism in the coral reef fish, Hypoplectrus nigricans (Serranidae). Anim Behav 28(2):620–633
Fischer EA (1984) Egg trading in the chalk bass, Serranus tortugarum, a simultaneous hermaphrodite. Ethology 66(2):143–151
Fischer EA (1988) Simultaneous hermaphroditism, tit-for-tat, and the evolutionary stability of social systems. Ethol Sociobiol 9(2-4):119–136
Fishelson L (1970) Protogynous sex reversal in the fish Anthias squamipinnis (Teleostei, Anthiidae) regulated by the presence or absence of a male fish. Nature 227(5253):90–91
Fromm PO (1980) A review of some physiological and toxicological responses of freshwater fish to acid stress. Environ Biol Fish 5(1):79–93
Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44(2):189–208
Godwin J, Luckenbach JA, Borski RJ (2003) Ecology meets endocrinology: environmental sex determination in fishes. Evol Dev 5(1):40–49
Guerrero-Estévez S, Moreno-Mendoza N (2010) Sexual determination and differentiation in teleost fish. Rev Fish Biol Fish 20(1):101–121
Hamilton WD (1967) Extraordinary sex ratios. Science 156(3774):477–488
Hamilton WD, Axelrod R (1981) The evolution of cooperation. Science 211(27):1390–1396
Harrington RW (1961) Oviparous hermaphroditic fish with internal self-fertilization. Science 134(3492):1749–1750
Hattori A (1991) Socially controlled growth and size-dependent sex change in the anemonefish Amphiprion frenatus in Okinawa, Japan. Jpn J Ichthyol 38(2):165–177
Ijiri S, Kaneko H, Kobayashi T, Wang D-S, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y (2008) Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78(2):333–341
Jonsson B, Jonsson N (2014) Early environment influences later performance in fishes. J Fish Biol 85(2):151–188
Kadota T, Osato J, Nagata K, Sakai Y (2012) Reversed sex change in the haremic protogynous hawkfish Cirrhitichthys falco in natural conditions. Ethology 118(3):226–234
Kuwamura T, Yogo Y, Nakashima Y (1993) Size-assortative monogamy and paternal egg care in a coral goby Paragobiodon echinocephalus. Ethology 95(1):65–75
Kuwamura T, Kadota T, Suzuki S (2014) Testing the low-density hypothesis for reversed sex change in polygynous fish: experiments in Labroides dimidiatus. Sci Rep 4:srep04369
Lee R, Gerking S (1980) Survival and reproductive performance of the desert pupfish, Cyprinodon n. nevadensis (Eigenmann and Eigenmann), in acid waters. J Fish Biol 17(5):507–515
Leonard JL (1993) Sexual conflict in simultaneous hermaphrodites: evidence from serranid fishes. Environ Biol Fish 36(2):135–148
Liew WC, Bartfai R, Lim Z, Sreenivasan R, Siegfried KR, Orban L (2012) Polygenic sex determination system in zebrafish. PLoS One 7(4):e34397
Linde M, Palmer M, Alós J (2011) Why protogynous hermaphrodite males are relatively larger than females? Testing growth hypotheses in Mediterranean rainbow wrasse Coris julis (Linnaeus, 1758). Environ Biol Fish 92(3):337–349
Luckenbach JA, Godwin J, Daniels HV, Borski RJ (2003) Gonadal differentiation and effects of temperature on sex determination in southern flounder (Paralichthys lethostigma). Aquaculture 216(1):315–327
Lutnesky MM (1994) Density-dependent protogynous sex change in territorial-haremic fishes: models and evidence. Behav Ecol 5(4):375–383
Magerhans A, Hörstgen-Schwark G (2010) Selection experiments to alter the sex ratio in rainbow trout (Oncorhynchus mykiss) by means of temperature treatment. Aquaculture 306(1):63–67
Magerhans A, Müller-Belecke A, Hörstgen-Schwark G (2009) Effect of rearing temperatures post hatching on sex ratios of rainbow trout (Oncorhynchus mykiss) populations. Aquaculture 294(1):25–29
Manabe H, Matsuoka M, Goto K, Dewa S-I, Shinomiya A, Sakurai M, Sunobe T (2008) Bi-directional sex change in the gobiid fish Trimma sp.: does size-advantage exist? Behaviour 145(1):99–113
Matsuda M, Nagahama Y, Shinomiya A, Sato T (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417(6888):559
Moore EC, Roberts RB (2013) Polygenic sex determination. Curr Biol 23(12):R510–R512
Moyer JT, Zaiser MJ (1984) Early sex change: a possible mating strategy of Centropyge angelfishes (Pisces: Pomacanthidae). J Ethol 2(1):63–67
Munday PL (2002) Bi-directional sex change: testing the growth-rate advantage model. Behav Ecol Sociobiol 52(3):247–254
Munday PL, Caley MJ, Jones GP (1998) Bi-directional sex change in a coral-dwelling goby. Behav Ecol Sociobiol 43(6):371–377
Munday PL, Buston PM, Warner RR (2006) Diversity and flexibility of sex-change strategies in animals. Trends Ecol Evol 21(2):89–95
