Nouvelle étude : comportement agressif des femelles russes et campbell avec des petits

[Sandrine1308 0]

Nouvelle étude super interessante trouvée sur le net sur le comportement agressif des femelles hamsters russes et campbell lorsqu'elles ont des petits.
Les femelles russes sont plus agressives que les campbell.
Les males campbell jouent un rôle essentiel avec les petits, pas les males russes.
Cependant, ils ont noté que laisser le mâle avec la femelle diminue significativement l'agressivité de la femelle lorsqu'elle a des petits chez le hamster russe et campbell.
Les types d'attaque portées sont différents chez le campbell et chez le russe.
Les coups portés par le campbell sont des attaques de type "boxing" (difficile à traduire mais compréhensible même en anglais) à 50% et 50% de morsures sur le ventre et les flancs.
Pour le hamster russe, les attaques sont à mini 90% des morsures sur le ventre et les flancs.
De vrais tites guerrieres les nanas russes !!!

Je vous joins l'étude ci-dessous en anglais, bien longue, mais l'abstract du début (résumé) est assez concis et suffisant.

AGGRESSIVE BEHAVIOR
Volume 31, pages 294–302 (2005)
High Maternal Aggression in Dwarf Hamsters
(Phodopus campbelli and P. sungorus)
Stephen C. Gammie1 and Randy J. Nelson2
1Department of Zoology and Neuroscience Training Program, University of Wisconsin, Madison,
Wisconsin
2Departments of Psychology and Neuroscience, The Ohio State University, Columbus, Ohio
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The defense of offspring, termed maternal aggression, is a highly conserved behavior in mammals,
including rodents. This study examined relative levels of maternal aggression in two closely related
dwarf hamster species, Phodopus campbelli and P. sungorus, that normally inhabit high latitude, boreal
environments. When tested with first litters and with the breeder male remaining with the female (for
P. campbelli the male is necessary for successful rearing of offspring), both species exhibited high levels
of maternal aggression with average duration of aggressive behavior480 sec for a 10 min test. For
P. sungorus, males are not required to rear offspring. P. sungorus females with either one or multiple
litters (singly housed after impregnation) exhibited significantly higher levels of aggression (4300 sec)
relative to females co-housed with the sires. In terms of species differences in attack style, P. campbelli
exhibited a boxing or clawing strategy forB50% of total attack time, but for P. sungorus, this form of
attack occurredo5% of the time. For P. sungorus, attacks to the vulnerable belly and flank
constituted490% of all attacks, but these regions were attacked B50% of the time for P. campbelli.
A survey of levels of maternal aggression of rodents in other genera suggests that maternal aggression
in Phodopus is at the high end of the spectrum. Results of this study suggest that the presence of the
breeder male may actually suppress aggression in P. sungorus. This fact, as well as its high level of
aggression and its distant relationship to mice and rats, suggest P. sungorus as a possible model
for future studies on the neurobiological basis of maternal aggression. The relationship between the
high rates of maternal aggression and life history strategy in Phodopus is discussed. Aggr. Behav.
31:294–302, 2005. r 2005 Wiley-Liss, Inc.
: : : : : : : : : : : : : : : : : : : : : : : : : : : : : : : : :
Keywords: aggression; Phodopus; nest defense; maternal behavior; parental behavior
INTRODUCTION
The protection of offspring in mammals can include fierce aggression against intruders,
termed maternal aggression. In rodents, infanticide by unrelated conspecifics occurs and
aggression (including biting and attacking) towards an intruder is required to protect the
Grant sponsor: National Institute of Health; Grant number: MH 57760 (to R.J.N.); Grant sponsor: National
Institute of Mental Health National Research Service Award MH; Grant number: 12371–01 (to S.C.G.).
nCorrespondence to: Stephen C. Gammie, 1117 W. Johnson St. Department of Zoology, University of Wisconsin,
Madison, WI 53706. E-mail: scgammie@wisc.edu
Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/ab.20087
r 2005 Wiley-Liss, Inc.
pups [Agrell et al., 1998; Wolff 1985, 1993]. Additionally, mouse strains that exhibit high
levels of infanticide toward non-related offspring (such as wild house mice and outbred mice)
also exhibit high levels of maternal aggression [Parmigiani et al., 1999]. In bank voles
(Clethrionomys glareolus) experimental increase in litter size elevates maternal aggression,
suggesting that in some rodent species, the level of parental investment also influences
maternal aggression [Koskela et al., 2000]. Decreased pup mortality is correlated with
increased wounding of the intruder in common voles (Microtus arvalis) [Heise and Lippke,
1997]. These findings indicate an adaptive role of maternal aggression in the protection of
offspring. Maternal aggression, then, likely represents an evolutionary trade-off, where
expression of the behavior can bring harm to the dam, but it can also dramatically increase
the survival and fitness of the offspring [Agrell et al., 1998; Heise and Lippke, 1997;
Maestripieri, 1992].
