Heritability of Boldness and Aggressiveness in the Zebrafish

Behav Genet (2013) 43:161–167 DOI 10.1007/s10519-013-9585-y ORIGINAL RESEARCH Heritability of Boldness and Aggressiveness in the Zebrafish Tolulope O. Ariyomo • Mauricio Carter Penelope J. Watt • Received: 8 October 2012 / Accepted: 15 January 2013 / Published online: 25 January 2013 Ó Springer Science+Business Media New York 2013 Abstract Behavioural traits that are consistent over time and in different contexts are often referred to as personality traits. These traits influence fitness because they play a major role in foraging, reproduction and survival, and so it is assumed that they have little or no additive genetic variance and, consequently, low heritability because, theoretically, they are under strong selection. Boldness and aggressiveness are two personality traits that have been shown to affect fitness. By crossing single males to multiple females, we estimated the heritability of boldness and aggressiveness in the zebrafish, Danio rerio. The additive genetic variance was statistically significant for both traits and the heritability estimates (95 % confidence intervals) for boldness and aggressiveness were 0.76 (0.49, 0.90) and 0.36 (0.10, 0.72) respectively. Furthermore, there were significant maternal effects accounting for 18 and 9 % of the proportion of phenotypic variance in boldness and aggressiveness respectively. This study shows that there is a significant level of genetic variation in this population that would allow these traits to evolve in response to selection. Edited by Stephen Maxson. T. O. Ariyomo (&)
P. J. Watt Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK e-mail: [email protected]; [email protected] M. Carter Center for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Cornwall Campus, Penryn, UK Keywords Heritability
Additive genetic variance
Boldness
Aggressiveness
Maternal effects
Personality traits Introduction Individuals can express distinctive behaviours that are consistent over time and context (Wilson et al. 1994) and these are referred to as personality traits, coping style or temperament (Koolhaas et al. 1999; Gosling 2001; Réale et al. 2007). These behavioural traits have been found in many vertebrate groups (Boissy 1995; Dall et al. 2004; Sih et al. 2004a, b; Réale et al. 2007; Bell et al. 2009) and may have significant fitness consequences (Smith and Blumstein 2008; Ariyomo and Watt 2012). Consistent behaviour within individuals of a population may be due to genetic or environmental effects or a combination of both (Brown et al. 2007). The additive genetic variance of a trait, that is, its heritability, is a requirement for predicting its response to selection (Falconer and Mackay 1996). Heritability is estimated by measuring the similarity between relatives and is often expressed as the proportion of phenotypic variance that can be attributed to additive genetic variance (Falconer and Mackay 1996; Wilson et al. 2010). However, similarity between relatives is not limited to genetic variation; environmental effects may also contribute (Falconer and Mackay 1996). There are various sources of environmental variation and one that is considered to be important is that of the mother’s phenotype and its influence on her offspring’s phenotype; so called maternal effects (Falconer and Mackay 1996; Kruuk and Hadfield 2007). Maternal effects can help influence the behavioural responses of offspring to the environment (Bonduriansky and Day 2009; Stamps and Groothuis 2010) in ways that differ from 123 162 genetic inheritance, for example, through maternal provisioning during ontogeny, which may affect development and behaviour (Qvarnström and Price 2001). Maternal effects may persist throughout the life of the offspring and they may inflate the additive genetic variance and heritability if not accounted for (Wilson et al. 2010). Two widely studied personality traits are boldness and aggressiveness. Boldness is the propensity of an individual to take risks (Wilson et al. 1994), whereas aggression is any behaviour that may be deemed confrontational (Olivier and Young 2002). Aggressiveness can be used to gain access to mates, resources and maintain dominance (Larson et al. 2006; Ang and Manica 2010). Boldness and aggressiveness are behavioural traits that can facilitate the success of foraging (Stamps 2007; Dyer