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Bibliography on Sexual Selection - BIO 608 Theory
Three Model Systems/Case Studies (guppies, sticklebacks, cockroaches) Although there are many excellent studies of sexual selection on a wide spectrum of fish species, two species stand out as being especially appropriate for this review: 1. the guppy, Poecilia reticulata, which has internal fertilization and females that give birth to fully independent juveniles (see Meffe and Snelson 1989, for review); 2. the threespine stickleback, Gasterosteus aculeatus, which has external fertilization and male parental care of the developing eggs and newly hatched fry (see Wootton 1976, for review). Although these two species have very different mating systems and reproductive biology, they share much in common in terms of sexual selection and signaling between the sexes. We caution that these species exhibit enormous geographical variation (guppies, Endler 1977, 1978; sticklebacks, Bell and Foster 1994), so the results that we cite here are not true for all populations within a species; we discuss some of these "exceptions" below. In both species, males develop a carotenoid-based, orange to red breeding coloration (guppies, Houde 1987; sticklebacks, Wootton 1976), and this breeding coloration is positively correlated with carotenoids in the diet (guppies, Kodric-Brown 1989; sticklebacks, Bakker, personal communication, see also Frischnecht 1993); positively correlated with condition index (weight scaled to length: guppies, Nicoletto 1991, 1993; sticklebacks, Milinski and Bakker 1990, Frischknecht 1993, Bakker and Mundwiler 1994); positively correlated with courtship intensity (guppies, Nicoletto 1993; sticklebacks, Bakker and Milinski 1991); and positively correlated with female preference (guppies, Houde 1987, Endler and Houde 1995; sticklebacks, Bakker 1993). Finally, if males of both species are experimentally infected with parasites, parasitized males have reduced breeding coloration and are less preferred by females than non-parasitized controls (guppies, Houde and Torio 1994; sticklebacks, Milinski and Bakker 1990). A clear pattern has emerged; male breeding coloration, energy reserves, courtship display rate, parasite load, and attractiveness to females are all interrelated. Considerable information is also known about the spectral sensitivities and the visual ecologies of each species. For example, based on microspectrophotometry of visual pigments, both species have four sets of retinal cone cells (guppies, Archer 1988, Rush 1995; sticklebacks, Baube in press, Baube personal communication), which includes a set of ultraviolet cones, and three sets of cones in the "human-visible" wavelengths. In sticklebacks, both spectral sensitivity and male breeding coloration have been shown to correlate with the photic environment. In "tea-stained" lakes in British Columbia, Canada, the short wavelengths attenuate rapidly, which creates a "reddish" photic environment; whereas, in mesotrophic lakes there is a broader spectrum of wavelengths of light (McDonald and Hawryshyn 1995, McDonald et al. 1995). There is a tendency for male breeding coloration to be black (rather than red) in these tea-stained lakes (Reimchen et al. 1985). Using optic nerve recording, McDonald and Hawryshyn (1995) found that sticklebacks in tea-stained lakes have their peak spectral sensitivity shifted to longer wavelengths relative to fish in mesotrophic lakes. McDonald et al. (1995) hypothesized that black breeding coloration may be favored in tea-stained lakes, due to its higher contrast against a red background than would be the case for red breeding coloration. They tested this hypothesis with females from a mesotrophic lake, where males have the more typical red breeding coloration. They examined female preference for red or black male video images against a red or blue background, which roughly approximated the two photic environments. They found that females preferred red males against a blue background, but black males against a red background, which supports their hypothesis (McDonald et al. 1995). Thus it appears that photic environment can affect spectral sensitivity and female preference of male breeding coloration. It would now be interesting to examine condition dependence and honest signaling in non-red or black males from these tea-stained lakes. In guppies, it appears that geographic variation in male coloration depends more on predation regime than on photic environment (Endler 1977, 1978). Basically, orange breeding coloration is negatively correlated among populations with the intensity of predation on guppies. Female preference for male orange coloration is stronger in populations with lower predation intensities (Endler and Houde 1995). In addition, Endler and Houde (1995) also found that male orange coloration correlates with the photic environment; orange coloration increases with the water orange ratio (i.e. the relative transmission of long wavelengths through the water, which is calculated as the integral of 400-550nm absorbance divided by the integral of 550-700nm absorbance; see Endler and Houde 1995) among populations. Interestingly, this appears to be the opposite trend found in sticklebacks. In sticklebacks, redder photic environments are correlated with black breeding coloration, and female preference for black males over red males (McDonald and Hawryshyn 1995; McDonald et al. 1995; Reimchen et al. 1985). In guppies, a redder photic environment is correlated with stronger preference for orange colored males (Endler and Houde 1995). A possible resolution to this disparity is that tea-stained stickleback habitat attenuates the short wavelengths more completely than comparable guppy habitat (guppy habitat, Endler 1991; stickleback habitat, McDonald et al. 1995). In both guppies and sticklebacks, when the color of the ambient light is manipulated to coincide with male breeding coloration (thus reducing color contrast of the male ornament), female preference for male coloration disappears (guppies, Long and Houde 1989; sticklebacks, Milinski and Bakker 1990). It would be interesting to conduct artificial selection experiments where photic environment is manipulated, and to look for evolutionary responses in spectral sensitivity, female preference and male coloration. A common feature of all the above cited studies on condition dependence and honest signaling in guppies and sticklebacks is that they are all based on visual cues. It would be interesting to see if other sensory modalities play a role in honest signaling in these species.
