Behavioral Ecology Advance Access originally published online on June 22, 2006
Behavioral Ecology 2006 17(5):779-783; doi:10.1093/beheco/arl016
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Mating preference of female zebrafish, Danio rerio, in relation to male dominance
Department of Biology, University of Leicester, University Road, Leicester LE1 7RH, UK
Address correspondence to R. Spence. E-mail: rs153{at}le.ac.uk.
Received 25 November 2005; revised 29 March 2006; accepted 8 May 2006.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Mating success tends to be skewed toward dominant males, though female mate preferences may not always correlate with male dominance. In this study, we investigated the mating preferences of female zebrafish, Danio rerio, in the absence of male–male competition. We paired females sequentially with males of known dominance rank, using a nested, repeated measures design, with egg production as a measure of female mate preference. We predicted that females would spawn more frequently and produce larger clutches when paired with males of higher dominance rank. We found significant differences among females in the size of clutches produced and among males in the size of clutches received, but these differences were independent of male dominance rank. Male body size was not related to either dominance rank or clutch size received. These results indicate that females vary clutch size in relation to the males with which they are paired but that they do not favor dominant males. Thus, male competition may normally override female mate preference in zebrafish.
Key words: assortative mating, mate choice, oviposition, pheromone, territoriality.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Sexual selection, that is, selection arising through competition over mates and matings, results from differential mating success among males (Darwin 1871
). The strength of sexual selection depends on the sex difference in the variance in mating success for each sex; the greater the difference, the more opportunity there is for selection to operate (Shuster and Wade 2003). Variance in male reproductive success arises through competition among males for mates and through female mating preferences (Andersson 1994).
Despite the considerable research effort directed toward both of these mechanisms, their relative contribution to sexual selection is poorly understood (Qvarnström and Forsgren 1998; Wong and Candolin 2005). Traditionally, the 2 processes were viewed as complementary, females preferring male traits that are correlated with dominance, such as red coloration in 3-spined sticklebacks Gasterosteus aculeatus or body size in Japanese medaka Oryzias latipes (Howard et al. 1998; Candolin 1999). However, in other cases, male competition may reduce opportunities for female choice. In the cockroach Nauphoeta cinerea, the composition of social pheromones preferred by females differs from that which signals male dominance (Moore A and Moore P 1999), whereas in European bitterling, Rhodeus sericeus, male courtship vigor is a better predictor of female preference than dominance (Reichard et al. 2005). Thus, although mating success tends to be skewed in favor of dominant males, the fitness outcomes to females can vary across taxa (Qvarnström and Forsgren 1998; Moore et al. 2001; Wong and Candolin 2005).
Female preference can be difficult to demonstrate experimentally in species in which male competition plays a significant role in the mating system; where animals are allowed to interact freely, females may mate with the dominant male by default. To control for the effects of male competition, dichotomous choice designs are often employed, with preferences inferred from the amount of time a female spends in association with males differing in a particular trait. There are a number of problems with such designs. First, presenting females simultaneously with 2 extremes of the trait in question can result in amplification of a preference effect (Wagner 1998). Under natural conditions, variation in a trait is more likely to be normally distributed. Further, female preference is multifactorial, and any trait selected a priori may be correlated with other, uncontrolled traits. Second, many studies do not take account of within- and between-female variations in preferences. Third, preference is inferred rather than demonstrated empirically. Although association time has been shown to correlate with mating preference in some species, in others it does not (Fuller 2003). Finally, females may employ cryptic forms of choice, such as variation in the rate of oviposition, differential allocation to eggs, and postcopulatory sperm selection (Burley 1986; Lifjeld et al. 1994; Eberhard 1996).
