Behavioral Ecology Advance Access originally published online on March 3, 2007
Behavioral Ecology 2007 18(3):556-562; doi:10.1093/beheco/arm011
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Behavioral syndromes and the evolution of correlated behavior in zebrafish
a Department of Biology and Center for the Integrative Study of Animal Behavior, Indiana University, Bloomington, IN 47405, USA b Department of Biological Sciences and Center for Reproductive Biology, University of Idaho, Moscow, Idaho 443051, USA
Address correspondence to E.P. Martins. E-mail: emartins{at}indiana.edu.
Received 6 August 2006; revised 24 January 2007; accepted 2 February 2007.
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ABSTRACT |
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Studies of "behavioral syndromes" in different populations and species of animals can be used to shed light on the underlying mechanisms of evolution. For example, some personality syndromes suggest the existence of an underlying hormonal link, whereas other relationships between boldness and aggression appear to be the result of similar selective pressures. Here, we used 1 wild-derived and 2 laboratory strains of zebrafish (Danio rerio) to examine relationships among 5 behavioral measures: shoaling, activity level, predator approaches, latency to feed after a disturbance, and biting to a mirror stimulus. We found evidence of an activity syndrome, as if underlying metabolic costs influence variation in multiple forms of behavior. Evidence for a relationship between boldness and aggression was also apparent but depended both on strain and which specific behavior patterns were identified as measures of "boldness." Although some comparisons of laboratory and wild-derived strains were consistent with a domestication syndrome, others were not. Most observed relationships were relatively weak and occasionally inconsistent, arguing against strong underlying genetic linkages or pleiotropic effects relating any of the behavioral measures. Instead, it may be more important to study the details of selective context or the long-term impact of linkages between some, but not all, of a large set of genes influencing complex behavioral traits. We found profound differences among strains in most behavior patterns, but few sex differences. One strain (TM1) was consistently different from the others (SH and Nadia) being more social, more likely to approach predators, and taking less time to recover from disturbance than were the other 2 strains.
Key words: activity, aggression, behavioral syndromes, boldness, evolution, domestication, genetic correlation, metabolic syndrome, phenotypic correlation, zebrafish.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Many behavior patterns occur in tightly linked suites or "syndromes" (see reviews by Sih, Bell, and Johnson 2004
; Sih, Bell, Johnson, and Ziemba 2004). In some cases, studying complex behavior such as multimodal communicative displays as examples of behavioral syndromes ensures that we consider also emergent properties that appear only when multiple sensory elements are combined (e.g., Hebets 2005). In other cases, an observed link between behavioral phenotypes encourages us to search for a single underlying genetic or physiological mechanism. For example, studies of a boldness and aggression syndrome have encouraged further exploration of underlying hormonal explanations (e.g., Veenema et al. 2003). Syndrome studies can also shed light on phenotypic evolution. Both functional and mechanistic relationships between behavioral traits can constrain the directions in which evolution can occur and be crucial to the "evolvability" of complex phenotypes (e.g., Beldade et al. 2002; Hansen et al. 2003). Here, we estimate the magnitude of behavioral syndromes in zebrafish (Danio rerio), a popular model organism in genetic, developmental, and neurobiological research, thereby setting the stage for future research into the genetic basis of behavioral syndromes.
We focus on 3 syndromes that have been commonly reported in the behavioral literature: (1) boldness and aggression, (2) general metabolic response, and (3) domestication. An aggression–boldness syndrome has been found in numerous animals (see review by Koolhaas et al. 1999). In fish, it was classically documented in stickleback (Huntingford 1976) and is supported by more recent studies of cichlids (Brick and Jakobsson 2002) and trout (Schjolden et al. 2005). Bell (2005) suggests that in stickleback, the syndrome exists only in populations with high predation levels and is thus likely due to selection acting on multiple aspects of the phenotype simultaneously rather than a common underlying mechanism. Brown et al. (2005) showed that boldness in a tropical poeciliid is related not only to predation but also to growth rate and body size, suggesting the importance of metabolic factors also. Similar complexes of behavioral traits have been described in a wide variety of birds and mammals as a distinction between "proactive" and "reactive" personalities and has been linked to changes in the hypothalamic–pituitary–adrenal (HPA) system which influences many behavior patterns (e.g., Veenema et al. 2003).