Summary And Directions For Future Research Behavioral ecology theory, particularly sexual selection theory and resource acquisition theory, makes specific predictions on communication between the sexes during courtship and mate choice. If signals are costly to produce, then theory predicts that signalers should produce signals in direct proportion to their condition. Receivers should be well adapted to discriminate the level of signal being produced, and thus the signaler's condition. Sensory ecology provides a wealth of information on physiological mechanisms underlying signal production and signal detection; thus, a great deal remains to be learned by integrating behavioral and sensory ecology. It appears that male visual cues do honestly signal condition to females in many cases; however, this issue has not been addressed explicitly for other sensory modalities. It seems plausible that acoustical and mechanosensory cues may also be condition dependent. However, chemical cues primarily seem to signal a fish's sex and reproductive state. It may well be that different sensory modalities signal different aspects of overall condition. It is clear, however, that integration of behavioral and sensory ecology, with regard to the question of sexual selection and resource acquisition, is still in its infancy. Below we make some specific suggestions for directions for future research.
1. Other measures of condition. Throughout this discussion, we have focused primarily on stored energy reserves (measured directly or estimated as being proportional to weight scaled to length) as our measure of condition; however, body size and immunocompetence may also be important determinants of lifetime reproductive success. First, consider body size. It has been well documented in fishes that survival and fecundity depend more on body size (i.e. mass) than on age (e.g. Werner and Gilliam 1984, Sargent et al. 1987). Large fish have higher rates of fecundity, mating success, and survival than small fish (Werner and Gilliam 1984, Gross and Sargent 1985, Andersson 1994). Thus, body size is clearly an important component of overall condition in fishes. Second, consider immunocompetence (Hamilton and Zuk 1982, Folstad and Karter 1992). In many fishes, females avoid parasitized males (see Andersson 1994 for review). In guppies and sticklebacks, certain parasites result in a reduction of male orange or red, carotenoid-based breeding coloration (Houde and Torio 1994, Milinski and Bakker 1990, but see Folstad et al. 1994), and in Arctic charr, male red breeding coloration is positively correlated lymphocyte density in the blood (Skarstein and Folstad 1996). How one measures immunocompetence may be problematic, but future research on immunocompetence, sexual selection, and the potential role of carotenoids should be very rewarding. We suggest that empiricists explore how body size, energy reserves, and immunocompetence interact to determine lifetime reproductive success, and that theoreticians explore the implications of these interactions for multi-modality honest signaling.
2. Search for condition indicating traits. We suggest that empiricists determine whether or not any of the traits that they study (e.g. morphology, signal production, signal detection) are correlated with condition (e.g. weight scaled to length). Condition can be estimated as Weight/Lengthb where b represents the allometric coefficient between weight and length, which can be estimated by non-linear regression of W versus L, or by log-log regression (Bolger and Connolly 1989). Alternatively, condition can be estimated as the residuals about a W versus L regression line, or one can compute partial correlations between potential condition indicators and weight, while holding the effects of length constant. Preliminary studies in our laboratories suggest that components of fin morphology and of breeding coloration may be correlated with condition, in some cases in both sexes of fishes. We are pursuing this further.
