Behavioral Ecology Advance Access originally published online on June 6, 2008
Behavioral Ecology 2008 19(5):998-1005; doi:10.1093/beheco/arn059
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Context-dependent mate choice in relation to social composition in green swordtails Xiphophorus helleri
Division of Environmental and Evolutionary Biology, Institute of Biomedical and Life Sciences, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, UK
Address correspondence to N.J. Royle, who is now at Centre for Ecology and Conservation, School of Biosciences, University of Exeter, Cornwall Campus, Penryn, Cornwall TR10 9EZ, UK. E-mail: n.j.royle{at}exeter.ac.uk.
Received 4 December 2007; revised 24 April 2008; accepted 26 April 2008.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Comparative evaluation mechanisms of mate choice in relation to social composition of potential mates have not been considered in nonhuman animals. Models of rational decision making suggest that when choice is based on absolute values, the addition of a third option should take choices from the original 2 options in proportion to their original shares and not result in an increase in the absolute preference for any of the 3 options in the set. However, studies of foraging behavior have shown that choice alternatives are often not irrelevant, specifically when preference is based on 2 or more dimensions (multiple cues) and when the third option is an asymmetrically dominated "decoy" (i.e., it has a lower value than both original options on one dimension but is only lower than one of the 2 original options on the other dimension). Asymmetrically dominated decoys are predicted to increase preference for the option that dominates it on both dimensions if mate choice is context dependent. We tested whether mate choice is dependent on or independent of social context in green swordtails, a species where females commonly use multiple cues in mate choice decisions. Addition of a third, decoy, male to the set of options resulted in females shifting preference away from the phenotype of male that each preferred in binary comparisons. Consequently, although mate choice was context dependent, the asymmetrically dominated decoy effect was not observed. Instead, females showed negative frequency-dependent preference for the rare-male phenotype, which may act to maintain genetic variation under sexual selection.
Key words: maintenance of variation, phenotypic plasticity, rational choice, sexual selection, social environment.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Animals are commonly very choosy in their mate choice, which implies strong fitness consequences of this decision (Andersson 1994
; Jennions and Petrie 1997). Mate choice is a key decision making process in most animals' lives, having important potential genetic benefits for offspring via increased reproductive success (Fisher 1930) or viability (Zahavi 1975). In species where males do not provide parental care, in order for females to derive an indirect benefit from a mating bias, there needs to be detectable variation among males in signals that indicate fitness (Kokko et al. 2003). Females commonly choose mates based on the assessment of multiple male ornaments, which may function to improve the accuracy (or reduce the costs) of assessment of male quality (Møller and Pomiankowski 1993; Johnstone 1996; Candolin 2003).
However, the information contained in these multiple signals may not always covary positively (Roberts and Gosling 2003), and, more generally, signals from multiple traits may provide different information in different contexts (Houston 1997; Royle et al. 2002; Candolin 2003). Unless conditions are constantly static, mate choice preferences may not be adaptive in all environments (Welch 2003), and plasticity of preference becomes beneficial. Under such circumstances, in order to make effective decisions, animals may have to acquire information from environmental and social sources (Danchin et al. 2004). This may be either individually acquired personal information, gained through a process of trial and error, or social information, acquired vicariously through monitoring the behavior of others (Danchin et al. 2004). Such social information can be based on intentional communication, such as signals, or based on inadvertent social cues (public information), such as mate choice copying (Dugatkin and Godin 1992; Dugatkin 1996; Danchin et al. 2004).