The second syndrome we consider is a relationship between activity and other forms of behavior that is commonly attributed to a general metabolic response. Measures of activity may be related to measures of other behavior because of time budget conflicts (e.g., time spent feeding vs. time spent defending a nesting site) or because activity level may approximate metabolism (reviewed in Sih, Bell, Johnson, and Ziemba 2004). For example, Budaev (1997a,b; see also Budaev and Zhuikov 1998) found relationships between activity level, exploratory behavior, and shoaling in fish. Activity level is also associated with many other forms of behavior in flies (e.g., Meffert et al. 2002; Higgins et al. 2005). In other cases, individuals that are more active in the absence of predators are often also more active when predators are present (e.g., Sih et al. 2003; Brodin and Johansson 2004).
Third, we consider domestication, a complex of behavioral, morphological, and physiological changes due both to intentional selection for desirable traits as well as inadvertent selection and a reduction of natural selection (e.g., Huntingford 2004). For example, in Dmitry Belyaev's classic Farm-Fox experiment (summarized by Trut 1999), silver foxes selected only for tameness evolved many additional behavioral characteristics of the domestic dog such as barking, whining, and licking of their handlers. This finding suggests that there may be a common underlying mechanism such as a pleiotropic gene or hormone with multiple effects that links these very different behavior patterns. Decreases in fearfulness are common with domestication (e.g., jungle fowl: Schutz et al. 2001; trout: Alvarez and Nicieza 2003), as are changes in aggression, although the variation in the direction of observed aggressive shifts (increased: Ruzzante 1994; Einum and Fleming 1997; Metcalfe et al. 2003; decreased: Fleming et al. 1996; Berejikian et al. 1997; Hedenskog et al. 2002; no difference: Johnsson et al. 1996; Yamamoto and Reinhardt 2003) suggests that domestication may also involve selection acting on multiple phenotypes simultaneously rather than an underlying shared mechanism.
Comparison of behavioral syndromes in different populations and across different taxonomic levels offers a way to distinguish between phenotypic associations resulting from underlying mechanisms and correlated selection. For example, Bell (2005) found that an aggression–boldness syndrome observed in one population of stickleback fish was unlikely to be the result of underlying genetic correlations because it was not also observed in a second population of the same species. Baer and Lynch (2003) concluded that relationships between body size and life history traits observed both within and between populations offered evidence of strong pleiotropic constraints on body size evolution. This comparative approach is limited given growing evidence that genetic correlations also evolve and hence often differ among populations (see review by Steppan 2002). But similar phenotypic correlations observed both within and across populations suggest an underlying genetic association or pleiotropic physiological mechanism, and differences across populations argue for differential selective regimes (e.g., Badyaev and Hill 2000) or different genetic structures (e.g., Service 2000) and suggest that syndromes do not necessarily constrain the selective responses of behavior because their underlying genetic or physiological basis can be uncoupled.
Zebrafish are an ideal species for studying the genetic basis of behavioral syndromes because of their extensive use as a model organism by developmental biologists and the comprehensive toolkit of genetic techniques that are consequently available, including a multitude of distinct, artificially selected strains and a complete genome sequence. While we know little about zebrafish behavior and natural history, recent studies have found that although fish from natural populations form shoals of 2–10 individuals (Pritchard et al. 2001), individuals are aggressive to one another and able to monopolize resources (Hamilton and Dill 2002; Spence and Smith 2005). Aggression is present in males as well as in females (Pritchard 2001), and females prefer to associate with males rather than with other females (Delaney et al. 2002). Recent studies comparing the behavior of laboratory and recently derived wild-caught strains found that laboratory strains exhibit characteristics commonly associated with domestication (e.g., higher growth rates, decreased startle response) and that strain differences in "boldness" have a genetic basis (Wright et al. 2003, 2006; Robison and Rowland 2005). In contrast, zebrafish aggression and shoaling behavior is more malleable, sometimes depending on the social history of the tested individuals. Engeszer et al. (2004) showed that zebrafish's preference for horizontal stripes depended on the social context during early development, whereas Moretz et al. (2006) showed that tendency to shoal can be altered even in adults after exposure to particular social contexts.
