Behavioral Ecology Advance Access originally published online on December 15, 2005
Behavioral Ecology 2006 17(2):255-259; doi:10.1093/beheco/arj021
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Male but not female pipefish copy mate choice
Department of Population Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18 D, SE-752 36 Uppsala, Sweden
Address correspondence to M.S. Widemo. E-mail: maria.widemo{at}ebc.uu.se.
Received 7 March 2005; revised 20 October 2005; accepted 11 November 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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If mate choice is costly, an individual may reduce the costs of choice by observing and copying the mate choice of others. Although copying has received much attention during the past 10 years, evidence of copying is not very strong, partly because of problems with distinguishing copying from other mechanisms creating similar mating patterns. I conducted an aquarium experiment using the deep-snouted pipefish Syngnathus typhle, a species with reversed sex roles and mutual mate choice. I tested whether copying occurred both during male and female mate choice. The results showed that males, but not females, displayed more toward an individual, which they perceived as popular among others, and this was interpreted as male mate choice copying. While being the first evidence of copying in a sex-role–reversed species, the sex difference in behavior mirrors the sex-role pattern and begs the question whether we should predict copying only in females in other species with mutual choice but conventional sex roles.
Key words: copying, cultural evolution, mutual mate choice, pipefish, sex-role reversal, Syngnathus typhle.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Along with the increasing recognition of mate choice as an important evolutionary force, there has been an increased interest in mechanisms of decision making. There is today a broad agreement among scientists that mate choice has evolved due to the benefits to the chooser, but the underlying desicion-making mechanisms are far less explored (Gibson and Langen, 1996
). Copying the mate choice of others has been suggested as a strategy for choosing individuals to reduce their costs of choice. Mate choice copying has been defined as an increased probability of a female to choose a particular male as mate as a result of observing another female choosing him (Gibson et al., 1991). From a theoretical point of view, copying is an interesting phenomenon for two reasons. It allows a trait (preference) to spread nongenetically in a population and can thus be an example of cultural evolution (Brooks, 1998). Furthermore, copying is likely to produce an increased variance in male mating success (Marks et al., 1994) and thereby giving rise to an increased potential for sexual selection (Wade, 1979, but see Marks et al., 1994).
There are, however, several alternative mechanisms that might result in the same mating pattern in a population. Brooks (1998) therefore makes the important distinction between "true-" and "pseudo-copying," the former defined as an increased probability that a female will mate with a certain male after observing him mate with another female (sensu Pruett-Jones, 1992), a trait conferring fitness benefits per se, by reducing costs of choice. On the other hand, "pseudocopying" lumps together other phenomena, such as females herding to avoid male harrassment (conspecific cueing, McComb and Clutton-Brock, 1994) or increased male display rate (and thus attractiveness) as a result of recent mating (Galef and White, 1998), all producing the same mating pattern as copying would (see Westneat et al., 2000, for a discussion). The best way to demonstrate the occurrence of mate choice copying would therefore be experiments controlling for these alternative mechanisms.
Mate choice copying has been demonstrated conclusively only in a few species, and the prevalence and importance of the phenomenon is debated (Brooks, 1998). To date, convincing experimental evidence of copying stems from studies of fish; female Japanese medaka (Oryzias latipes) (Grant and Green, 1996) and both sexes of sailfin mollies (Poecilia latipinna) copy (Schlupp and Ryan, 1997; Schlupp et al., 1994; Witte and Ryan, 1998), the latter also being the only example so far of male mate choice copying (Schlupp and Ryan, 1997). Guppies (Poecilia reticulata) are extensively studied in this respect, but not all experimenters agree. Dugatkin et al. have in a series of experiments found evidence of copying (Briggs et al., 1996; Dugatkin, 1998; Dugatkin and Godin, 1992, 1993, 1998), but other studies with similar design on guppies from other populations found no signs of copying (Brooks, 1996, 1999; Lafleur et al., 1997). In three-spined sticklebacks (Gasterosteus aculeatus), the tendency of females to lay eggs in nests that already contain eggs may be explained by copying or as a tactic to reduce the risk of the eggs being eaten by the father through a dilution effect (Goldschmidt et al., 1993; Patriquin and Godin, 1998).
