On Evolution

13. Genetic Mating Systems and Reproductive Natural Histories of Fishes

Avise has taught ornithology throughout his career (among many other courses), and thus was well aware that molecular markers had revolutionized thought about avian mating systems. In particular, they challenged conventional wisdom that most songbirds are strictly monogamous. Markers revealed that foster progeny (resulting from stolen fertilizations or egg dumping) occur in the nests of many avian species. In the mid-s, much of the Avise lab converted from phylogeographic studies to genetic assessments of parentage and mating systems in many kinds of creatures, especially fish. At that time, fishes were a near-virgin taxonomic group for genetic research on reproductive behaviors in nature, almost completely ignored by molecular ecologists despite the existence of a rich natural history literature. The great diversity of procreative modes in fishes puts those of birds (for example) to shame, as this chapter reviewing relevant genetic discoveries attests. (For more on nature’s peculiarities genetically revealed, see the author’s Genetics in the Wild [].) Fish have remarkably diverse reproductive behaviors. A rich natural -history literature documents mating systems ranging from pelagic group spawning to cooperative breeding to social monogamy. Subsequent to spawning, adult care of fertilized eggs and larvae may be nonexistent, confined to one gender, biparental, or communal. When parental care is offered, it may take such varied forms as oral or gill brooding, use of natural or constructed nests, internal gestation by a pregnant mother or by a pregnant father, or open-water guarding of fry. Genetic Mating Systems and Reproductive Natural Histories of Fishes 13 Most genetic studies of mating behaviors in fish have been conducted on species displaying parental care of offspring. In the bony fishes (Osteichthyes), approximately  of the  taxonomic families () contain at least some species in which adults provide direct postzygotic services, and in nearly  of those families, the primary or exclusive custodian is the male. Parental care by males alone is otherwise extremely rare in the vertebrates other than anuran amphibians . Thus, the evolutionary elaboration of paternal devotion makes fishes particularly favorable for testing traditional parental-investment and sexual-selection theories originally motivated by research on mammals and birds, where females typically are the primary caregivers . Also intriguing for genetic analysis are alternative reproductive tactics (ARTs) within a species, or sometimes even within an individual during its lifetime. An example of the latter occurs in sequential hermaphroditic species in which an individual fish may switch its gender (and associated mating behavior) from female to male or vice versa. Both sex-changing and nonchanging fish are present in some populations. Most fish species have separate sexes (i.e., are gonochoristic), and, within a gender, ARTs may be prevalent. In theory, a male fish may maximize the number of eggs he fertilizes by being quicker than rivals in “scramble competition,” monopolizing mates or resources such as nests or territories, exploiting the resources of other males via reproductive parasitism, or cooperating or trading with resource holders via mutualism or reciprocity. Two or more such tactics are often observed in a population. For example, four types of males co-occur in the ocellated wrasse (Symphodus ocellatus): large “bourgeois” males that build nests and tend progeny; small males that parasitize (or cuckold) a bourgeois spawner by sneaking into a nest and “stealing” some of the fertilization events; medium-sized males that defend another male’s nest from sneakers, but also court females and occasionally spawn; and extra-large males (pirates) that temporarily usurp the nest of another male.  On Evolution In another example, male salmon spawn either as full-sized anadromous adults after returning from the sea, or as dwarf precocious parr that have remained in freshwater. In marker-based parentage analyses of Atlantic salmon (Salmo salar), parr have been shown to fertilize widely varying proportions (–) of the total eggs in various populations. They also produce physiologically superior spermatozoa , a feature that partially compensates for their behavioral subordinance to dominant anadromous males. The ARTs of anadromous salmon and resident parr appear tied to an individual’s environmental exposure, but ARTs in some species might be genetically hardwired. Rearing fry under controlled conditions can help in evaluating developmental plasticity, as has been demonstrated with respect to alternative trophic morphs in several fish species. Regardless of their mechanistic basis, ARTs are common in fish, their occurrence facilitated by the prevalence in this group of external fertilization, a high incidence of paternal investment, and extensive intrasexual size variation attendant with indeterminate...