In this study, we measure the magnitude of phenotypic associations between 5 behavior patterns: aggression, shoaling behavior, latency to feed after disturbance, activity level, and predator response. We focus on associations indicative of the 3 behavioral syndromes outlined above, relating measures of aggression and boldness, of activity with other behavior patterns, and of behavior patterns that typically change with domestication (including also recovery from disturbance and predator approaches). We compare relationships within and across 3 strains of zebrafish to identify those that are not only large but consistent.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study species
Zebrafish are small cyprinids native to rivers of Pakistan, India, and Bangladesh (Eaton and Farley 1974
; Spence et al. 2006). Under laboratory conditions, zebrafish are reproductively active throughout the year and are easily maintained (Westerfield 1995). We tested the behavior of individuals from 3 strains of zebrafish, all of which were raised from eggs in similar environmental conditions. The TM1 strain is derived from zebrafish acquired from a pet store in 1986 and is now 30 generations removed from that point (Robison and Rowland 2005). The TM1 strain (mean standard length [SL] = 31 mm, standard error [SE] = 0.3) has a green fluorescent protein transgene that is detectable as a visible green emission when exposed to ultraviolet light (Gibbs and Schmale 2000). Individuals of the Nadia strain (mean SL = 26 mm, SE = 0.3) tested in our experiment were only 5 generations removed from wild-caught fish (for details, see http://zfin.org) and exhibit several behavioral and morphological differences from TM1 fish that suggest that Nadia have not yet evolved in response to the laboratory environment (Robison and Rowland 2005). The third strain, SH or Scientific Hatcheries, (mean SL = 29 mm, SE = 0.4) is more similar to TM1 in that it was developed in the early 1990s and is available commercially from Scientific Hatcheries in Huntington Beach, CA. However, unlike the TM1 strain that is maintained by breeding small numbers of individuals, SH fish are reared and bred in large numbers, approximating conditions one would expect to find in commercial fish hatcheries (e.g., trout hatcheries). The 3 strains have thus evolved under very different selective regimes. We used mass breedings of adults from each strain to generate subjects for our experiment, raising animals under standard conditions in pure-strain groups until they were 5 months of age (adults). Hatchlings were kept in small groups in beakers and fed Paramecium caudatum for the first 15 days. Juvenile zebrafish were then moved to 21-l aquaria in groups of 10 where they were fed a diet of brine shrimp and flake food twice daily. All aquaria were visually isolated from one another and were housed in a constant temperature aquatic laboratory (28.5 °C) on a 14:10 h light:dark cycle, as typical to promote breeding and rapid development. The laboratory is serviced by a US Filter organic carbon filter water treatment system that delivers water to each tank separately and continually.
Behavioral measures
We measured the behavior of 84 fish, including 15 males and 15 females from the TM1 strain, 22 males and 8 females from the Nadia strain, and 11 males and 13 females from the SH strain. As in Moretz et al. (2006), we used a large testing arena (115-l aquarium) to measure 3 types of behaviors: leaving shoal, activity level, and predator approaches. Leaving shoal was scored as the number of times (in 5 min) that the subject fish moved more than 14 cm horizontally away from a stimulus shoal (4 fish of the same strain as the subject), visible to the subject through a solid Plexiglas barrier. Leaving shoal might be interpreted as a measure of boldness with bold individuals moving away from the shoal more often than wary individuals. Because of the lack of acclimation period immediately before the trial began, leaving shoal might also be interpreted as an inverse measure of the fish's tendency to form groups when recovering from a stressful situation. The stimulus shoal was then obscured from view by an opaque Plexiglas barrier, and activity level was estimated as the number of lines crossed on a horizontal grid during 5 min, including both forwards and backwards motion. Finally, a second, opaque barrier was lifted, revealing a stationary epoxy model (SL= 83.5 mm, body depth = 3.2 mm), painted white with black bars to mimic the appearance of a cichlid (Etroplus canarensis) found in the same geographic areas as zebrafish. We scored predator approaches as the number of times (in 5 min) that the subject moved within 14-cm horizontal distance of the predator. Subjects with high predator approach scores might be considered to be "bold." Note that all 3 behavioral metrics are related to each other in that they were measured in the same testing arena and all 3 involved measurements of locomotion.
Subjects were then moved to a small holding tank (21 l) to measure latency to feed and biting. Live brine shrimp were placed in the tank at the same time as the subject, and we recorded latency to feed in seconds. Because the fish were offered the opportunity to eat immediately after a major disturbance (being netted and placed in a new tank), we interpret latency to feed as a measure of stress recovery or perhaps boldness. Because latency to feed may also reflect individual variation in hunger, all fish were tested 5–6 h after the most recent feeding. After, test subjects remained resting, visually isolated from all other fish, until the next morning (at least 18 h later) when we scored biting by placing a mirror at one end of an individual's tank and recording the number of bites directed at the image over a 5-min period. As explained further in Moretz et al. (2006), biting to a mirror has been mostly interpreted as a measure of aggression (Gerlai 2003; Marks et al. 2005) but may also indicate a more general measure of social motivation or the intent to interact with a social partner. Tests in the large arena were videotaped for later scoring, whereas tests in the small holding tank were scored in real time by a single observer (JAM). All tests took place early in the morning, within 1 hour of lights being turned on and before daily feeding.