Social and environmental effects on mate choice preferences have, until relatively recently, been largely ignored (Owens et al. 1999; Walling et al. 2008) with the bulk of interest focusing on the effects of prior exposure to males (e.g., Collins 1995; Gabor and Halliday 1997; Hebets 2003) and mate choice copying (see references in Danchin et al. 2004). Mate choice copying may make assessment of potential mates more efficient (Nordell and Valone 1998), especially when the available options are very similar in quality (Valone and Templeton 2002), and can be strong enough to reverse previous choices of individuals (Dugatkin and Godin 1992; Witte and Noltemeier 2002). Recent empirical work also suggests that mate choice rules can be plastic with respect to changes in operational sex ratio (Jirotkul 1999) and population density (Welch 2003), environmental factors such as predation risk (Reynolds et al. 1993; Godin and Briggs 1996; Gong and Gibson 1996; Johnson and Basolo 2003), and social information gathered through intentional communication, such as signalling prospective parental care (Warner et al. 1995). Such behavioral mechanisms in mate choice may play a role in maintaining genetic variation in traits important for reproductive success and consequently be an important source of variation in organismal fitness (Hughes et al. 1999). However, little is known about the effect of the social composition of potential mating partners on the plasticity of mate choice decisions (Alonzo and Sinervo 2001). Comparative evaluation mechanisms of mate choice in relation to social composition of potential mates have not been considered in nonhuman animals but are likely to offer new insights into many outstanding problems in mate choice and sexual selection (Bateson and Healy 2005).
Models of rational decision making suggest that when choice is based on absolute values, the addition of a third option should take choices from the original 2 options in proportion to their original shares (constant-ratio rule; Luce 1959). In addition, if choice is fixed, it should not be possible for the addition of a third option to increase the absolute preference for any of the 3 options in the set (principle of regularity; Tversky and Simonson 1993). However, studies of foraging choice in humans (e.g., Huber et al. 1982) and other animals (e.g., Shafir 2002; Bateson et al. 2002, 2003) show that choice alternatives are often not irrelevant, specifically when the options vary in 2 different dimensions (e.g., quality and quantity of food) and when the third option is an asymmetrically dominated decoy (i.e., option C has a lower value than both options A and B on dimension 1 but is only lower than option A, not B, on dimension 2). If choice is relative and depends on the quality of the alternatives, rather than being of absolute value, the addition of such a decoy should increase the preference for the dominant option (A in this example) (Bateson et al. 2003). If random dilution occurs, on the other hand, any preference exhibited during binary choice should increase with the addition of a third alternative, regardless of the nature of the decoy (Bateson et al. 2003). Although there are many parallels between choices made during foraging and those made during mate choice, the fundamental difference is that the fitness consequences of choice will be potentially much greater when choosing mates compared with choosing food items. Consequently, context-dependent effects may be different when choosing mates compared with choosing food.
Green swordtails Xiphophorus helleri provide a well-documented example of a species where there is evidence for female choice in the apparent absence of direct benefits, and females use more than one cue in mate choice. Males of these small, live-bearing, Central American fishes develop a long ornamental tail streamer at maturation, the "sword." Females generally prefer larger bodied males, but after controlling for body size, they have a strong preference for males with longer swords (Basolo 1990, 1998b), thus providing an excellent study system for choice along more than one signal dimension. Research using computer-altered video sequences of courting males has shown that the maintenance of this preference may reflect a bias for large apparent size: females prefer longer tailed males because they look larger (Rosenthal and Evans 1998). This suggests that males evolved a long sword as an inexpensive means of achieving a large apparent size (Rosenthal and Evans 1998) and that both body size and sword length may be sexually selected (Basolo and Wagner 2004). However, long sword length is costly in terms of swimming performance (Basolo and Alcaraz 2003) and is also attractive to predators (Rosenthal et al. 2001; Basolo and Wagner 2004). In addition, larger bodied males tend to have an advantage in male–male competition (Morris et al. 1992; Beaugrand and Cotnoir 1996; Beaugrand 1997), so maintenance of a long sword may only be affordable for high-quality males (Royle et al. 2006) and be favored when natural selection pressures acting against sword length are low.
If mate choice is based on absolute values (i.e., the preference is fixed across social environments), we would not expect females to change their preferred ranking of 2 males on the addition of a third male to the set of options. Here we tested whether mate choice is dependent on or independent of social context in relation to 2 different cues used by females in green swordtails (body size and sword length). The results show that females do change preference when a third, decoy, male is added; however, contrary to predictions from models of asymmetrically dominated decoys, females show negative frequency-dependent preference for the male phenotype that least resembles the male they preferred when only 2 males were available. This facultative shift in choice behavior and rare-male effect could provide a mechanism for the maintenance of genetic variation under selection (e.g., Kotiaho et al. 2008) and indicates that interpretation of apparent mating preferences may be misleading if based solely on binary choice comparisons.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Mate choice protocol
Our approach was to use 2 different asymmetrically dominated decoys (each of which acts as a decoy for one of the 2 binary choice options; Bateson et al. 2003
). This allowed a test of whether choices were context-dependent violations of regularity or random dilution effects (Bateson et al. 2003). Use of only a single asymmetrically dominated decoy does not allow differentiation between these alternatives (e.g., Bateson et al. 2002). We used first-generation wild green swordtails collected from Belize for all trials.
