Preparing Offspring for a Dangerous World: Potential Costs of Being Wrong

Adaptive maternal responses to stressful environments before young are born can follow two non-exclusive pathways: either the mother reduces current investment in favor of future investment, or influences offspring growth and development in order to fit offspring phenotype to the stressful environment. Inducing such developmental cues, however, may be risky if the environment changes meanwhile, resulting in maladapted offspring. Here we test the effects of a predator-induced maternal effect in a predator-free postnatal environment. We manipulated perceived predation-risk for breeding female great tits by exposing them to stuffed models of either a predatory bird or a non-predatory control. Offspring were raised either in an environment matching the maternal one by exchanging whole broods within a maternal treatment group, or in a mismatching environment by exchanging broods among the maternal treatments. Offspring growth depended on the matching of the two environments. While for offspring originating from control treated mothers environmental mismatch did not significantly change growth, offspring of mothers under increased perceived predation risk grew faster and larger in matching conditions. Offspring of predator treated mothers fledged about one day later when growing under mismatching conditions. This suggests costs paid by the offspring if mothers predict environmental conditions wrongly.     

The response of some prosimian primate mothers to their own anesthetized infants

Six lemur mothers of three different species and oneGalago crassicaudatus mother were observed in the presence of their own anesthetized infants. Two of the lemur mothers spent only very brief periods sitting near their infants and seldom groomed them; the other four spent over half of the infant immobility period in close proximity to their infants and groomed them frequently. Four lemur mothers groomed the ano-genital region of their infant at least once. None of the lemur mothers picked up or carried her immobilized infant, as has been reported for some higher primate mothers, although one lemur mother used her hands to pull the infant toward her ventrum while sitting on the floor. Five lemur mothers rejected their infants when the infants displayed disoriented behavior while emerging from anesthesia. The galago mother retrieved her anesthetized infant in her jaws but dropped the infant several times while attempting to groom it. These results suggest very tentatively that prosimian mothers lack the ability shown by mothers of some higher primate species to improvise protective ways of behaving toward helpless infants.     

Chemical mediation of reciprocal mother–offspring recognition in the Southern Water Skink (Eulamprus heatwolei)

Abstract Kin recognition has been demonstrated to play an important role in the social structure of a wide range of animals. Most studies to date have examined parent–offspring recognition only in species that provide offspring with direct parental care, however, there are several advantages to parent–offspring recognition even in the absence of direct parental care. In this study we investigated reciprocal mother–offspring recognition in the Australian scincid lizard Eulamprus heatwolei, a species that does not show direct parental care. We examined whether neonates could discriminate between their mothers and unrelated females, and whether females could discriminate between their offspring and unrelated neonates, via chemical cues, using retreat site selection experiments. We conducted trials when neonates were 1 and 4 weeks old to investigate whether responses are maintained as neonates age. We found that both neonates and mothers could discriminate between related and unrelated individuals when neonates were 1 week old. Mothers were more likely to take refuge under tiles treated with the odours of their own offspring, while neonates spent less time in areas treated with the odours of unrelated females. At 4 weeks of age, mothers no longer exhibited discriminatory behaviour between their offspring and unrelated neonates, while neonates were more likely to associate with the odour of any female over the odourless control. We hypothesize that reciprocal mother–offspring recognition in E. heatwolei reduces interference competition between mothers and their offspring and also may be important in habitat selection and territory establishment.     

Mother guarding: how offspring may influence the extra-pair behaviour of their parents

In this paper we propose a novel form of social control of mate choice. Through mother guarding, offspring can help in protecting the paternity of their father by preventing their mother from engaging in extra-pair matings. We present a model that predicts the circumstances under which mothers should be selected to seek or avoid extra-pair matings, and existing offspring should be selected to prevent or promote such matings. In its simplest form, our model shows that offspring are selected to mother guard as long as the viability of extra-pair young is less than twice that of within-pair young; when the relative viability is greater, offspring are selected to promote extra-pair mating by their mother. If the existing offspring are not necessarily sired by their mother's social mate, then the potential for conflict is further reduced. We also consider whether offspring have an interest in the extra-pair reproduction of their fathers. We show that when the costs of the father's infidelity to the mother's brood are high, existing offspring are selected to prevent extra-pair mating by their father; when such costs are low, offspring are selected to promote extra-pair mating by their father. In principle, our model applies to all species where offspring show delayed dispersal and where breeding pairs raise multiple broods or litters. This situation exists in, but is not limited to, the majority of cooperatively breeding species. The significance of this model with regard to our current understanding of the evolution of extra-pair behaviour in such species is discussed.     