Statistical analyses
Relationships between measures of boldness (leaving shoal, predator approaches, and possibly latency to feed after a disturbance) and aggression (biting) would provide evidence for an aggression–boldness syndrome. Relationships between our single measure of activity level and each of the 4 other behavior patterns would provide evidence of an activity syndrome. Domestication is expected to influence boldness, aggression, and also stress recovery (as reflected in our measure of latency to feed after a disturbance). We thus began our analyses by estimating the magnitude of pairwise relationships between behavioral measures using Pearson product–moment correlations as our measure of effect size. To avoid multiple comparisons, and because of the potential importance of sex and strain effects, we did not conduct hypothesis tests on the correlation coefficients themselves. Instead, we combined data from all 3 strains and used analyses of variance (ANOVAs) to estimate the same pairwise relationships, but now including also sex and strain as predictors. Note that F values based on Type III sums of squares in these analyses are identical regardless of which behavior pattern is set as predictor (X) and which is identified as the response (Y). Because this approach still resulted in 10 tests of related data, we further applied a Bonferroni correction, considering only results with P < 0.005 as being statistically significant, and limiting our attention to the single F value that describes the trait relationship. We then used a multivariate analysis of variance (MANOVA) to test the overall effects of sex and strain and a sex by strain interaction effect on behavior. We square-root transformed leaving shoal and predator approaches and natural-log transformed latency to feed to obtain normal and homoscedastic residuals in the ANOVAs and MANOVA. All analyses were performed using SAS (2002).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Evidence of syndromes
Individual zebrafish that were more active also approached the predator dummy more often (Figure 1 and Table 1), leading to a significant relationship between 2 behavioral measures (F = 9.7; degrees of freedom [df] = 1,73; P = 0.003, Table 2), suggestive of an activity syndrome. This was the only pairwise relationship that was both large and consistent across all 3 strains (Table 2). A possible activity syndrome was also supported by an apparent relationship between activity levels and the tendency to leave the vicinity of the shoal (in TM1 [r = 0.52] and SH [r = 0.33] but not Nadia [r = 0.02]) and between activity levels and latency to feed after a disturbance (only in SH fish [r = –0.49], Table 1). Because these other relationships were larger in some strains than in others (Table 1), they were not statistically significant when tested across all 3 strains (Table 2).
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There was also a suggestion of a boldness–aggression syndrome in the relationships between biting and some measures of boldness (leaving shoal and latency to feed after disturbance), but not others (predator approaches, Table 1). But once again, the details were inconsistent across strains and hence were not evident in the across-strain tests. Both Nadia and TM1 fish that bit more often at a mirror stimulus were also more likely to leave the immediate vicinity of a shoal (r = 0.32 for Nadia, r = 0.24 for TM1), but SH fish showed a weaker pattern in the opposite direction (r = –0.11, Table 1), such that the overall relationship was not statistically significant when subjected to the conservative Bonferroni criterion (Table 2). Similarly, biting was related to latency to feed, but this pattern differed critically across strains (Table 1) and was hence not significant overall (Table 2). TM1 fish that bit frequently took less time to feed after a disturbance, SH that bit more often took more time to feed after a disturbance, and there was no relationship between these 2 behavioral measures in the Nadia (Table 1). We found no evidence of a relationship between biting to the mirror stimulus and predator approaches (–0.1 < r < 0.2, Table 1).
Our results suggest a domestication syndrome in that individual SH which fed quickly after a disturbance (a measure of stress recovery) were also more active (r = –0.49), less likely to bite at a mirror stimulus (r = 0.43), and more likely to approach a predator (r = –0.42, Table 1). But these patterns were not strong in the other 2 strains or showed conflicting patterns. For example, TM1 fish that fed rapidly after a disturbance actually bit more often to the mirror stimulus (r = –0.28), and Nadia showed no strong relationships between latency to feed after a disturbance and other measures. Thus, again, these domestication relationships were not confirmed by the ANOVA tests because of inconsistencies in the pattern across strains (Table 2).
Sex and strain differences
Sex differences in behavior were small (Table 3). Male zebrafish were more active, took longer to feed after a disturbance, approached the predator dummy, and left the vicinity of a shoal more often than did females. But when behavior patterns were tested simultaneously in a MANOVA, neither sex differences (Wilks' 
= 0.86; F = 1.87; df = 5,58; P = 0.1137) nor interactions between sex and strain (Wilks' = 0.80; F = 1.39; df = 10,116; P = 0.1939) were statistically significant.