The experiment used 2 dimensions known to be of similar importance in mate choice in swordtails: body size and sword length (Rosenthal and Evans 1998). Unrelated males of the same total length, but differing body size (standard length, i.e., body length, measured along the midline, not including the caudal fin) and sword length (measured from the tip of the sword to the base of the caudal fin), were formed into pairs (N = 60 males, to form 30 pairs). Two other males from different families to the test males were assigned to each pair as either body decoys (Db) or sword decoys (Ds). Consequently, each group comprised 4 males. Within each quartet, the body decoy male had a larger body size than the S male (long-sworded male) but was smaller on both dimensions than the B male (large-bodied male). Conversely, the sword decoy male was smaller on both dimensions than the S male but had a longer sword than the B male (Figure 1). For logistic reasons, some decoy males were used in more than one quartet, so a total of 103 males were used in the experiment. However, each combination of males was unique, and each target male was used only once (see earlier). All males (and females) were reared individually in tanks that did not allow them prior experience of male–male competition. Consequently, males did not appear to have any conception of their relative quality, and there was no evidence of male–male competition via visual means alone.
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A single female, from a different family to any of the males used in the comparisons, was used to test preference in 3 treatments that utilized each group of 4 males (i.e., a total of 30 different females). As a result, the same female was made to choose, successively, between the same B and S males in 3 different contexts (with the order of presentation of contexts systematically controlled):
- binary: B versus S;
- trinary with body decoy: B versus S versus Db; and
- trinary with sword decoy: B versus S versus Ds.
These treatments allow investigation of the rules used by females to choose among males differing in appearance because the competing hypotheses yield a set of contrasting predictions:
- (a)If sword length acts to increase apparent size, then there should be no difference in preference (averaged across all females) between B and S in the binary treatment group (1).
- (b)If mate choice is consistent and based on absolute differences, then an individual female's ranking of the B and the S male that she sees should not change among binary and trinary treatment groups, regardless of the number of choices or the type of decoys available (constant-ratio rule; Luce 1959
).
- (c)If random dilution as a consequence of the increase in the number of choices occurs, any preference seen in the binary treatment should increase in both trinary treatments, regardless of the decoy.
- (d)If mate choice is context dependent and the asymmetrically dominated decoy effect operates (Tversky and Simonson 1993
), the presence of Db in treatment 2 should increase the relative preference for B males, whereas in treatment 3, Ds should increase the relative preference for S males.
- (e)If positive violations of regularity of preference are observed, absolute preference for B males in treatment 2 and S males in treatment 3 should be higher than in treatment 1 (binary).
- (f)However, if the addition of a decoy increases the relative preference for the competitor, then context-dependent mate choice is based on rarity or extremeness aversion (where addition of a third choice leads to consistent bias against only one of the 2 extremes; Tversky and Simonson 1993
).
