Intrauterine position modulates maternal behaviors in female mice

Intrauterine position (IUP), the proximity of a fetus relative to same and opposite sex fetuses, is a reliable predictor of the direction and intensity of social and regulatory behaviors in adult male and female mice. In the present experiment, female Rockland-Swiss (R-S) mice who had resided in utero between two females (OM) and females who had resided between two males (2M) were compared with respect to five indices of maternal behavior: Spontaneous parental responses exhibited toward neonates; nestbuilding during pregnancy; aggression during pregnancy; aggression during lactation; and reproductive/lactation performance. There was no significant difference between 0M and 2M females in their spontaneous parental responses toward neonates or their level of nestbuilding behavior during pregnancy. However, when tested for aggression during pregnancy and lactation, 2M females exhibited aggression on a greater number of test days during pregnancy than did 0M females. Also, during pregnancy and lactation, 2M females displayed more lunges and attacks toward adult male intruders than 0M females. Although 0M females tended to have larger litters than 2M females, the animals did not differ with respect to any other measure of reproductive/lactation performance. Intrauterine position, therefore, modulates some aspects of maternal behavior but apparently not others.     

Effects of preweaning nutrition on weight gain during pregnancy in mice

Previous work has shown that preweaning litter size affects the response of adult mice to dietary induced obesity, with animals reared in small litters showing increased hyperphagia and weight gain. The present work addressed whether a similar effect would be seen in the weight changes normally accompanying pregnancy and lactation. B6D2F2 mice were reared in small (4), medium (8) and large (12) litters. Adult females from each of these conditions were mated with males from medium litters and their body weight and food intake measured throughout pregnancy and lactation. Food intake increased during pregnancy and correlated with the dams' litter size, but the amounts consumed by all groups appeared similar. This was also true of maternal weight gain during pregnancy, pup weight and litter size. During lactation, the only differences were that animals which had been reared in large litters ate more food and weaned heavier pups than those in medium litters. These results differ from those previously obtained on dietary induced obesity, supporting different regulatory mechanisms in the two conditions.     

Sex hormones differentially influence voluntary running activity, food intake and body weight in aging female and male rats

The aim of this study was to examine the longer-term effects of reduced gonadal hormones on food intake, food efficiency, voluntary running activity and body weight in mature male and female rats, compared to age-matched controls. We hypothesized that hormonal effects would differ for rats that were not rapidly growing and our results are consistent with this hypothesis. 6-8?month male and female rats were divided into four groups: Female and male control groups and a female and male experimental group. Control groups were intact for 46?weeks. Experimental groups were intact during Phase I (16?weeks), ovariectomized or orchidectomized during Phase II (20?weeks), and received estrogen or testosterone hormone replacement therapy (HRT) during the final Phase III (10?weeks). Food intake and running distance were monitored daily and body weight was recorded weekly for 46?weeks. Contrary to findings for young and growing animals, we did not observe a (1) stabilization of food intake in female rats following OVX, (2) loss of body weight with ORX in males, or (3) complete restoration of running activity in ORX males given testosterone, compared to females given estrogen. Feeding efficiency was not affected by aging in females or males. Loss of estrogen increased energy intake whereas reduced testosterone in males resulted in a negative energy balance. Findings suggest variable hormonal effects for aging male/female rats.     

Comparative and evolutionary dimensions of the energetics of human pregnancy and lactation

