Behavioral Ecology Advance Access originally published online on July 9, 2007
Behavioral Ecology 2007 18(5):905-909; doi:10.1093/beheco/arm059
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Strategic egg allocation in the zebra fish, Danio rerio
Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK
Address correspondence to A.M.J. Skinner. E-mail: amjskinner{at}fsmail.net.
Received 6 December 2006; revised 15 May 2007; accepted 24 May 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Females across a range of taxa have been shown to differentially allocate their reproductive resources according to the attractiveness of their mate. Previous studies demonstrated a female preference for larger males in the zebra fish but have so far failed to uncover a size-mediated difference in male mating success, possibly due to the effects of male–male competition. By controlling for male–male competition in the present study, we show that females strategically allocate their reproductive resources (i.e., eggs) toward larger males. When females were mated sequentially with a large and small male, they released a greater number of eggs to the second male when he was large than when he was small. Furthermore, there was also a trend for females to release a greater proportion of their eggs to the first male when he was large. Across females, the total number of eggs laid by each female increased with the average standard length of the male pair, whereas the number of eggs laid to the second male also increased with his standard length. This study represents one of the first attempts at identifying differential allocation in a resource-free egg scatterer and suggests that female preferences may play a greater role in the reproductive success of males in this species than previously envisaged.
Key words: differential allocation, egg number, zebra fish.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sexual selection represents the selection for behavioral, morphological, or physiological traits that increase an individual's chance of reproductive success (Andersson 1994
). Darwin (1871) recognized 2 processes of sexual selection, notably intrasexual selection (usually male–male competition), whereby males competed for mating access to females, and intersexual selection (usually female choice), whereby females showed preferences in their selection of mates. Female (and male) mate choice is now known to be an important and often ubiquitous part of the reproductive behaviors of many taxa, operating as it does on a range of physical and behavioral traits and leading to considerable variation in the relative reproductive success of the chosen sex (Bateson 1983).
Differential allocation (DA) refers to the case where females vary their investment of reproductive resources (e.g., clutch size, parental effort, egg quality) according to the attractiveness of their mate (Burley 1986) and has been demonstrated across a range of taxa from insects to birds (Sheldon 2000). Among fish species, little evidence is reported for DA except among gobioid and blennioid species in which males hold and defend nesting sites (Hastings 1988a, 1988b; Cote and Hunte 1989) and in the obligate male mouth-brooding Banggai cardinalfish Pterapogon kauderni (Kolm 2002). In all these cases, female preferences for larger males are presumed to bring about the greater clutch sizes or mass observed for the larger males of each species. Where males appear to provide no resources other than sperm, such as in resource-free egg-scattering species, there appears to be little or no evidence for DA (but see Katano and Maekawa 1997).
The zebra fish, Danio rerio, is a group-spawning, egg-scattering member of the Cyprinid family found throughout southern Asia (Laale 1977). Its ease of maintenance and ability to produce large numbers of transparent eggs has made it an ideal species for studies ranging from developmental genetics to ecotoxicology (Grunwald and Eisen 2002), yet little is known about the species' natural history and in particular its mating system (Laale 1977). Pyron (2003) showed that both female mate choice and male–male competition occur in this species and, more specifically, that females prefer to associate with larger males. However, Pyron (2003) did not test whether this female preference resulted in any variation in male reproductive success and so it is unclear whether an association preference equates to a mating and reproductive preference in this species.
Spence and Smith (2006) investigated the variation in male reproductive success in zebra fish in relation to male dominance, and although they found significant differences in the reproductive success of individual males, this was not related to either dominance or body size. They suggested that female preferences might operate on factors other than male dominance or body size or else that male–male competition may override such preferences. Nevertheless, there is some indication that female zebra fish tend to release more eggs per oviposition event to large versus small males during single-pair encounters, which suggests that females may be able to control how they allocate their clutch to potential mates (Skinner 2004). In both the above-described studies (Skinner 2004; Spence and Smith 2006), females were only allowed access to one male during each daily mating period, and so females could not directly assess 2 males during the period of oviposition.
