Do Female Fish Prefer to Spawn in Nests with Eggs for Reasons of Mate Choice Copying or Egg Survival?

The University of Chicago

Do Female Fish Prefer to Spawn in Nests with Eggs for Reasons of Mate Choice Copying orEgg Survival?Author(s): Ian JamiesonSource: The American Naturalist, Vol. 145, No. 5 (May, 1995), pp. 824-832Published by: The University of Chicago Press for The American Society of NaturalistsStable URL: http://www.jstor.org/stable/2463003 .

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Vol. 145, No. 5 The American Naturalist May 1995

DO FEMALE FISH PREFER TO SPAWN IN NESTS WITH EGGS FOR REASONS OF MATE CHOICE COPYING OR EGG SURVIVAL?

IAN JAMIESON*

Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand

Submitted August 2, 1993; Revised May 4, 1994; Accepted May 31, 1994

Abstract.-When a female is more likely to mate with a male because other females have mated with him, the female is said to be "copying" the mate choice of others. Much of the discussion of copying has centered around lekking birds. However, reviews on the subject have also pointed to experimental studies of fish and female preferences for males with eggs in their nest as evidence for the existence of copying. I question this claim by arguing that these studies may indicate that females prefer to spawn in nests with eggs because the presence of eggs increases the quality of a spawning site through increased egg survival, not because eggs signify a previous female's mate choice. The two hypotheses may not always be mutually exclusive, but data on female preference for nests with an intermediate number of eggs or eggs in the earlier stages of development are more in line with the egg survival hypothesis than the mate choice copying hypothesis.

Models of sexual selection and the evolution of female preferences assume that females choose their mates independently (Harvey and Bradbury 1991). Recently, it has been suggested that this might not always be strictly the case. Some females' mate choice decisions may be influenced by the behavior of other females; in other words, females may be "copying" the mating decisions of others (Brad- bury 1981; Losey et al. 1986; Wade and Pruett-Jones 1990; Dugatkin 1992; Gibson and Hoglund 1992; Pruett-Jones 1992). Copying may be adaptive if direct male assessment is costly and/or some females are less able to discern high-quality males (Losey et al. 1986; Pruett-Jones 1992). Copying, like independent female mate choice, may therefore be an important component of the process of sexual selection because it can lead to increased variance of male mating success (Wade and Pruett-Jones 1990).

Pruett-Jones (1992) recently reviewed some of the empirical evidence support- ing female copying. The species he lists (table 1, p. 1003) can be divided into two categories: those with internal fertilization, no male parental care, and in which copying females base their mating decision on mating activity of other females (e.g., lekking mammals and birds, guppies); and those with external fertilization, exclusive male parental care, and in which the copying females base their mating decision on physical evidence that other females have already mated with a particular male (e.g., presence of eggs in a male's nest in fish species with paternal

* E-mail: [email protected].

Am. Nat. 1995. Vol. 145, pp. 824-832. ? 1995 by The University of Chicago. 0003-0147/95/4505-0010$02.00. All rights reserved.



FEMALE COPYING IN FISH 825

care). In the latter category, there is, clear evidence that females preferentially lay their eggs in nests of males who already have eggs.

Pruett-Jones (1992) defined copying behavior as a type of nonindependent choice that occurs when a female's decision to mate with a particular male is influenced by whether that male has previously mated. He also noted that behavior other than female copying could result in nonindependent distributions of male mating success. For example, when females prefer certain habitats or mating sites and such preferences influence the females' exposure to males, then the choice of mates may also be nonindependent. Pruett-Jones argued that the term copying be restricted to mate choice behavior and that other forms of nonindependent choice such as habitat or mating site selection be referred to as conspecific cueing. He went on to suggest that the acceptance of evidence of female copying in fish with male parental care was tentative, as there are several other possible explanations for females' preference for spawning in nests with eggs other than for reasons of mate choice (see also Dugatkin 1992).

The aim of this article is to propose that the cited examples of female copying in fish species with external fertilization and male parental care do not comply with the spirit of the definition of mate choice copying as set forth by Pruett-Jones (1992). I will attempt to show that female preference for spawning in nests with eggs may be related more to the presence of eggs directly affecting egg survival than to eggs signaling a previous female's mate choice. I will refer to this distinction as female behavior dealing with spawning site selection versus mate choice copying. Furthermore, I will show that although the researchers working with these fish species have used the term copying to describe female preferences for males who are already mated, most of them clearly interpreted the adaptiveness of this behavior in terms of egg survival and not in terms of mate choice (e.g., good genes).