- (b)If mate choice is consistent and based on absolute differences, then an individual female's ranking of the B and the S male that she sees should not change among binary and trinary treatment groups, regardless of the number of choices or the type of decoys available (constant-ratio rule; Luce 1959
Mate choice trials were based on methodology previously used successfully to investigate mate choice in swordtails (e.g., Basolo 1998a, 2002a; Morris et al. 2001; Aspbury and Basolo 2002) but conducted in a trichotomous, rather than a dichotomous, mate choice arena (Figure 2). At each treatment round the female was placed in the central compartment inside an inverted piece of opaque acrylic tubing to screen her from visual contact with males during the settling period (Morris et al. 2001). In binary comparisons, males occupied compartments 2 and 3 only, with compartment 1 being screened off with opaque acrylic (Figure 2). In trinary comparisons, all 3 compartments were occupied by males. The order of presentation of different treatments to females was varied systematically for successive groups of males to control for order effects (background context; Waite 2001). In addition, males were moved anticlockwise between compartments in successive treatments to control for compartmental side bias by females. Treatments lasted 9 min, with 9 min settling time between each successive treatment, based on previously published acclimation and trial times (Basolo 1998a, 2002a; Aspbury and Basolo 2002). Each treatment for each quartet of males was filmed from above using a digital video camera, mounted 90 cm directly above the tank. The time (seconds) spent by the female in each preference zone (Figure 2) was obtained by playback of the films and was used as a measure of preference for each male (e.g., Basolo 1998a; Morris et al. 2001). This has been found to correlate with mating success in the field in the closely related Xiphophorus nigrensis (Ryan et al. 1990). Females were defined as being in a preference zone if their whole head was in the compartment. Temperature was maintained at a constant 23 °C, with full spectrum (UV+) lighting and ultraviolet transmitting (UV+) acrylic partitions between compartments (Lucite International UK, Darwen, Lancashire, UK). The use of acrylic partitions between compartments ensured that there was no chemical communication between individuals, which may affect mate choice outcomes (e.g., Hankinson and Morris 2003).
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Data analysis and biometrics
Proportions were arcsine square-root transformed, where appropriate, following Kolmogorov–Smirnov tests for normality (Zar 1996
). For repeated measures analysis of variance (ANOVA), residuals from the model were also tested to ensure normality of distribution. All tests are 2 tailed. Absolute proportions of time spent with each kind of male were used to test for violations of regularity of preference and were calculated as the total amount of time a female spent in the preference zone of a given male, divided by the total amount of time spent in all preference zones (e.g., time with B/[time with B + time with S] for binary and B/[B + S + D] for trinary groups). Relative proportions were used to test for violations of the constant-ratio rule and were calculated as the total amount of time a female spent in the preference zone of B males, divided by the total amount of time spent in the preference zones of both B and S males (i.e., B/[B + S], regardless of whether a third male was present or not).
Even if the females do not have any kind of mating preference at all, by chance alone, we would sometimes observe association patterns deviating from 50:50. Consequently, we devised a probability test for how much the relative female preference must change from a binomial to a trinomial mate trial for this to be a significant change in preference at a 5% risk level, given that the null expectation is changing from 50:50 to 33:33:33. Our starting point is to look at the female preference for male type B (large-bodied males) in the binomial test, measured as the proportion of time (out of the total of 540 s) she spends associating with him. We call this observed preference p1. The deviation, d1, from the expected 0.5 preference is then d1 = p1 – 0.5, and the proportional deviation, D, from the expected preference of 0.5 is given by D = d1/0.5. If the individual is consistent in her preference between the binomial and trinomial test situations, her preference for male type B should not deviate from (1 + D) (1/3) in the trinomial test, which is therefore the expected preference, p2, in the trinomial test. However, this will also occur at times due to chance alone, so we need to know the expected frequency distribution of abs{[(1 + D) (1/3)] – p2}, which also gives our test statistic, Z.
The test statistic Z is derived as follows. We draw 540 numbers from a continuous uniform random distribution, 
U(0,1), corresponding to the number of seconds in the preference tests. Numbers <0.5 are deemed to indicate preference to male type B, and hence, their overall frequency gives us an estimate of p1, and we can calculate d1, D, and p2. We then draw another set of 540 numbers from a random distribution identical to the first one but independent from it. We can then calculate Z = abs{[(1 + D) (1/3)] – p2}. We ran this 100 000 times to obtain a probability distribution. The 95% percentile of this distribution gives the Z value at 
= 0.05. This is 0.0395. Consequently, a Z value equal to or >0.0395 indicates a significant change in a female's preference between the binomial and trinomial test situations.
