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AMER. ZOOL., 38:59-69 (1998) Sexual-Selection Models for Exaggerated Traits are Useful but Constraining1 GEORGE W. BARLOW 2 Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, California 94720-3140 SYNOPSIS. Science is driven by productive hypotheses and technology, but these may sometimes limit the questions posed. For instance, Fisherian runaway sexual selection and related hypotheses have helped us understand the evolution of exaggerated visual sexual dimorphism. Species with indistinguishable sexes, however, may use different behavioral mechanisms when pairing and thus possess different adaptations. In the monomorphic Midas cichlid (Amphilophus citrinellum), females chose large aggressive males in a restrained situation, as sexual selection predicts, but males did not choose. The nuchal hump of males swells coincidently with pair formation. However, overly large humps were shunned by females while the normal-size hump facilitated sex recognition. This species is polychromatic, and pairs mate assortatively by color in Nicaragua. Some have suggested the Midas cichlid might therefore show how sexual selection produces explosive speciation of cichlids in Africa. All females, however, are biased toward normal-color males. The color of gold morphs modulates aggressive responses of the other fish. All else equal, the benefit to gold in a fight equals 15% more weight than the opponent. Pair formation succeeds best when the typically smaller female of a pair is relatively more aggressive than the male. The pair combination, gold male with normal female, is difficult to produce; making the female the same size as the male removes the disability. Pair formation is a negotiated process in which the male tests the aggressiveness of the female relative to self. That puts the behavioral mechanisms of the male and female in conflict. way we think about research problems, where theory provides metaphorical An apparatus, tool or technique that opens new doors to biological questions is "tools." Productive theories, such as that seductive. Witness the impact of the light underlying runaway sexual selection, need and then of the electron microscope, or now not but can wind up narrowly posing only of PCR. Such technology tempts scientists those questions falling within the theory's to frame only questions that can be an- envelope. Further, its seductive ideas can swered using the technology, instead of de- inspire near evangelical zeal and thereby veloping new methods to answer problems deter other approaches. At the peak of excitement about the generated from theory or from contrary empirical findings. In animal behavior, tech- adaptationist program, one statement attribnology has had less dramatic impact; two uted to J. B. S. Haldane summed up the tools, however, are the audiospectrogram attitude. He said, in essence, it matters not {e.g., Marler and Isaac, 1960), and televi- how the match is lit so long as it is lit. sion animation {e.g., Clark and Uetz, 1990; Evolution can proceed along different paths to reach the same solution. Some followers Macedonia and Stamps, 1994). The allure of new "tools" extends to the seemed to take the statement to mean discovering how the match is lit is of no consequence to evolutionary questions. Hal1 From the Symposium Animal Behavior: Integra- dane's own research indicates the contrary tion of Ultimate and Proximate Causation presented at (Spurway and Haldane, 1953). the Annual Meeting of the Society for Integrative and I hope to demonstrate the utility of atComparative Biology, 26-30 December 1996, at Altending to how mechanisms, denned as bebuquerque, New Mexico. 2 E-mail: [email protected] havior and morphology, provide insights INTRODUCTION 59 60 GEORGE W. BARLOW into mating behavior in a monogamous cichlid fish and thereby raise questions about adaptive significance. The central theme is the following: Extreme sexual dimorphism stimulated the theory of Fisherian sexual selection. Specific hypotheses about sexual selection concentrated on exaggerated sexual differences in species that come together only briefly to mate. Behavioral tasks such as recognition of species and sex are usually assumed rather than analyzed. That focus has detracted from our investigation of species with long-term bonding in which initial attractiveness does enter in but is only part of the story. The processes enabling sustained, peaceful relationships may not be revealed in the standard choice experiment. The study of these mechanisms offers a rich opportunity for understanding both proximate and ultimate mechanisms of behavior. I concentrate on the Midas cichlid, Amphilophus citrinellum, an abundant fish in the lakes and rivers of Nicaragua, whose sexes are indistinguishable. Most of the coverage will be on how males and females in this pair-bonding species form pairs. How might inter-sexual selection enter the picture, and how do the fish recognize species and sex? Does early experience with the care-taking parents play a role? And what are the consequences of the striking color polymorphism for mating? Does mating in this polychromatic fish provide a reasonable example of how mate choice could account for the radiations of African cichlids? The first example illustrates straightforward sexual selection for size and aggressiveness in the male Midas cichlid. FEMALE CHOICE FOR QUALITY OF MALE Consistent with sexual-selection theory, females of the related, modestly dimorphic convict cichlid 'Cichlasoma' nigrofasciatum, prefer large males (Noonan, 1983; Keenleyside, 1985). Although the two sexes of the Midas cichlids are so similar that most of the time they are indistinguishable, males in nature (Barlow, 