mise à jour du
14 décembre 2008
Dev Psychobiol
Genetic and Littermate Influences on Yawning
in Two Selectively Bred Strains of Rats
Alejandro Moyaho, Margarita Baraja, Araceli Ugarte, José R. Eguibar
Instituto de Fisiologia Benemerita Universidad Autonoma de Puebla Mexico
Tous les travaux de MR Melis & A Argiolas 
Tous les travaux de M Eguibar & G Holmgren


ABSTRACT: This study was made to separate genetic from postnatal maternal influences on yawning in two strains of Sprague-Dawley rats selected for high- (HY) and low-yawning frequency (LY). Foster mothers of the two strains reared litters of pups in the four possible combinations and yawning was recorded in a novel environment when the adult offspring were 75-day-old. Yawning frequency of males and females was affected by pup strain but not by the strain of the foster mothers, when litter size was made constant; HY adult offspring yawned more than LY adult offspring. Yawning frequency was higher in HY male offspring than in HY female offspring. An interaction term between pup sex and the strain of the foster mothers revealed that while males reared by LY mothers yawned more than males reared by HY mothers, females reared by HY mothers yawned more than females reared by LY mothers. Mean frequency of yawning increased with the sex ratio of HY litters. These findings indicate that genetic and genotype-correlated littermate effects influence yawning frequency of adult offspring in response to a novel environment.
INTRODUCTION Prenatal and postnatal environment and genotype are determining factors in the variation of the behavior of mammals, but the contribution of one factor relative to the other is difficult to quantify because they are confounded during rearing. Even though behavioral differences between animal strains reared in identical conditions should be the result of differences in genotype, they are not; they are still confounded with the prenatal and postnatal maternal environment and with the interaction among siblings.
An approach to separate them is to use cross-fostering of pups between strains, which would reveal the presence of postnatal genotype-correlated maternal effects. Cross-fostering has been used in mice and rats to demonstrate the influence of the maternal environment on behavior that is typically a direct response to stimuli from the environment. For example, behaviors such as emotionality, aggressive behavior, and social dominance, manipulatory and exploratory behavior have been analyzed in cross-fostering studies (Francis, Diorio, Liu, & Meaney, 1999; Ressler, 1963). A maternal effect on developmentally fixed behaviors has seldom been analyzed, perhaps because such behaviors are unlikely to be modified by experience. Previous studies, however, have found that the maternal environment, prenatal and postnatal, has a huge effect on a wide range of physiological and behavioral responses, for example, to stress (Liu et al., 1997; McCarty, Cierpial, Murphy, Lee, & Fields-Okotcha, 1992; Vallee et al., 1997).
These studies suggest that behaviors such as yawning, which is developmentally fixed (Baenninger, 1997) and responsive to stressful events (Moyaho & Valencia, 2002) could be also affected by the maternal environment. Some of the physiological mechanisms of yawning, the neural structures and neurotransmitter systems involved have been studied and identified (Argiolas & Melis, 1998;Collins et al., 2007; Dourish & Cooper, 1990), although other aspects such as its adaptive significance and development are less comprehended (Gallup & Gallup, 2008; Schiller, 2002). It seems that learning is not required for yawning to occur, for human fetus and newborns yawn (De Vries, Visser, & Prechtl, 1982; Sherer, Smith, & Abramowicz, 1991).
However, there is evidence that yawning can in rats vary their frequency and temporal distribution in response to mild stress (Moyaho & Valencia, 2002). This study investigated whether genotype-correlated maternal environment affects yawning in two Sprague- Dawley strains of rats which were selectively bred for high- (HY) and low-yawning (LY) (Urba´ -Holmgren et al., 1990). The HY strain was established by recording yawning of a sample of 2-month-old male rats from which a male that yawned 22 times per hour was crossed with one of his sisters.
Then he was crossed with his F1 daughters. Afterwards the HY strain was maintained by brother &endash; sister mating, selecting HY animals. The LY strain was sustained by brother &endash; sister mating, selecting LY animals (Urba´ -Holmgren et al., 1990). Yawning frequency is highest during the last light hour but feeding is more potent than light in maintaining a daily rhythm in yawning (Holmgren et al., 1991). HY rats also groom more than LY rats in a novel environment (Eguibar & Moyaho, 1997) and show lower scores of emotional reactivity in an open field test (Moyaho, Eguibar, & Dő´az, 1995). Since litter size may have an effect on behavioral and physiological traits of adult offspring (Coutellier, Friedrich, Failing, Marashi, & Wurbel, 2008), this study also investigated the influence of litter size on yawning.
DISCUSSION This study was done to separate postnatal from genetic influences on yawning of HY and LY rats. The main finding was that yawning is influenced by genetic factors but not by the postnatal maternal environment. Yet, the yawning of HY rats increased with male-biased sex ratio of litters. In addition, a sexual dimorphism was found in the yawning of HY rats, which was more frequent in male than in female rats. By contrast, male and female LY rats did not show any difference in yawning frequency, perhaps because the numbers of this behavior in this strain were too low to detect a statistical difference.