FEMALE PREFERENCE FOR NESTS WITH EGGS

The fish species Pruett-Jones (1992) listed as showing evidence of females preferentially laying eggs in nests of males who already have eggs were the river bullhead (Cottus gobio), the fathead minnow (Pimephales promelas), and the fantail darter (Etheostoma flabellare). To this list I would add the tessellated darter (Etheostoma olmstedi) (Constantz 1985), the damselfish (Chrysiptera cyanea) (Gronell 1989), the garibaldi (Hypsypos rubicundus) (Sikkel 1989), and the Mediterranean blenny (Aidablennius sphynx) (Kraak and Videler 1991). I would also add the three-spined stickleback (Gasterosteus aculeatus) based on the results of a recent study by Goldschmidt et al. (1993). Pruett-Jones omitted sticklebacks because there was evidence that females of this species were choosing males based on differences in male behavior, which was a consequence of whether the male had eggs in his nest (Jamieson and Colgan 1989). However, in their population, Goldschmidt et al. did not detect any difference in male behavior due to the presence or absence of eggs and hence concluded that females were basing their mating decision directly on whether eggs were present in the male's



826 THE AMERICAN NATURALIST

nest. (Differences between Goldschmidt et al.'s results and those obtained by Jamieson and Colgan are discussed in more detail elsewhere [Jamieson 1994].)

External fertilization and female choice for high-quality spawning sites has undoubtedly been an important determinant of male-male competition in fish and predisposes such species to the evolution of male parental care (for reviews, see Ridley 1978; Blumer 1979; Perrone and Zaret 1979; Baylis 1981; Gross and Shine 1981; Gross and Sargent 1985). Males defend a spawning or nest site from other males and attempt to attract females to the site through courtship and bright coloration. Male fish will spawn with several females, and the maximum number of eggs they can obtain is usually limited by the size of the nest or spawning substrate. Once a clutch is obtained, the male will clean, fan, and guard the eggs. Unlike most species of birds, parental care does not involve feeding, and therefore a large number of offspring can be cared for as easily as a few (Williams 1975; Wittenberger 1981).

Before any males have obtained eggs, females may spawn with the largest males who tend to defend the better-quality nest sites (Marconato and Rasotto 1983; Constantz 1985; Bisazza and Marconato 1988), or they may spawn ran- domly among a group of males (Unger and Sargent 1988). Once a clutch is obtained, the presence of eggs appears to be the prime determinant of subsequent male mating success (Bisazza and Marconato 1988; Unger and Sargent 1988; Gronell 1989; Knapp and Sargent 1989; Sikkel 1989; Kraak and Videler 1991). Experimental evidence indicates that when male characteristics such as body size, coloration, and behavior are controlled, females prefer to spawn with males who have eggs in their nest over males with empty nests (Marconato and Bisazza 1986; Bisazza and Marconato 1988; Unger and Sargent 1988; Gronell 1989; Knapp and Sargent 1989; Sikkel 1989; Kraak and Videler 1991). A male may even be preferred over a larger individual if he has recently spawned eggs in his nest (Bisazza and Marconato 1988). Female preference for nests with eggs is also believed to be the driving force behind the evolution of egg mimicry (Knapp and Sargent 1988) and of alloparental care in which males will kidnap eggs (Rohwer 1978) or take over the nest site and care for the eggs of another male (Constantz 1985; Bisazza and Marconato 1988; Unger and Sargent 1988; Gronell 1989).

Why should females prefer to spawn in nests with eggs? The presence of eggs could signify that a male has been found attractive by other females; that is, females use the presence of eggs to copy the mate choice decisions of other females (Ridley 1978; Goldschmidt et al. 1993). As mentioned above, copying could be adaptive if assessing male quality is costly or if differences in male quality are difficult to discern for some females (Losey et al. 1986; Pruett-Jones 1992). Variation in male quality in general may be difficult to discern, especially for young inexperienced females (Bradbury 1981), although predicted differences in the pattern of mate choice behavior between older and younger females has only been demonstrated in guppies (Poecilia reticulata) (Dugatkin and Godin 1993).

