- 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.
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-
- 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).
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- 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).
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- 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.
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