Here we use egg production to evaluate female mate preference in the zebrafish, Danio rerio. The zebrafish is a small (30- to 40-mm body length) tropical cyprinid fish, native to the floodplains of North Eastern India and Bangladesh (Barman 1991). It is easily maintained in the laboratory and is an important model organism in developmental biology and genetics (Granato and Nüsslein-Volhard 1996). Under benign laboratory conditions, zebrafish breed all year; spawning is influenced by photoperiod and takes place within approximately an hour of exposure to light after darkness (Hisaoka and Firlit 1962). Females spawn at frequent but irregular intervals, approximately every 1–2 days, all mature ova being released during a single spawning session (Eaton and Farley 1974). Ovulation is induced via male gonadal pheromones (van den Hurk and Resink 1992), whereas analogous pheromones released by females after ovulation induce courtship behavior in males (van den Hurk and Lambert 1983).
Zebrafish typify a basic mating pattern common to many cyprinid fishes; they are group spawners and eggs scatterers (Breder and Rosen 1966). However, females appear to be choosy with respect to sites for oviposition. Moreover, some males are territorial during the daily spawning period and attempt to monopolize access to oviposition sites, which may affect female reproductive success (Spence and Smith 2005). The aim of the present study was to establish whether female zebrafish exhibit mating preferences independently of male–male interactions and whether these correlate with male dominance. We also aimed to address the problems associated with dichotomous choice designs outlined above. First, we ranked males according to dominance, using 4 ranks rather than just 2. Then females were paired sequentially with males of different dominance ranks, allowing them the opportunity to spawn in the absence of competition. We repeated each pairing 3 times and used clutch size as a measure of female mating preference. Our preliminary observations showed that there is wide variation in clutch size both within and among female zebrafish, suggesting that females might modulate oviposition rate in relation to their spawning partners. Clutch size adjustment is one of the few modes of cryptic choice available to species with external fertilization (Eberhard 1996) and has been demonstrated across a range of taxa (Côte and Hunt 1989; Rintamaeki et al. 1998; Arnqvist and Danielsson 1999; Reyer et al. 1999; Parker 2003).
We tested the prediction that females spawn more frequently and produce larger clutches when paired with males of higher dominance rank. Because females were paired with different males, clutch size could vary independently between males and females. As female preference may be independent of male dominance, rejection of the null hypotheses would be dependent on demonstrating firstly a significant difference among males in clutch size received and secondly that such a difference was related to male dominance rank. The repeated measures design increased the chances of any such effect being detected.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The experiment was carried out between 20 August and 1 September 2004, using 30 male and 30 female zebrafish obtained from commercial suppliers. Fish were housed in an environmentally controlled room with a 14:10 h light:dark cycle (08:00 AM to 10:00 PM) with water on a recirculating system at 27 °C. Throughout the experiment, fish were fed 3 times each day with a mixture of frozen bloodworm, brine shrimp, and high protein commercial fish pellets (Cyprico Crumble Excellent). The mean ± SD standard length (from the tip of the snout to the origin of the caudal fin) of males was 35.6 ± 1.8 mm and females 36.7 ± 2.3 mm. Prior to the start of the experiment, males and females were kept separately in 60-l aquaria measuring 60 (length) x 40 (height) x 40 (width) cm. Males and females were randomly assigned to treatment or control groups, females being distinguished by the presence of genital papilla.
The experimental design consisted of pairing females with males of different dominance ranks and counting the number of eggs they produced. We determined male dominance rank as follows: each group of 4 males was placed in a 60-l glass aquarium together with 4 haphazardly selected females. A single plastic box measuring 150 (length) x 100 (width) x 40 (depth) mm, covered with 2-mm nylon mesh and 4 plastic plants, was placed in the back left-hand corner of each aquarium as a spawning site. Male zebrafish readily establish and defend territories around such artificial spawning sites; a territorial male typically emerges at the start of the first spawning period and remains in possession of the territory over successive days (Spence and Smith 2005). On the morning of the following day, we observed the fish during the first hour after the lights came on and identified and removed the territorial male in each group. We repeated this procedure on subsequent days to identify the second-, third-, and fourth-ranked males. None of the females were reused in the next stage of the experiment.