Here we investigated in more detail whether females allocated eggs differently to 2 males of different size (large and small) during a single mating period using a paired crossover design. By using the crossover design, we are able to build on previous studies by investigating female mating preferences in the absence of direct male–male competition. More specifically, we allowed females sequential mating access to a male while maintaining visual and olfactorial contact with a second male, so allowing females to assess both partners during the release of their eggs (Wagner 1998). Given the visual association preference shown by females for larger males (Pyron 2003), we predicted that females would allocate more eggs to the larger male of each pair.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Experimental subjects
The experiment was carried out using zebra fish obtained as adults in a single batch from a commercial aquarium supplier, and it is assumed that all fish were the same age. All fish were housed in groups of 10–15 in single sex aquaria in a temperature-controlled (27 ± 1 °C) recirculating aquarium facility with a 12:12 h light:dark cycle and fed ad libitum twice a day with freshly hatched brine shrimp and commercial flake food. Hisaoka and Firlit (1962)
previously demonstrated that an interspawn period of 5–10 days is optimal for obtaining viable eggs; therefore, all individuals used in the experiment were mated 5–8 days prior to them being used in the experimental procedure, using nonexperimental subjects, in order to control for any effects that previous mating experience may have on the propensity to mate again. Furthermore, to control for any effects of familiarization, experimental groups were formed from individuals in nonadjacent tanks. Standard length, defined as the distance from the tip of the snout to the tip of the caudal peduncle, was recorded to the nearest millimeter for all individual subjects using a metal rule.
Experimental design
Matings took place in isolated plastic tanks (22 x 35.5 x 21 cm) that had plastic net partitions across their middle. The mesh size of the netting was around 1 mm to allow the passage of visual and olfactorial cues while reducing the chances of eggs moving between compartments. The sides and backs of the tanks were covered in black plastic to prevent visual disturbance from adjacent tanks, and the bottom of each tank lined with marbles to prevent egg cannibalism (Westerfield 1995). Each tank contained approximately 7 l of fresh aquarium water.
Pairs of males (n = 48) were randomly selected from the total population on the proviso that within each pair males differed by at least 2 mm in their standard length (mean difference 3.8 ± 1.7 mm; range 2–8 mm). The standard length of males classed as large (30.6 ± 1.1 mm) was significantly greater than that of males classed as small (26.8 ± 1.6 mm) across the 48 pairs used (t-test: t = 13.67; degrees of freedom [df] = 85; P < 0.001). At 4:00 PM on the day before mating took place, a male pair was added to one side of each mating tank and a female was added to the other side. Female zebra fish ovulate and oviposit simultaneously in the morning (Lee et al. 1999), but they require pheromonal stimulation prior to this period in order to do so (Chen and Martinich 1975). Furthermore, recent work by Gerlach (2006) showed that the presence of male pheromones can enhance both the number and viability of eggs laid by a female. By setting up tanks the evening before, we, therefore, allowed not only the necessary pheromonal stimulation but also the females to assess both males simultaneously.
Immediately after lights up the following morning (09:00 AM), one male (large, L, or small, S) was carefully netted from the male holding compartment and added to the female holding compartment and left to mate for 10 min. To ensure balance in the design, half of the females received the small male first (mating sequence S1L2) and the other half received the large male first (mating sequence L1S2). After 10 min, the female was then carefully netted and added to the compartment holding the second male. Again, the pair was left to mate for 10 min. Once both males had been allowed to mate for 10 min all 3 fish were removed from the apparatus and returned to the stock tanks, and the number of eggs released in each compartment counted. No males or females were reused in subsequent replications. Only females that released eggs to both males were used in the subsequent analysis because failure to release eggs to a male may indicate exhaustion of egg supplies or disruption of oviposition due to disturbance rather than female choice per se.
Statistical analysis
Egg allocation data for the sequential matings were analyzed using split-plot analysis of variance (ANOVA), with females acting as the block component and male size category (S or L), time of mating (first or second) and mating group (females following mating sequence S1L2 vs. females following mating sequence L1S2) entered as categorical variables (Diaz-Uriarte 2002). Furthermore, to better approximate the assumptions associated with this parametric test, the egg counts were square root transformed prior to analysis.
Comparisons between the 2 groups of females (S1L2 vs. L1S2) were carried out using 2-sample t-tests (2-tailed). Where variances were significantly different, the degrees of freedom were adjusted using the Welch modification (Welch 1938). The percentage of eggs released to the first male was analyzed using a general linear model (GLM) incorporating binomial errors with a logit link and weighted by the total number of eggs oviposited. First male size was entered as a categorical variable and its significance assessed using an F-test of deletion to account for overdispersion (Crawley 2003). This test assesses the significance of a variable by removing it from the model and then testing the resulting change in residual variation for significance using a conventional F-test (Crawley 2003). To test whether male size relative to female size also affected egg allocation, we incorporated the ratio of female standard length to first male standard length into the egg proportion model as an additional continuous variable. As before, significance was assessed using an F-test of deletion.