The purpose of this article is to compare the energetics of reproduction for human and other primates in order to evaluate the extent to which human reproductive energetics are distinct from other primates and other large‐bodied placental mammals. The article also evaluates the energetics of human and primate gestation and lactation using data from a variety of different populations living under different environmental circumstances. Energetics refers to energy intake and expenditure, and changes in body fat stores. Human and nonhuman primates have longer periods of gestation and lactation and slower prenatal and postnatal growth than other mammals of similar size. This reduces daily maternal energy costs. The development of sizable fat stores is not unique to humans, but fat stores are typically greater in human females and may play a greater role in reproduction. The strategies used to meet the energy costs of pregnancy vary among populations of humans and nonhuman primates and among humans interindividual variability is high. In pregnancy, some increase energy intake but others apparently do not. Increases in metabolic efficiency are evident in some human populations, whereas decreases in physical activity occur, but are not seen in all human or primate populations. Lactation is more energetically costly on a daily basis among humans and nonhuman primates, but has not been as well studied. It appears that both nonhuman and human primates tend to increase energy intake to meet in part the cost of lactation. They also use other strategies such as relying on body tissue stores, reductions in physical activity, and/or increases in metabolic efficiency to meet the remainder of the cost. It is also clear that human females in different populations and different women in the same population use a different combination of strategies to meet the cost of lactation. Am. J. Hum. Biol. 14:584–602, 2002. © 2002 Wiley‐Liss, Inc.     

Energetic consequences of being a Homo erectus female

Body size is one of the most important characteristics of any animal because it affects a range of behavioral, ecological, and physiological traits including energy requirements, choice of food, reproductive strategies, predation risk, range size, and locomotor style. This article focuses on the implications of being large bodied for Homo erectus females, estimated to have been over 50% heavier than average australopithecine females. The energy requirements of these hominins are modeled using data on activity patterns, body mass, and life history from living primates. Particular attention is given to the inferred energetic costs of reproduction for Homo erectus females based on chimpanzee and human reproductive scheduling. Daily energy requirements during gestation and lactation would have been significantly higher for Homo erectus females, as would total energetic cost per offspring if the australopithecines and Homo erectus had similar reproductive schedules (gestation and lactation lengths and interbirth intervals). Shortening the interbirth interval could considerably reduce the costs per offspring to Homo erectus and have the added advantage of increasing reproductive output. The mother would, however, incur additional daily costs of caring for the dependent offspring. If Homo erectus females adopted this reproductive strategy, it would necessarily imply a revolution in the way in which females obtained and utilized energy to support their increased energetic requirements. This transformation is likely to have occurred on several levels involving cooperative economic division of labor, locomotor energetics, menopause, organ size, and other physiological mechanisms for reducing the energetic load on females. Am. J. Hum. Biol. 14:551–565, 2002. © 2002 Wiley‐Liss, Inc.     

Energetic limits on reproduction: Maternal food intake

We examined the factors influencing maternal food intake and pup growth in Norway rats. Mother rats allowed pups in naturally large litters to grow at a slower rate than pups in naturally small litters. Pups reared by dams in a warm ambience (26°C) gained weight more slowly than dams at 22°C, and maternal food intake but not weight gain was depressed in the high ambient temperature. Pup growth at 18°C was unimpaired, with those dams eating no more and gaining no less weight than dams at 22°C. Nest material, however, was found to be essential for the successful rearing of young at cooler ambient temperatures. While restriction of food during gestation resulted in a marginally lower weight gain for the pups during the first 2 weeks postpartum, the dams appeared not to mobilize corporal stores or increase their food intake during lactation. Heavy body weight mothers did not eat any more, nor did they gain any less weight nor rear larger pups than light body weight dams. Rat mothers increased their consumption of a diet diluted with non-nutritive fiber to equal the nutritive intake of their controls, with their pups not differing in their growth rate. Pups reared by dams eating a high quality diet grew faster than pups with dams on the control diet. Food intake by mother rats is required during lactation relative to the amount of milk that is delivered to the pups, rather than to an absolute amount of food. Lactating females with a concurrent pregnancy neither increase their food intake nor appear to mobilize their corporal stores to deal with the added energetic drain of pregnancy. Indeed, their young grew somewhat more quickly than pups nursed by dams that were simply lactating. Taken as a whole, these results suggest that Norway rat dams apparently do not monitor and defend a maximal pup growth rate. Rather, rat dams seem to continue to defend their own homeostasis, and by doing so, allow the young to grow and survive under a wide variety of circumstances.     