In addition to the rodent species listed above, maternal aggression has been studied in rats
and mice, including wild and transgenic mice (for review, see Lonstein and Gammie, 2002);
prairie voles (Microtus ochrogaster) [Gammie and Nelson, 2000; Villalba et al., 1997]; and
Djungarian hamsters (Phodopus campbelli) [Vasilieva and Sokolov, 1994]. Only latency to
attack and percent of time aggressive were documented for P. campbelli. Although an
understanding of the neurobiological basis of maternal aggression is being developed in rats
and mice [Lonstein and Gammie, 2002], the identification of an additional rodent species
(ones distantly related to mice and rats) as a model for studying maternal aggression would
provide an excellent opportunity for determining what elements of maternal aggression
circuitry are conserved evolutionarily within rodents. The presence of high levels of maternal
aggression would be an important criterion for a model system.
Phodopus campbelli and P. sungorus, are two related species of dwarf hamster that
inhabit high northern latitudes (B50 degree N latitude for both species). For P. campbelli,
the mean monthly temperatures never exceed 15 1C, the mean temperatures in January
are below
30 1C, and more than half of the annual 210 mm rainfall occurs in July and
August [Wynne-Edwards, 1998]. For P. sungorus, the average temperature never falls
below
20 1C for any month, and the average rainfall is twice that for P. campbelli
[Wynne-Edwards, 1998]. It has been proposed that because of the relatively difficult
reproductive environment and short breeding season, as a genus, Phodopus has the most
compressed reproductive cycle of any mammal [Newkirk et al., 1997]. Within 36 days of first
mating, one litter can become independent, a second litter can be born, and a third litter can
be conceived [Newkirk et al., 1997; Parkening and Collins, 1991]. For P. campbelli the
presence of the sire is critical for successful rearing of offspring in its environment, whereas
for P. sungorus the presence of a sire is not critical. In P. campbelli sires assist during
parturition [Jones and Wynne-Edwards, 2000] and help the dam to dissipate heat [Wynne-
Edwards, 1998].
The correlation of maternal aggression with levels of investment in offspring (described
above) and the limited number of pups produced each year (because of the life history
and compressed reproductive cycle of Phodopus) lead to speculation that Phodopus may
exhibit high levels of maternal aggression. The aim of this study was to examine
maternal aggression in this genus to determine whether Phodopus may be a model system
for studying the neurobiological basis of maternal aggression in future studies. Given
the differences in the role of sires between the two species, it was also important to
determine whether, and if, rearing conditions affected levels of maternal aggression in
P. sungorus.
Maternal Aggression in Dwarf Hamsters 295
METHODS
Animals and Husbandry
Adult dwarf hamsters (P. campbelli and P. sungorus) from breeding colonies were used in
this study. Colonies were originally established from animals obtained from Katherine
Wynne-Edwards (Queens University, Kingston, ON, Canada). Before pairing, animals were
group housed with same-sex siblings. Paired animals were housed in polypropylene cages
(27.87.513 cm) in a colony room with constant temperature and had constant access to
food and tap water. All animals were housed in the same room in LD conditions with a
reverse 15:9 light/dark cycle (lights on 2400h Eastern Standard Time). Males are required for
the rearing of P. campbelli offspring, so breeder males remained housed with females during
lactation. For P. campbelli, 13 lactating females (B2 months old, 1st litter) were tested for
maternal aggression. For P. sungorus, three different groups were tested for maternal
aggression. 1) 13 lactating females (B2 months old, 1st litter) with breeder males housed with
females during lactation (conditions identical as for P. campbelli); 2) 4 lactating females
(B2 months old, 1st litter) with breeder males removed from home cage after females became
pregnant; 3) 11 lactating females (B6 months old, multiple litters—mean=6.1) with breeder
males removed from home cage after females became pregnant.