Consequences of Premature Weaning on the Reproduction of Mothers and Offspring in Laboratory Mice

A decrease of energy expenditure per offspring is expected to benefit the mother by increasing the number of offspring she can produce, and to inflict costs upon the young by decreasing their reproductive value. To evaluate the benefit-cost functions of shortened suckling times in house mice, the young were separated from their mothers prior to natural weaning. During two following litters of mothers and young, time of birth and numbers born were recorded. The impact of the resulting effects on the lifetime reproduction of mothers and young were evaluated by model calculations assuming population equilibrium, exponential population growth or exponential growth limited by population breakdowns.     

Living in a dangerous world decreases maternal care: a study in serotonin transporter knockout mice

Adverse early experiences can profoundly influence the adult behavioral profile. When pregnant and lactating mice are confronted with soiled bedding of unfamiliar males (UMB), these stimuli signal the danger of infanticide and thus simulate a “dangerous world”. In a previous study, offspring of UMB treated mothers were shown to display increased anxiety-like behavior and reduced exploratory locomotion as adults, compared to mice treated with neutral bedding (NB, “safe environment”). The aim of this study was to elucidate the mechanisms conveying these effects of living in a “dangerous world” to offspring behavior. We hypothesized the mother to be the major link and focused on the influence of UMB on maternal stress hormones and behavior. Thus, we investigated fecal corticosterone metabolites (CM) and maternal care of pregnant and lactating mice either treated with NB or UMB. The offspring were subsequently tested for their anxiety-like and exploratory behavior. Mothers treated with UMB showed a significantly higher increase of fecal CM following the initial treatment, than NB treated mothers, indicating that the odor cues of potentially infanticidal males represented an ethologically relevant stimulus. Whereas the hormonal stress response habituated, living in a “dangerous world” led to a distinct and consistent reduction of maternal care behavior, particularly concerning the duration of licking and grooming the pups. Surprisingly, we could not confirm our former findings of altered phenotypes in the offspring of UMB treated mothers. In summary, we hypothesize that the frequently described effects of early life adversity on the offspring's behavioral profile are mediated primarily by maternal care in altricial rodents.     

Offspring recognition by mother crab spiders with extreme maternal care

Maternal care is provided by several spider species, but there are no reports of mother spiders recognizing their young, which suggests that maternal care can be exploited by unrelated individuals. Diaea ergandros, a crab spider with extreme, sacrificial maternal care, does accept unrelated spiderlings (ca. 43.9% of spiderlings) into its nest in areas of high nest density. However, a field and a laboratory experiment with mother spiders and natural and adoptive spiderlings demonstrated that mothers did recognize their own offspring. Recognition was not expressed in survival as adopted (unrelated) spiderlings had similar survival rate to that of natural offspring. Instead it was displayed in growth; mother D. ergandros caught large prey items for their own offspring, but not for adopted spiderlings, and so natural offspring grew more than adopted spiderlings. Also, mothers produced trophic oocytes, which are important for the sacrificial care that influences spiderling survival, only when they lived with their own offspring.     

Inheritance of optimal foraging behaviour in Columbian ground squirrels

Summary I examined the potential inheritance of the ability of Columbian ground squirrels (Spermophilus columbianus) to select an optimal diet. I calculated the diet that would maximize daily energy intake for each of 21 adult females and their litters, using a linear programming optimization model for each individual. The absolute value of the difference between an individual's predicted optimal diet and observed diet (deviation from an optimal diet) was used as a measure of an individual's foraging ability. The foraging ability of individuals was consistent over time and in different foraging environments, so I considered foraging ability to be a potentially heritable trait.Inheritance was determined from correlations of mother and offspring foraging ability. I experimentally removed some mothers just as they weaned their offspring so that offspring could not be influenced by their mother while learning to forage, while leaving the other mothers to raise their litters normally. In both cases, offspring strongly resembled their mother in foraging ability. However, offspring with mothers absent exhibited significantly larger deviations from their optimal diet. Offspring with mothers absent appeared to imitate their mother's diet during lactation, and this tendency partially explained their greater deviation. Consequently, offspring appear to inherit the ability to forage optimally from their mother, perhaps through observational learning or imitation. There may also be a genetic basis to foraging ability, but uncontrolled maternal effects in the experiment prevent a proper test for it.     