Critical periods of susceptibility to short-term energy challenge during pregnancy: Impact on fertility and offspring development

In female mammals, reproduction is tightly regulated by energy status and food availability. Although acute energetic challenges inhibit female reproductive behavior and gonadotropin secretion, less attention has been given to the effects of short-term energetic challenge on pregnancy and gestation. Furthermore, species differences in pregnancy physiology necessitate more detailed analyses of specific pregnancy models. Here, we studied musk shrews, which display induced ovulation and obligate delayed implantation, and whose reproductive physiology is tightly linked to metabolic status. We tested whether acute energetic challenges of varied degrees given at specific pregnancy stages (including before and after delayed implantation) have different effects on gestational outcome and offspring postnatal development. We found that 48 h of either 40% or 50% food restriction, which reduced body weight and strongly inhibited sexual behavior, had minimal effects on pregnancy success and litter dynamics when administered early in gestation (pre-implantation). However, < 30% of females experiencing short-term food restriction later in gestation successfully gave birth (versus ≥ 70% of ad-libitum fed controls), and the pups of these food-restricted females exhibited a 30% slower postnatal growth trajectory. Interestingly, although pregnancy success and litter dynamics were unaffected by food restriction before implantation, gestation length was increased by metabolic challenges experienced at this time, indicating that energy status may regulate the timing of implantation. We conclude that 1) there are critical periods of pregnancy, particularly after implantation, when short-term, mild energetic challenges have significant impacts on fertility and offspring postnatal development, and 2) delayed implantation may have evolved, in part, as a buffering mechanism to prevent pregnancy failure during impaired energy balance in early gestation.     

Signals that link energy to reproduction: Gastric fill,bulk intake,or caloric intake?

Reproductive processes are inhibited by deficits in the availability of metabolic fuels, and this inhibition increases the chances of survival during energetic challenges and optimizes reproductive success by delaying energetically costly processes until fuels become available. The mechanisms that link energy availability to reproduction are unknown, and thus, in this study we tested the hypothesis that estrous cycles are most sensitive to sensory signals from bulk intake and gastric fill as opposed to signals from caloric intake or the availability of intracellular oxidizable fuels. The caloric content of a standard laboratory chow diet was diluted by 25, 50, or 75% with the largely indigestible fiber, cellulose, and fed to food-deprived, female hamsters throughout day 2 of the estrous cycle (ovulation and estrous behavior normally occur on day 4). The bulk intake/gastric fill hypothesis was not supported because bulk intake increased the more the diet was diluted, whereas the frequency of hamsters showing normal 4-day estrous cycles decreased with diet dilution, along with decreases in caloric intake and in plasma insulin concentrations. Rate of gastric emptying did not change significantly with diet dilution. Although consumption of a diluted diet significantly lengthened the estrous cycle, it did not affect incidence of pregnancy, litter size or pup weight. Thus, when hamsters ingest sufficient energy to support estrous behavior, they fully recover reproductive potential. In summary, neither bulk intake nor gastric fill provides critical signals necessary for reproduction, consistent with the idea that reproduction is primarily responsive fuel availability.     

Overlapping litters and reproductive performance in the domestic rabbit

Rabbits (Oryctolagus cuniculus), like many small mammals, have a marked postpartum estrus, and during the breeding season, are often both pregnant and lactating. We examined reproductive performance and allocation of resources by rabbit mothers with overlapping litters under presumably optimal conditions of unrestricted food, standardized litter size, and young reproductive age. Even under these conditions, females raising overlapping litters incurred higher costs in terms of greatly increased food intake and pup mortality than females raising nonoverlapping litters. Despite such costs, females with overlapping litters raised a larger total number of young to weaning than females without the load of simultaneous lactation and pregnancy. By more than doubling food intake during lactation, females maintained a stable baseline body weight throughout the study, suggesting that this, in a species with low fat reserves, might have priority over the short-term raising of a maximum number of young. Contrary to the expectation that females with overlapping litters would allocate more resources to their senior young, no appreciable difference in number, growth, or survival between pups of senior and junior litters was found either at birth or weaning. While this might reflect a strategy in this opportunistic breeder of distributing reproductive chances similarly between senior and junior litters, it is now necessary to investigate females' breeding strategy when resources are limited.     