In addition to the aforementioned analyses, egg count data (total eggs laid, eggs laid to first male, eggs laid to second male) were also analyzed separately in relation to male and female standard lengths (entered as continuous variables) using GLMs incorporating Poisson error structures. To account for overdispersion in these data, square root–transformed egg counts were used, and the significance of male and female standard length was assessed using F-tests of deletion.
All analyses were conducted in R version 2.1.1 (R Development Core Team 2005), and the values reported are mean ± standard deviation unless otherwise stated. Where comparisons are made between the 2 groups of females (S1L2 vs. L1S2), the reported values are written in the order "small male first versus large male first."
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RESULTS |
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Of the 48 pairs of males used, females released eggs to both males in 30 cases with females releasing eggs to only one male (n = 3) or neither male (n = 15) in the other 18 cases. Females released a mean total of 174.1 ± 89.8 eggs (n = 30; range 23–343 eggs) to male pairs with larger females releasing a greater total number of eggs (GLM: F1,27 = 4.495; P = 0.043). In addition, when female size was controlled, it was found that females also released more eggs to male pairs with a greater average size (GLM: F1,27 = 6.330; P = 0.018). On average, and by chance, females that received a small male first were both larger (30.8 ± 1.1 mm vs. 28.5 ± 2.2 mm; t-test: t = 3.54; df = 21; P = 0.002) and released a greater total number of eggs (207.6 ± 89.8 eggs vs. 140.7 ± 78.9 eggs; t-test: t = 2.17; df = 27; P = 0.039) than females receiving a large male first. However, there was no significant difference between these 2 groups of females in the mean (paired) male standard length (29.0 ± 0.9 mm vs. 28.7 ± 1.2 mm; t-test: t = 0.77; df = 26; P = 0.446).
Females released significantly more eggs to the first male (irrespective of the males size) than the second male (ANOVA: F1,28 = 22.84; P < 0.001), but there was no significant within-female effect of male size (ANOVA: F1,28 = 1.27; P = 0.270). There was a significant effect of mating group with females receiving a small male first releasing a greater mean number of eggs to each male than females receiving a large male first (103.8 ± 68.6 eggs vs. 70.3 ± 61.7 eggs; ANOVA: F1,28 = 5.17; P = 0.031). It should be noted, however, that due to the limited degrees of freedom available in a 2 x 2 crossover design that a mating group effect cannot be statistically distinguished from a potential male size-by-time interaction in the analysis (Diaz-Uriarte 2002). Furthermore, separate analysis of the data for the number of eggs released during each time point showed that there was a male size-by-time interaction (Figure 1). Although there was no difference between the 2 groups of females in the mean number of eggs released during the first time period (129.3 ± 69.8 eggs vs. 105.5 ± 67.8 eggs; t-test: t = 0.95; df = 27; P = 0.352), females released a greater number of eggs to the second male when he was large than when he was small (78.3 ± 59.1 eggs vs. 35.1 ± 25.0 eggs; t-test: t = 2.60; df = 18; P = 0.018).
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There was no significant difference in the proportion of the total clutch of eggs released to the first male, though there was a tendency for females receiving a large male first to release a greater proportion (62.93 ± 23.13% vs. 75.28 ± 14.21%; GLM: F1,28 = 3.39; P = 0.076). Females did not, however, adjust the proportion of eggs they released to the first male on the basis of their relative sizes (GLM: F1,27 = 1.94; P = 0.175).
During the first mating period, there was no significant effect of either male (GLM: F1,27 = 0.02; P = 0.880) or female standard length (GLM: F1,27 = 1.09; P = 0.306) on the number of eggs females released. Similarly, there was no effect of female standard length on the number of eggs released during the second mating period (GLM: F1,27 = 0.02; P = 0.880). During the second time period, females released more eggs with larger males (GLM: F1,27 = 11.13; P = 0.002; Figure 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The results presented here suggest that female zebra fish preferentially allocate eggs to larger males that are known to be more attractive to females (Pyron 2003
). Although female zebra fish released most of their eggs to the first male they encountered irrespective of his size relative to the second male, females released more eggs to the second male when he was large than to second males who were small. In addition, females that mated with smaller males first tended to release a smaller proportion of their total clutch to these males. Comparisons across females revealed that the total number of eggs laid increased with (mean) male standard length and second male standard length, confirming the increased allocation to larger males.
DA has been demonstrated in a number of taxa including insects and mammals, although the majority of studies have concerned birds (Rutstein et al. 2004; Sheldon 2000 and references therein). Among fish, studies of DA have been generally restricted to species with male parental care (Hastings 1988a, 1988b; Cote and Hunte 1989; Kolm 2002) with the exception of one study conducted on the resource-free mating system of the Japanese minnow (Katano and Maekawa 1997). Where male parental care is present, the strategic allocation of larger clutches to preferred males can most easily be explained if such males are better able to protect or provide for their offspring. However, where males provide no additional resources beyond their sperm, DA becomes more difficult to understand (Petrie and Williams 1993; Cunningham and Russell 2000).