Inhibition of firefly luciferase by general anesthetics: effect on in vitro and in vivo bioluminescence imaging

Bioluminescence imaging is routinely performed in anesthetized mice. Often isoflurane anesthesia is used because of its ease of use and fast induction/recovery. However, general anesthetics have been described as important inhibitors of the luciferase enzyme reaction.

Aim

To investigate frequently used mouse anesthetics for their direct effect on the luciferase reaction, both in vitro and in vivo.

Materials and Methods

isoflurane, sevoflurane, desflurane, ketamine, xylazine, medetomidine, pentobarbital and avertin were tested in vitro on luciferase-expressing intact cells, and for non-volatile anesthetics on intact cells and cell lysates. In vivo, isoflurane was compared to unanesthetized animals and different anesthetics. Differences in maximal photon emission and time-to-peak photon emission were analyzed.

Results

All volatile anesthetics showed a clear inhibitory effect on the luciferase activity of 50% at physiological concentrations. Avertin had a stronger inhibitory effect of 80%. For ketamine and xylazine, increased photon emission was observed in intact cells, but this was not present in cell lysate assays, and was most likely due to cell toxicity and increased cell membrane permeability. In vivo, the highest signal intensities were measured in unanesthetized mice and pentobarbital anesthetized mice, followed by avertin. Isoflurane and ketamine/medetomidine anesthetized mice showed the lowest photon emission (40% of unanesthetized), with significantly longer time-to-peak than unanesthetized, pentobarbital or avertin-anesthetized mice. We conclude that, although strong inhibitory effects of anesthetics are present in vitro, their effect on in vivo BLI quantification is mainly due to their hemodynamic effects on mice and only to a lesser extent due to the direct inhibitory effect.     

Effects of early antigen exposure through lactation on later specific antibody responses in mice

This study characterized totally the effects of early Ag exposure by the suckling route on later specific antibody responses. When mother mice of BALB/c or C57BL/6 strains were injected with deaggregated human gamma-globulin (HGG) immediately after delivery, total amounts of HGG in sera of offspring increased until 2 wk of age. The catabolism of transferred HGG was extremely slow and the half-life was about 3 wk in both strains. Hence, small amounts of Ag in mothers, 0.5 micrograms in C57BL/6 and 50 micrograms in BALB/c, could tolerize their offspring effectively. As these were minimum tolerogenic doses, the strain difference in ease of tolerance induction is apparent already during suckling. The study on timing dependent effects of HGG-specific antiserum on tolerance induction by mothers given 50 micrograms HGG demonstrated that the tolerance is achieved within the 1st wk of lactation in C57BL/6 offspring, but not in BALB/c offspring, and the restoration from the tolerance needs more than 6 wk under circumstances, supposedly, without free Ag. Whereas the tolerance was induced in a dose-dependent manner in each class of antibody, the dissociation of tolerant states between IgM, IgG, and IgE antibody classes was found in C57BL/6 offspring. It is interesting that C57BL/6 offspring were sensitized weakly, but significantly, by mothers given subtolerogenic doses. However, this was not apparent in BALB/c. Thus, the Ag dose and the animal strain are related closely to the consequences of this Ag exposure. The aging of suckling mice within the first 2 wk of life or immunomodulators administered early in life did not seriously affect the consequences. Studies on a cellular basis showed that the tolerance is caused by the selective defect in helper T cell function and the suppressor cell activity is not associated with the mechanisms. This contrasts with other models of oral tolerance.     