Maternal Aggression Behavioral Testing and Analysis
On the 8th day postpartum, the pups (and sire, if present) were removed from the home
cage and each female was exposed to a group housed, sexually naive intruder male of the
same species (B2 months old) for 10 min between 0800 and 1200 h. In other rodents, peak
maternal aggression occurs between day 4 and day 10 postpartum [Svare, 1990]. Intruder
males were never used more than once per day, were used forB3 tests each, and did not show
aggression towards dams. The pups (and sire) were removed from the cage 3 min prior to the
female behavioral test and each test session with an intruder male was recorded on videotape
and subsequently analyzed off-line to quantify aggressive behaviors by the female. In mice
and hamsters, removal of the pups from a mother just before an aggressive test does not
diminish the expression of maternal aggression [Siegel et al., 1983; Svare et al., 1981]. All
analyses of behavioral testing were performed by a single individual who was uninformed
about experimental conditions and treatments. Video analysis involved using pen and paper
and stopping and starting the tape for each attack event. The following features were
recorded for each test: latency to first attack, total number of attacks, and total time in
aggressive encounters. Further, the form or site of attack was recorded for each attack
including whether the attack involved clawing/boxing (directed towards the head) or involved
bites to a particular part of the body of the intruder, subdivided into the head/neck, flank, or
belly regions.
Clawing/boxing occurred when the animal was in an upright position and would either
throw single jabs with one paw or throw in quick sequence alternating paws towards the head
of the intruder. In most cases, the clawing/boxing did not result in direct contact with the
intruder. In these studies, all forms of aggression described above were combined to
determine mean time aggressive and latency to first attack was determined from the onset of
the test to the first appearance of any form of aggression that was quantified.
296 Gammie and Nelson
STATISTICAL ANALYSIS
For statistical analysis of behavioral differences among the three P. sungorus groups, a
one-way ANOVA was used. If statistical differences were found, pairwise comparisons were
made using a multiple comparison pairwise procedure (Student-Newman-Keuls method),
for normally distributed data. If the data were not normally distributed, then Dunn’s method
for pairwise comparisons was used. For four tests, maternal aggression testing was
terminated early due to wounding of the intruder. In each case, the number of attacks and
time aggressive was prorated for what would have been a full 10 min test. However, if these
numbers exceeded the highest numbers for that group, the individual was assigned instead the
maximum for that group to maintain a conservative estimate. In each of the four cases, the
prorated amount of aggression exceeded the highest levels assigned for a full 10 min test, so
the more conservative estimate was used. Additionally, the percentage of total time attacking
was determined for each individual and group was also examined. In the case of time to first
bite, if an animal was not aggressive, a time of 600s was assigned (the maximum possible for
the test). Mean differences were considered significant if po0.05.
RESULTS
Phodopus campbelli
Twelve out of 13 P. campbelli females exhibited aggression (93%) (Fig. 1A) and the mean
latency to first attack was B60 sec (Fig. 1B). Animals showed high levels of aggression with
the mean number of attacks greater than 20 (Fig. 1C) and the mean time aggressive greater
than 80 sec (Fig. 1D). The majority of attacks took the form of clawing or boxing the
intruder (B50% of the total attack time), but attacks to the flank, belly, and head/neck
Fig. 1. Levels of maternal aggression in P. campbelli in terms of A) % aggressive; B) time to first attack; C) number of
attacks; and D) total time aggressive. Bars represent means7S.E.M. E) provides a percentage breakdown of total
aggression by either the manner of attack (clawing/boxing towards the head of the intruder) or the site of biting attacks
(flank, head/neck, or belly region of the intruder).
Maternal Aggression in Dwarf Hamsters 297
region were also exhibited (Fig. 1E). For the test that was stopped early due to wounding of
the intruder, the female attacked the male for 153 out of 168 sec. The mean percentage of
total test time spent attacking the intruder was 13.177.1. In terms of number of pups, P.
campbelli had an average litter of 5.370.47.