Munday PL, Kuwamura T, Kroon FJ (2010) Bidirectional sex change in marine fishes. In: Cole KS (ed) Reproduction and sexuality in marine fishes: patterns and processes. University of California Press, Berkeley, pp 241–271
Munoz RC, Warner RR (2003) A new version of the size-advantage hypothesis for sex change: incorporating sperm competition and size-fecundity skew. Am Nat 161(5):749–761
Nakashima Y, Kuwamura T, Yogo Y (1995) Why be a both-ways sex changer? Ethology 101(4):301–307
Ospina-Alvarez N, Piferrer F (2008) Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 3(7):e2837
Pandian T (2012) Genetic sex differentiation in fish, vol 1. CRC Press, Boca Raton
Paul A, Kuester J (1987) Dominance, kinship and reproductive value in female Barbary macaques (Macaca sylvanus) at Affenberg Salem. Behav Ecol Sociobiol 21(5):323–331
Petersen CW (1991) Sex allocation in hermaphroditic sea basses. Am Nat 138(3):650–667
Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197(1):229–281
Robertson D (1972) Social control of sex reversal in a coral-reef fish. Science 177(4053):1007–1009
Rodgers E, Earley R, Grober M (2007) Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. J Fish Biol 70(6):1660–1668
Römer U, Beisenherz W (1996) Environmental determination of sex in Apistogrammai (Cichlidae) and two other freshwater fishes (Teleostei). J Fish Biol 48(4):714–725
Rubin DA (1985) Effect of pH on sex ratio in cichlids and a poecilliid (Teleostei). Copeia 1985(1):233–235
Saillant E, Fostier A, Haffray P, Menu B, Laureau S, Thimonier J, Chatain B (2003) Effects of rearing density, size grading and parental factors on sex ratios of the sea bass (Dicentrarchus labrax L.) in intensive aquaculture. Aquaculture 221(1):183–206
Schärer L, Janicke T, Ramm SA (2015) Sexual conflict in hermaphrodites. Cold Spring Harb Perspect Biol 7(1):a017673
Schartl M (2004) A comparative view on sex determination in medaka. Mech Dev 121(7):639–645
Schultheis C, Böhne A, Schartl M, Volff J, Galiana-Arnoux D (2009) Sex determination diversity and sex chromosome evolution in poeciliid fish. Sex Dev 3(2–3):68–77
Sharma K, Sharrna O, Tripathi N (1998) Female heterogamety in Danio rerio (Cypriniformes: Cyprinidae). Proc Natl Acad Sci India Sect B 68:123–126
Sopinka N, Capelle P, Semeniuk C, Love O (2017) Glucocorticoids in fish eggs: causes of variation and effects on offspring phenotype. Physiol Biochem Zool 90:15–33
Soto CG, Leatherland JF, Noakes DL (1992) Gonadal histology in the self-fertilizing hermaphroditic fish Rivulus marmoratus (Pisces, Cyprinodontidae). Can J Zool 70(12):2338–2347
St. Mary CMS (1994) Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction. Behav Ecol 5(3):304–313
Sunobe T, Nakazono A (1993) Sex change in both directions by alteration of social dominance in Trimma okinawae (Pisces: Gobiidae). Ethology 94(4):339–345
Tave D (1986) Genetics for fish hatchery managers. AVI, Westport
Tomlinson J (1966) The advantages of hermaphroditism and parthenogenesis. J Theor Biol 11(1):54–58
Uchida D, Yamashita M, Kitano T, Iguchi T (2002) Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J Exp Biol 205(6):711–718
Van Rooij J, Bruggemann J, Videler J, Breeman A (1995) Plastic growth of the herbivorous reef fish Sparisoma viride: field evidence for a trade-off between growth and reproduction. Mar Ecol Prog Ser 122:93–105
Volff J-N, Schartl M (2001) Variability of genetic sex determination in poeciliid fishes. Genetica 111(1):101–110
von Hofsten J, Olsson P-E (2005) Zebrafish sex determination and differentiation: involvement of FTZ-F1 genes. Reprod Biol Endocrinol 3(1):63
Walker S, Ryen C, McCormick M (2007) Rapid larval growth predisposes sex change and sexual size dimorphism in a protogynous hermaphrodite, Parapercis snyderi Jordan & Starks 1905. J Fish Biol 71(5):1347–1357
Warner RR (1988) Sex change and the size-advantage model. Trends Ecol Evol 3(6):133–136
Williams GC (1975) Sex and evolution, vol 8. Princeton University Press, Princeton
Yamahira K, Conover DO (2003) Interpopulation variability in temperature-dependent sex determination of the tidewater silverside Menidia peninsulae (Pisces: Atherinidae). Copeia 2003(1):155–159
Yamamoto T-O (1969) Sex differentiation. Fish Physiol 3:117–175
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Navara, K.J. (2018). The Truth About Nemo’s Dad: Sex-Changing Behaviors in Fishes. In: Choosing Sexes. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-71271-0_9
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