3. Honest signaling in both sexes. In most genetical models of sexual selection (e.g. Lande 1980, 1981; Kirkpatrick 1982), the limiting sex exhibits the mating preference and the limited sex exhibits the ornament. For this reason, most empirical studies have focused on sexual selection in the limited sex, typically males (see Andersson 1994 for review). However, in recent game theoretical models, Crowley et al. (1991) and Johnstone et al. (1996) found that under certain conditions it pays both sexes (i.e. the limiting and limited sexes) to be choosy. Even though females are the limiting sex in sticklebacks (e.g. Sargent and Gebler 1980), male sticklebacks do exhibit mate choice based on female body size and fecundity (Rowland 1982, 1989; Sargent et al. 1986), and females adopt a breeding coloration that signals when they are receptive to males (Rowland et al. 1991). Furthermore, in several species of the biparental cichlid genus, Cichlasoma, females are the more colorful sex (Turner 1993). Finally, most sex pheromone signals seem to be produced by females. We suggest that theoreticians develop genetical models of intersexual selection for both sexes simultaneously, and explore the coevolution of honest signaling in both sexes. We suggest also that empiricists look for condition dependence and honest signaling in both the limited and limiting sexes.
4. Sensory or pre-existing bias versus condition indicators. Throughout our discussion we have emphasized a coevolution between female preference and male ornament. There is evidence in swordtails (Xiphophorus) that the "sword" (i.e. a ventral extension of the caudal fin that develops as males reach maturity) may have evolved through a sensory or pre-existing bias in female preference (Ryan and Wagner 1987; Basolo 1990a, b, 1995a, b). Female Xiphophorus prefer males with swords, whether or not the males of their species have swords; in addition, female Priapella olmecae (the outgroup genus to Xiphophorus) also prefer males with swords (Ryan and Wagner 1987; Basolo 1990a, b, 1995a, b), even though swords are not known in this genus. Whether or not phylogenetic comparative data within the genus, Xiphophorus, supports the pre-existing bias hypothesis is controversial (Meyer et al. 1994, Basolo 1995a, Wiens and Morris 1996); however, Basolo's (1995b) recent demonstration of female preference for males with swords in the "sword-less" outgroup genus, Priapella, does favor this hypothesis. What about condition dependence in swordtails? Basolo (in press) found that male green swordtails (Xiphophorus helleri) on restricted diets produced swords as large as males that were fed ad libidum, despite the fact that males on the restricted diet had reduced growth in body size. These data suggest that swords may not be honest indicators of male quality. To our knowledge, sword length has not been compared to condition index or energy reserves within a species. It appears that morphological traits such as fin size reflect the conditions that prevailed when their development was initiated. As such, they may be relatively fixed and less reliable as "instantaneous" condition indicators than an ephemeral color pattern (see Kodric-Brown, this volume), which can reflect more short-term fluctuations in condition. This is certainly worth further investigation. Also, it would be interesting to see if the strength of female preference is correlated with mean male sword length among species of Xiphophorus, which may indicate a coevolution between female preference and male ornament in addition to the pre-existing bias.
5. Empirical studies that explore more than one sensory modality. Fish ethologists who study visual cues have traditionally separated their stimulus and focal fish with transparent glass or plastic partitions (e.g. Sargent and Gebler 1980). Users of transparent partitions are cautioned that not only do these partitions block chemical cues and the particle movement that is generated by low frequency mechanosensory cues (e.g. during a lateral display), but most of them are also effective filters of ultraviolet light, and many fishes are known be able to see ultraviolet light (Jacobs 1992; Archer 1988; Rush 1995). In fact, we have preliminary data for a poeciliid that males have UV breeding coloration, and that females prefer males behind UV transparent over UV filtering partitions (Rush et al. unpublished). We suggest that empiricists who study communication between the sexes explore two or more sensory modalities in combination. For sensory ecologists, this may require collaboration among research laboratories; however, behavioral ecologists might approach the problem with simple factorial experimental designs. If factorial-design experiments of mate choice indicate that sensory cues from two sensory modalities produce a greater response in the receiver than either cue alone (either additively or multiplicatively), then it becomes interesting to investigate how these modalities interact at both ethological and physiological levels. Alternatively, sensory biologists who have already determined that two sensory modalities interact on a physiological level can set the stage for behavioral ecological experiments.
References
Cockroaches (check out Allen Moore's webpage - this is the state of the art!)
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