The dimorphism in yawning between male and female HY rats indicates that sexual hormones play an important physiological role in the occurrence of this behavior in rats. This suggestion is consistent with the fact that apomorphine-induced yawning decreases in castrated rats and increases using androgenic hormones (Berendsen, 1981). As yawning is affected by the exposure of rats to mild stress events (Moyaho & Valencia, 2002), the difference in the frequency of this behavior shown between males and females may arise from differences in response to a novel environment. In agreement with this possibility is the evidence that male rats are more fearful than female rats when tested using a battery of novel/ threatening tests (Aguilar et al., 2003). Therefore, male HY rats may have yawned more because they are more sensitive to stress than are the females. The finding that males fostered to LY mothers yawned with a greater frequency than males fostered to HY mothers, and that the opposite effect was found for the females, suggests a difference between HY and LY foster mothers in the way they affect the yawning of males and females. This is a gender-related influence which cannot be explained by a mother strain effect, for it did not contribute significantly to the variation in yawning frequency.
These contrasting effects between rat strains can be caused by a genetic source of variation. For instance, variation in behaviors associated with maternal care in mice depends on epistatic interactions (i.e., between alleles at different loci; Peripato & Cheverud, 2002). Hence, variations in the maternal environment provided to male and female offspring could be, in part, caused by genetic differences between HY and LY foster mothers. The specific way in which the two strains of foster mothers influenced distinctly yawning frequency of male and female offspring cannot be established with certainty with the available data, but it is plausible to advance that the amount of care provided by the foster mothers could have differed between the two strains of rats with consequences for offspring's behavior in adulthood. Differences in the amount of care given to male and female pups have been previously reported.
For example, mothers spend more time licking the anogenital region of male than female pups (Moore & Morelli, 1979), possibly for the development of complete copulatory behavior. Similarly, variation in maternal care in rats is associated with individual differences in behavioral responses to stress (Francis et al., 1999). Furthermore, handling during the postnatal stage may later lessen response to stress (Liu et al., 1997). Thus, the differences in yawning frequency between females cared by HY and LY foster mothers and between males cared by HY and LY foster mothers could reflect variations in response to stress, for the adult offspring were observed in a novel environment (i.e., unfamiliar cages).
The fact that litter size, pup sex, and the interaction between pup sex and foster mother had affected yawning, suggests that postnatal environment does affect yawning. This is revealed by the finding that HY male offspring yawned more when the sex proportion was biased for males. Litter-size effects on behavior have been pre- viously reported (Dimitsantos, Escorihuela, Fuentes, Armario, & Nadal, 2007; Rodel, Prager, Stefanski, von Holst, & Hudson, 2008) and an intense competition for milk and maternal care commonly occur among siblings of some mammals during rearing with consequences in adulthood (Drummond, Va´ zquez, Sanchez-Colon, Martőnez-Gomez, & Hudson, 2000).
Yawning of HY adult male offspring could be an enhanced response to a stressful environment. Alternatively, the frequent yawning observed in male-biased litters could be the result of an excessive exposure to masculine factors (e.g., pheromones), a possibility which agrees with the finding of a sexual dimorphism in yawning. In either case, the finding indicates that yawning frequency is affected by postnatal factors. The response of the offspring to the environment provided by the foster mothers was another variable involved in yawning, and the finding that male and female HY rats yawned more frequently than male and female LY rats confirms the genotype-dependent frequency of yawning (Urba-Holmgren et al., 1990).
An unexpected outcome was that yawning scores of HY male rats diminished in the experimental condition of this study as compared to the average number of yawns reported in previous studies (Eguibar & Moyaho, 1997). Two are the reasons which may explain this discrepancy. First, HY male rats in this study were individually housed after weaning, while in the previous studies they were housed in groups. Second, the observation time of yawning in this study (0013 &endash; 1430 h) also differ from the other studies. If the housing condition were the main cause of the difference, it would suggest that yawning requires a social context for it to occur. It is known that lack of social interactions during postnatal care increases anxiety when the rats reach adulthood and are exposed to a novel environ- ment (File & Hyde, 1979).
Actually, housing rats individually after weaning is a strategy to increase sensibility to novelty (Gentsch, Lichtsteiner, & Feer, 1981). Observation time seems not to be a determining factor, but further studies will be necessary to discard this possibility. In summary this study found that yawning frequency can be affected by genetic factors and by the sex ratio of litters, probably as a consequence of the stress produced by male-male competition for maternal resources during rearing. The findings of this study contrast with the idea that yawning is a stereotyped and genetically determined behavior, suggesting a complex interaction between internal and external factors.