On the other hand, a female may prefer to spawn in nests with eggs not because eggs signal the mate choice decisions of other females but because the presence of eggs increases the nest's quality as a spawning site. Preferential spawning in




nests with eggs increases egg survival when the risk of predation of the female's eggs decreases as egg numbers increase-what is termed the "dilution effect" (see Sargent 1988). Male parental care and subsequent offspring survival have also been shown to increase as the number of eggs in a male's nest increases (Sargent 1988). Increased egg survival is the explanation favored by most workers who have demonstrated female preference for males with eggs even though they sometimes refer to this phenomenon as female copying. For example, Gronell (1989) concludes that female damselfish are "mating with male(s) which provide the best environment for their offspring, in this case, with the most eggs already in the nest. They are therefore copying the choices of other females and deriving the benefits of higher hatching success in nests containing more eggs" (p. 120).

This behavior is copying, in the broadest sense of the word. However, we need to distinguish between copying for reasons of mate choice in cases in which, for example, females are likely to obtain good genes for their offspring and preference for certain nest sites for reasons of increased egg survival; the latter should not be considered copying (see Pruett-Jones 1992). Although the nest site a male is defending might be considered an extended phenotype, I will argue below that it is still important to distinguish the factors driving female preferences for nests with eggs. While a female who mates with a previously mated male should still reap the same genetic benefits as the female(s) she has copied, the benefits of spawning in a nest with eggs, with respect to offspring survival, will change as eggs are added to a nest (Sargent 1988). The question is, To which of these two factors is the female more sensitive?

DISTINGUISHING BETWEEN MATE CHOICE AND NEST CHOICE

The problem at hand is that both the mate choice and egg survival hypotheses make the same general prediction: females should prefer to spawn in nests that already contain eggs. The two may not be mutually exclusive (see below), but it would be helpful if it could be shown that one hypothesis better explains certain aspects of female mating behavior than the other. For example, if females preferred males with eggs in their nest for reasons of mate choice then we might assume that the more eggs in a male's nest, the more "attractive" the male, and hence the more likely a copier female would be to spawn in his nest (fig. 1A). It is also predicted that the probability of egg survival through the dilution effect or increased parental effort also increases with egg number (Sargent 1988) (fig. 1B). This is particularly true in species in which eggs form a single layer on the nest substrate (see below). However, in some cases eggs deposited late in a nest can suffer greater mortality than those laid earlier and receive less parental care (Downhower and Brown 1981; Sikkel 1989). Sikkel (1989) demonstrated that female garibaldi preferred nests with eggs in the early rather than late stages of development, a result not predicted by the copying hypothesis.

There may also be disadvantages associated with spawning in nests with large numbers of eggs if the eggs form multilayer clumps in relatively small, covered nests such as those used by three-spined sticklebacks. For example, the last clutch spawned in the nest can be more vulnerable to predation or cannibalism




A

i H: Mate choice copying

0

NUMBER OF EGGS

B

| H: Egg survival

t 1~~~~~~~~~~~~~~~~~~

0

O 2

NUMBER OF EGGS

FIG. 1.-The predicted relationships between the number of eggs in the nest and the probability of female spawning for the mate choice copying (A) and egg survival (B) hypotheses. For B, egg survival could increase with increasing egg number if egg predation rates decreased or parental care rates increased (1). However, these advantages could quickly diminish if oxygen availability per egg declined as eggs in the nest became crowded, which would result in the probability of spawning being a decreasing function (2).

(Rohwer 1978; FitzGerald 1991; Goldschmidt et al. 1993), or it can result in the nest being too crowded, which causes increased competition for oxygen (Reebs et al. 1984; Belles-Isles et al. 1990). Therefore, if female sticklebacks were preferring males with eggs for reasons of egg survival, then they should prefer nests with intermediate number of eggs (fig. 1B)-again, a pattern not predicted by the copying hypothesis.