Phodopus sungorus
P. sungorus females that remained co-housed with the breeder male (as were P. campbelli
females) also exhibited high levels of maternal aggression. Eleven of 13 females exhibited
maternal aggression (Fig. 2A), the mean number of attacks were B5 (Fig. 2C), and the mean
time aggressive was greater than 85 sec (Fig. 2D) for the 10 min test. The mean percentage
of total test time spent attacking the intruder was 15.776.1. In terms of number of pups,
P. sungorus had an average litter of 5.570.31.
Removal of the male after impregnation in P. sungorus, though, resulted in a significant
elevation of maternal aggression in three measures of aggression. In terms of time to first
attack, females with the first litter with the mate removed attacked in a significantly shorter
period of time than first litter females with the male co-housed (Fig. 2B). Both females with
the first or multiple litters exhibited a higher mean number of attacks relative to first litter
females with the breeding male co-housed (Fig. 2C). Further, mean time aggressive was
Fig. 2. Levels of maternal aggression in P. sungorus in terms of A) % aggressive; B) time to first attack; C) number of
attacks; and D) time aggressive for three different treatments: (1) 1st litter with breeder male remaining in home cage
(except during testing) (white bars); (2) 1st litter with breeder male removed from home cage following impregnation of
female (black bars); and (3) females with multiple litters with breeder male removed from home cage after impregnation
of female (hatched bars). Bars represent means7S.E.M. E) provides a percentage breakdown of total aggression by
either the manner of attack (clawing/boxing towards the head of the intruder) or the site of biting attacks (flank, head/
neck, or belly region of the intruder). n=Po0.05; nn=Po0.01; one-way ANOVA.
298 Gammie and Nelson
significantly higher for females from either group with the breeder male removed relative to
first litter dams with the breeder male co-housed (Fig. 2D). No differences were observed in
any of these measures between first and multiple litter dams when the breeder male was
removed following impregnation. Three tests were terminated early due to wounding of the
intruder male. For all three females it was their first litter and the mated male had been
removed following impregnation of the female. For these three tests, the time attacking the
male out of the total test duration was: 126/130 sec; 220/233 sec; and 170/174 sec. The mean
percentage of total test time spent attacking the intruder was 52.076.6 for females with first
litters and the pups removed and 63.677.6 for females with multiple litters and the male
removed.
In P. sungorus, belly and flank were the predominant sites of attacks (Fig. 2E) and there
were no significant differences between the three groups in terms of percentage of attacks
towards different regions (P40.05, one-way ANOVA).
DISCUSSION
P. campbelli and P. sungorus exhibited comparable high levels of maternal aggression
(mean time aggressive480 sec for both) when the mated males remained co-housed with the
females. The main distinction between the two species was observed in the pattern of attack.
For P. campbelli, the majority of attacks involved clawing or boxing the intruder, but for
P. sungorus (across all three groups), clawing or boxing comprised B4% of the attacks
(Figs. 1E and 2E). In contrast, for P. sungorus (across all three groups) B93% of the attacks
hit either the belly or flank region. It is difficult to speculate why differences in attack style
exist between these species. P. sungorus females normally mate successfully with multiple
males, dominate males, and form stable intra-sexual dominance hierarchies, whereas
P. campbelli females remain in stable socially-monogamous relationships [Wynne-Edwards
and Lisk, 1987]. The differences in attack approach could relate to the different social structure
or it could have developed as a result of genetic drift and isolation of the two species.
Males of P. campbelli, but not males of P. sungorus, assist in the delivery and care of pups
[Scribner and Wynne-Edwards, 1994; Wynne-Edwards and Lisk, 1987]. The continued
presence of P. sungorus males in the home cage following impregnation does not affect pup
survival [Wynne-Edwards, 1998; Wynne-Edwards and Lisk, 1987]. However, results suggest
that although the presence of the male does not alter pup survival, it likely has a significant
negative effect on the full expression of maternal aggression. In terms of latency to attack,
number of attacks, and mean time aggressive (Figs. 2B–2D), maternal aggression was
elevated in females housed singly, compared to those that remained housed with their mate,
even if all other test conditions, including litter number, were identical. Application of
stressors to mice decreases levels of maternal aggression [Maestripieri et al., 1991; Pardon
et al., 2000], leading to speculation that the lower levels of maternal aggression in P. sungorus
females that remained co-housed with the breeder males may reflect an elevated stress
response in the dams produced by the male. The extent to which glucocorticoid levels in
lactating females are affected by the continued presence of a mated male, however, requires
further studies.