1976) and in the lab reach a larger size than do females (see Francis and Barlow, 1993, for an explanation). Further, the male of a freely formed pair is always appreciably larger than the female (Barlow, 1976; McKaye, 1986). Theory predicts a female cichlid prefers a large and also more aggressive male. Such males should be superior in obtaining and holding a territory, and in defending offspring against predators. However, a ceiling to this choice behavior is provided by the male: A large male is less likely to invest in defending a small female and her offspring (Coleman, 1993). Males in the Midas cichlid invest parentally about as much as females (Rogers and Barlow, 1991). So, a male should be just as choosy as a female (Trivers, 1972; Burley, 1981). He should prefer a large female because she provides more eggs, and an aggressive female because she can better defend the territory and offspring. In aquaria, female subjects were offered four normal-colored treatment males, viewed through one-way mirrors. When only size of male was varied, females chose the largest one. When males differed solely in aggressiveness, females selected the most aggressive one (Rogers and Barlow, 1991). To test whether those results had any meaning in a semi-natural situation, pairs were tested in a pond (Rogers and Barlow, 1991). The pairs were first formed in separate enclosures, so mate choice was not an issue. The testing was simplified by the fish: Males carry the bulk of territorial defense, and when pairs of cichlids fight pairs, each sex engages the same sex of the other pair (Barlow, 1991). As predicted, larger males were better at holding a breeding territory. The more aggressive males were the most active in defending their offspring. Thus, it pays a female to pick a large, aggressive male. This outcome is consistent with conventional views of the benefits of sexual selection and helps explain selection for larger, more aggressive males. Male size and aggressiveness can be viewed as exaggerated traits resulting from sexual selection. Males, in contrast, did not choose among the females. As will be explained further on, the reason for this was that intersexual interaction was precluded. Some results now follow that are contrary to predictions made by models of sexual selection. UTILITY OF SEXUAL SELECTION WHAT IS THE NUCHAL HUMP FOR? Males of many kinds of bony fishes have a prominent nuchal hump on top of the head (Barlow and Siri, 1997). The function of this conspicuous dimorphism, oddly, has never been experimentally investigated, and its role has received scant attention. Males of the Midas cichlid acquire a nuchal hump, but it is prominent only during pair formation. After that, the swelling recedes. The hump remains in a reduced state through the long period of care of freeswimming young (Bleick, 1975; Barlow, 1976). Why does the male change his appearance this way? My favored starting hypothesis was stimulated by the theoretical spirit of the times: The hump of the male is an exaggerated trait that has been either intra- or intersexually selected. Several hypotheses are available for intersexual selection of exaggerated traits, such as runaway selection (Fisher, 1930), sensory bias or exploitation (Ryan, 1990; Basolo and Endler, 1995), an indicator to the female that the male has stored fat in preparation for parental duties (Searcy, 1982; Burley, 1985), higher resistance to parasites (Hamilton and Zuk, 1982), and advertises good genes (Kodric-Brown and Brown, 1984), perhaps because of hydrodynamic drag (Zahavi, 1975). All predict that the larger the hump, the more the female should prefer that male. We considered and rejected other hypotheses, such as antipredation, improved hydrodynamics, and a bumper in fights (Barlow and Siri, 1997). We excluded fat storage because fat content falls during swelling (Bleick, 1975). We ruled out species recognition because co-occurring related cichlids express the hump in much the same way. That left two plausible hypotheses, sex recognition and quality of male. In nature, males ready to breed express a modest nuchal hump (illustrated in Barlow and Siri, 1997) but females never do. In captivity, however, where the fish are well fed and little exercised, some males develop persistent humps that are vastly larger than any ever seen in the wild. Some related cichlids in Central America have huge persistent humps (Meek, 1904). Thus we as- 61 sumed selection could produce and maintain such a colossal hump if it offered a selective advantage. We therefore proffered four lifelike dummy Midas cichlids with humps that we called none, medium (the normal modestly enlarged hump), large and huge. If females responded progressively more to ever larger humps, that would indicate intersexual selection but would not rule out sex recognition. If, however, females responded most to the dummy with the normal size of hump, that would be evidence for sex recognition, and would rule out sexual selection. Females responded significantly the most to dummies with the normal hump, supporting sex recognition but rejecting sexual selection. Males did not differ significantly in their responses to the dummies, though they reacted most to the dummy with no hump; that response profile is also consistent with sex recognition because lack of a hump bespeaks a female. Sexual selection was a useful starting hypothesis, and in its broadest meaning (Andersson, 1994) could apply here. However, as Andersson defined sexual selection, it is virtually synonymous with mate choice and becomes an umbrella covering species and sex recognition. As such, the term loses utility. It also detracts from sorting out the underlying behavioral mechanisms. MATE CHOICE IN RELATION