The energetic costs of rough-and-tumble play in the juvenile rat.

The metabolic costs of rough-and-tumble play behavior were studied in juvenile rats. Using indirect calorimetry, it was determined that energy expenditure during play is increased by 66-104% over the resting metabolic rate, indicating that play accounts for between 2% and 3% of the total daily energy budget of the rat. In a subsequent experiment, food intake and body weight were monitored for 3 weeks in rats allowed to play for 1 hr/day and in rats not allowed to play. While the body weights of the two groups did not differ significantly from each other, those rats allowed to play ate 7% more over the 3-week period than did those rats not given an opportunity to play. These data are consistent with previous reports describing the energetic costs of mammalian play, with play accounting for less than 10% of the daily energy budget in three species tested so far. These data are also consistent with viewing play as a type of exercise and may lead to a better understanding of putative benefits of this behavior.     

The effect of cholecystokinin-octapeptide on food intake and consummatory behavior in lactating rats.

Rats are less sensitive to the satiating effect of CCK-8 during some reproductive states such as estrus and proestrus, and in ovariectomized rats following the administration of estradiol and progesterone. The sensitivity of rats to CCK-8's effect on food intake decreases as lactation progresses. During lactation, prolactin and progesterone levels are elevated. Implantation of ectopic pituitaries increases prolactin levels in males and females as well as progesterone levels in females. To evaluate whether or not prolactin elevation modifies CCK's effect on feeding, we studied the effect of CCK-8 on food intake during the early dark cycle in male and female rats implanted with ectopic pituitaries. As previously demonstrated, prolactin levels were elevated in both male and female pituitary-implanted rats and progesterone levels were elevated in the female rats. CCK-8 inhibited food intake in sham-operated male rats, but did not reliably decrease early dark cycle food intake in sham-operated or pituitary-implanted female rats or pituitary-implanted male rats. Thus an elevation in prolactin levels does not appear to modify the effect of CCK-8 on food intake in female rats. We also evaluated the effect of CCK on consummatory and maternal behavior in lactating rats. CCK-8 altered the meal patterns of lactating rats primarily by decreasing the rate of food consumption and increasing the latency to the first meal. The latency to the first meal of rats receiving CCK was increased during early and mid-lactation and the PW period, but not during late lactation compared to that of the saline-injected rats. CCK-8 did not modulate any of the maternal behaviors studied.(ABSTRACT TRUNCATED AT 250 WORDS)     

Food intake,body composition and blood lipids following treadmill exercise in male and female rats

Body weight gain, food intake, body composition and blood lipids of male and female Osborne Mendel rats were compared on the same exercise treadmill program. To mimic their nocturnal habits, rats were exercised daily at the beginning of the 12 hour dark cycle and food intake was measured for both light and dark cycles. After a 10 day treadmill adaptation period, the duration of exercise was successively increased over a 12 day period until 60 min/day at 21.3 meters/min was reached. Relative to their respective controls, exercised male rats showed a reduction in body weight and light cycle food intake while female runners showed no change in body weight or food intake. Exercise resulted in a decrease in percent body fat in both males and females while only male runners increased percent protein. Both males and females reduced serum triglycerides while serum cholesterol was reduced only in the males. The short term exercise program produced highly significant changes in the males while the females were more resistant to the same exercise regimen.     

