Yolk testosterone modulates persistence of neophobic responses in adult zebra finches, Taeniopygia guttata
Introduction
In many animal species including humans, behavioral phenotype often varies individually (e.g. Boissy, 1995, Gosling, 2001, Sih et al., 2004). Identifying the underlying mechanisms for inter-individual differences in behavior is of crucial importance for the understanding of how variation in individual behavior is maintained within animal populations. Individual differences in behavioral patterns in many animal species are known to be under the control of genetic factors (Øverli et al., 2002, Drent et al., 2003, van Oers et al., 2004, Fairbanks et al., 2004, Dingemanse and Réale, 2005). However, there is increasing evidence that the development and expression of individual behavior is also strongly affected by non-genetic, maternal influences (e.g. Clark and Galef, 1995, Forstmeier et al., 2004, van Oers et al., 2004, Crews and Groothuis, 2005). One mechanism through which mothers can influence offspring behavior is maternal programming through hormones. Exposure to maternal steroid hormones during embryonic development is well known to have organizing effects on brain and behavior in many vertebrates (Clark and Galef, 1995, Collaer and Hines, 1995, Rhen and Crews, 2002). In birds, yolk androgens have been shown to influence boldness and competitive behavior of chicks (Eising and Groothuis, 2003, Daisley et al., 2005, von Engelhardt et al., 2006) as well as social dominance and sexual behavior in adults (Strasser and Schwabl, 2004, Eising et al., 2006). However, the organizational effects of egg steroids on adult behavior are still not very well known. Given that hormones often act on various target tissues (e.g. Ketterson and Nolan, 1999), they have the potential to modify the organization of a wide array of different behaviors. One important aspect is the role of androgens in controlling the persistence of specific behavioral patterns. Studies on poultry show that intramuscular administration of T in young chicken increases their persistence of attention to particular stimuli but reduces their ability to adjust to a new situation (e.g. Andrew and Rogers, 1972, Rogers, 1974, Andrew, 1975). We hypothesized that yolk androgens could have a similar organizational effect on persistence behavioral patterns and the ability to shift attention in adult birds.
In this study, we therefore examined long-term effects of yolk testosterone (T) on neophobia and its persistence in adult zebra finches (Taeniopygia guttata). Previous work on this species has shown that there is considerable variation in the amount of androgens deposited within and among clutches (Gil et al., 1999, Rutstein et al., 2005, Gilbert et al., 2005). Differential androgen transfer with respect to mate attractiveness or diet (Gil et al., 1999, Rutstein et al., 2005, Sandell et al., 2007) and sex-specific effects of yolk androgens on offspring begging and growth (von Engelhardt et al., 2006) suggest strategic investment and hence maternal programming in zebra finches. Neophobia, i.e. the fearfulness towards novel situations or stimuli, influences behavioral flexibility and has therefore been suggested to be an important factor affecting the ability to colonize new areas (e.g. Greenberg, 1990, Martin and Fitzgerald, 2005). Moreover, individual differences in neophobia are likely to translate into differences between behavioral phenotypes since neophobia is known to be correlated with other behaviors such as dominance or learning (e.g. Verbeek et al., 1996, van Oers et al., 2003, Boogert et al., 2006).
We experimentally manipulated yolk hormone levels in zebra finch eggs by in ovo injection of either T dissolved in sesame oil (T-eggs) or sesame oil only (control eggs). Offspring hatched from either T-or control eggs were subjected to a sequential series of behavioral tests in which we measured the reaction towards novel food, habituation to novel food and reaction to the a novel object when introduced after habituation. Sequential testing allowed us to compare learning effects between the treatment groups. Introduction of a novel object after some period of habituation enabled us to study how a learned behavioral pattern would change in case of a disturbance.
Section snippets
Animals and housing
Birds subjected to egg treatment and behavioral tests (see below) were bred in the laboratory facilities at Lund University, Sweden. The birds were maintained under constant light (14 L:10 D cycle) and temperature conditions (20 ± 2°C). Commercial finch seed, cuttlebone and water were provided at libitum. Juveniles were removed from their natal cages at 45–55 days of age and housed unisexually in cages (80 × 40 × 80) with 4–5 birds per cage. Individuals assigned to the same cage were matched with
Response to novel food and habituation
Body mass at the beginning of the experiment did not differ between treatment groups, but females weighed slightly more than males (egg treatment, F1,35.7 = 0.61, p = 0.44; sex, F1,32.8 = 5.09, p = 0.031; egg treatment × sex interaction, F1,28.9 = 0.34, p = 0.56). Seventy-eight percent of the variation in individual body mass was explained by the effect of sharing the same biological mother (χ2 = 14.7, df = 1, p < 0.001).
In the first trial, the latency to approach did not differ significantly between T- and
Acknowledgments
We thank Kent Andersson, Marina Arbetman and Marcus Ljungqvist for helping with data collection and assistance with animal caretaking. We thank three anonymous for comments that significantly improved the quality of the manuscript. The study was financed through grants from the Swedish Research Council (to M.S.). The experiment was approved by the Malmö/Lund ethical committee for animal research.
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