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Chapter: The Diversity of Fishes: Biology, Evolution, and Ecology: Fishes as social animals: reproduction

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Gender roles in fishes - Reproductive patterns among fishes

Although the vast majority of fishes are gonochoristic, with sex determined at an early age and remaining fixed as male or female, a significant number of fishes can function as males or females simultaneously or sequentially.

Gender roles in fishes

Although the vast majority of fishes are gonochoristic, with sex determined at an early age and remaining fixed as male or female, a significant number of fishes can function as males or females simultaneously or sequentially. The environmental correlates and evolutionary causes of sex change in fishes have been the subject of considerable study and speculation.


Sex reversal has evolved, apparently independently, in perhaps 34 families belonging to 10 orders, including moray eels (Anguilliformes), loaches (Cypriniformes), lightfishes (Stomiiformes), killifishes (Atheriniformes), swamp eels (Synbranchiformes), flatheads (Scorpaeniformes), boxfishes (Tetraodontiformes), and at least 24 perciform families (including snooks, seabasses, tilefishes, emperors, rovers, porgies, threadfins, angelfishes, bandfishes, damselfishes, wrasses, parrotfishes, and gobies) (Devlin & Nagahama 2002; DeMartini & Sikkel 2006). Sex changers can be either: (i) simultaneous hermaphrodites, capable of releasing viable eggs or sperm during the same spawning; or (ii) sequential hermaphrodites, functioning as males during one life phase, and as females during another. Among sequential hermaphrodites, protandrous fishes develop first as males and then later change to females, whereas protogynous fishes mature first as females and then later become males. Variations on these patterns exist, such as protogynous populations with some males that develop directly from juveniles, or simultaneous hermaphrodites that lose the ability to function as one sex (Smith 1975; Warner 1978; Sadovy & Shapiro 1987; Lutnesky 1994).


Protogyny is by far the most common form of hermaphroditism, exhibited in at least 17 tropical marine families, which is about one-fi fth of reef families (DeMartini & Sikkel 2006). In a classic study, Robertson (1972) found that the Indo-Pacific Cleaner Wrasse,Labroides dimidiatus, formed harems of one large male and up to 10 females. Breeding access to the male was determined by a behavioral dominance hierarchy or peck order, the largest female dominating the next smallest and so on. If the top (alpha) female was removed, the next largest female assumed her role and everyone else moved up a step. If the male was removed, the alpha female began courting females within an hour and developed functional testes within 2 weeks (see also Kuwamura 1984).


Protogyny in wrasses can take other forms. In the Caribbean Bluehead Wrasse, Thalassoma bifasciatum, fish usually begin life as predominantly yellow females or similarly colored males (“initial phase” coloration). Any of the initial phase fish can change into larger, “terminal phase” males, which also develop a blue head, a black-and-white midbody saddle, and a green posterior region. Large males set up territories over coral heads that females prefer as spawning sites. Some females are intercepted by and spawn with groups of up to 15 smaller males, but the largest, pairspawning males have the highest spawning success. A territory- holding male may receive 40–100 spawnings per day, whereas a nearby group-spawning male may receive only one to two matings, and his sperm will often be diluted by the gamete output of other males in the group (Warner et al. 1975; Warner 1991). Other well-studied protogynous species include the anthiine serranid, Anthias squamipinnis, a pair-spawning species that forms large aggregations in which females may outnumber males by 36 : 1. The precision of social control of sex change in this species is remarkable: if nine males are removed from a large group, nine females change sex to replace them. Sex change to male in Anthias also occurs if the female : male ratio exceeds a threshold value (Shapiro 1979, 1987). The commonness of protogyny probably reflects the fact that most teleosts, including gonochoristic species, differentiate first as nonfunctional females.


Protandry has been reported in moray eels, loaches, lightfishes, platycephalids, snooks, porgies, threadfins, damselfishes, and crediid sandburrowers. The popular clown or anemonefishes (Amphiprion spp., Pomacentridae) live in groups of two large and several small individuals in an anemone. Only the two largest fish in an anemone are sexually mature, the largest individual being female and the next largest being male. Although smaller fish may be as old as the spawning individuals, the behavioral dominance of the mature pair keeps these smaller males from maturing and growing, and a dominance hierarchy exists among the smaller males. In essence, “low ranking males are psychophysiologically castrated” (Fricke & Fricke 1977, p. 830). If the female dies, the male changes sex to female and the next largest fish in the group takes over his former role and grows rapidly (Allen 1975; Moyer & Nakazano 1978). This inconvenient truth was judiciously sidestepped in the otherwise biologically accurate movie, Finding Nemo. In fact, Nemo’s dad, Marlin, should have become Nemo’s mother.


Simultaneous hermaphroditism (=cosexuality, synchronous hermaphroditism) is least common, known from only four shallow water families (muraenids, rivulids, serranids, gobies) and most of the 16 families in the deepsea order Aulopiformes (lizardfishes, Synodontidae, are the bestknown exception) (Smith 1975; Warner 1978; St. Mary 2000; Devlin & Nagahama 2002). Three species of New World cyprinodontiform rivulids are capable of selffertilization (Kryptolebias spp. of South America and the mangrove rivuline,Kryptolebias marmoratus, of North and Central America). Self-fertilization in Kryptolebias is internal, producing clonal populations of homozygous, genetically identical hermaphroditic fish. Functional males can be produced depending on temperature and day length (Harrington 1971, 1975; Taylor 1992). Cyprinodontiform fishes are often colonists of small streams on islands and other seasonally adverse habitats. Selffertilization may be one means of assuring mates in low density populations that frequently become isolated, a scenario that could also be applied to the deepsea aulopiforms.