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In contrast, we found robust and significant strain differences in behavior (Wilks'
= 0.55; F = 4.04; df = 10,116; P = 0.0001). Although these strain differences were evident in all the behavior patterns (Figure 2 and Table 3), they were most pronounced in biting to a mirror (F = 10.0; df = 2,62; P = 0.002) and latency to feed after a disturbance (F = 3.4; df = 2,62; P = 0.04). TM1 individuals bit the mirror stimulus more often and fed more quickly after a disturbance than did individuals of the other 2 strains (Table 3).
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As might be expected for a nondomesticated strain, individual Nadia were less active, less aggressive (bit the mirror less often), and less bold (feeding less soon after disturbance and approaching the predator less) than were individuals of the TM1 laboratory strain (Figure 2). Nadia also left the shoal slightly more often than did TM1 fish. The domestication syndrome was not confirmed, however, by results from the SH laboratory strain. Individual SH fish were often more similar to Nadia (wild derived) than to individuals of the TM1 laboratory strain (Figure 2) and were less aggressive and more likely to leave the vicinity of the shoal than were either of the 2 other strains. The 2 laboratory strains (SH and TM1) were more similar to each other than to the more recently domesticated Nadia strain only in activity level (Table 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our study finds relationships between behavior and activity level in 3 strains of zebrafish and weaker evidence of a boldness–aggression syndrome and a domestication syndrome in some, but not other, strains. In the latter 2 cases, the direction of the relationship in the syndrome also depended on the strain. In fact, strain differences in nearly every behavior pattern were pronounced, whereas sex differences were generally small.
Specifically, we found relationships between activity level and (1) tendency to approach a predator in all 3 strains, (2) tendency to move away from a shoal (TM1 and SH, but not Nadia), and (3) latency to feed after a disturbance (SH only). These results are consistent with the growing body of evidence that many forms of behavior are constrained by underlying metabolic costs (reviewed in Sih, Bell, Johnson, and Ziemba 2004). As reviewed by Meffert et al. (2002; see also Higgins et al. 2005), many forms of behavior in flies are also tightly associated with activity level. Similar associations have also been found between activity level, exploratory behavior, and shoaling (Budaev 1997a,b; Budaev and Zhuikov 1998). In part, these relationships in our own and other studies may be explained by similarities in the underlying scoring procedure—we might expect predator approaches or exploratory behavior to be associated with activity level when these behavior patterns are scored in terms of locomotion about an arena. In our own study, the lack of some relationships that involved measures of locomotion (e.g., between leaving shoal and predator approaches) suggests that the observed activity syndrome goes beyond a relationship between scoring metrics.
We found relationships between boldness and aggression, but the relationships depended on both strain and the details of the behavior patterns being considered. Nadia and TM1 that bit more frequently tended to be more willing to leave the vicinity of a shoal, but the opposite pattern was seen in the SH strain. Similarly, the relationship seen in TM1 fish between biting and quick feeding after a disturbance was reversed in SH fish (SH that bit more often took longer to feed after a disturbance) and was not at all present in Nadia fish. Bell (2005) suggests that the boldness–aggression syndrome is more likely to be present in populations with high predation levels. Although the SH strain is maintained in a predator-free environment, competition from conspecifics in high-density–rearing environments may have had a similar evolutionary effect to high predation. Further studies comparing the selective impact of conspecific competition and predation levels may be warranted. Similarly, strain differences in the direction of the observed relationships suggest that although some fish strains exhibit "proactive" and "reactive" personalities similar to those described for birds and mammals, further research is needed to determine whether and how these personalities may be related to an underlying HPA axis.
Although we found several major differences between 2 zebrafish strains (TM1 and Nadia) suggestive of a domestication syndrome (consistent with that proposed by Robison and Rowland 2005), data for a third strain (SH) did not support this conclusion. This is similar to previous results showing that fish domestication has had highly variable effects on behavior. Domestication has lead to increases (e.g., Einum and Fleming 1997; Metcalfe et al. 2003), decreases (Fleming et al. 1996; Berejikian et al. 1997; Hedenskog et al. 2002), and no change (Johnsson et al. 1996; Yamamoto and Reinhardt 2003) in fish aggression. As shown in our study, laboratory strains of zebrafish can vary dramatically in their behavior. Wild-type zebrafish strains derived from different natural populations can also vary markedly in behavior (Wright et al. 2003). Thus, the wild/domesticated dichotomy may not be a sufficient description of the differences in evolutionary history, genetic background, and selective regime.