After ranking, males were randomly assigned to adjacent 20-l glass aquaria measuring 40 (length) x 30 (height) x 25 (width) cm, where they remained throughout the experiment. Opaque barriers were placed between aquaria to prevent visual interactions between neighboring fish. We lined each aquarium with aluminum mesh (mesh size 6 x 3 mm) to protect the eggs from cannibalism. Four plastic plants were placed on top of the mesh. On the day after completion of the dominance ranking exercise, females were randomly assigned to males. We used a nested, repeated measures design with 6 replicates, each comprising 4 females and 4 ranked males; each female was paired with each of the 4 males on 3 separate occasions (Figure 1). Each female was placed with one male for 24 h and then assigned to the next male. We repeated this process for 12 days. A Latin square design was used to randomize the order in which the females were paired with males while ensuring that each female was placed with a different male each day for 4 days. In addition, a fifth pair of fish was included in each replicate and left together for the entire duration of the experiment in order to partially control for any effects on the spawning cycle due to daily reassignment of treatment females.
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Each morning we removed the fish, mesh, and plants from each aquarium and swept it with a fine mesh hand net to collect all the eggs that had been spawned during the past 24 h. Males were then returned to the same aquarium and females assigned to the next male. This procedure was carried out between 09:15 AM and 12:00 PM each day. We counted the eggs and fixed them in 4% formalin. The same protocol was followed for control pairs, though in their case the same fish were always replaced together.
At the end of the experiment, the standard lengths of all fish were measured to the nearest 0.1 mm. One of the males died on the second day of the experiment, so this replicate was restarted with a replacement male and a further dominance ranking exercise that included the replacement male.
Data analysis
We tested all data for normality using a Kolmogorov–Smirnov test and for equality of variance using Bartlett's test. To test for male and female influence on variance in clutch size, we used the Scheirer–Ray–Hare extension of the Kruskal–Wallis test, as a nonparametric equivalent of the two-way analysis of variance (ANOVA) (Sokal and Rohlf 1995). This procedure involves ranking the data, performing a two-way ANOVA, and testing the ratio H (computed as SS/MStotal) as a 
2 variable. We used a nested, repeated measures design, with experimental fish nested within replicates and trial as a repeated measure. Female interspawning interval and body size correlated significantly with clutch size (P < 0.05) and were used as covariates in the analysis. A Mann–Whitney U-test was used to compare egg production between treatment and control females and an unpaired t-test to compare body size. A chi-squared test was used to test whether the number of clutches obtained by males differed in relation to male dominance rank, with the null expectation that the number of clutches did not differ among dominance ranks. A correlation was used to test for a relationship between male dominance rank and clutch size. We used a nested one-way ANOVA to test for a difference in male body size among dominance ranks, together with a correlation between dominance rank and ranked body size within replicate.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean ± SD clutch size (i.e., eggs spawned in each 24-h period) was 185 ± 149.5, N = 180, for treatment females and 169 ± 146.0, N = 42, for controls. The mean ± SD daily number of eggs spawned over the entire 12 days (i.e., including days without spawning) was 116 ± 148.4, N = 288, for treatment females and 103 ± 140.4, N = 72, for controls. The maximum clutch size observed was 765. There was no significant difference between treatment and control females in either clutch size (Mann–Whitney U-test: U = 3408, N1 = 42, N2 = 180, P = 0.322), mean daily number of eggs (Mann–Whitney U-test: U = 9402, N1 = 69, N2 = 288, P = 0.476), or female body size (unpaired t-test: t9 = 1.77, P = 0.110).
All experimental females spawned, though some failed to spawn with some males. On average, treatment females spawned at least once with 3 out of their 4 mates, whereas none of the controls failed to spawn. The mean ± SD interspawning interval of treatment females was 1.6 ± 0.85 days, N = 180 (range 1–6), and control females 1.5 ± 0.60 days, N = 42 (range 1–3). One of the treatment females spawned on each of the 12 days, whereas the maximum number of spawnings among control females was 8. Clutch size did not decrease during the course of the experiment (Pearson correlation rp = –0.50, N = 12, P = 0.101). Clutch size was correlated with interspawning interval for both treatment (Spearman's rank correlation: rs = 0.29, N = 180, P <0.001) and control females (Pearson's correlation: rp = 0.39, N = 42, P = 0.011).