The other species of simultaneous hermaphrodites occur among the small hamlets (HypoplectrusSerranus). Each individual is physiologically capable of producing sperm and eggs at the same time, but behaviorally these fishes function as only one sex at a time during a spawning bout. In Caribbean hamlets (Hypoplectrus), spawning bouts can last for several hours, during which time members of a pair alternate sex roles, one fish first behaving as the “female” and releasing eggs and then behaving as the “male” and releasing sperm (Pressley 1981; Fischer & Petersen 1987). The eastern Pacific Serranus fasciatus is a haremic, sexchanging, simultaneous hermaphrodite: one male guards and spawns with several hermaphrodites that act as females. If the male is removed, the largest hermaphrodite changes into a male (Fischer & Petersen 1987). Serranines have separate external openings for the release of eggs and sperm (in addition to an anus), which may prevent internal or accidental self-fertilization. Self-fertilization may occur in some serranines, but only in aquaria (Thresher 1984).


One additional group of fishes departs from normal gonochoristic gender roles. Livebearers in Mexico and Texas includeparthenogenetic “species” that are all-female but require the sperm from males of other species to activate cell division in their eggs. Parthenogenesis in livebearers takes two forms: gynogenesis and hybridogenesis (Fig. 21.1). Gynogenetic females are usually triploid and produce eggs that are also 3N. These eggs are activated by sperm from other species, but no sperm material is incorporated; hence daughters are genetically identical to their mothers. Hybridogenetic females, in contrast, are diploid and produce haploid eggs that, during the reduction division of meiosis, keep the maternal genes and discard the paternal genes. Upon mating, these eggs unite with sperm from males of another species, forming a new, diploid hybrid daughter (no sons are produced). When the daughter mates, she again produces eggs that are haploid and “female”. Hence the maternal lineage is conserved and the male’s genetic contribution is lost after one generation. These parthenogenetic “species” are thought to have arisen originally as hybrids between Poeciliopsis monachafemales and males of four congeners, P. lucidaP. occidentalisP. latidens, and P. viriosa. The males of the four species are the usual sperm donors during mating. An additional species, the Amazon Molly, Poecilia formosa, is diploid and gynogenetic. Sperm from two other species (P. mexicana and P. latipinna) activate the eggs, but contribute no genetic material (Schultz 1971, 1977; Vrijenhoek 1984). Natural gynogenesis has also been reported for the cyprinid Cyprinus auratus gibelio (Price 1984).


Figure 21.1

Parthenogenesis in Mexican livebearers. (A) In gynogenesis, a triploid female (designated MLL, shorthand for Poeciliopsis monacha-lucida-lucida) produces 3N eggs that are activated but not fertilized by sperm from a male P. lucida (L´). A daughter identical to the mother is produced. (B) In hybridogenesis, a diploid mother (ML, for P. monacha-lucida) produces haploid eggs (M) that contain only the maternal genome. Sperm from P. lucida (L´) combine to form a diploid daughter (ML´), but this male component will be discarded again during gamete production and all future eggs will continue to have solely monacha genes. After Vrijenhoek (1984) and Allendorf and Ferguson (1990).

An immediate question that arises is how natural selection maintains males that waste gametes so wantonly. Apparently, dominance hierarchies among “donor male” populations of live-bearers exclude many males from mating with conspecific females. These are often the males that participate in the parasitized, heterospecific spawnings. Satellite or peripheral males that have very low reproductive output are characteristic of many vertebrate species (these are often the sneakers and streakers discussed below), providing an abundance of otherwise unused sperm (Moore 1984). Additionally, laboratory tests of mate preferences in sexual females show that sexual females are more attracted to males that the females observed courting gynogenetic females. Apparently a male can increase his chances of mating with a sexual female if he spends time courting asexual females because sexual females copy the choices made by female gynogens. It is not known whether sexual females prefer males that mate with sexual females over those that mate with gynogenetic females (Schlupp et al. 1994).


Certain generalities arise from surveys of sex change in shallow water fishes, as do exceptions. Sex change is largely a tropical and subtropical, marine phenomenon (Policansky 1982c; Warner 1982). Cool temperate marine and freshwater sex changers are known (e.g., loaches, bristlemouths, swamp eels, wrasses, gobies) but are relatively uncommon compared with tropical marine hermaphrodites. Patterns often follow familial lines, all members of a family being either protandrous or protogynous (although there are both protogynous and protandrous species among moray eels, seabasses, porgies, damselfishes, and gobies, and some serranids are clearly simultaneously hermaphroditic). 


However, population differences are becoming increasingly well known in sex-changing fishes. The Cleaner Wrasse, Labroides dimidiatus, is haremic under some conditions but forms pairs under others. Bluehead Wrasse, Thalassoma bifasciatum, are dominated by territorial-spawning males on small reefs with small populations, but by groupspawning males on large reefs with dense populations. Resource limitation, either food availability or reef size, and population size are frequent determinants of variation in mating systems. Clearly, sex change and mating systems respond to environmental variability (see Thresher 1984; Shapiro 1991; Warner 1991; Devlin & Nagahama 2002; Oldfield 2005).

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