TO COLOR The Midas cichlid originally attracted attention because it is strikingly polychromatic in many of the lakes in Nicaragua. About 8% of the adults of both sexes are gold because they have lost their melanophores at various ages, revealing the underlying xanthophores (Barlow, 1976; Dickman et al, 1988). We call the prevailing gray morph normal. A convincing explanation for the apparently stable polychromatism has not emerged (but see Dickman et al, 1990). Polychromatism and color-assortative mating in the Midas cichlid have inspired conjecture about sympatric speciation (McKaye, 1980; McKaye and Stauffer, 1986; Meyer, 1990). Assortative mating was reported in a seminatural pond (Bar- 62 GEORGE W. BARLOW low, 1976) and in a lake in Nicaragua (McKaye and Barlow, 1976). In the lake, separation by color was more complete; about 95% of pair members were the same color. A reasonable conclusion is the different colored morphs choose one another as mates. Thus, discovery of a behavioral mechanism in mate choice shaped thinking about the Midas cichlid as a model for speciation in the African Great Lakes. However, how that assortative mating arises was not known. We therefore asked whether a Midas cichlid would choose its own color morph for a mate when given an unfettered choice. Early experience with parents or siblings has been implicated in mate choice by cichlids (Greenberg, 1963; Siepen and Crapon de Caprona, 1986); that could accelerate speciation, if other conditions are met (Maynard Smith, 1966). The first test of "sexual imprinting" (Barlow and Rogers, 1978) was ambiguous and less rigorous than the second (Barlow et al., 1990). The second addressed whether color of parents, siblings or self influenced choice of mate. Each female subject was repeatedly offered a choice of a new gold and new normal male. The treatment males were presented behind a one-way mirror, precluding interactions. As before, male subjects did not respond when prevented from interacting with the female. The choices of the females were muted by their tendency to visit back and forth between the males, and so choice was detected only statistically. Females were not influenced by their own color. The colors of their parents and siblings had a slight effect. The clearest difference was a significant bias among females from all rearing conditions for males having the normal color pattern. Weber (1976) reached the same conclusion with the related convict cichlid, ' C nigrofasciatum. That outcome indicated female Midas cichlids have an inherent bias for the normal color pattern. Some other forces must consequently be working to produce assortative mating. Vacillating by the females suggested that color differences are not of primary importance and that they are weighed against other aspects of the males, such as aggressiveness. The males, who were matched for size, could view other males out of the females' line of vision, and they interacted with them. Variation in that interaction probably influenced female choice (see below). EFFECT OF GOLD COLOR ON AGGRESSION Aggressiveness of the fish has a central role in pair compatibility. So it is important to understand how aggression is modulated. Gold coloration profoundly affects the fish that perceives it (see also Evans and Norris, 1996). The response depends on the context, however (McKaye and Barlow, 1976; Barlow and Francis, 1988; Barlow and Siri, 1994): When a dominant fish responds to a gold subordinate, in comparison with a normal-colored one, then the dominant fish increases attacking. But if the subject is itself subordinate, or uncertain, then a gold opponent depresses aggressiveness. The probability of winning also varies with the size of the contestants. When the normal morph is 15% heavier than the gold one the probability of either winning is 50% (Barlow, 1983). Hence being gold confers an advantage equivalent to being 15% heavier than the normal opponent, all else equal. With both contestants the same color, a weight difference as small as 2% can tip the outcome toward the heavier fish (Barlow et al., 1986) so a 15% difference is consequential. Other experiments proved that golds and normals are equally aggressive (Barlow and Wallach, 1976; Barlow and Siri, 1994). The effect is thus not genetically linked to coloration but is instead a property of the perception of gold. I stress this because the point is regularly misunderstood to mean that golds are the more aggressive morph. PAIR FORMATION AS AN INTERACTION The long prevailing perception of pair formation in monogamous cichlids had the male establishing a breeding territory where the female approached him (Baerends and Baerends-van Roon, 1950). However, evidence is accumulating suggesting pair formation may precede or be coincident with setting up a territory (McKaye, 1977; Barlow, 1991). UTILITY OF SEXUAL SELECTION In the field, pairs of Midas cichlids apparently form within loose aggregations. Then they move into the breeding area where they cooperate in obtaining a territory. Observing the moment of pair formation in nature, however, is difficult. In a large artificial pool, females competed for males within heterosexual groups in a way previously unseen in confined aquaria (unpublished data, G.W.B.). A crucial step is when some female swims head on at the dominant male while expanding her opercles, normally a threat gesture. The male mirrors her behavior, as though testing her resolve. At the last moment, she veers off and the two fish brush one another in passing, a behavior pattern called slipping. Females compete with one another, one proposes to the male, and the male accepts or rejects her. This is central to understanding assessment and pairing in this species. All