Courtship and Mate Choice in Fishes: Integrating Behavioral and Sensory Ecology1

AMER. ZOOL., 38:82-96 (1998) Courtship and Mate Choice in Fishes: Integrating Behavioral and Sensory Ecology1 ROBERT CRAIG SARGENT2, VICTOR N. RUSH, BRIAN D. WISENDEN3, AND HONG Y. YAN T. H. Morgan School of Biological Sciences, Center for Ecology, Evolution and Behavior, University of Kentucky, Lexington, Kentucky 40506-0225 SYNOPSIS. Sexual selection theory predicts a coevolution between male sexual ornamentation and female preference. The implication of this prediction for sensory ecology is that there should be a tight coupling between the physiology of male signal production and the physiology of female signal reception. Indicator models of sexual selection predict that male ornamentation is correlated with male condition, and that female preference is correlated with male ornamentation. Indicator models of sexual selection have a conceptual overlap with resource acquisition and investment models of behavioral ecology. Empirical studies with fishes, particularly with guppies (Poecilia reticulata) and threespine sticklebacks (Gasterosteus aculea- tus), suggest a strong connection between acquired resources, male condition, male ornamentation, male courtship, and female preference. INTRODUCTION selection, which can be defined as the dif- Whereas behavioral ecology focuses on ferential ability of different phenotypes to how major categories of behavior such as obtain mates and reproduce, due to two avoiding predators, feeding, mating, paren- forms of intraspecific interaction: 1. com- tal care, contribute to fitness (Krebs and petition within a sex for access to mates or Davies, 1987; Sargent, 1990), sensory ecol- to resources for mating (intrasexual selec- ogy focuses on the sensory adaptations to tion); and, 2. mate choice between the sexes accomplish these classes of behavior (Du- (intersexual selection). Morphology and be- senbery, 1992). If the behavior of interest havior conducive to fighting ability (e.g., involves intraspecific interaction and com- antlers in deer) are thought to have evolved munication, such as courtship and mate through intrasexual selection; whereas, choice, then integrating these two ap- morphology and behavior involved in proaches can reveal insights into how and courtship (e.g., the peacock's tail) are why signalers and receivers are coadapted. thought to have evolved through intersexual selection (see Andersson, 1994, for review). Since Darwin's (1871) landmark treatise, In most species, females are the limiting evolutionary biologists have been fascinat- sex; that is, female reproduction is limited ed by the phenomena of sexual dimorphism primarily by resources, whereas male repro- and sexual selection. Darwin was particu- duction is limited primarily by the number larly intrigued by his observation that the of females with whom they mate (Bateman, males of most species have elaborate or- 1948; Williams, 1975). Consequently, most naments that are ostentatiously displayed studies of sexual selection have focused on during intrasexual competition and court- males. ship; thus, he proposed his theory of sexual Darwin (1871) himself recognized that these ornaments must have survival costs ' From the Symposium Animal Behavior: Integra- for their bearers; thus, he hypothesized that tion of Ultimate and Proximate Causation presented at the Annual Meeting of the Society for Integrative and the survival costs of male ornamentation Comparative Biology, 26-30 December 1996, at Al- are offset by benefits in obtaining mates. buquerque, New Mexico. An implication of Darwin's theory of sex- 2 To whom correspondence should be addressed; E- ual selection is that male ornaments act as mail: [email protected] signals to rival males, females, or both. ' Current address: Department of Biological Sci- ences, University of Alberta, Edmonton, Alberta, Can- There has been relatively little analytical ada T6G-2E9. modeling of intrasexual selection; however, 82 COURTSHIP AND MATE CHOICE IN FISHES 83 genetic models of intersexual selection il- an estimate of energy reserves by scaling lustrate that through assortative mating, weight to length (see Bolger and Connolly male ornaments and female preferences [1989] for review). This is the definition of may coevolve (e.g., Fisher, 1915, 1930; "condition" that we will adopt here; how- O'Donald, 1980; Lande, 1980, 1981; Kirk- ever, other state variables are clearly im- patrick, 1982). This coevolutionary process, portant determinants of fitness as well. between signaler and receiver, has profound There is considerable empirical support implications for sensory ecology. Not only for the importance of energy reserves for would one predict a correlation between reproductive success in fishes (see Sargent male ornament and female preference, but [1997] for review). First, it is well known also a coupling of the underlying physiol- that energy reserves decline during the ogies of male signal production and female breeding season, and that fishes that have signal reception. not reproduced have higher energy reserves We are intrigued by a particular class of at the end of the breeding season that fishes sexual selection models, which are collec- that have reproduced (e.g., Unger, 1983; tively referred to as indicator models (see Sargent, 1985; Reznick and Braun, 1987; Andersson, 1994, for review). In these Chellapa et al, 1989; FitzGerald et al, models, male ornaments evolve to "indi- 1989; Sabat, 1994). Second, many studies cate" or "honestly signal" some aspect of manipulate diet or ration, and these studies male phenotypic quality, genetic quality, or show that individuals that receive more both, and female preference evolves to be supplemental food have higher reproductive correlated with the degree of male orna- success, survival between brood cycles, or mentation (e.g., Zahavi, 1975, 1977; Ham- both (e.g., Townshend and Wootton, 1984; ilton and Zuk, 1982; Hasson, 1989, 1997; Ridgway and Shuter, 1994). Third, Sargent Grafen, 1990a, b; Folstad and Karter, 1992; (unpublished) found with fathead minnows Price et al, 1993; Wolf et al, 1997). These (Pimephales promelas) that "condition in- models provide a conceptual basis for un- dex" (i.e., weight scaled to length) at the derstanding what is being signaled by beginning of the breeding season is posi- males. In addition, these models provide a tively correlated with the amount of stored conceptual link to the dynamics of resource neutral lipids, and with the number of off- acquisition, and subsequent investment of spring produced during the breeding sea- acquired resources into components of fit- son. Thus, acquired resources are clearly ness (e.g., Houston and McNamara, 1988; tied to reproductive output in fishes. Mangel and Clark, 1988). Behavioral strategies are said to be "con- Animals acquire resources throughout dition-dependent" if an individual's best their lives. Although these resources are in- strategy depends on its condition, or on its corporated into the phenotype in a variety condition relative to that of other members of different ways, they ultimately contribute of the population. For example, during to an animal's fitness, or lifetime reproduc- male-male competition for females in fish- tive success (e.g., Houston and McNamara, es, larger males court females, whereas 1988; Mangel and Clark, 1988; Williams, smaller males attempt to mate forcibly or 1992; Sargent, 1990; Sargent et al, 1995). sneakily (see Gross, 1984, 1996 and Farr Behavioral ecologists use the term "condi- 1989, for reviews). Females may benefit by tion" to refer to an animal's overall quality mating with high condition males directly in terms of acquired resources, with the im- (i.e., phenotypic benefits such as more re- plicit assumption that higher condition sources for offspring, lower levels of patho- leads to higher fitness. Within the paradigm gens that could infect the female or off- of dynamic optimization, "condition" can spring), or indirectly (i.e., genetic benefits be thought of as all axes in the state space inherited by the offspring, e.g., Moore, that are relevant to fitness (e.g., body size, 1994). If females do benefit by mating with energy reserves, immunocompetence). high condition males, then sexual selection However, fisheries biologists have tradition- theory predicts that males will "honestly ally used the term, "condition," to refer to signal" their overall quality to prospective 84 R. C. SARGENT ETAL. females, and that females will base their 1993; sticklebacks, Bakker and Milinski, mate choice on these male signals (Zahavi, 1991); and positively correlated with fe- 1975, 1977; Kodric-Brown and Brown, male preference (guppies, Houde, 1987; 1984; Grafen, 1990a, b; Price etal., 1993). Endler and Houde, 1995; sticklebacks, Bak- Honest signaling theory assumes that sig- ker, 1993). Finally, if males of both species nals are costly to produce, and that a given are experimentally infected with parasites, level of signal is more costly for low-con- parasitized males have reduced breeding dition than high-condition males. Many of coloration and are less preferred by females the predictions of honest signaling have than non-parasitized controls (guppies, been supported in fishes (see below). Thus, Houde and Torio, 1994; sticklebacks, Mil- sexual selection theory potentially has inski and Bakker, 1990). A clear pattern has broad implications for sensory ecology and emerged; male breeding coloration, energy intraspecific communication. reserves, courtship display rate, parasite load, and attractiveness to females are all

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