Although other behavioral syndrome studies have reported correlation values (r) ranging from 0.4 to 0.8 (Huntingford 1976; Hedrick 2000; Sih et al. 2003; Bell and Stamps 2004; Ward et al. 2004; Bell 2005), such strong correlations may have only a short-term effect on behavioral evolution. Over time, strong phenotypic or genetic correlations decrease differences among individuals in a population. Thus, unless correlational selection is acting on the 2 traits or the animals exist in environments that fluctuate over time (Roff 1996), the originally strong phenotypic or genetic correlations are likely to disappear as the 2 traits reach fixation. Alternatively, weak, but persistent, genetic correlations may have a more profound evolutionary impact when considered over long periods of time, especially for behavioral traits that are influenced by tens or hundreds of genes (e.g., Anholt et al. 2003; Flint 2003). In these cases, strong genetic linkages between subsets of these genes may produce only weak phenotypic correlations, which over long periods of time have profound effects on the direction of evolutionary change. Comparative studies that infer selection from interspecific variation (e.g., Hansen 1997; Prum 1997) are needed to determine when behavioral syndromes measured in a single generation are sufficiently large to lead to long-term behavioral evolution.
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ACKNOWLEDGEMENTS |
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We thank Erin Churchill and Candice Clark for animal husbandry help. Padrick Anderson and Jennifer Wright assisted in scoring videotaped trials. Erin Kelso, Cuauhcihuatl Vital, Saúl Nava, Mayté Ruiz, and Winnie Ho provided numerous suggestions on earlier versions of the manuscript. We are grateful also to Anne Houde and 2 anonymous reviewers for helpful comments. This research was supported in part by a National Science Foundation award to E.P.M. (IOB-0543491) and by a National Science Foundation and Idaho University EPSCoR award (EPS-044789) to B.D.R. All experiments comply with current laws of the United States of America and with the Animal Care Guidelines of Indiana University (BIACUC protocol approval #: 05-096).
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Alvarez D, Nicieza AG. Predator avoidance behaviour in wild and hatchery-reared brown trout: the role of experience and domestication. J Fish Biol (2003) 63:1565–1577.[CrossRef][ISI]
Anholt RRH, Dilda CL, Chang S, Fanara JJ, Kulkarni NH, Ganguly I, Rollman SM, Kamdar KP, Mackay TFC. The genetic architecture of odor-guided behavior in Drosophila: epistasis and the transcriptome. Nat Genet (2003) 35:180–184.[CrossRef][ISI][Medline]
Badyaev AV, Hill GE. The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure. Evolution (2000) 54:1784–1794.[CrossRef][ISI][Medline]
Baer CF, Lynch M. Correlated evolution of life-history with size at maturity in Daphnia pulicaria: patterns within and between populations. Genet Res Comb (2003) 81:123–132.
Beldade P, Koops K, Brakefield PM. Modularity, individuality and evo-devo in butterfly wings. Proc Natl Acad Sci USA (2002) 99:14262–14267.
Bell AM. Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol (2005) 18:464–473.[CrossRef][ISI][Medline]
Bell AM, Stamps JA. Developmental differences between individuals and populations of sticklebacks, Gasterosteous aculeatus. Anim Behav (2004) 68:1339–1348.[CrossRef][ISI]
Berejikian BA, Tezak EP, Schroder SL, Knudsen CM, Hard JJ. Reproductive behavioral interactions between wild and captively reared coho salmon (Oncorhynchus kisutch). Ices J Mar Sci (1997) 54:1040–1050.
Brick O, Jakobsson S. Individual variation in risk taking: the effect of a predatory threat on fighting behavior in Nannacara anomala. Behav Ecol (2002) 13:439–442.
Brodin T, Johansson F. Conflicting selection pressures on the growth/predation—risk trade-off in the damselfly. Ecology (2004) 85:2927–2932.[ISI]
Brown C, Jones F, Braithwaite V. In situ examination of boldness-shyness traits in the tropical poeciliid, Brachyraphis episcopi. Anim Behav (2005) 70:1003–1009.[CrossRef][ISI]
Budaev SV. Personality in the guppy (Poecilia reticulata): a correlational study of exploratory behavior and social tendency. J Comp Psych (1997a) 111:399–411.[CrossRef]
Budaev SV. Alternative styles in the European wrasse, Symphodus ocellatus: boldness related schooling tendency. Environ Biol Fishes (1997b) 49:71–78.[CrossRef]
Budaev SV, Zhuikov AY. Avoidance learning and personality in the guppy (Poecilia reticulate). J Comp Psych (1998) 112:92–94.[CrossRef]
Delaney M, Follet C, Ryan N, Hanney N, Lusk-Yablick J, Gerlach G. Social interaction and distribution of female zebrafish (Danio rerio) in a large aquarium. Biol Bull (2002) 203:240–241.