Lekking behavior should facilitate copying because of the aggregation of conspecifics. The empirical evidence from lekking species is, however, somewhat confusing. In black grouse (Tetrao tetrix), Höglund et al. (1995) found an increased probability for a male to obtain matings if he had a female dummy in his territory. But in an observational study, Höglund et al. (1990) found that only in one out of eight lek-years was the number of consecutive copulations high enough to deviate from a random distribution of copulations, thus making copying (or some other mechanism) a rare explanation for the copulation pattern. In sage grouse (Centrocercus urophasianus), copying was inferred from observational data (Spurrier et al., 1994), but an aviary experiment failed to demonstrate copying (Gibson et al., 1991), perhaps due to the unnatural aviary situation. Female great snipes (Gallinago media) do not copy the choice of others (Fiske et al., 1996), nor do fallow deer ewes (Dama dama) (McComb and Clutton-Brock, 1994), the latter being the only mammalian species hitherto studied.
In the experiment reported here, I tested both males' and females' tendency to copy the mate choice of conspecifics, while controlling for the alternative explanations mentioned above. I did this by allowing a male to choose between a female courted by other males (the female being unaware of this) and a female not courted by other males in the male copying treatment and vice versa when the female tendency to copy was investigated. This design eliminates herd (or schooling) as well as display effects. I conducted the study on the deep-snouted pipefish (Syngnathus typhle), which is a suitable species for several reasons. It is well studied with regard to sexual selection, which facilitates the design of experiments. Both males and females exhibit preferences for large individuals of the opposite sex, males prefer parasite-free females over parasitized ones (see Berglund, 2000, for a review) and females prefer males with swollen brood pouches over males with flat ones (Widemo MS, unpublished data). Fish used in the experiment were therefore matched for all these traits to obtain a balanced design. The deep-snouted pipefish lives in eelgrass (Zostera marina) meadows along the European coast, the mating season is relatively short and synchronized, with many individuals looking for mates at the same time (Vincent et al., 1995). There is thus a possibility for mate choice copying in both sexes, and because both male and female mate choice affects offspring quality (Sandvik et al., 2000), copying may have evolutionary consequences. The species is sex-role reversed, that is, females are the most intensively competing sex, have a sexual ornament, and males are more choosy than females (Berglund, 2000).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The experiment was carried out at Klubban Biological Station and Kristineberg Marine Research Station in Fiskebäckskil, Sweden, in 1999. In early May, the fish were caught by trawling eelgrass meadows in the vicinity, and the fish were kept, sexes apart, in 225-l tanks until the start of the experiment. The mate choice arena consisted of a 50 x 40 x 70–cm (depth) aquarium divided into five compartments (Figure 1). A transparent plexiglass wall between the focal fish (compartment e) and the other compartments allowed the focal fish to see all other fish. The object fish were situated in the middle compartments b and c, separated by an opaque wall. Flanking these (in a and d) were the model fish, where the model fish in compartment a could observe the object fish in b through a one-way mirror (the copy situation), while the model fish in d could not see the object fish in c due to an opaque plexiglass wall (the noncopy situation). The one-way mirror effect was obtained by hanging 40-W light bulbs (Philips) approximately 15 cm above each of the two object compartments. To compensate for potential increase in female display rate as a result of the mirror between compartments a and b, a mirror was placed in c as well. Thus, in the example in Figure 1, in the left-hand part of the aquarium the focal male has the possibility to copy the "mate choice" of the model males in a, whereas in the right-hand side, there will be no copying as the model males in d cannot see the female in c and thus cannot show any interest in her.