Both field and experimental evidence indicates that the probability of a female stickleback entering a nest and spawning is greater when one clutch of eggs is already present in the nest than when two or more clutches are present (Belles- Isles et al. 1990; Goldschmidt et al. 1993). There may be a conflict of interest between males and females with respect to the optimum number of eggs in a nest, since males continue to court and lead females to their nest well after the first clutch of eggs is obtained (Belles-Isles et al. 1990). However, the need to care for those eggs gradually reduces the time spent courting to the point where males stop courting gravid females and spend most of their time fanning the eggs (Jamieson et al. 1992). From the male's perspective, an additional clutch of eggs should be accepted as long as the fitness payoff is greater than if he did not accept a new clutch. From the female's perspective, however, eggs laid later in the spawning sequence may have a lower probability of survival than those laid earlier (see above), and the female may be better off to seek another nest in which to spawn.

Of course, the two hypotheses may not be mutually exclusive. Goldschmidt et al. (1993) coined the term selective copying to denote that female sticklebacks may be copying the mate choice of other females by preferring to spawn with males who already had eggs but remained selective as to the number of eggs in the nest. This may well be the case, but if the match between female preference and egg survival were very close, as seems to be the case in sticklebacks, it would suggest that females are more sensitive to changes in spawning site quality than mate quality. On the other hand, if female preference for nests with eggs regularly "overshot" the optimum range that would maximize egg survival, then females might be more sensitive to mate quality as measured by the presence of numerous clutches of eggs. It may also be interesting to determine whether the degree of sensitivity to these factors is age- or experience-dependent, with younger females more likely to copy older females and thus more likely to spawn in overcrowded nests, for example. Further empirical work is needed to tease these components apart.

THE EVOLUTIONARY CONSEQUENCES OF FEMALE PREFERENCE FOR NESTS WITH EGGS

Irrespective of whether females are choosing to spawn with particular males on the basis of other females' mate choice or increased egg survival, preferential spawning in nests with eggs can still increase the variance of male mating success and hence increase the opportunity for sexual selection. Pruett-Jones (1992) agrees that several different processes can change the distribution of matings from that expected under independent choice but argues that distinction between these processes is important. In species in which females copy each other's mate choice, selection may act on mating preferences. In species in which females exhibit nonindependent preferences for particular spawning sites (what Pruett- Jones refers to as "conspecific cueing"), selection may act on patterns of nest site selection.

For example, traits such as large body size and aggression would allow males to secure and defend high-quality spawning sites, which includes taking over




nests containing eggs of other males (Constantz 1985; Bisazza and Marconato 1988; Unger and Sargent 1988). Other traits such as bright coloration and courtship displays may function to indirectly signal male quality (see, e.g., Milinski and Bakker 1990), but they may also function in initially attracting a female's attention to a male's territory so that she can then inspect the male's nest site (Baylis 1981; Gronell 1989). Once at the nest, the female's decision to spawn may depend on the quality of the nest site, which can be positively influenced by the presence of eggs, as argued above. Therefore, alloparental care (Unger and Sargent 1988; Gronell 1989) and egg mimicry (Knapp and Sargent 1989) would have evolved to influence the female's spawning decision after she has been attracted to a nest site. Such males are not necessarily "cheaters," as a positive correlation has been shown between these traits and offspring survival (Unger and Sargent 1988; Knapp and Sargent 1989). Nevertheless, unlike most sexually selected traits, alloparental care and egg mimicry evolved to make the male's nest site rather than the male himself more attractive to females. These factors are consistent with the idea that females are sensitive to variation in nest site suitability and that the presence of eggs improves the quality of nest sites.

In conclusion, with the intense interest currently being shown in female copying of mate choice, more care is needed in distinguishing between copying and other forms of nonindependent selection behavior. Fish species in which females show a preference for spawning in nests with eggs are often cited as examples of female copying. However, evidence such as female preference for nests with intermediate numbers of eggs or nests with eggs in the early stages of development rules out the possibility that the only reason that females choose nests with eggs is because eggs indicate a previous female's mate choice.

ACKNOWLEDGMENTS

I wish to thank R. Poulin, S. Pruett-Jones, J. Waas, and the University of Otago Behavioral Ecology Discussion Group for their helpful comments on the manuscript. Research on mate choice in fish presently being conducted by myself and my students is supported by the University of Otago and New Zealand Lot- tery Grants Board.

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Do Female Fish Prefer to Spawn in Nests with Eggs for Reasons of Mate Choice Copying or Egg Survival?