Intake and hedonics of calcium and sodium during pregnancy and lactation in the rat

These experiments sought to distinguish whether increased calcium intake during pregnancy and lactation in the rat is due to arousal of a specific calcium appetite, with altered taste hedonics, as occurs with sodium depletion, to reduced taste sensitivity, or to the hyperdipsia of reproduction. We find that, during pregnancy and lactation, CaCl(2) intake is not increased more (in fact less) than intakes of control tastants, MgCl(2) and quinine HCl, and multiparous dams do not have a greater calcium intake than primaparous dams. Changes in taste reactivity to CaCl(2) and to NaCl do not correlate with changes in intake of these minerals during pregnancy or lactation, suggesting that alterations in hedonics or sensitivity do not explain the increased intake of these minerals. Taken together with the increased intake of all the tastants, it may be that the increased intakes of calcium and sodium during reproduction are not due to respective specific appetites or to a general mineral appetite but rather to the reproduction-increased ingestion that may meet all the dam's increased mineral and nutrient requirements. Differences in the degree of increased intakes of tastes may be due to specific alterations in their transduction during reproduction.     

Effects of diet and obesity on body weight regulation during pregnancy and lactation in the rat

The effects of obesity level and cafeteria feeding were studied in rats during pregnancy and lactation. The non-fetal weight gain in pregnancy was three times greater with the cafeteria diet than with chow, indicating that fat deposition is not regulated at an optimal level during pregnancy. There was a strong negative correlation between postpartum weight and weight change during lactation. Obese rats were finicky in that their weight changes in lactation were exaggerated when the diet was changed between pregnancy and lactation. Pup growth rate was proportional to maternal energy intake but in this experiment not related to maternal protein, fat or carbohydrate intake. In obese rats switched to chow, intake was inadequate for normal pup growth. Thus, the weight gains in pregnancy are not regulated at a set level, and the weight change in lactation appears to compensate for the weight gain in pregnancy.     

Prenatal stress alters maternal aggression in mice

Prenatal stress (heat and restraint) reduced pregnancy-induced and elevated postpartum aggression in Rockland-Swiss (R-S) albino female mice. Though prenatally-stressed females were indistinguishable from control animals with respect to parental behavior during the virgin state, the former displayed slightly lower levels of nestbuilding during early pregnancy, and delivered slightly more male offspring at parturition. The young born to prenatally-stressed females exhibited deficits in birth weights and body weight gain in contrast to pups delivered by control females. The anogenital distances of prenatally-stressed females were shorter than those of control females, suggesting that alterations in fetal testosterone exposure may be responsible for disruptions in behavior and reproduction.     

Nocturnal feeding pattern in the prepubertal rat: influence of the ventromedial hypothalamus (VMH)

Daily feeding patterns, food intake and changes in body weight of male and female prepubertal rats were observed across a period from 21 to 50 days of age. Light/dark differences in feeding were found for both males and females throughout the recorded period, with feeding occurring predominantly during the dark period. The light/dark difference in feeding behavior gradually increased as the animals developed. Bilateral lesions placed in the VMH of female rats at 21 days of age disrupted the light/dark differences in feeding behavior primarily by decreasing dark period feeding. These lesions further resulted in a period of hypophagia and retarded body weight gain as well as a delay in pubertal onset. These data indicate that prepubertal rats regulate their feeding behavior so that food intake occurs principally during the dark period and that the integrity of the VMH is necessary for this regulation.     

Male and female 5-HT(1B) receptor knockout mice have higher body weights than wildtypes.

5-HT(1B) receptors have a regulatory role in serotonergic activity and influence feeding behavior and body weight. Because the absence of 5-HT(1B) receptors may cause changes in this regulation, body weight was measured in male and female 5-HT(1B) receptor knockout (5-HT(1B) KO) and wildtype (WT) mice from weaning until the age of 30 weeks. In both genders, 5-HT(1B) KO mice had a higher body weight than WT mice (17% and 9%, respectively). Body weight was significantly higher for males over the entire period and for females from Week 18 onwards. Absolute food and water consumption were related to body weight. However, relative to body weight, males consumed more than females. 5-HT(1B) KO males drank strikingly more water. Housing mice singly reduced food and water intake in males, but not in females. Plasma leptin levels and most organ weights did not differ between genotypes, indicating that higher body weight in 5-HT(1B) KO mice is not related to obesity. Relative to body weight, brains and adrenals were larger in females, while heart and liver were smaller. Kidneys were smaller in females, but larger in 5-HT(1B) KO mice, while lungs showed opposite effects. Spleen and testes were smaller in 5-HT(1B) KO mice. Although 5-HT(1B) KO males are more aggressive, testosterone levels were not different from WT mice. Basal corticosterone levels were similar in all groups and increased in response to mild stress, particularly in females. Lifelong absence of 5-HT(1B) receptors in mice resulted in clear phenotypic differences in body weights and food and water intake. Lacking this receptor increases body growth, without signs of obesity. A potential genetic background effect influencing this phenotype is discussed.     