Spence and Smith (2005) described territorial behavior over spawning sites in male zebra fish and shown that such males tend to be larger than nonterritorial males. Females may therefore choose larger males in order to maximize the chances of their offspring hatching in a suitable environment. However, little is known regarding the presence of territoriality in wild zebra fish, particularly given the short spawning period. Larger males may also be chosen because they have superior genes relative to smaller males and so provide a greater benefit to a female's offspring (Kirkpatrick and Ryan 1991). For example, in at least one population of the guppy Poecilia reticulata, larger males were shown to produce faster growing offspring with the daughters subsequently benefiting from higher reproductive success due to their larger body size (Reynolds and Gross 1992).
Larger males may be preferred because they represent a superior fertility prospect (Sheldon 1994) and, among fish species, for example, male size was shown to correlate positively with both ejaculate size (Zbinden et al. 2001; Pilastro et al. 2002) and sperm length (Skinner and Watt 2007). In the case of the zebra fish, females release their eggs in a series of ovipositions rather than all at once, with as many as 43 such events occurring in the first 20 min after lights up (Skinner 2004). Repeated matings are known to deplete male sperm reserves in at least 2 fish species (Nakatsuru and Kramer 1982; Petersen et al. 2001), and so it is possible that larger males may provide females with a reduced risk of infertility. However, in the zebra fish, although testes size increases with body size (Skinner 2004), no effect of male size has been found on egg fertility (Skinner AMJ and Watt PJ, unpublished data) or sperm quality (Skinner 2004).
One of the fundamental assumptions associated with the DA hypothesis states that there should be a trade-off between current and future reproductive effort, such that females withholding effort in the present hope to gain (directly or indirectly) from mating with superior males in the future (Sheldon 2000). In this study, however, we found that females released most of their eggs to the first male they encountered, irrespective of his size relative to the second male. Given the above assumption, how do we explain this result?
In the laboratory environment, zebra fish are capable of spawning all year round, yet their reproductive activity is restricted to a 1-h period after dawn (Westerfield 1995). This temporal restraint leads to frenetic activity with pairs spawning as often as twice a minute (Skinner 2004) and as little as 9 s after lights up (Skinner A, personal observation). Oviposition in the zebra fish occurs after the pursuit of the female by a male (or males) (Darrow and Harris 2004). In many taxa, male harassment is costly to females because it reduces the time they have available for feeding and vigilance (Clutton-Brock and Parker 1995), as well as increasing the risks of disease and/or parasite transmission (Borgia and Collis 1989). Furthermore, in at least one fish species, the sailfin molly Poecilia latipinna, such costs were also shown to be male size dependent, with females spending less time feeding when in the presence of small versus large males (Schlupp et al. 2001).
In the zebra fish, small males spawn more frequently than large males (Skinner 2004). Small males may therefore impose larger costs on females in terms of the energy required by females to avoid spawning with them. Female resistance to male harassment can also be costly in terms of a female's future reproductive success through the retention of nonspawned eggs. For example, overripening of retained eggs is known to reduce egg viability and fertility in a number of fish species (Billard 1988; de Gaudemar and Beall 1998), including the zebra fish (Hisoaka and Firlit 1962). Given the time limitations placed on sexually receptive female zebra fish, perhaps the rapid, indiscriminate oviposition behavior observed during the first time period is an adaptation to balance the costs associated with future mate location and discrimination versus those associated with current spawning avoidance and egg retention.
In the present study, females who mated with a large male second were, by chance, larger and released a greater total number of eggs than females who mated with a small male second. Although it is possible, therefore, that the male size effect seen during the second period was simply an artifact of this difference in female size and resources, that females who mated with a large male second also tended to release a smaller proportion of their total clutch to the first male suggests that these resource differences are not the whole answer. In addition, comparisons between females revealed male size effects to be independent of female size.
This study shows that female zebra fish are able to allocate reproductive resources differentially to males based on their size. Given the apparent resource-free nature of this mating system, it seems likely that larger males either provide superior genes to a female's offspring and/or that the costs associated with mating with larger males are lower than those associated with small males though this remains to be tested. We recommend that future studies in this species investigate the potential benefits afforded to females from mating with differently sized males.
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ACKNOWLEDGEMENTS |
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We thank Jens Rolff, Terry Burke, and 2 anonymous referees for comments on an earlier draft.
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