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As model fish, I used one larger and one smaller in size than the focal fish in each model compartment. The reason for this was twofold. It increases the chance that at least one of the model fish might find the object fish interesting and perform courtship displays toward it. Earlier experiments with this choosy species have shown that even at the peak of mating season not all individuals will choose any out of two partners (Sandvik et al., 2000
), perhaps because none of them matches its preference. Thus, using two model fish would increase the probability of the desired courtship behavior to occur in the model compartment. The second reason for this design was that on the one hand, it has been suggested that observing a small (younger) individual's mate choice may be a poor indicator of mate quality if this smaller fish is less experienced than the focal fish itself, and more reliable information is to be gained by observing larger individuals with more experience (Dugatkin and Godin, 1992). On the other hand, in this species, female-female competition is severe (Berglund and Rosenqvist, 1993; Berglund et al., 1989, 1997), larger females suppress reproduction in smaller, subordinate ones (Berglund, 1991), and male-male antagonistic behaviors occur (personal observation) though the function of these are less explored. A larger model fish, especially in female choice replicates, may thus potentially deter the focal fish from courting. The solution to this dilemma was to use one larger and one smaller fish, and I applied the same design to both female and male choice replicates for them to be comparable. The object fish were matched for size and parasite load (number of visible black spots on the skin) within replicates, and all fish used were sexually mature, that is, males had fully developed brood pouches and females had bellies swollen with ripe eggs. I randomized between replicates whether the "copy" situation was on the right or the left side of the aquarium and whether female or male choice replicates were run. To reduce measurement errors, all measurements was done by one person, and the size matching was administered by a different person.
I sampled the focal fish's position (in front of a, b, c, or d) and all sexual behaviors of all fish every 30 min for 7.5 h. Sexual behaviors noted were ornament display and courtship dance (see Berglund et al., 1997, for description of behaviors). Nonparametric tests were used where data did not have (and could not be transformed to) a normal distribution. In the analyses of display, I used a generalized linear mixed model assuming a Poisson distribution of errors (SAS 6.12, GLIMMIX macro). All tests are two tailed.
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RESULTS |
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The copy and the noncopy object fish did not differ in size, neither in male choice nor in female choice replicates (Table 1). Also, model fish did not differ in size between the copy and noncopy side of the aquarium (Table 1). The display rate did not differ between copy and noncopy object fish (Wilcoxon matched-pairs tests, male choice replicates: N = 23, Z = 0.35, p = .73; female choice replicates: N = 22, Z = 1.52, p = .13), thus the experiment was balanced with respect to these factors. As intended, I found a higher frequency of sexual displays among the copy model fish compared to the noncopy model fish (Wilcoxon matched-pairs test, male choice replicates: N = 23, Z = 2.20, p = .028; female choice replicates: N = 22, Z = 2.20, p = .028).
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In male choice replicates, focal fish were not observed more often in the copy half of the aquarium (Wilcoxon matched-pairs test, N = 23, Z = 0.36, p = .72). The focal males were sampled on average 4.4 times in front of the copy object female and 3.1 times in front of the noncopy object female, but the difference was not significant (Wilcoxon matched-pairs test, N = 23, Z = 1.42, p = .16). Focal males did, however, display significantly more often in the copy half of the aquarium: these displays were exclusively directed to the object females and significantly more often to the copy object female than the noncopy object female (Wilcoxon matched-pairs test, N = 23, Z = 2.00, p = .045; Figure 2).
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Female focal fish were not observed more often in the copy half of the aquarium (Wilcoxon matched-pairs test, N = 22, Z = 0.76, p = .45) and showed no preference for the copy object male over the noncopy object male in terms of position (Table 2, Figure 2) or display in the copy versus noncopy side of the aquarium (Wilcoxon matched-pairs test, N = 22, Z = 0.49, p = .62) or in front of the copy versus noncopy object male (Table 2, Figure 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Male deep-snouted pipefish did copy the choice of other males. Males displayed more in the copy half of the aquarium, and the display was directed to the female. The experimental design excludes at least some alternative explanations for the observed male behavior. Due to the one-way mirrors, none of the object females could see their respective model males, and this prevented a difference in display rate beween object females. Furthermore, conspecific cueing or schooling behavior cannot explain the results, as there were equally many fish in each half of the aquarium, and these were matched for size and sex. The males did not display toward the model males but toward the female, so the focal male behavior cannot be explained by a preference for a site where sexual behavior took place (the copy model compartment)or as a male-male competition display. The only observed difference between the copy and the noncopy side was the increased display rate by the copy model fish, indicating a sexual interest in that object fish to which the focal males responded by displaying to that female.