The number of spawnings obtained by treatment males ranged from 3 to 10, compared with a range of 5–8 spawnings for control males. There was no significant difference in body size among male dominance ranks (F3,20 = 0.44, P = 0.730) and neither was there a correlation between dominance rank and ranked body size within replicate (Spearman's rank correlation: rs = 0.00, N = 24, P = 1.00). There was no correlation between male body size and mean clutch size received (Pearson's correlation: rp = –0.28, N = 24, P = 0.183).
After controlling for interspawning interval and female body size as covariates, we found a significant difference among treatment females in the size of clutches produced (Scheirer–Ray–Hare test: 
= 1158, P <0.001). There was also a significant difference among treatment males in clutch size received (Scheirer–Ray–Hare test: = 1194, P <0.001). In light of the reservations of Toothaker and Chang (1980) concerning the Scheirer–Ray–Hare test, we followed their recommendation and also conducted a parametric analysis on untransformed data, testing male and female factors separately and using the covariates only when testing for a female effect on clutch size. In this case, we detected no significant female effect (analysis of covariance: F54,214 = 1.07, P = 0.356) on clutch size, though there was a significant male effect (ANOVA: F54,216 = 1.41, P = 0.045). The distribution of clutches did not differ significantly among dominance ranks (
= 0.58, P = 0.900), and there was no correlation between ranked clutch size and dominance rank within replicate (Spearman's rank correlation: rs = –0.27, N = 24, P = 0.208). Thus, although females did spawn more frequently and produce more eggs with some males than others, this effect was not related to male dominance rank.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The aim of this study was to investigate female mating preferences in the absence of male–male competition in zebrafish, with a prediction that females would prefer dominant males. After controlling for the effects of interspawning interval and female body size, we found a significant difference in the size of clutches produced among treatment females. There was also a significant difference among treatment males in clutch size received. These results suggest that females consistently spawn more frequently and produce larger clutches with some males than others. However, this effect was not related to male dominance rank. The design employed in this study allowed us to separate male and female contributions to variance in clutch size; females were paired with each male within a replicate on 3 separate occasions. It should be noted that the significant male effect appeared to be stronger than the female effect because the female effect was not detected in a parametric analysis of untransformed (but nonnormal) data. As noted above, it is the male effect that is of interest in this study because clutch size might differ among females for reasons other than the male they are paired with, in addition to differing as a function of the variables we identified and controlled for as covariates.
The ability of females to vary egg production in response to different mating opportunities has been demonstrated in a number of fish species. In the redlip blenny, Ophioblennius atlanticus, both the probability of spawning and the number of eggs released was greater with larger than smaller males (Côte and Hunt 1989). In Chinook salmon, Oncorhynchus tshawytscha, where males provide no parental care, females were observed to delay spawning successive clutches when paired with smaller males (Berejikian et al. 2000). Also, Fu et al. (2001) found that female bluegill sunfish, Lepomis macrochirus, attempt to increase fertilization success by producing more eggs in the presence of sneaker males, as do female European bitterling, Rhodeus sericeus (Smith and Reichard 2005). Variation in egg volume has also been proposed as a form of female mate preference in fishes (Kolm 2001).
Our experimental design employed 3 trials in order to control for the natural spawning cycle of females, although our results show that females are capable of spawning every day for at least 12 days. Females sustain comparable spawning rates in nature, although spawning is more seasonal (R Spence and C Smith, unpublished data). Twenty-four hours was sufficient duration for each trial; Eaton and Farley (1974) showed that exposure of female zebrafish to a male, even for a few hours, was sufficient to induce ovulation. Moreover, ovulation only takes place during mating (Laale 1977), so there was little risk of preferences being affected by previous suitors (Bakker and Milinski 1991). The repeated measures design of the experiment, with randomization of the order of pairing, also controlled for any such effects.