et al. 2009), dispersal (Réale and Festa-Bianchet 2003), reproduction (Godin and Dugatkin 1996; Ariyomo and Watt 2012) and survival (Biro and Stamps 2008; Smith and Blumstein 2010), though they may have a negative impact on reproductive success and longevity (Sih et al. 2004b; Sih and Watters 2005; Stamps 2007; Smith and Blumstein 2008). Furthermore, boldness and aggressiveness are often closely linked to fitness (Réale and Festa-Bianchet 2003; Dingemanse and Realé 2005; Smith and Blumstein 2008; Ariyomo and Watt 2012) and they may alter the selective environment of other traits, such as morphological and physiological traits, and by so doing influence their evolution (Blomberg et al. 2003). For a trait to respond to selection, it must show phenotypic variation among individuals, have a significant genetic component and affect fitness (Dingemanse and Realé 2005; Bijma 2011). Selection favours alleles that show higher fitness so traits under intense selection should have little or no additive genetic variance as the selected alleles become fixed in a population thus resulting in low heritability estimates (Elimination hypothesis: Jones 1987; Merilä and Sheldon 1999; Hoffmann 1999; Stirling et al. 2002). The aim of this study was to estimate the proportion of additive genetic variance underlying phenotypic variation in boldness and aggressiveness in the zebrafish and to estimate the variance attributable to maternal effects in both traits. Previous work has shown that, in the zebrafish, boldness and aggressiveness vary among individuals and that both traits are highly repeatable (Wright et al. 2003; Robison and Rowland 2005; Wilson et al. 2009; Norton et al. 2011; Ariyomo and Watt 2012), which suggests that they are genetically determined. Furthermore, both traits significantly affect reproductive fitness (Smith and Blumstein 2008; Ariyomo and Watt 2012). Therefore, we predicted that boldness and aggressiveness would have low additive genetic variance and thus low heritability estimates. We also predicted that maternal effects would be 123 Behav Genet (2013) 43:161–167 weak since zebrafish are egg scatterers with no parental care (Spence et al. 2008). Materials and methods Adult zebrafish were used (LWT strain) in this study and they came from laboratory maintained stock. Twenty males (standard length ± SE 27.30 ± 0.23 mm) and twenty females (standard length ± SE 26.98 ± 0.22 mm) were housed separately in two tanks (30 cm 9 15 cm 9 24 cm) in a re-circulatory system maintained at 27 °C, under a 12:12 h light/dark photoperiod with a 40 min dusk and dawn period. The fish were fed twice daily with dry fish food and brine shrimp. Behavioural testing Behavioural testing for boldness and aggressiveness was similar to that described in Ariyomo and Watt (2012). The open field test has been shown to be the most valid measure of boldness (Burns 2008) and was therefore used to determine boldness in this study. A high rate of movement and the extent of the utilisation of a novel tank were used as a measure of boldness because it showed the exploratory and risk taking ability of a fish (Burns 2008; Ariyomo and Watt 2012) in an unfamiliar environment. Previous studies have measured boldness and exploratory behaviour (Norton et al. 2011; Wisenden et al. 2011) and found a correlation between the two, which suggests these behaviours are similar. Subjects were placed in a novel tank (48 cm 9 26 cm 9 22 cm), with the base marked into 24 rectangles (each 8 cm 9 5.5 cm) and filled with 3 L of dechlorinated water heated to 26 °C. The number of lines crossed in 180 s after a 60 s acclimation period was recorded for each individual. Individuals that crossed more lines and utilized the inner and outer rectangles on the base of the tank were deemed bold, while those that crossed the fewest lines and did not utilize the inner and outer rectangles on the base of the tank and the tank as a whole were deemed shy. Lighting during the experiments was provided by two 18 W daylight fluorescent tubes placed approximately 34 cm above the tank. Individuals tested for boldness in the open field assays were rested and then tested after 48 h for aggressiveness using the mirror test (Gerlai et al. 2000; Moretz et al. 2007a, b; Ariyomo and Watt 2012). In zebrafish, aggressive acts include nipping, biting and short bouts of fast swimming towards an opponent (Gerlai et al. 2000). The number of aggressive interactions made by a fish towards its mirror image was recorded. Individuals with the most number of aggressive interactions were deemed aggressive Behav Genet (2013) 43:161–167 while those with few aggressive interactions were deemed non aggressive. Size matched males and females were paired up randomly for behavioural traits. Pairs were placed in tanks (23.5 cm 9 12.5 cm 9 17.5 cm) with two layers of marbles on the bottom to serve as a spawning site, and they were left overnight. Pairs were separated at the same time every morning and the eggs that had been spawned between the marbles were pipetted into Petri dishes. Any unfertilized or dead eggs were removed after 24 h. Fish were left for 1 week to recover and they were mated again with different partners so that each male spawned with two females. In total 40 spawnings were conducted resulting in 40 broods. Eggs that had been transferred to Petri dishes were left to hatch. After 15 days, larvae were transferred into tanks (23.5 cm by 12.5 cm by 17.5 cm) on a recirculatory system, with centrally filtered and heated water kept at 27 °C. The fry were fed commercial fry food ad libitum for 8 weeks. At 2 months old, the offspring in the broods were tested for boldness and aggressiveness. For logistical reasons, and to reduce the time taken to test the offspring, if a brood was less than thirty, all were tested, but if a brood was greater than thirty then a subset of twenty individuals were randomly selected and tested for boldness and aggressiveness. This amounted to 482 offspring, approximately 63 % of the offspring. Offspring were not sexed. The number of offspring tested ranged from 3 to 27 within a brood. 163 and aggressiveness were fitted with the default parameters, and the plots showed some autocorrelation. Therefore, models were rerun with longer iterations (Wilson et al. 2010) based on nitt = 650,000, thinning interval = 100, burn in period = 150,000. We checked whether the priors specified earlier had any influence on the outcome of the analysis by dividing the phenotypic variance between the priors of genetic and residual effects, so that a larger proportion was assigned to the genetic effect (0.95) and the rest to the residual (0.05) (Wilson et al. 2010). Rerunning the models showed that the outcome of the analysis was not different from the previous models. Maternal effects (VM) were estimated by adding the maternal identity to the first models specified for boldness and aggressiveness as random effect and we added another prior for a random effect (Kruuk 2004; Wilson et al. 2010) so that VP was further partitioned into VA ? VM ? VR. The posterior distributions of the estimates of the additive genetic (animal), maternal and residual (units) variances were also rerun with the longer iterations used above. Deviance information criteria (DIC) were used to detect the statistical significance of the additive genetic and maternal components of the models. The statistical significance of the genetic estimates (i.e. how different they were from zero) was assessed using 95 % confidence intervals (CI) for the heritability estimates, and the maternal effects were calculated from the posterior distributions using the highest-posterior-density function (HPD interval, library coda; (Hadfield 2010). Statistical analysis Results Data analysis was carried out using the R statistical package version 2.11.2 (R Development Core Team 2011). Data on the boldness and aggressiveness of the parent fish were anaylsed using a two sample t test to compare the personality traits of the male and female parents. Spearman’s rank correlation (q) was used to test whether brood size was correlated with boldness and aggression levels. We estimated the genetic component of the phenotypic variation in boldness and aggressiveness using the animal model, and the whole pedigree (i.e. parents and offspring) was used. We estimated the narrow sense heritability of boldness and aggressiveness (h2) as the proportion of phenotypic variance (VP) that could be attributed to additive genetic variance (VA) (that is, h2 = VA/VP) with univariate animal models using the R package MCMCglmm. We specified the priors for the genetic variance (VA) and residual effects (VR) by splitting the observed phenotypic variance (VP) evenly between the genetic variance (VA) and the residual effects (VR). The posterior distributions of the estimates of the additive genetic (animal) and residual (units) effects for boldness Overall, the adult males were found to be bolder than the adult females (t = 2.816, p = 0.008 (two-tailed), df = 32.38), but there was no significant difference between males and females in aggressiveness (t = -0.555, p = 0.58 (two-tailed), df = 47.08). There was no correlation between brood size and boldness (Spearman correlation: q = 0.61, p = 0.10) or brood size and aggressiveness (Spearman correlation: q = 0.56, p = 0.10). For boldness and aggressiveness, all variance estimates were significantly different from zero (Tables 1, 2) and the posterior DIC comparison with the model versus the restricted genetic model was statistically significant (boldness: 4,518.979—only residuals; 4,478.145—additive genetic and maternal components; aggressiveness: 2,996.9—only residuals; 2,862.7—additive genetic and maternal components). For boldness, the additive genetic variance accounted for 76 % of the total phenotypic variance while the maternal effects accounted for 18 % (Table 1). For aggressiveness, the additive genetic variance accounted for 123 164 Behav Genet (2013) 43:161–167 Table 1 Estimates of the variance components of boldness, the proportion of variances from a univariate model (with maternal identity as a random effect) and their corresponding 95 % confidence intervals Component Variance Var. 95 % CI Prop. Var. Prop. Var. 95 % CI VA 4,149.47 2,990.83, 5,042.77 0.76 = h2 0.49, 0.90 VM 661.52 0.18 0.05, 0.43 VR 341.47 136.65, 3,098.17 107.97, 930.85 0.06 0.02, 0.17 h2 proportion of variance in boldness attributable to additive genetic variance Table 2 Estimates of the variance components of aggressiveness, the proportion of variances from a univariate model (with maternal identity as a random effect) and their corresponding 95 % confidence intervals Component Variance Var. 95 % CI Prop. Var. Prop. Var. 95 % CI VA 13.97 3.09, 36.23 0.36 = h2 0.10, 0.72 VM 3.32 0.75, 8.73 0.09 0.02, 0.19 VR 21.61 9.84, 29.95 0.55 0.19, 0.79 2 h proportion of variance in aggressiveness attributable to additive genetic variance 36 % of the total phenotypic variance in the second model while the maternal effects accounted for 9 % (Table 2). Discussion In this study, male zebrafish were found to be bolder than the females but both sexes were equally aggressive, which is in line with previous findings by Moretz et al. (2007a). However, it appears that detecting sex differences in aggression is a function of the measure of aggression used, and some studies have shown differences in aggressiveness between the sexes (Filby et al. 2010; Paull et al. 2010; Norton et al. 2011; Dahlbom et al. 2011; but see Dahlbom et al. 2012) based on social ranks rather than the mirror test used here and by Moretz et al. (2007a, b). It has been argued that the mirror test may not recreate all aspects of an aggressive encounter because of differences in brain activity and hormonal responses between animals exposed to a mirror image and those exposed to a real opponent (Oliveira et al. 2005; Hirschenhauser et al. 2008; Desjardins and Fernald 2010; Dijkstra et al. 2012). However, these authors seem to agree that the mirror image elicits aggressive responses. The heritability estimate for boldness was found to be high (0.76) while that of aggressiveness was moderate 123 (0.36), and both estimates are comparable to heritability estimates of personality traits in studies conducted on other vertebrates (exploratory scores: great tits, Parus major, h2 = 0.22–0.61, Dingemanse et al. 2002; h2 = 0.10–0.78, Drent et al. 2003; but see Chervet et al. 2011) and invertebrates (boldness: h2 = 0.2–0.8; dumpling squid, Euprymna tasmanica, Sinn et al. 2006). Contrary to our prediction, our results indicate that there were significant additive genetic components underlying phenotypic variation in boldness and aggressiveness in the zebrafish tested. Given that the population used in this study was relatively small and far removed from the original stock, these estimates are still high enough to cause the behavioural traits to evolve in response to selection (Waldmann 2001; Blomberg et al. 2003). In this study, the fact that the heritability estimate for aggressiveness was lower than the heritability estimate for boldness