The Influence of the Early Rearing Environment on the Development of Paternal Care in African Striped Mice

In some biparental mammals, paternal care is important for offspring development and survival. We investigated the influence of the early post‐natal environment on the development of paternal care in the naturally paternal desert‐dwelling African striped mouse (Rhabdomys pumilio). Our aim was to establish whether the expression of paternal care in adult sons is influenced by their experience of paternal care. Offspring were raised in one of three conditions: both parents raised young; mothers raised young alone; and mothers raised young alone but were separated from the father with a barrier. The paternal care behaviour of sons was investigated when they were adults. Contrary to expectations, adult sons raised by the mother alone displayed greater levels of huddling behaviour of their own pups compared to sons raised by both parents. This response appears to be influenced by the early mother–son relationship, because mothers raising pups alone compensated for the absence of fathers by increasing the time spent with pups compared to mothers raising pups with fathers. The mechanisms underpinning the development of paternal care are not apparent in our study. Nonetheless, the development of paternal care is condition‐dependent in male striped mice, indicating that the potential for greater levels of care occurs in the absence of the father and concomitant compensation of maternal care during early development.     

Vocal recognition in free-ranging vervet monkeys

Screams of free-ranging juvenile vervet monkeys were played to a group containing their mothers and two ‘control’ females who also had offspring in the group. Mothers and controls were separated from their offspring at the time. Mothers' responses showed significantly shorter latency and longer duration than controls'; mothers were also significantly more likely to approach the speaker. Playbacks significantly increased the probability that controls would look at the mother; a majority of controls did so without any apparent cue from the mother. Results demonstrate that adult female vervets can distinguish their offsprings' screams from those of other immatures, and they suggest that vervets are able to associate specific screams with specific individuals and these individuals with their mothers.     

黑柄炭角菌(乌灵菌)粉改善睡眠作用以及对小鼠大脑神经递质及其受体的影响

本研究探讨了黑柄炭角菌菌核乌灵菌粉的改善睡眠作用以及对小鼠大脑神经递质及其受体的影响。144例小鼠随机分为低、中、高3个剂量(0.25、0.5和1.0 g/kg bw)的乌灵菌粉实验组和1个空白对照组,进行了30 d的灌胃干预,从小鼠睡眠行为和其大脑组织中神经递质及其受体两个方面进行分析。结果显示,乌灵菌粉无直接催眠作用,对小鼠正常生长和体重增长无显著影响。相比于对照组,乌灵菌粉3个剂量实验组巴比妥钠诱导的入睡潜伏期均显著缩短(P<0.05),戊巴比妥钠阈下剂量下入睡动物数均有增加,戊巴比妥钠诱导的睡眠时间仅有中、高两个剂量组显著增加(P<0.05),低剂量组睡眠时间增加不显著(P>0.05)。低、中、高3个剂量组小鼠大脑组织中γ-氨基丁酸A型受体(GABA_AR)表达量均显著上升(P<0.05),γ-氨基丁酸B型受体(GABA_BR)表达量却显著下降(P<0.05),5-羟色胺(5-HT)和γ-氨基丁酸含量均显著上升(P<0.01)。综上所述,乌灵菌粉具有明显的改善睡眠功效,其作用机制可能是通过提高脑中5-HT和GABA含量,促进小鼠大脑组织中GABA_AR受体表达来实现。     

Transgenerational plasticity in Silene vulgaris in response to three types of stress

• The environment experienced by plants can influence the phenotype of their offspring. Such transgenerational plasticity can be adaptive when it results in higher fitness of the offspring under conditions correlated with those experienced by the mother plant. However, it has rarely been tested if such anticipatory parental effects may be induced with different environments.
• We grew clonal replicates of Silene vulgaris under control conditions and three types of stress (nutrient deficiency, copper addition and drought), which are known from natural populations of the species. We then subjected offspring from differently treated mother plants to each of the different stress treatments to analyse the influence of maternal and offspring environment on performance and several functional traits.
• Current stress treatments strongly influenced biomass and functional traits of the plants, mostly in line with responses predicted by the theory of functional equilibrium. Plant performance was also influenced by maternal stress treatments, and some effects independent of initial size differences remained until harvest. In particular, stressed mothers produced offspring of higher fitness than control plants. However, there was no evidence for treatment‐specific adaptive transgenerational plasticity, as offspring from a mother plant that had grown in a specific environment did not grow better in that environment than other plants.
• Our results indicate that the maternal environment may affect offspring traits and performance, but also that this transgenerational plasticity is not necessarily adaptive.