Females did not appear to copy the choice of other females. There was no tendencies for females to spend more time or display more in the copy situation compared to the "noncopy" situation, despite the higher display rate in the copy model compartment. There was a significant interaction of sex and treatment (Table 2, Figure 3) meaning that males displayed significantly more toward the copy object compared to the noncopy object, whereas females did not. The sex difference in copying behavior makes sense as males are the more choosy sex and appears to have more scope for choice in the wild. Females of this species exhibit preferences too, both for male size and brood pouch thickness, but to what extent females have the opportunity for choice in the wild is less known. The operational sex ratio is usually (but not always) skewed toward males, leaving females with little choice (Vincent et al., 1995). The key to the sex difference in copying behavior may lie in the different potential reproductive rates of the two sexes. A female produces many more eggs than a male can receive, so to a male, the relatively low risk of egg depletion in an already mated female may be outweighed by the benefit of obtaining high-quality eggs. To a female, on the other hand, mating with an already mated male may be less beneficial, as she will not be able to deposit as many eggs in this male's pouch, compared to in an unmated male. Moreover, males may be more pressed for time than females. The male brood pouch, which is absent in winter, deteriotates rather quickly if not filled with eggs. Males must then rebuild the pouch before they can mate, which takes time, while females ripen eggs continuously during the whole summer. It is thus probable that there is a stronger selection pressure on males than on females to reduce the costs of choice in terms of this time constraint, and copying others may be one way of doing that.
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Previous mate choice experiments on this species have shown that position is a good indicator of preference, and it is highly correlated with sexual displays (Berglund, 1993). In the current experiment, males were not observed more often in front of the object when copying. This is probably an effect of the experimental design. The focal fish appeared to move around in the aquarium more than in other experiments (e.g., Sandvik et al., 2000
), where fewer (two) choice options and individuals were present. The increase in movements may simply be due to the increased amount of information to take in or may arise because the current design creates more complicated surroundings that take more time to explore. Also, there was no no-choice option, that is, nowhere the focal fish could stay without being close to some other fish, which means that in this study focal fish that were indifferent to mating were included. Another difference from previous designs is the lack of plastic zostera plants to rest in, which might have caused the focal fish to move more around. Taken together, these factors can explain that males did not spend more time in front of their preferred female, but it does not alter the interpretation of the results as a whole because an active display by males is a strong indicator of preference. Despite the interest in copying during the last decade, especially from theoreticians, the empirical evidence for copying is not very extensive. Perhaps the biggest problem is that there are so many alternative mechanisms that may explain copying-like mating patterns, so a very careful experimental design is required to conclude that copying occurs. This may unfortunately exclude some species as suitable for this type of studies and therefore limit our possibilities to reach an understanding of the generality and occurence of this phenomenon.
There have not, to my knowledge, been any attempts to employ a mutual mate choice scenario in models of mate choice copying. Should we expect copying to occur as often among males as among females in species with mutual choice? In the deep-snouted pipefish, sex roles are reversed and males are more choosy, but both sexes choose when they have the possibility to do so and both sexes have well-developed preferences accruing benefits to the chooser. Still, it is only males that copy the choice of other males. This indicates that although being a prerequisite for copying, a functional mate choice is not sufficient per se to explain the occurrence of copying. We need to invoke some additional explanation to why copying has or has not evolved. Furthermore, my results may indicate that in species with conventional sex roles and mutual choice, we should expect females to show copying behavior more often than males, but this remains to be tested.
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ACKNOWLEDGEMENTS |
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I would like to thank Anna Billing for excellent assistance both in the field and later, in the lab, for keeping a clear mind when helping to solve the difficult fish size–matching puzzle. I have also benefited from Anders Berglund and Gunilla Rosenqvist's experience and cooperation during field work. A. Berglund, Stein Are Sæther, Katja Räsanen, Innes Cuthill, and two anonymous referees gave comments and statistical advice. Funding was obtained from the Nansen Endowment, from the Royal Swedish Academy of Science, and from Uppsala University.
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