suggests that aggressiveness is under more intense selection in this strain of zebrafish (Hoffmann 1999; Careau et al. 2011). Zebrafish are known for their aggressive behaviour towards conspecifics (Spence et al. 2008; Paull et al. 2010) and aggressive behaviours, such as displays and chases, are used by zebrafish to maintain dominance (Spence et al. 2008; Watt et al. 2011). Being dominant is important in zebrafish because it allows individuals to gain access to territories, mates and resources (i.e. spawning sites and food) (Spence et al. 2008). This means that non-aggressive individuals may not have access to resources and consequently have reduced fitness. Alternatively, the lower heritability estimate for aggressiveness could have been due to high residual variance associated with this trait. Although, we did not partition the residual variance into its components, this high variance is likely to be due to environmental variance not accounted for in this study. Given the nature of aggression and its function in zebrafish, the social environment could have had a more significant impact on the phenotypic variance in this trait (Moore et al. 1997; Wolf et al. 1998, 1999; Wilson et al. 2009; McGlothlin et al. 2010) than for boldness. The high estimate of heritability recorded in this study for boldness may be because in the laboratory there is little or no environmental variation since food and the physicochemical properties of the water are controlled, which reduces the residual variance and so results in high heritability estimates in captive animals (Lush 1949; Falconer and Mackay 1996; Drent et al. 2003; Kruuk 2004). Brood size did not appear to have any effect on boldness and aggressiveness. Our results show significant maternal effects accounting for 18 and 9 % of the proportion variances in boldness and aggressiveness respectively, indicating that the mother has an influence on the development of boldness and aggressiveness in her offspring. From this study, we do not know the relative contributions of genetic and environmental maternal effects to the estimate. In a study conducted on the exploratory-boldness behavioural syndrome in zebrafish, Behav Genet (2013) 43:161–167 Wisenden et al. (2011) found that irrespective of the father’s personality, offspring of exploratory mothers always showed high exploratory behaviour, suggesting that maternal effects for behavioural traits may be commonly found in zebrafish. Significant maternal effects on the expression of behavioural traits of offspring have been shown to occur in a variety of animals (great tits: P. major: Van Oers et al. 2004; sticklebacks: Gasterosteus aculeatus: Giesing et al. 2011) through the deposition of various substances into the eggs, and these effects can persist into adulthood and across generations (Taylor et al. 2012). Zebrafish are egg scatterers that show no parental care (Spence et al. 2008) and so maternal effects in such a system may occur through egg provisioning before spawning (Wright et al. 2003). Studies have shown that the rearing conditions that the mother experiences can influence the degree to which hormones are integrated into her eggs and consequently affect the behavioural phenotype of her offspring (Schwabl 1993; Stratholt et al. 1997; McCormick 1998; Eising et al. 2001; Gil 2008; Leatherland et al. 2010; Storm and Lima 2010; Giesing et al. 2011) in a way that may enhance their fitness. For example, Giesing et al. (2011), in a recent study on three-spined sticklebacks (G. aculeatus), showed that the eggs of mothers exposed to a predator had elevated concentrations of cortisol and the juveniles of predator exposed mothers formed tighter shoals. In conclusion, we have shown that in this population of zebrafish, boldness and aggressiveness have heritable components and so are able to respond to selection. Furthermore, there are significant maternal effects on the expression of these behavioural traits by the offspring. Maternal experience from her interaction with the environment, shaped by natural selection, may cause the transmission of information through the eggs and consequently, directly or indirectly, shape the fitness of her offspring. Thus, maternal effects on offspring phenotype may be adaptive (Heath and Blouw 1998; Mousseau and Fox 1998; Giesing et al. 2011). 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