but one of the studies to this point had prevented behavioral interaction between the subjects and the treatment fish. The experiments were purposely so designed despite believing interaction is paramount. That was done because of fear the responses of the treatment fish to the subject would override the effect of the variable being manipulated, such as size or color. The next experiment employed a situation that not only permitted interaction but depended on it. The immediate objective was to probe alternative predictions about the role of interaction in pair formation. In the process of forming a pair, many of the modal action patterns used are the same as those in a fight. The focus was therefore on determining the difference in aggressiveness between a male and a female that favored successful pair formation. The plan of the experiment was generated by three hypotheses (Barlow, 1992). The first, called parity, hypothesized that male aggression is a balance between selection for defending the territory and selection against being too aggressive to mate with the female. It predicted an optimal difference in aggressiveness with the male being the more aggressive mate. The second hypothesis was complementarity: To minimize intrapair fighting, some 63 ideal sum of the male's and female's aggressiveness is optimal. The third hypothesis was female choice for the most aggressive male. This is a direct application of the sexual-selection model, such as proposed by Noonan (1983) for ' C nigrofasciatium. The results (Barlow, 1992) falsified all three hypotheses. The exercise, however, revealed the role of relative aggressiveness in pairing. It also demonstrated a conflict in behavioral mechanisms that runs contrary to simplistic views of mate choice. Normal females were the test subjects. They were given a choice of two appropriately larger normal males of about the same size. We wanted to determine female choice first when restrained by a barrier and then ask whether the same female could successfully mate with the unrestrained male of her choice. On the first day, the female could visit both of two males. The males were held back by a large-mesh screen that permitted exchange of visual, chemical, possibly acoustic, and hydrodynamic stimuli and slight physical contact. On the second day, the screen was removed. Being smaller than the males, the female could pass through slits adjusted to her size but the larger males could not. One crucial detail: The aggressiveness of all three fish was quantified in the test arena on the day before the observations by presenting a mirror to each fish. Female choice was refreshingly crisp. She spent all or nearly all her time with only one male instead of visiting back and forth as in earlier experiments. However, even here simple extrapolation to the natural, unrestrained situation can be misleading. When the barrier was taken away, 43% of the females either did not or could not pair with the male of choice. The usual cause of failure was excessive attacking by the male. Of the rejected females, 29% switched to and paired with the male they had previously neglected. Clearly, female choice was overridden by male rejection. But why did those pairings fail? To test the parity hypothesis, I had plotted the sum of male and female courtship 64 GEORGE W. BARLOW as a function of the difference in aggression scores for each pair. When the barrier was in place, no relationship emerged. Although the male and female seemed to interact through the barrier, in actuality they behaved semi-independently. Each was to a degree insensitive to the actions and responses of the other. For instance, some males repeatedly dashed at the screen and bit it in an attempt to attack the female. The females continued to court instead of withdrawing. When the barrier was removed, a clear pattern of behavioral interaction emerged in the successful pairs: The more the previously measured aggression score of the female exceeded that of the male, the larger became the sum of their combined courtship acts, and conversely the smaller the sum of aggressive behavior. Pairing success, as measured by total courtship, was not just a matter of more aggressive females, nor of just less aggressive males. The relative score was the powerful predictor. Even though the differences in relative size were small, the unintended variation in size also influenced pairing. Increasing female size equated to increasing aggressiveness. The larger the female relative to the male, the more the pair courted. The experiment demonstrated the primacy of relative aggressiveness between the male and the female. It also showed that aggressiveness and size can be traded off. Gold color is tantamount to size or aggressiveness, gold should also have a profound effect on mating. EFFECT OF COLOR ON MATING SUCCESS Although the following comes from an early experiment, it makes more sense now in light of female bias for normal color and the effect on pairing of relative size and aggression. In his doctoral research here, David Noakes noticed that producing compatible pairs of gold males and normal females was difficult. That led to the following experiments (Barlow et ah, 1977). We used all four combinations of color and sex, and the female of each pairing weighed 15% less than the male, a typical size difference in nature. First, we recorded time needed for a female to spawn when a screen separated her from a male. All pair combinations spawned on average in 14 days. Restraining the fish prevented differences from emerging. The experiment was repeated, but now the screen was opened. Those pairs with normal females failed quicker (mean two days) than those with gold females (mean six days). We