Test males did not differ in total length (B males = 73.97 ± 1.72 mm, S males 74.02 ± 1.66 mm; paired t-test t29 = 0.21, P = 0.84) but differed in body length (B > S) and sword length (S > B; see Figure 1). Decoys were similar in total length to one another (Db males = 67.90 ± 1.83 mm, Ds males = 68.61 ± 1.69 mm; paired t-test t29 = 0.80, P = 0.43). Db males were midway between B and S males in body length (dimension 1) and smaller than both B and S males in sword length (dimension 2; Figure 1), whereas Ds males were midway between S and B males in sword length but smaller than both B and S males in body length (Figure 1).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The total time spent by females in the preference zones did not differ among the 3 treatments that they experienced (Friedman nonparametric repeated measures test;
2 = 4.47, 2 degrees of freedom, n = 30, P = 0.11). There was no overall bias in preference for either B or S males in the binary group (paired t-test of amount of time spent with B male vs. amount of time spent with S male, t29 = 1.50, P = 0.15). Only 3 out of 30 females preferred the same male in the binary as in the 2 trinary treatments. Consequently, mate choice was not consistent among treatments.
Regularity of female preference
The mean absolute proportion of time spent with B males was significantly reduced by the presence of a third male, by 49% in trinary Db (paired t-test, t29 = 3.94, P < 0.0005) and by 36% in trinary Ds treatments (t29 = 3.19, P = 0.003), compared with when there was only a binary choice. On the other hand, the mean absolute proportion of time spent with S males did not differ between the binary and trinary treatments, whether the latter involved the Ds (t29 = 1.57, P = 0.13) or Db decoy (t29 = 0.26, P = 0.80). Consequently, there were significant overall violations of regularity of preference, but this affected only B males (Figure 3a). The addition of a third, decoy, male of either sort therefore shifted attention away from large-bodied (B) males but had no effect on the absolute proportion of time females spent with long-sworded (S) males.
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Relative preference and the constant-ratio rule
Repeated measures ANOVA showed a significant effect of treatment on relative preference (F2,58 = 3.39, P = 0.04). The relative preference for B compared with S males did not differ between the binary and Ds trinary treatments (simple contrasts; F1,29 = 0.15, P = 0.70) but decreased by 31% between the binary and the Db trinary treatments (simple contrasts; F1,29 = 5.43, P = 0.027). This indicates violation of the constant-ratio rule, but in the opposite direction to that expected from models of choice with asymmetrically dominated decoys (Figure 4a).
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Probability test
If we compare the absolute preference for the large-bodied (B) male in the binomial comparison with the absolute preference for the same male in the trinomial treatment with the body decoy, only 3 out of 30 females had Z scores of <0.0395 (see Materials and Methods). In other words, the great majority of females had a greater change in mate preferences between the binomial and trinomial tests than would be expected by chance alone. If these 3 females are removed from the database and the data reanalyzed, the results are not affected (regularity of preference, P < 0.005; constant-ratio rule, P = 0.025). This is the same general result whichever specific binary–trinary comparison is made (binomial vs. trinomial body decoy or binomial vs. trinomial sword decoy).
Another way of looking at this is to conduct 1-sample t-tests of the Z values against the critical value of 0.0395. For all possible comparisons, the population Z scores are significantly higher than the critical value (all P < 0.0005). This means the differences between binomial and trinomial comparisons are not just due to random deviations from the underlying null distributions indicating no choice (i.e., 50:50 and 33:33:33).
Analysis of subgroups
These effects are stronger when splitting females into subgroups based on their choice of male in binary comparisons, where it becomes clear that the addition of a third male resulted in a shift in preference away from the preferred binary choice. For females that preferred B males when given a binary choice (i.e., over 50% of the time spent in preference zones was with B; N = 20), their absolute preference for B males dropped by approximately 60% in the trinary Db treatment (t19 = 7.34, P < 0.0005) and by almost 53% in the trinary Ds treatment (t19 = 5.60, P < 0.0005), compared with that in the binary comparison (violation of regularity of preference; Figure 3b). This resulted in a significant corresponding decrease in relative preference for B over S males (F2,38 = 10.18, P < 0.0005), in both Db (48%; simple contrasts; F1,19 = 26.96, P < 0.0005) and Ds treatments (29%; simple contrasts; F1,19 = 9.63, P = 0.006), indicating a violation of the constant-ratio rule (Figure 4b).