Sex differences in the effects of voluntary activity on sucrose-induced obesity

Sedentary, adult rats of both sexes fed Purina chow and a 32% sucrose solution overate, gained excess weight and had higher Lee Indexes of obesity than control animals fed only Purina chow. The magnitude of these effects was similar in the males and females. Animals of both sexes fed the sucrose diet showed a slower rate of weight loss during food deprivation than the chow controls. Access to an activity wheel led to a reduction in caloric intake and the elimination of obesity in male rats. In the chow fed male rats activity led to a smaller, transient suppression in caloric intake and a slightly lower level of body weight than the sedentary chow controls. Access to activity did not affect body weight in the female rats in either dietary condition. Rather, both active groups of female rats appeared to compensate for the energy cost of voluntary activity by a small increase in food consumption. Long-term exposure to activity was associated with more rapid weight loss during food deprivation in both males and females. These data reveal that high levels of activity and obesity can co-exist when normal female rats are fed a palatable diet but that activity eliminates this form of obesity in the male rat.     

Age-related changes in adaptive macronutrient intake in swimming male and female Lou rats

To evaluate the age-related changes in capacity to adjust the nutrient intake to needs, self-selecting male and female Lou/C/jall rats of 4, 6, 12, 16 and 23 months of age were submitted to a swimming exercise. They were given 6 consecutive days of moderate intensity training (3 x 15 minutes per day). Exercise and postexercise periods were compared with results from the pretraining period. During swimming, a body weight loss and a decrease in both caloric intake and fat selection were observed. This effect was more marked in older groups compared to 4 month-old groups. An increase in protein intake was observed in females, specially in older groups, whereas no effect was seen in males. The ability to increase caloric ingestion and regain weight during the postexercise period decreased with advancing age and was better in females than in males. We also showed an age-related effect on the recovery of initial nutrient intake rate that was more pronounced and more precocious for males. Moreover, males tended to decrease their protein intake, whereas females significantly increased it. The present findings suggest a decrease of capacity of adjusting feeding behavior to metabolic needs in aged rats, may be due to a deterioration of the central control of food intake.     

Effects of perinatal octylphenol on ultrasound vocalization,behavior and reproductive physiology in rats

A rodent diet containing paraffin wax was designed to administer the environmental estrogen octylphenol (OP) to nonpregnant, pregnant and lactating rats. The estrogenic activity of OP via this diet was first confirmed in ovariectomized adult animals: 20 mg OP/kg/day increased the mitoses in the vaginal epithelium, and 60 mg OP/kg/day stimulated mitoses in the uterine luminal epithelium. The effects on a variety of reproductive and nonreproductive parameters were then investigated in the offspring of dams fed OP (100-250 mg/kg/day during gestation and lactation). A number of modest reproductive and morphological effects observed in the offspring including decreased body weights in adults of both sexes, disrupted vaginal cyclicity and decreases in seminiferous tubule diameter and testis, kidney, spleen and ovary weights. Behavioral effects included increased sexual arousal in males, increased sexual motivation in females towards a female teaser and increased motor activity by females. Ultrasonic vocalizations by pups at Postnatal Day (PND) 7 were reduced in number and duration in both sexes. There were no effects of perinatal OP on ano-genital distance, prepuce separation, aggressive behavior or adult ultrasound vocalization. These observations confirm that the dietary intake of estrogenic amounts of OP during pregnancy and lactation can have a wide variety of effects in the offspring.