concluded that gold color inhibits male aggressiveness. About half of the pairs failed in all colorcombinations except for one: Gold male crossed with normal female stood out from the others because only 14% of the pairs were successful. Pair formation in this and many other species of pair-bonding cichlids looks at first like a ritualized fight. We reasoned that the smaller size of the normal female, compounded by the imposing color of the gold male, made her too timid. Recall that gold color in a contest confers an advantage worth 15% by weight. We predicted that if gold males were paired with normal females equal in size, her increase in size would compensate for his color advantage. That was the case. Mating success climbed to about 60%, the same as, or better than, the other color combinations with small females. Thus, the results accord with those on the role of relative aggressiveness in promoting pair formation. DISCUSSION The nuchal hump as a sexually selected trait Understandably, and following Darwin (1871), theory underlying sexual selection has focused predominantly on exaggerated sexual dimorphism. The well-known models include Fisher's (1930) runaway-selection, sensory bias or exploitation (Ryan, 1990; Basolo and Endler, 1995), physical fitness for parentally care-taking (Burley, 1985; Hoelzer, 1989), and good genes in general (Kodric-Brown and Brown, 1984); resistance to disease (Hamilton and Zuk, 1982) and the handicap principle (Zahavi, 1975). All of these attempt to account for exaggerated traits and therefore necessarily UTILITY OF SEXUAL SELECTION rest on a supernormal type of behavioral mechanism (Tinbergen, 1951; Baerends and Kruijt, 1973) in which bigger or more ornamented is better. The example of the nuchal hump in the Midas cichlid, however, demonstrated that bigger is not necessarily better (Barlow and Siri, 1997). Females responded most to an intermediate size of hump, and one that corresponded to the size typically seen on males in nature. The males, in contrast, reacted most to dummies with no hump; lack of a hump signifies female. Selecting the correct sex does play a role in one's fitness. By that criterion, choice based on the presence or absence of the nuchal hump could be considered sexual selection. So classifying it, however, detracts from more specific behavioral adaptations such as sex and species recognition. Mate choice and sexual conflict The focus on exaggerated traits was initially productive. With some exceptions (Burley, 1977), workers concentrated their efforts on species that are highly dimorphic, typically polygynous, and meet only briefly for fertilization. Those dimorphic species, however, may prove an example of a biological "tool" that detracts from the pursuit of other aspects of mating behavior. A monomorphic species, such as the Midas cichlid, presents a different challenge and possibly different answers. I consider it monomorphic because the sexes are visually indistinguishable even though in pairs the female is invariably smaller than the male. I do this because the male and female look alike and their size distributions overlap as adults. Burley (1981) categorized a species as indistinguishable if the individuals reveal a morphological clue to their sex only at certain times. Many such monomorphic species exist in diverse taxa. Judging from our experiments, if they have prolonged pairing, mating is more than initial preference. In one respect, only, pairing in the Midas cichlid fits the scenario for exaggerated traits. Given a choice, females prefer the larger and more aggressive male (Rogers and Barlow, 1991). The problem is that her preference can conflict with and be coun- 65 tered by that of the male. Males reject females that are not aggressive enough in relation to the male's aggressiveness (Barlow, 1992). Therefore, mate choice in this pairbonding species with similar-appearing sexes, is a negotiated relationship between male and female; it is not a simple matter of choice as is so typical for polygynous species {e.g., Weatherhead, 1990). These findings give us pause and compel one to think about the possible adaptiveness of such a mating arrangement. Why males of a biparental species should prefer more aggressive and large, hence fecund, females is easy to understand, as is female preference for large, aggressive males. But that puts the two sexes in conflict. Females may not be able to form pairs with such males. Does that mean in nature successful males are the less aggressive ones? How would that work? The negotiated nature of pairing was also demonstrated in the experiments on mate choice (Barlow et al., 1990) as contrasted with forced pairings (Barlow et al., 1977). Female choice of male by color morph, when made through a one-way mirror, was for the normal color. We (Barlow et al., 1990) concluded that her choice was driven by innate recognition of the primitive color pattern. But when males and females were placed together pair-wise, only about 50% of the pairs could successfully form, and that included normal male with gold female. One combination, gold male with normal female, had a success rate of about one-third of that. Thus one behavioral mechanism, the inherent preference for normal color, is overridden by other behavioral mechanisms. Gold color, because of its effect on the aggressiveness of the other fish, profoundly influences the likelihood of forming a functioning pair. Unfortunately, we still do not understand why, in nature, most fish pair assortatively by color. The answer must lie in some combination of behavioral mechanisms. One of the most prominent of these is probably the effect of gold on the process of negotiating a "peace treaty." Mate choice and speciation in