Personality in captivity: More exploratory males reproduce better in an aviary population

Highlights

• We assayed the exploratory behaviour of zebra finches in a social foraging context.

• We then assessed their reproductive behaviour in a social aviary over 72 days.

• More exploratory males made more breeding attempts and raised more nestlings.

• Extra-pair paternity and the tendency to breed were not related to personality.

• Our results suggest that personality influences an important aspect of fitness.

Abstract

The existence of animal personality is well-established across a wide range of species, with the majority of evidence for this being obtained from individuals held in captivity. However, there has been little work assessing the influence of commonly-measured personality traits on fitness, which is pertinent when the genetic basis of personality is considered. We measured whether the reproductive behaviour and success of zebra finches in a captive mixed-sex aviary environment was influenced by an aspect of their personality, their exploratory behaviour in a single-sex social aviary. We found that more exploratory males made a greater number of breeding attempts and raised more nestlings than less exploratory males. These results were not confounded by extra-pair paternity, which was not related to personality, or by the individuals that did not initiate any reproductive attempts at all. Our work provides evidence that attributes of personality may influence the degree to which individuals cope with, and thrive in a captive environment and this should be accounted for in both experimental design and the interpretation of results. Furthermore, this suggests that there may be selection on these traits as part of the domestication process.

Introduction

Personality is defined as inter-individual differences in behaviour that are consistent over time and/or context (Carere and Maestripieri, 2013). Much work has been conducted on measuring animal personality in captivity (Carere and Maestripieri, 2013), but there has been little focus on relating these personality differences to fitness attributes, despite the known genetic basis of variation in personality traits between individuals (van Oers et al., 2005). Personality differences in the wild have been hypothesized to be maintained when they contribute to consistent individual differences in life history traits such as productivity, reproductive success, growth and survival but trade-offs occur between these traits (Réale et al., 2007, Stamps, 2007); for example, one personality type might generally lead to higher reproductive success but also lower survival (Biro and Stamps, 2008). Moreover, the pace-of-life syndrome hypothesis (Réale et al., 2010), predicts that proactive individuals (which tend to display personality traits such as high exploratory and risk-taking behaviour) are more likely to maximize current over future reproduction than reactive individuals (Wolf et al., 2007). A meta-analysis of work comparing personality with fitness (Smith and Blumstein, 2008), found that both in captivity and the wild, bold individuals had reduced survival compared with shy individuals. However, in captivity, individuals are usually not subject to predation risk and often receive resources such as food ad libitum (McPhee, 2003), which may allow, all else being equal, the bold individuals to prosper and pass on this trait to their offspring (Roberts et al., 2011). In support of this hypothesis, Smith and Blumstein's (2008) meta-analysis found a small positive effect of boldness on reproductive success for captive/domesticated populations but not wild populations which was higher in males but significant in both sexes. Interestingly, no effect of exploratory behaviour on reproductive success was found in the meta-analysis, but only a small positive effect on survival (Smith and Blumstein, 2008). However, the relationships between personality traits and fitness attributes may vary from species to species and in different environments or situations. In wild great tits Parus major, for example, both survival and reproductive success have been shown to be linked to exploratory behaviour, but these relationships vary dependent on an individual's sex and the environmental conditions (Dingemanse et al., 2004). Moreover, in female North American red squirrels Tamiasciurus hudsonicus, activity in a captive novel environment (exploratory behaviour) was found to be negatively correlated with survival in the wild (Boon et al., 2008).

In the zebra finch Taeniopygia guttata, breeding behaviour is a major area of focus, with breeding experiments conducted in small breeding cages or aviaries (Griffith and Buchanan, 2010). Typically, studies utilize sub-sampling by focusing only on those individuals that manage to breed, with unsuccessful breeders not contributing to experimental datasets (especially for the research focused on reproductive behaviour or physiology) and not contributing to the next generation of laboratory stock. However, in any one experiment, the propensity of individuals to breed, which partner they select to breed with or the comparative number of offspring produced may be linked to their personality, leading to bias in the experimental design, and potentially in the interpretation of results, particularly with respect to attempting to relate experimental results back to adaptive outcomes in wild populations. Schielzeth et al. (2011) found that in the zebra finch, the repeatable personality trait neophilia, or speed of approach to a novel object, was not significantly correlated with overall reproductive success, promiscuity or extra-pair paternity in captive aviaries. However, manipulating the sex ratios in the aviaries was found to influence the correlations between neophilia and the proportion of extra-pair paternity, suggesting that neophilia is tied in with variation in reproductive strategies, especially in males. Furthermore, exploratory behaviour has been shown to influence partner-selection specificity and consistency in the female zebra finch (David and Cézilly, 2011). Two previous studies in birds have shown that socially monogamous pairs with more similar (assortative) levels of the two personality traits (exploratory behaviour and aggression), tended to raise foster offspring in better condition than pairs with dissimilar (disassortative) personalities (Both et al., 2005, Schuett et al., 2011a). Moreover, in one zebra finch study when both members of a pair had high levels of exploration and aggression, they raised offspring in a better condition than any other pair combination (Schuett et al., 2011a). Finally, when given the opportunity to choose between mates, female zebra finches have been shown to select males on the basis of their exploratory behaviour per se (considering their own personality in their choice), with intermediate or highly exploratory females preferring apparently highly exploratory males (Schuett et al., 2011b). Such studies therefore indicate the potential importance of personality variation to reproductive success in the short-term.

Here, we examined the extent to which the breeding success of zebra finches in a common captive environment, a large outdoor aviary, was influenced by their exploratory behaviour. Prior to our breeding trial, we measured exploratory behaviour in a social foraging context in the same aviary environment, but in different social groups. Second, we measured the reproductive success of the behaviourally tested pairs. Following the predictions of the pace-of-life hypothesis (Réale et al., 2010), we predicted that the more exploratory individuals would have greater reproductive success in the aviary. Our work builds on previous work (Schuett et al., 2011a), by considering zebra finches breeding in a larger captive environment in which inter-individual competition and positive and negative social interactions can take place as they do in wild free-living populations of this species (Mariette and Griffith, 2013, Zann, 1996).