Approaching the genomics of risk-taking behavior

Abstract

Individual animals differ in their propensity to engage in dangerous situations, or in their risk-taking behavior. There is a heritable basis to some of this variation, but the environment plays an important role in shaping individuals' risk-taking propensity as well. This chapter describes some of the challenges in studying the genetic basis of individual differences in risk-taking behavior, arguing new insights will emerge from studies which take a whole-genome approach and which simultaneously consider both genetic and environmental influences on the behavior. The availability of genomic tools for three-spined stickleback, a small fish renowned for its variable behavior, opens up new possibilities for studying the genetic basis of natural, adaptive variation in risk-taking behavior. After introducing the general biology of sticklebacks, the chapter summarizes the existing literature on the genetic and environmental influences on risk-taking behavior, and describes the overall strategy that our group is taking to identify inherited and environmentally responsive genes related to risk-taking behavior in this species. Insights gleaned from such studies will be relevant to our understanding of similar behaviors in other organisms, including ourselves.

Figure 4.1

The replicated evolution of risk-taking behaviors in sticklebacks provides a natural experiment for testing candidate genes. This idealized map of Scotland shows the movement of sticklebacks from the ocean (on left) into freshwater rivers following glacial retreat. Sticklebacks inhabiting water bodies with abundant predators independently evolved increased levels of risk-taking behavior (dark fish) compared to sticklebacks inhabiting water bodies without predators (light fish).

Figure 4.2

Individuals vary in their propensity to take risks. This histogram shows the distribution of exploratory movements of individuals in the presence of a predator. Methods: Juvenile sticklebacks from several populations were brought into the lab and the number of times an individual moved during 15 min in the presence of a predator was recorded. Mean=4.6, S.D.=3.39, n =218.

Figure 4.3

Risk-taking behavior in sticklebacks is repeatable. The Y-axis shows the rank order time spent freezing in the presence of a live predator. Time (the observation number) is on the X-axis. Each line represents a different individual; each point represents the measure of that individual on each observation day. Methods: On seven different occasions over the course of 2 months, individual sticklebacks were presented with a live pike and their behavioral response recorded. Repeatability was calculated as in Lessels and Boag (1987), R =0.68, F_6,42 =13, p <0.001. From Bell et al. (2009).

Figure 4.4

There is genetic variation for risk-taking behaviors among families. The data show the mean (±S.E.) number of exploratory movements in an unfamiliar environment of different families from two different populations, Putah Creek (gray) and the Navarro River (black). Methods: The exploratory behavior of lab-reared sticklebacks from 22 different families (2–5 full sibs/family) were measured at 7 months of age. Data were analyzed with a nested ANOVA with family and population as fixed factors (Population: F_21,102 =21, p <0.0001; Family(Population): F_20,102 =2.1, p =0.003).

Figure 4.5

There is a genetic basis to behavioral differences between populations. These data show the standardized mean (±S.E.) number of bites at food while in the presence of a predator for wild-caught parents and their lab-reared offspring from two different populations, Navarro and Putah (Bell, 2005). Methods: The willingness to forage in the presence of a predator was measured on wild-caught adults from the two populations. Full-sib offspring from the two populations were reared under standardized laboratory conditions and measured for willingness to forage in the presence of a predator at adulthood. Both the parents and offspring of fish from Putah Creek took more bites in the presence of a predator (Parents: F_1,75 =14.3, p <0.0001; Offspring: F_1,44 =18.4, p <0.0001).

Figure 4.6

Paternal care improves antipredator behavior. This is Fig. 1 from Tulley and Huntingford (1987). The strength of avoidance shown to a model pike by sticklebacks from the Mar Burn, where predators are abundant, and from Inverleith Pond, where predators are absent with (“N”) and without (“O”) paternal care.

Figure 4.7

Risk-takers have lower serotoninergic activity. Predator inspection was negatively correlated with serotonergic activity, as measured by the turnover of serotonin (5-HT) to its metabolite 5-hydroxyphenylacetic acid (5-HIAA), 15 min after presentation of the predator. From Bell et al. (2007). Methods: Juvenile sticklebacks were measured for their behavioral reaction to a live pike predator and then sacrificed after 15 min, their brains removed and quickly deep frozen. Tissue was homogenized in 4% perchloric acid with an internal standard and monoamines were measured using HPLC with electrochemical detection as in Øverli et al. (1999). The correlation between individual levels of predator inspection and serotonergic activity was statistically significant (r =−0.669, n =9, p =0.049).

Figure 4.8

Breathing rate is an endophenotype for risk-taking behavior. The number of opercular beats in 15 s after handling is positively correlated with predator inspection (Bell et al., 2009). Methods: Individuals were subjected to brief handling stress and the number of opercular beats was counted. At least 24 h after, the fish was presented with a live pike and the number of predator inspections in 15 min was recorded. The partial correlation coefficient (controlling for population) is statistically significant (r =0.211, n =168, p =0.006) and was not related to body size.