cichlids The complexity of pair formation in pairbonding cichlids should be a caveat to using 66 GEORGE W. BARLOW assortative mating in the Midas cichlid as a model for speciation among the brieflypairing African cichlids. Evolutionary biologists have sought a plausible mechanism for the spectacular radiation there of cichlids into hundreds of species, many of them polychromatic. The most frequently proposed mechanism is sexual-selection (Kosswig, 1947; Dominey, 1984; Mayr, 1984). In this scenario, some females prefer to mate with one color morph and other females prefer the other color; that is the "foot in the door" that leads to a separation of one gene pool into two (see also Seehausen, 1996, recently summarized in Stauffer et al., 1995). The relevance of the Midas cichlid to this situation was noted by McKaye (1980, 1991). He found that pairs of gold morphs breed in relatively deep water while the predominant normal gray morphs breed in shallow water. Based on assortative mating and differential depth distribution, he suggested the two morphs were potentially two species. Meyer (1990) discovered that the pharyngeal jaw apparatus (PJA) of the Midas cichlids is also polymorphic and might present an avenue for sympatric speciation. Liem (1973) had argued the PJA of cichlids is an innovation that facilitated the radiation of the African species. The polychromatism of the Midas cichlid correlated with diet and depth distribution. Unclear, however, was whether the difference is genetic or phenotypic (Meyer, 1990); Axel Meyer has now confirmed that the morphs do not differ genetically (personal communication). Meyer further suggested color of morph and type of PJA covary. The differences were significant, but they applied only to one lake during one season. From the conjunction of depth distribution of snails and breeding, PJA type and assortative mating by color, and following Maynard Smith (1966), Meyer guardedly suggested this situation might be an instance of sympatric speciation in the making, and with unspecified relevance to radiations in the African Great Lakes. Later workers on the African cichlids {e.g., Greenwood, 1991), have cited the papers of McKaye (1980) and Meyer (1990) as providing a possible model for understanding speciation through female preference of male color. The Midas cichlid, however, is inappropriate for the situation in Africa. It and allied species (Barlow and Munsey, 1976) may be undergoing a modest radiation in Nicaraguan lakes (Stauffer et al., 1995; personal communication, E. van den Berghe), but color differences are slight, such as a more yellowish cast to one putative species. The three described sibling species are all colored alike, and one of them, Amphilophus labiatum, is polychromatic in much the same way as is the Midas cichlid (Barlow and Munsey, 1976). Likewise, most of the undescribed species are polychromatic. If assortative mating by color were the key to sympatric speciation in Nicaragua, then the different species should have been all gold or all normal. We should find sibling species, some of which are all-gold and some of which are all normal. That the different and apparently recently evolved species are all much the same color is also contrary to the proposition that color differences have lead to their speciation (see Seehausen, 1996). Rather, because most of the other cichlids in Central America are differently colored (Barlow, 1974), color differences appear to reinforce speciation rather than produce it. Why doesn 't the polychromatic Midas cichlid speciatel The key issue in the Midas cichlid, however, is assortative mating. What prevents them from evolving into two species? The reason appears to lie in the timing of the loss of melanophores, the change in color from normal to gold. Within a cohort from a single pair, color change commonly occurs first in juveniles that are about six months old, but some adults may still be normal in color when two or more years old. Some first-generation offspring of wild-caught fish did not change color until they were five years old. Yet they breed first when about 18 months old. K. R. McKaye (personal communication) has recently seen juveniles in Lake Xiloa that have metamorphosed when about one month old, but the situation there has been disturbed by humans. 67 UTILITY OF SEXUAL SELECTION Commonly, a fish could, therefore, mate and reproduce first as a normal morph then later as a gold one. That would break down the separation into genetically different groups even in the presence of assortative mating. One way to keep the gene pools separate would be for the fish to imprint on the color of their parents. The young are protected by their parents for about one month, so they have ample opportunity to learn about the color of their parents and clearly do (Noakes and Barlow, 1973). However, for mating, they do not imprint on their parents' color (Barlow et al, 1990). The choice experiment as a possibly constraining "tool" The seeming conflict in the findings for restrained versus unrestrained mating should give both encouragement and caution to experiments on mate choice when potential mates are presented behind barriers, or as TV images or dummies. Such experiments are invaluable in teasing out the behavioral mechanisms, but they need to be interpreted guardedly, especially when not gauged against the natural situation. The role of the concept of sexual selection The concept of sexual selection has proved productive in understanding evolution. But now use of the term has broadened so beyond the Fisherian model that it encompasses nearly all aspects of mating, and in monogamous as well as polygynous species. Even species recognition is explained as sexual selection, at