Paternal Behavior and Offspring Aggression

نویسندگان

  • Catherine Marler
  • Brian C. Trainor
  • Ellen Davis
چکیده

Aggression can have a critical impact on the functioning of societies. Some aspects of aggression have received considerable attention, such as links between parenting behavior and offspring aggression in humans. Although acknowledged as being important to the understanding of human aggression, animal aggression has been relatively unstudied. Recent mammalian animal research is emerging that addresses issues relevant to the study of parenting and aggression. This has been accomplished primarily by focusing on nontraditional mammalian model systems. We integrate human and nonhuman animal studies to (a) further elucidate the potential impact that the behaviors of fathers have on offspring aggression, (b) study the influence of paternal behavior on the behavior of offspring and transfer of aggression across generations, and (c) explore neural and physiological underpinnings for variation in paternal behavior and aggression. KEYWORDS—aggression; paternal behavior; arginine vasopressin; testosterone; progesterone The developmental origins of aggression have long been a subject of discussion in psychology. There is a widespread belief that the behavior of parents has potent effects on aggression in their offspring, but the vehicle for these effects is usually unclear. An important research priority is to identify the biological mechanisms that underlie and help guide changes in both aggression and parental behavior, particularly in response to social conditions. We have identified particular aspects of parental behavior that have a strong long-term influence on the aggressive behavior of their offspring and have identified the mechanisms through which this influence occurs in an animal species. AGGRESSION AND PARENTING IN HUMANS The most extensive research on associations between parental and offspring behavior has focused on human maternal behavior. Child abuse and neglect by mothers have both been associated with higher levels of offspring aggression (Serbin & Karp, 2004). Furthermore, a positive association has frequently been found between offspring aggression and such parental behaviors as restrictive discipline. In comparison, a more responsive or warm style of mothering has been associated with lower levels of aggression. Paternal behavior also has emerged as a strong predictor of offspring aggression. For example, harsh parenting has been found to have a stronger effect on children’s aggression when it originates from the father than when it originates from the mother (e.g., Chang, Schwart, Dodge, & McBride-Chang, 2003). Overall, offspring aggression has been found to be negatively associated with warmer parenting styles and positively associated with harsh or restrictive discipline. Recently, researchers have begun investigating whether parental behaviors and aggression can be transmitted behaviorally across multiple generations. For example, harsh and punitive parenting has been found to transfer across generations, possibly through learning, and has been associated with high aggression levels in subsequent generations (Serbin & Karp, 2004). This far-reaching impact of parenting behavior on subsequent generations can potentially influence the functioning of societies. A NEED FOR CAUSAL ANIMAL-MODEL SYSTEMS Animal studies are important for establishing the behavioral, physiological, and neurological mechanisms underlying variation in paternal and aggressive behaviors, largely because of the difficulties in experimentally altering those mechanisms over a long period of time in humans (Serbin & Karp, 2004). Because paternal involvement in raising offspring is rare among mammals, the impact of the father’s behavior on paternal and aggressive behavior of offspring has been understudied. However, rodent species in which both parents care for offspring, such as the prairie vole (Microtus ochrogaster) and the California mouse Address correspondence to Catherine Marler, 1202 West Johnson Street, Psychology Department, University of Wisconsin, Madison, Wisconsin 53706; e-mail: [email protected]. CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE Volume 14—Number 3 163 Copyright r 2005 American Psychological Society (Peromyscus californicus), are emerging as valuable model systems, particularly for studying the physiological andneurological bases of paternal behavior. Studies of these animals complement those that have investigated the role and biological underpinnings of maternal behavior. BEHAVIORAL MECHANISMS UNDERLYING CHANGES IN PATERNAL OR AGGRESSIVE BEHAVIORS The most extensive studies of how parental behavior affects offspring behavior have examined, at a physiological and neural level, the influence of maternal licking and grooming on stress reactivity in rat pups (Meaney, 2001). Interestingly, these maternal behaviors are transferred nongenetically across generations; rats raised by mothers that expressed less maternal care showed less maternal care as adults even when the mothers were not directly related to them genetically. However, animal studies have neglected to examine changes in offspring aggressiveness in response