Similar effects occur for females that preferred S males in the binary comparison (N = 10), but in the opposite direction. Absolute preference dropped by 66% in the trinary Ds treatment (t9 = 5.24, P = 0.001) and by 57% in the trinary Db treatment (t9 = 3.50, P = 0.007) compared with their binary choice (violation of regularity of preference; Figure 3c). Their relative preference for S males also decreased (F2,18 = 5.18, P = 0.017), but only during the trinary Ds treatment (47%; simple contrasts; F1,9 = 26.41, P = 0.001) not the trinary Db treatment (simple contrasts; F1,9 = 1.85, P = 0.21; violation of the constant-ratio rule; Figure 4c). These effects are masked in the analysis of the whole data set because there was no overall preference for B or S males when females were given a binary choice (see earlier) and the shift in preferences were in opposite directions to each other so had a tendency to cancel each other out.
These results show that the addition of a third male, acting as an asymmetrically dominated decoy, leads to marked shifts in the type of male preferred by females. This occurred in conjunction with a nonrandom dilution effect. The basis of this change in preference (polarization), which was dependent on context, appeared to be a preference for relative rarity, rather than extremeness aversion.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The results demonstrate a novel, plastic female mate choice determined by social context independent of mate choice decisions made by other females (e.g., Dugatkin 1996
). Females showed no significant overall preference for either long-sworded or large-bodied males when given a binary choice between them, but addition of a third male (acting as an asymmetrical decoy) shifted the preference of individual females away from the phenotype of male that each preferred in the binary comparison. This shift in preference away from the target to the competitor is comparable to the result found by Bateson et al. (2002) in a study of foraging choice in hummingbirds and, because we controlled for random dilution effects through the use of 2 different decoys (Bateson et al. 2003), indicates that the female swordtails utilized a comparative evaluation mechanism in their mate choice. Moreover, our results cannot be explained by state-dependent valuation of choice (e.g., Pompilio et al. 2006), as no prior learning experience was involved, and females were presented with choices sequentially, controlling for order effects. Hence, swordtail mate choice is highly context dependent on social composition of available males, and sword length and body size appear to act as nonmutually exclusive components of a multicomponent signal. Because the overwhelming majority of experimental studies of mate choice in animals have involved females choosing between just 2 males, our results indicate that the preferences that they exhibit in such a protocol may not be representative of their choices in a more realistic setting where they may be exposed to several males.
There were significant overall violations of regularity of preference by females, but this mainly affected large-bodied (B) males. The direction of these effects was unexpected in that the addition of a decoy did not increase the preference for the "dominant" male (i.e., S in the Ds treatment and B in the Db treatment), as predicted from models of asymmetric decoys (e.g., Luce 1959; Tversky and Simonson 1993), but instead reduced the preference for B males (i.e., a dilution effect). In addition, the relative preference for B males compared with S males decreased in the Db treatment and remained unchanged in the Ds treatment, which violated the constant-ratio rule, but not as predicted from the asymmetric decoy models (where preference for B males would be expected to increase in the Db and decrease in the Ds treatments, respectively). Consequently, addition of a decoy does neither increase the preference for the dominant male alternative nor result in random dilution but acts to polarize preference (Tversky and Simonson 1993). The results of the analysis of subgroups relating to initial preference in the binary treatment suggest that this pattern is mainly due to preference for relatively novel phenotypes, rather than an aversion against large-bodied males per se; thus, females that preferred the larger sworded male in the binary trials reduced their preference for that trait when a third male, also with a larger sword, was present (and equivalent changes in preference were seen for females that preferred the larger bodied male in binary choice). So the addition of a third male to the set of mate choice options results in nonrandom dilution of absolute preferences and a shift in preference away from the type of male preferred in a binary choice.