This study did not test a group of females with multiple litters in which the sire remained
with the dam, so therefore we cannot determine whether it was lack of the sire or the effect of
multiple litters that contributed to the high levels of maternal aggression in these dams. One
Maternal Aggression in Dwarf Hamsters 299
additional caveat is that P. sungorus females that remained co-housed with males may have
been pregnant. Postpartum estrus occurs onBpostpartum Day 0, so at the time of testing the
dams may have been in the early stages of gestation and the hormonal changes due to
pregnancy might have altered aggression. Whether or how pregnancy might influence levels
of maternal aggression in P. sungorus would need to be determined in future experiments.
Relative Maternal Aggression Between the Genus Phodopus and Other Genera
Phodopus exhibited high levels of maternal aggression (80–300 sec for a 10 min test). It is
difficult to conduct a meta-analysis of levels of maternal aggression across a range of rodent
species because of variability in testing procedures (e.g., duration of test), scoring procedures
(e.g., measures of aggression analyzed), intruder characteristics (size, sex, and age), and
housing conditions (including light cycles). Additionally, for rodents that were originally
caught from the wild, the duration or number of generations in captivity varies. The species
in this study have been maintained in the laboratory since 1990. Yet another source of
variability is the test date during lactation. For some species, such as Syrian hamsters
(Mesocricetus auratus), test day does not influence levels of aggression [Siegel et al., 1983], yet
for other species, including mice, peak aggression occurs between postpartum days 4 and 10
[Svare, 1990]. Given these caveats, though, the levels of maternal aggression in both
Phodopus species are at the high end compared with rodents in other genera. For example, for
a 10 min test, the following mean durations of maternal aggression have been reported for the
following species or strains: C57 mice, from 20 sec to 35 sec [Gammie et al., 2000; Gammie
and Nelson 1999]; outbred CD–1 mice, B30 sec [Ferrari et al., 2000]; wild mice (fourth
generation in lab), B150 sec, [Ferrari et al., 2000]; prairie voles, B40 sec [Gammie and
Nelson, 2000]; bank voles, B40 sec on day 3 of lactation and B20 sec on day 8 [Koskela
et al., 2000]; and rats, B35 sec [Flannelly et al., 1986]. Unfortunately, for a large number of
studies on maternal aggression in rodents, the total time aggressive by the female is not
reported. Similar to our findings, the previous study on maternal aggression in P. campbelli
reported a latency to first attack of 84 sec and all females exhibited aggression [Vasilieva and
Sokolov, 1994]. As indicated above, though, other measures of aggression were not examined
in that study. For maternal aggression in Syrian hamsters, B20 attacks for a 10 min period
were reported for three studies [Siegel et al., 1983; Wise, 1974; Wise and Pryor, 1977]. These
numbers are consistent with the number of attacks seen for the two hamster species in this
study. However, because those studies on hamsters did not report the mean time aggressive, it
is difficult to know whether overall levels of aggression were similar between the dwarf and
Syrian hamsters.
In many rodent species (for example, prairie deer mice and prairie voles), non-lactating
females also exhibit aggression, but the intensity is far less than for maternal females [Ayer
and Whitsett, 1980; Bowler et al., 2002]. Additionally, most studies on non-maternal
aggression report either latency to attack or an aggression score, but not mean time
aggressive. Therefore, comparisons of levels of maternal aggression in Phodopus to other
forms of female aggression in different species is difficult.
Phodopus as a Model for Studies of Maternal Aggression
Findings of high maternal aggression in Phodopus are consistent with the hypothesis that
with elevated parental investment and subsequent increased direct fitness per offspring,
maternal aggression increases. Given the high levels of maternal aggression (4300 sec mean
300 Gammie and Nelson
time aggressive, depending on condition, for a 10 min test), P. sungorus may prove to be an
ideal model for studies of the neural basis of maternal aggression. Additionally, the relatively
stable number of offspring and short gestation time in P. sungorus would act to decrease
variability in other maternal behaviors and to provide rapid resources for neurobiological
analysis. From a comparative perspective, studies of Phodopus are extremely useful because
they are distant relatives to mice and rats (the subjects of most studies on maternal
aggression). Thus, P. sungorus may provide an opportunity as an outgroup to test any
hypothesis generated in mice and rats and allow for an examination of whether or how, with
conserved behaviors, the neural basis of that behavior is conserved. Additionally, further
comparisons between P. sungorus and P. campbelli could be made to determine the neural
basis for the different forms of attacks used by two closely related species.
ACKNOWLEDGMENTS
The authors thank Kyle Blake, Marvin Chang, Justin Friske, Steve Kinsey, and Lindsay
Theis for technical assistance.
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