least in a solitary species (Ryan and Rand, 1993). Plants manifest sexual selection (Arnold, 1994), and so do sperm (Willson, 1990). This perspective has been put forth by a number of authors (Andersson, 1994) and is expressed by Wiley and Posten (1996, p. 1372): "Sexual selection is best defined as a difference in fecundity as a result of heritable differences in access to mates." Although this perspective has stimulated abundant good research, such an over-arching view can detract from sorting out and comprehending other aspects of mating behavior. An understanding of the behavioral mechanisms of mate choice provokes hypotheses about ultimate explanations. And ultimate explanations stimulate more focused questions about behavioral mechanisms. To understand the evolution of behavior, both proximate and ultimate explanations are needed. ACKNOWLEDGMENTS I am grateful to many people too numerous to mention, unfortunately, who have contributed to this program in ways large and small over the years, but they are all thanked. I am also indebted to Ron Coleman for his careful reading of the manuscript and for stimulating differences with anonymous referees. The National Science Foundation, U.S.A., supported the program over several years, as did the Committee on Research at the University of California, Berkeley, for which I say thank you. REFERENCES Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton. Arnold, S. J. 1994. Is there a unifying concept of sexual selection that applies to both plants and animals? Amer. Nat. 144:S1-S12. Baerends, G. P. and J. M. Baerends-van Roon. 1950. An introduction to the study of the ethology of cichlid fishes. Behaviour Suppl. 1:1-242. Baerends, G. P. and J. P. Kruijt. 1973. Stimulus selection. In R. A. Hinde and J. Stevenson-Hinde (eds.), Constraints on learning, pp. 23-50. Academic Press, London. Barlow, G. W. 1974. Contrasts in social behavior between Central American cichlid fishes and coralreef surgeon fishes. Amer. Zool. 14:9—34. Barlow, G. W. 1976. The Midas cichlid in Nicaragua. In T. B. Thorson (ed.), Investigations of the ichthyofauna of Nicaraguan lakes, pp. 333-358. School of Life Sciences, University of Nebraska, Lincoln. Barlow, G. W. 1983. Do gold Midas cichlid fish win fights because of their color, or because they lack normal coloration? A logistic solution. Beh. Ecol. Sociobiol. 13:197-204. Barlow, G. W. 1991. Mating systems among cichlid fishes. In M. H. A. Keenleyside (ed.), Cichlid fishes, behaviour, ecology and evolution, pp. 173— 190. Chapman and Hall, New York. Barlow, G. W. 1992. Is mating different in monogamous species? The Midas cichlid fish as a case study. Amer. Zool. 32:91-99. Barlow, G. W. and R. C. Francis. 1988. Unmasking affiliative behavior among juvenile Midas cichlids (Cichlasoma cithnellum). J. Comp. Psychol. 102: 118-123. Barlow, G. W., R. C. Francis, and J. V. Baumgartner. 68 GEORGE W. BARLOW Echelle and I. Kornfield (eds.), Evolution of fish 1990. Do the colours of parents, companions and species flocks, pp. 231—249. University of Maine self influence assortative mating in the polychroat Orono Press, Orono. matic Midas cichlid? Anim. Behav. 40:713-722. Barlow, G. W. and J. W. Munsey. 1976. The red devil- Evans, M. R. and K. Norris. 1996. The importance of Midas-arrow cichlid species complex in Nicaracarotenoids in signaling during aggressive intergua. In T. B. Thorson (ed.), Investigations of the actions between male firemouth cichlids (Cichlaichthyofauna of Nicaraguan lakes, pp. 359-369. soma meeki). Behav. Ecol. 7:1-6. School of Life Sciences, University of Nebraska, Fisher, R. A. 1930. The genetical theory of natural Lincoln, Nebraska. selection. Dover, New York. Barlow, G. W. and W. Rogers. 1978. Female Midas Francis, R. C. and G. W. Barlow. 1993. Social control cichlid's choice of mate in relation to parents' and of primary sex differentiation in the Midas cichlid. to own color. Biol. Behav. 3:137-146. Proc. Nat. Acad. Sci. U.S.A. 90:10673-10675. Barlow, G. W., W. Rogers, and R. V. Cappeto. 1977. Greenberg, B. 1963. Parental behavior and imprinting Incompatibility and assortative mating in the Miin cichlid fishes. Behaviour 21:127-144. das cichlid. Beh. Ecol. Sociobiol. 2:49-59. Greenwood, P. H. 1991. Speciation. In M. H. A. Barlow, G. W., W. Rogers, and N. Fraley. 1986. Do Keenleyside (ed.), Cichlid fishes. Behaviour, ecolMidas cichlids win through prowess or daring? It ogy and evolution, pp. 86-102. Chapman and depends. Behav. Ecol. Sociobiol. 19:1-8. Hall, New York. Barlow, G. W. and P. Siri. 1994. Polychromatic Midas Hamilton, W. D. and M. Zuk. 1982. Heritable true cichlids respond to dummy opponents: Color, confitness and bright birds: A role for parasites? Scitrast and context. Behaviour 130:77-112. ence 218:384-387. Barlow, G. W. and P. Siri. 1997. Does sexual selection Hoelzer, G. A. 1989. The good parent process of sexaccount for the conspicuous head dimorphism in ual selection. Anim. Behav. 38:1067-1078. the Midas cichlid? Anim. Behav. 52:573-584. Keenleyside, M. H. A. 1985. Bigamy and mate choice Barlow, G. W. and S. J. Wallach. 1976. Colour and in the biparental cichlid fish Cichlasoma nigrofaslevels of aggression in the Midas cichlid. Anim. ciatum. Behav. Ecol. Sociobiol. 17:285-290. Behav. 24:814-817. Kodric-Brown, A. and J. H. Brown. 1984. Truth in Basolo, A. L. and J. A. Endler. 1995. Sensory biases advertising: The kinds of traits favored by sexual and the evolution of sensory systems. Trends selection. Amer. Nat. 124:309-323. Ecol. Evol. 10:489. Kosswig, G. 1947. Selective mating as a factor for Berghe, E. van den. Appalachian Environmental Labspeciation in cichlid fish of East African lakes. oratory, Gunter Hall, Frostburg, Maryland 21532. Nature 179:604-605. Bleick, C. R. 1975. Hormonal control of the nuchal Liem, K. F. 1973. Evolutionary strategies and morhump in the cichlid fish Cichlasoma cithnellum. phological innovations: Cichlid pharyngeal jaws. Gen. Comp. Endocrin. 