Green swordtail females apparently use a form of negative frequency-dependent mate choice, basing their decisions on the composition of the set of males from which they are choosing. It is generally considered that a preexisting receiver bias favoring swords has contributed to the evolution and exaggeration of swords, based on evidence that females of closely related swordless species in the Priapella/Xiphophorus complex generally share the preference for swords shown by sworded species (Basolo 2002b, and references therein; but for an alternative view, see Meyer 1997). However, there is evidence for evolutionary lability in preference for this trait. An unsworded species of platy Heterandria bimaculata shows active discrimination against sworded males (probably as a means of avoiding costs of heterospecific matings with X. helleri; Basolo 2002b), and there is no congruence between the sexes in terms of a bias in favor of swords in X. helleri (females show positive preference, whereas males show negative preference with respect to swords), indicating that the preference is labile and that swords may have different signalling functions in different social contexts (Basolo 2002a). In addition, female preference for long-sworded males decreases under increased predation risk for sworded males, showing that recent memory can override the preexisting bias (Johnson and Basolo 2003), and, in Xiphophorus birchmanni, female preference for elaboration of male traits has apparently been reversed (Wong and Rosenthal 2006). The present study suggests that a preference for rarity or novelty (e.g., Burley 1986; Lyon et al. 1994) in the context of the social composition of potential mates may help explain the evolution and maintenance of swords. The reasons for the expression of such rare-male effects are not clear but may be related to inbreeding avoidance or by-products of selection for novel visual cues in a different context, such as foraging (Hughes et al. 1999).
Previous work on color patterns in guppies Poecilia reticulata has provided evidence for rare or "redundant" male advantage in mate choice (Farr 1977, 1980; Hughes et al. 1999; Eakley and Houde 2004), but facultative, negative frequency-dependent shifts in mate choice, as shown in the current study, have not previously been demonstrated. Such behavior indicates that mate choice in swordtails may be highly plastic. If the adaptive value of traits varies among environments (Hunt et al. 2004), then it would pay to be plastic in mate choice preference. The success of this strategy depends on the reliability of cues to predict the environment that offspring will experience (Qvarnström 2001). If male success depends on the frequency of different phenotypes in the population, then mate choice preference based on social composition may be adaptive. The current experiment indicates that the sword is part of a multicomponent signal, each component of which has equivalent effects (Rosenthal and Evans 1998), depending on the context. In this respect, the sword could be viewed as a context-dependent "backup signal" (Johnstone 1996), where it gives partial information on a single male currency (quality in a particular social environment).
Very little is known about the degree of plasticity of indirect benefits across environments (Welch 2003), but previous theoretical work suggests that context-dependent female choice can be adaptive and act to maintain genetic variation (Alonzo and Sinervo 2001). In side-blotched lizards Uta stansburiana, there are several genetically based color morphs, which each have a different behavioral strategy and which cycle between years, as their relative genetic quality depends on morph frequency (Alonzo and Sinervo 2001). A robust prediction from a game theoretical model of context-dependent mate choice in this system is that females should always prefer the rare morph when populations are in the boom phase of the cycle, as rare morphs have a genetic advantage. Hence, female choice for good genes can maintain genetic alternatives when such games are cyclical (Alonzo and Sinervo 2001).
Very little is known about the population fluctuations of green swordtails in nature, but in principle, a similar effect may operate to maintain swords in swordtail fishes if female choice is based on rarity or novelty, with rare phenotypes preferred when populations increase. Any population bias in preference when males of different phenotypes are present in similar frequencies (i.e., binary) will be countered by the polar opposite effect when males of different phenotypes are present in different frequencies to one another (i.e., trinary). So, although sword length is ultimately constrained by natural selection, the benefits of having a smaller body size but a long sword compared with having a large body and a short sword are likely to depend strongly on the composition of the competing males in the population. A broad parallel may be drawn here with changes in the consequences of dominance relations from dyadic encounters to mixed assemblages in 2 species of sympatric, incipient cichlid fishes. Red males of the species Pundamilia nyorerei were found to be more aggressive than, and dominant over, (blue) males of the species Pundamilia pundamilia in dyadic encounters. However, in mixed groups, this effect disappeared as red males are more aggressive to other red males, so the costs and benefits of being red were dependent on social context (Dijkstra et al. 2005).
Context-dependent mate choice and the use of such multiple cues may help to explain the paradox of the lek (Tomkins et al. 2004), as the attractiveness of a male may vary according to the background social composition against which females are making their choice; this would maintain genetic variation under selection for male quality.
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FUNDING |
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Biotechnology and Biological Sciences Research Council to J.L. and N.B.M (17/S15807).
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ACKNOWLEDGEMENTS |
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Thanks to John Laurie, Helcia Lepatik, June Freel, Craig Walling, and Graham Adam for help with fish husbandry. Four anonymous referees provided valuable comments on previous versions of the manuscript.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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