to such maternal behaviors as licking and grooming. One recent correlational study suggested that maternal huddling with pups and grooming of pups may decrease aggression of adult male offspring when individuals encounter other males in neutral or unfamiliar territory, but does not decrease aggression in resident males when they encounter an intruder in their home cage or territory (Bester-Meredith & Marler, 2003). Neutral-arena aggression tests may be more stressful for the animal in question than resident–intruder tests are for residents, and therefore changes in maternal huddling and grooming may influence neutral-arena aggression. This will be an interesting target for further research. Only recently have animal models focused on how paternal behavior influences offspring aggression and whether resident– intruder aggression can be transferred across generations nongenetically via paternal behavior, particularly pup retrievals. Retrievals back to a nest or away from danger may be a protective style of parenting analogous to protective behaviors found in primates (Fairbanks, 1996). Alternatively, they may be a rougher style of parental behavior, as pups are grasped just behind the forelegs and lifted off of the ground and can be brought back to the nest or to some other location. Studies have revealed that male California mice raised by the less paternal and less aggressive white-footed mouse display less aggression and fewer pup retrievals as adults than those raised by their own species, without a difference in paternal huddling or grooming behavior towards pups. In California mice, there is a positive association between adult-offspring resident–intruder aggression and paternal retrievals but not other paternal behaviors (Bester-Meredith & Marler, 2003). Furthermore, artificially increasing paternal pupretrieval behavior (by placing pups outside of the nest) without causing a change in paternal huddling/grooming behavior increases resident–intruder aggression of both male and female pups (Frazier, Cravens, Trainor, & Marler, 2005). Thus we have identified how a specific paternal behavior can influence offspring aggression in California mice. The data suggest a difference between paternal behaviors such as pup retrievals and other paternal behaviors such as huddling and grooming in their effects on offspring behavior. In the retrieval manipulation study discussed above, we also decreased paternal huddling and grooming in a subset of animals by castrating the males (Marler, Bester-Meredith, & Trainor, 2003; Frazier, Cravens, Trainor, & Marler, 2005). This manipulation of the fathers caused an increase in corticosterone (a stress hormone) in the adult male offspring (Frazier, Cravens, Trainor, & Marler, 2005). Such a result would be predicted in light of studies by Meaney and colleagues demonstrating that a decrease in maternal huddling and grooming can affect the stress responsiveness of offspring (Meaney 2001). Castrating the fathers did not alter resident–intruder aggression of the offspring. In contrast, while the retrieval manipulation altered resident–intruder aggression, it did not alter corticosterone levels of offspring. The independence of these paternal behaviors in their effects on offspring is further supported by the finding that the frequency of pup retrievals is statistically independent of the frequency of other parental care behaviors such as huddling and grooming (Marler et al., 2003). These data suggest that paternal retrievals may influence offspring resident–intruder aggression independently of huddling and grooming. As mentioned earlier, however, changes in paternal huddling and grooming may influence aggressive responses to stress in adult offspring. The effect of retrievals on aggression may go beyond a single generation. Male California mice that were raised by whitefooted mice and were therefore exposed to fewer paternal retrievals during development also retrieved their own pups less (reviewed by Marler et al., 2003). Some paternal and aggressive behaviors are positively correlated in males (Marler et al., 2003). Based on these studies, we predict that future generations exposed to fewer paternal retrievals will also be less aggressive. We hypothesize that certain parental and aggressive behaviors are positively associated and are perpetuated from generation to generation. Future studies investigating physiological or neurological mechanisms mediating this effect in California mice may prove valuable as an animal model for understanding the underlying mechanisms for the intergenerational transmission of aggression in humans. NEURAL AND PHYSIOLOGICAL MECHANISMS UNDERLYING CHANGES IN PATERNAL AND AGGRESSIVE BEHAVIORS To understand human parenting and aggression, it will be of the utmost importance to integrate animal behavioral studies with studies of the biological mechanisms underlying changes in paternal and aggressive behaviors. The simplest set of mechanisms for shaping aggression and paternal behavior within the same sex and species would be hormones or neurochemicals that 164 Volume 14—Number 3 Paternal Behavior and Offspring Aggression

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تاریخ انتشار 2005