Eaton RC, Farley RD. Spawning cycle and egg production of zebrafish, Brachydanio rerio, in the laboratory. Copeia (1974) 1974:195–204.[CrossRef]
Einum S, Fleming IA. Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J Fish Biol (1997) 50:634–651.[CrossRef][ISI]
Engeszer RE, Ryan MJ, Parichy DM. Learned social preference in zebrafish. Curr Biol (2004) 14:881–884.[CrossRef][ISI][Medline]
Fleming IA, Jonsson B, Gross MR, Lamberg A. An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). J Appl Ecol (1996) 33:893–905.[CrossRef]
Flint J. Analysis of quantitative trait loci that influence animal behavior. J Neurobiol (2003) 54:46–77.[CrossRef][ISI][Medline]
Gerlai R. Zebrafish: an uncharted behavior genetic model. Behav Genet (2003) 33:461–468.[CrossRef][ISI][Medline]
Gibbs PDL, Schmale MC. GFP as a genetic marker scorable throughout the life cycle of transgenic zebrafish. Mar Biotech (2000) 2:107–125.
Hamilton IM, Dill LM. Monopolization of food by zebrafish increases in risky habitats. Can J Zool (2002) 80:2164–2169.
Hansen TF. Stabilizing selection and the comparative analysis of adaptation. Evolution (1997) 51:1341–1351.[CrossRef][ISI]
Hansen TF, Armbruster WS, Carlson ML, Pelabon C. Evolvability and genetic constraint in Dalechampia blossoms: genetic correlations and conditional evolvability. J Exp Zool (2003) 296B:23–39.
Hebets E. Attention-altering signal interactions in the multimodal courtship display of the wolf spider Schizocosa uetzi. Behav Ecol (2005) 16:75–82.
Hedenskog M, Petersson E, Jarvi T. Agonistic behavior and growth in newly emerged brown trout of sea-ranched and wild origin. Aggress Behav (2002) 28:145–153.[CrossRef][ISI]
Hedrick AV. Crickets with extravagant mating songs compensate for predation risk with extra caution. Proc R Soc Lond B (2000) 267:671–675.[Medline]
Higgins LA, Jones KM, Wayne ML. Quantitative genetics of natural variation of behavior in Drosophila melanogaster: the possible role of social environment on creating persistent patterns of group activity. Evolution (2005) 59:1529–1539.[CrossRef][ISI][Medline]
Huntingford FA. The relationship between antipredator behavior and aggression among conspecifics in the three-spined stickleback. Anim Behav (1976) 24:245–260.[Medline]
Huntingford FA. Implications of domestication and rearing conditions for the behavior of cultivated fishes. J Fish Biol (2004) 65:122–142.
Johnsson JI, Petersson E, Jonsson E, Bjornsson BT, Jarvi T. Domestication and growth hormone alter antipredator behaviour and growth patterns in juvenile brown trout, Salmo trutta. Can J Fish Aquat Sci (1996) 53:1546–1554.[CrossRef]
Koolhaas JM, Korte SM, De Boer SF, Van Der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ. Coping styles in animals: current status in behaviour and stress-physiology. Neurosci Biobehav Rev (1999) 23:925–935.[CrossRef][ISI][Medline]
Marks C, West TN, Bagatto B, Moore FBG. Developmental environment alters conditional aggression in zebrafish. Copeia (2005) 2005:901–908.[CrossRef]
Meffert LM, Hicks SK, Reagan JL. Nonadditive genetic effects in animal behavior. Am Nat (2002) 160:S198–S213.[CrossRef][ISI]
Metcalfe NB, Valdimarsson SK, Morgan IJ. The relative roles of domestication, rearing environment, prior residence and body size in deciding territorial contests between hatchery and wild juvenile salmon. J Appl Ecol (2003) 40:535–544.[CrossRef]
Moretz JA, Martins EP, Robison BD, Forthcoming. The effects of early and adult social environment on zebrafish (Danio rerio) behavior. Environ Biol Fishes (2006).
Pritchard VL. Behaviour and morphology of the zebrafish, Danio rerio [PhD dissertation] (2001) Leeds, UK: University of Leeds.
