Group Sex, Sex Change, and Parasitic Males: Sexual Strategies Among the Fishes and Their Neurobiological Correlates

Sexual selection, in the form of intrasexual competition and mate choice, has driven the evolution of a variety of sexual phenotypes amongst the vertebrates (Andersson, 1994). As a result, vertebrate species utilize many different approaches to acquire fertilizations. Humans and other primates show a wide range of sexual behaviors, but this range is dwarfed by the remarkable variation seen in advanced fishes. The goals of this review are (a) to acquaint the reader with the tremendous sexual diversity exhibited by fishes, (b) to demonstrate how this diversity provides unique opportunities to examine the neurobiological correlates of vertebrate sexual strategies, and (c) to highlight the parallels between the neuroendocrine correlates of the sexual strategies of fish with the mechanisms underlying sexual phenotypes in other vertebrates, showing the utility of fish studies for understanding sexual variation in general.

Key alternative morph, GnRH, shaker, social behavior, teleost, vasopressin, vasotocin.

Fishes Are Sexually Diverse Vertebrates

One way to appreciate the diversity of fishes is to compare fishes to vertebrate taxa with which we are more familiar: birds and mammals. There are approximately 4,400 different species of mammals and over double the number of species of birds, around 9,700. Although this may seem like a large number of species, fishes make up the bulk of the vertebrates, with over 24,500 species, or over five times the diversity seen in mammals (see Figure 1; Nelson, 1994; Pough, Heiser, & McFarland, 1996). In this review, we will focus on euteleost fishes, such as bass, halibut, perch, and salmon, which account for over 90% of all fish species (Nelson, 1994). The high species diversity and rapid evolution of the euteleosts resulted in a high degree of phenotypic plasticity, a feature most evident in the realm of phenotypic sex.

Euteleost fishes range in sexual phenotypes from species with permanent sexes, such as cichlids, to species such as the bluehead wrasse and bluebanded gobies that change sex once in their lives. Other fish even change sex multiple times within a lifetime, as in the Japanese goby, Trimmer okinawae (see Figure 2). Great variation can also exist within a species, with numerous examples showing multiple male morphs and the potential for multiple female morphs (Henson & Warner, 1997; Taborsky, 1994, Taborsky, 2001). In the ocellated wrasse, Symphodus ocellatus, four different male strategies have been observed in the same population (Taborsky, Hudde, & Wirtz, 1987). Large males maintain nests and care for eggs while small males are parasitic spawners (sneakers). Mid-sized males, called satellites, help the large males by defending nests against sneakers in exchange for the occasional chance to court and spawn with females. The largest males, dubbed "pirates" dominate over nesting males and take over their nest tubes. In some cases, particularly in other Symphodus species, they fertilize eggs in the nesting males' nests and leave them "under the care" of the nesting males (Taborsky, 1994; van den Berghe, 1988). Females can also show variation in sexual phenotype. In the bluehead wrasse, Thalasomma bifasciatum, females express two mating tactics: group spawning and pair spawning. Both of these tactics are seen within a single population. As with male strategies, female strategies seem to be size dependent: The largest females only spawn with one male at a time, whereas smaller females primarily spawn in groups (Warner, 1984a, 1985; Warner & Hofman, 1980). The variation in sexual phenotypes for males and females of S. ocellatus and T bifasciatum exemplify the diverse alternative reproductive tactics used by fish, and there are many more examples among other fish species (for comprehensive reviews of reproduction and sexuality in fishes, see Breder & Rosen, 1966; Taborsky, 1994).

The environmental potential for polygamy (EPP) provides one useful organizing principle for understanding the evolution of diverse sexual phenotypes and mating systems in fishes. The EPP describes the degree to which resources are distributed or aggregated, such that a limited number of individuals can control access to a large amount of required resources and, as a result, monopolize mates who seek those resources (Emlen & Oring, 1977). Male monopolization of mating resources results in polygyny or the acquisition of multiple females by a limited number of top-ranked males. Because of this, there is tremendous pressure to acquire resources and a resultant skew in male reproductive success greatly benefiting the monopolizers. For males that cannot dominate resources (discussed in detail subsequently), several alternative strategies are available, including (a) maintain nonreproductive status and wait to become large enough to dominate a resource (see the example that follows), (b) help the reproductive dominant and by association get some access to the opposite sex (e.g., satellite tactic in S. ocellatus), or (c) cheating the system to obtain resources (e.g., sneak spawning in S. ocellatus).