26:198-208. Systemat. Zool. 22:425-441. Burley, N. 1977. Parental investment, mate choice, Macedonia, J. M. and J. A. Stamps. 1994. Species and mate quality. Proc. Nat. Acad. Sci. U.S.A. 74: recognition in Anolis grahami (Sauria, Iguanidae): 3476-3479. Evidence from responses to video playbacks to conspecific and heterospecific displays. Ethology Burley, N. 1981. Mate choice by multiple criteria in 98:246-264. a monogamous species. Amer. Natur. 117:515528. Marler, P. and D. Isaac. 1960. Song variation in a population of brown towhees. Condor 62:272Burley, N. 1985. The organization of behavior and the evolution of sexually selected traits. Amer. Orni283. thol. Union, Ornithol. Monogr. 37:22-44. Maynard Smith, J. 1966. Sympatric speciation. Amer. Clark, D. L. and G. W. Uetz. 1990. Video image recNatur. 100:637-650. ognition by the jumping spider, Maevia inclemens Mayr, E. 1984. Evolution of fish species flocks: A (Araneae: Salticidae). Anim. Behav. 40:884-890. commentary. In A. A. Echelle and I. Kornfield (eds.), Evolution offish species flocks, pp. 3—11. Coleman, R. M. 1993. The evolution of parental inUniversity of Maine Press, Orono. vestment in fishes. Department of Zoology, University of Toronto, Toronto. McKaye, K. R. 1977. Competition for breeding sites Darwin, C. 1871. The descent of man and selection between the cichlid fishes of Lake Jiloa, Nicarain relation to sex. John Murray, London. gua. Ecology 58:293-302. Dickman, M. C , C. Annett, and G. W. Barlow. 1990. McKaye, K. R. 1980. Seasonality in habitat selection Unsuspected cryptic polymorphism in the polyby the gold color morph of Cichlasoma citrinelchromatic Midas cichlid. Biol. J. Linn. Soc. 39: lum and its relevance to sympatric speciation in 239-249. the family Cichlidae. Env. Biol. Fish. 5:75-78. Dickman, M. C , M. Schliwa, and G. W. Barlow. 1988. McKaye, K. R. 1986. Mate choice and size assortative Melanophore death and disappearance produces pairing by the cichlid fishes of Lake Jilod, Nicacolor metamorphosis in the polychromatic Midas ragua. J. Fish. Biol. 29:135-150. cichlid (Cichlasoma citrinellum). Cell Tiss. Res. McKaye, K. R. 1991. Sexual selection and the evo253:9-14. lution of the cichlid fishes of Lake Malawi, Africa. In M. H. A. Keenleyside (ed.), Cichlid fishes. BeDominey, W. J. 1984. Effects of sexual selection and haviour, ecology and evolution, pp. 241-257. life history on speciation: Species flocks in AfriChapman & Hall, New York. can cichlids and Hawaiian Drosophila. In A. A. UTILITY OF SEXUAL SELECTION McKaye, K. R. and G. W. Barlow. 1976. Competition between color morphs of the Midas cichlid, Cichlasoma citrinellum, in Lake Jiloa, Nicaragua. In T. B. Thorson (ed.), Investigations of the ichthyofauna of Nicaraguan lakes, pp. 465—475. School of Life Sciences, University of Nebraska, Lincoln. McKaye, K. R. and J. R. Stauffer. 1986. Description of a gold cichlid (Teleostei: Cichlidae) from Lake Malawi, Africa. Copeia 1986:870-875. Meek, S. E. 1904. The fresh-water fishes of Mexico north of the Isthmus of Tehuantepec. Field Columbian Mus. Publ. 93, Zool. Ser. 5:1-252. Meyer, A. 1990. Ecological and evolutionary consequences of the trophic polymorphism in Cichlasoma citrinellum (Pisces: Cichlidae). Biol. J. Linn. Soc. 39:279-299. Noakes, D. L. G. and G. W. Barlow. 1973. Crossfostering and parent-offspring responses in Cichlasoma citrinellum. Z. Tierpsychol. 33:147—152. Noonan, K. C. 1983. Female mate choice in the cichlid fish Cichlasoma nigrofasciatum. Anim. Behav. 31:1005-1010. Rogers, W. and G. W. Barlow. 1991. Sex differences in mate choice in a monogamous biparental fish, the Midas cichlid (Cichlasoma citrinellum). Ethology 87:249-261. Ryan, M. J. 1990. Sexual selection, sensory systems and sensory exploitation. Oxford Surv. Evol. Biol. 7:157-195. Ryan, M. J. and A. S. Rand. 1993. Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47:647-657. Searcy, W. A. 1982. The evolutionary effects of mate selection. Ann. Rev. Ecol. Syst. 13:57-85. Seehausen, O. 1996. Distribution of and reproductive 69 isolation among color morphs of a rock-dwelling Lake Victoria cichlid (Haplochromis nyererei). Ecol. Freshw. Fish. 5:195-202. Siepen, G. and M.-D. Crapon de Caprona. 1986. The influence of parental color morph on mate choice in the cichlid fish Cichlasoma nigrofasciatum. Ethology 71:187-200. Spurway, H. and J. B. S. Haldane. 1953. The comparative ethology of vertebrate breathing. Behaviour 6:8-34. Stauffer, J. R., Jr., N. J. Bowers, K. R. McKaye, and T. D. Kocher. 1995. Evolutionary significant units among cichlid fishes: The role of behavioral studies. Amer. Fisher. Soc. Symp. 17:227-244. Tinbergen, N. 1951. The study of instinct. Oxford University Press, Oxford. Trivers, R. L. 1972. Parental investment and sexual selection. In B. Campbell (ed.), Sexual selection and the descent of man, pp. 136-179. Aldine, Chicago. Weatherhead, P. J. 1990. Secondary sexual traits, parasites, and polygyny in red-winged blackbirds, Agelaius phoeniceus. Behav. Ecol. 1:125-130. Weber, P. G. 1976. The effect of female color, size, dominance and early experience upon mate selection in male convict cichlids, Cichlasoma nigrofasciatum Giinther (Pisces, Cichlidae). Behaviour 56:116-135. Wiley, R. H. and J. Poston. 1996. Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50:1371-1381. Willson, M. F. 1990. Sexual selection in plants and animals. Trends Ecol. Evol. 5:210-214. Zahavi, A. 1975. Mate selection—a selection for a handicap. J. Theor. Biol. 53:205-214. Corresponding Editor: Paul A. Verrell