We controlled for the effects of disturbance due to the daily changes of mate by using a control group of fish that were paired for the duration of the experiment, but which experienced daily capture and egg removal. Although there was no difference in mean egg production between treatment and control fish, the treatment fish showed a greater range in the number of times they spawned. This variation may indicate increased variance in egg production in the treatment group in response to changes in mates, though it could also be a function of a larger sample size of the treatment group.
The failure to detect a correlation between male rank and number and size of clutches received indicates that male competition may normally override female mate preference in zebrafish. If dominance does play a role in determining mating preferences among female zebrafish, this does not appear to relate to cues which females can detect in isolated males. Studies with both 3-spined sticklebacks, Gasterosteus aculeatus, (Candolin 1999) and sex role–reversed pipefish, Sygnathus typhle (Berglund and Rosenqvist 2001), have shown that signal expression can change during competition and thus affect choice. However, in both these species, female preference correlates with male dominance. A number of studies in other species have shown that females do not necessarily prefer dominant males; male dominance does not always predict mate quality, and there may be fitness costs associated with choosing a dominant male (Qvarnström and Forsgren 1998, Holland and Rice 1999; Byrne and Roberts 2004).
We did not find a relationship between male body size and either clutch size received or male dominance rank, although in a previous study, territorial male zebrafish were found to be larger than nonterritorials (Spence and Smith 2005). Our failure to detect a relationship between male size and dominance rank may be because with our design it was only possible to test for an effect within replicates, effectively reducing our sample size to 6. However, the lack of a relationship between male body size and clutch size received is a robust result, supported by a large sample size and repeated measures design. This finding appears to contradict that of Pyron (2003), who showed that females prefer to associate with larger males. The discrepancy between studies probably reflects differences in experimental design; Pyron (2003) used a dichotomous choice test with 2 groups of males selected on the basis of size differences, whereas we selected males at random from an experimental population without large size variation and focused on differences in dominance. We do not exclude the possibility that females might show a preference for larger males when compared simultaneously with smaller males or that dominance and size correlate in males.
Although the present study suggests that female zebrafish exhibit mating preferences that are independent of male dominance, it is unclear how these preferences can be maintained. One possibility is that under natural conditions not all matings involve male competition. Another is that dominant males may not, in fact, gain significantly superior reproductive fitness (Spence et al. 2006). The fact that spawning is confined to a brief period at dawn, results in high temporal clustering of receptive females, allowing little opportunity for males to monopolize females (Emlen and Oring 1977). Although alternative mating tactics have traditionally been viewed as undermining female choice (Taborsky 1998; Jones et al. 2001), this will not be the case if sneaker males are those preferred by females, as has been shown in European bitterling (Smith and Reichard 2005).
Further research is necessary to determine the mechanism underlying the female preferences observed in this study. Assortative mating may relate to genetic compatibility. Incompatibility avoidance has been proposed as influencing female mating preferences and may promote polyandry as an adaptive mating strategy (Zeh JA and Zeh DW 2003). Assortative mating based on genetic compatibility can reduce the intensity of sexual selection on males. Investigating interactions between maternal and paternal genomes in the zebrafish may be a fruitful avenue for further research as it is a tractable laboratory species, and its genetics are well understood (Grunwald and Eisen 2002). In view of the role played by pheromones in the reproductive behavior of both sexes, it is possible that mating preferences may be based on olfactory cues.
In conclusion, both male–male competition and female preference may operate in the zebrafish mating system, although female preference was not correlated with male dominance in the present study. Instead, the 2 mechanisms may operate in opposition, resulting in a low overall opportunity for sexual selection. Further research is needed to examine the significance of female oviposition decisions in the zebrafish mating system and the role of olfactory cues in determining the basis of mate preference.
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ACKNOWLEDGEMENTS |
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We are grateful to Martin Reichard for his suggestions regarding experimental design and to Coppens International for providing their high protein fish feed pellets. We thank Steve Le Comber, Eamonn Mallon, Mark Pyron, Martin Reichard, Penny Watt, and an anonymous referee for their insightful comments on the manuscript. R.S. and C.S. designed the study; R.S. conducted the experiment, analyzed the data, and wrote the paper.
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