Pritchard VL, Lawrence J, Butlin RK, Krause J. Shoal choice in zebrafish, Danio rerio: the influence of shoal size and activity. Anim Behav (2001) 62:1085–1088.[CrossRef][ISI]
Prum RO. Phylogenetic tests of alternative intersexual selection mechanisms: trait macroevolution in a polygynous clade (Aves: Pipridae). Am Nat (1997) 149:668–692.[CrossRef][ISI]
Robison BD, Rowland W. Zebrafish (Danio rerio) as a model organism in conservation biology: behavioral variation among wild and domesticated strains. Can J Fish Aquat Sci (2005) 62:2046–2054.[CrossRef]
Roff DA. The evolution of genetic correlations, an analysis of patterns. Evolution (1996) 50:1392–1403.[CrossRef][ISI]
Ruzzante DE. Domestication effects on aggressive and schooling behavior in fish. Fish Aquac (1994) 120:1–24.
SAS. SAS for Windows 9.1 (2002) Cary (NC): SAS Institute, Inc.
Schjolden J, Backstrom T, Pulman KG, Pottinger TG, Winberg S. Divergence in behavioural responses to stress in two stains of rainbow trout (Oncorhynchus mykiss) with contrasting stress responsiveness. Horm Behav (2005) 48:537–544.[CrossRef][Medline]
Schutz KE, Forkman B, Jensen P. Domestication effects on foraging strategy, social behaviour and different fear responses: a comparison between the red junglefowl (Gallus gallus) and a modern layer strain. Appl Anim Behav Sci (2001) 74:1–14.[CrossRef][ISI]
Schutz KE, Kerje S, Jacobsson L, Forkman B, Carlborg O, Andersson L, Jensen P. Major growth QTLs in fowl are related to fearful behavior: possible genetic links between fear responses and production traits in a red junglefowl x white leghorn intercross. Behav Genet (2004) 34:121–130.[CrossRef][ISI][Medline]
Service PM. The genetic structure of female life history in D. melanogaster: comparisons among populations. Genet Res (2000) 75:153–166.[CrossRef][ISI][Medline]
Sih A, Bell A, Johnson JC. Behavioral syndromes: an ecological and evolutionary overview. TREE (2004) 19:372–378.[Medline]
Sih A, Bell A, Johnson JC, Ziemba RE. Behavioral syndromes: an integrative overview. Quart Rev Biol (2004) 79:241–277.[CrossRef][Medline]
Sih A, Katts LB, Mauer EF. Behavioural correlations across situations and the evolution of antipredator behavior in a sunfish-salamander system. Anim Behav (2003) 65:29–44.[CrossRef][ISI]
Spence R, Fatema MK, Reichard M, Huq KA, Wahab MA, Ahmed ZF, Smith C. The distribution and habitat preferences of the zebrafish (Danio rerio) in Bangladesh. J Fish Biol (2006) 69:1435–1448.[CrossRef][ISI]
Spence R, Smith C. Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish, Danio rerio. Anim Behav (2005) 69:1317–1323.[CrossRef][ISI]
Steppan SJ. Comparative quantitative genetics: evolution of the G matrix. TREE (2002) 17:320–327.
Trut LN. Early canid domestication: the farm-fox experiment. Am Sci (1999) 87:160–169.[CrossRef][ISI]
Veenema AH, Meijer OC, de Kloet ER, Koolhaas JM. Genetic selection for coping style predicts stressor susceptibility. J Neuroendocrinol (2003) 15:256–267.[CrossRef][ISI][Medline]
Ward AJW, Thomas P, Hart PJB. Correlates of boldness in three-spined sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol (2004) 55:561–568.[CrossRef][ISI]
Westerfield M. The zebrafish book (1995) Eugene (OR): Institute of Neuroscience, University of Oregon.
Wright D, Nakamichi R, Krause J, Butlin RK. QTL analysis of behavioral and morphological differentiation between wild and laboratory zebrafish. Behav Genet (2006) 36:271–284.[CrossRef][ISI][Medline]
Wright D, Rimmer LB, Pritchard VL, Krause J, Butlin RK. Inter and intra-population variation in shoaling and boldness in the zebrafish (Danio rerio). Naturwissenschaften (2003) 90:374–377.[CrossRef][ISI][Medline]
Yamamoto T, Reinhardt UG. Dominance and predator avoidance in domesticated and wild masu salmon Oncorhynchus masou. Fish Sci (2003) 69:88–94.[CrossRef]
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