     

The effects of twinning and maternal experience on maternal-filial social relationships in confined beef cattle

The objective of this investigation was to assess the maternal-filial social relationships of Hereford beef cattle as influenced by maternal experience of the dam (primiparous vs. multiparous) and number of offspring (one vs. two calves). Calves were temporarily separated from their dams during the first week after parturition, and the behavioral responses of mother and young were noted during and following separation.Contact and contact-seeking behaviors between twins and their mothers began to decline by the 5th or 6th day post-partum. Over the same period, contact behaviors exhibited by single calves and their dams remained stable or increased in frequency. Mothers of twins were less responsive to their calves than mothers of singles both during and following separation, and twins interacted with alien females more frequently than single-born young. It is proposed that insufficient milk production by Hereford dams bearing two calves provides an incentive for twins to parasitize the milk supply of alien mothers and, thus, become less dependent on their natural mothers. Social feedback between mother and twins may be further reduced by dams dividing their maternal attentiveness between two offspring.In general, experienced cows were more responsive to separation from their offspring than inexperienced heifers. Cows and their calves exhibited more frequent contact and contact-seeking behavior than heifers and their young.     

Oxygen consumption in offspring tawny owls Strix aluco is associated with colour morph of foster mother

In several colour polymorphic species, morphs differ in thermoregulation either because dark and pale surfaces absorb solar radiation to a different extent and/or because morphs differ in key metabolic processes. Morph-specific thermoregulation may potentially account for the observation that differently coloured individuals are frequently not randomly distributed among habitats, and differ in many respects, including behaviour, morphology, survival and reproductive success. In a wild population of the colour polymorphic tawny owl Strix aluco, a recent cross-fostering experiment showed that offspring raised and born from red mothers were heavier than those from grey mothers. In the present study, we tested in the same individuals whether these morph-specific offspring growth patterns were associated with a difference in metabolic rate between offspring of red and grey mothers. For this purpose, we measured nestling oxygen consumption under two different temperatures (laboratory measurements: 4 and 20°C), and examined the relationships between these data sets and the colour morph of foster and biological mothers. After controlling for nestling body mass, oxygen consumption at 20°C was greater in foster offspring raised by grey foster mothers. No relationship was found between nestling oxygen consumption and coloration of their biological mother. Therefore, our study indicates that in our experiment offspring raised by grey foster mothers showed not only a lower body mass than offspring raised by red foster mothers, but also consumed more oxygen under warm temperature. This further indicates that rearing conditions in nests of grey mothers were more stressful than in nests of red mothers.     

How mothers find their pups in a colony of Antarctic fur seals

In Antarctic fur seals, Arctocephalus gazella, mothers must identify their own young among hundreds or even thousands of pups, if they are to invest in their own offspring and avoid misdirecting their parental care. When returning to their breeding colony from a foraging trip of several days at sea, mothers have to find and identify their young before suckling can occur. There appears to be little confusion about which pup belongs to a mother, and adoption is absent or rare. Using behavioral observations, we investigated the means by which female Antarctic fur seals identified their pups in a breeding colony of about 750 mother-pup pairs on Kerguelen Island. We evaluated the importance of vision, scent communication, vocalizations, and rendezvous locations as possible explanations of how mothers find their pups. Every pup that a mother examined, whether her own or not, exchanged naso-nasal inspection with her, suggesting a strong role for olfactory communication in individual recognition. Both mothers and pups called to each other, and mothers that searched for pups over a longer period gave more calls and encountered more pups. Thus, vocalizations may have been used to attract pups that might be offspring. Nursing usually occurred in the same place from the end of one maternal visit to the colony and the arrival at the beginning of the next visit, suggesting that nursing locations may serve as a meeting place, or rendezvous, for mothers and pups. These results suggest that finding pups is a two-stage process for females, in which pups for sampling are attracted by calls or examined at the previous nursing location, and then individual identification is made by olfactory cues.     

Carcinogenic potential of Indian alcoholic beverage (country liquor).

Epidemiological studies reveal that alcohol consumption is a risk factor for the cancer of the mouth, larynx, esophagus and various other organs. Of the various alcoholic beverages consumed in India, country liquors are widely consumed and that too by the economically weak section of the society. The present paper describes the experiments designed to investigate the effect of one brand of country liquor from Maharashtra State, India (which was found to be more potent in our earlier mutagenicity studies) for its carcinogenicity in two strains of mice and Syrian golden hamsters. The experimental animals received 10% liquor in drinking water from 2 months of age for 16 months. One percent ethanol treated animals served as positive controls. Together with long term bioassays, the transplacental carcinogenic effect of country liquor in the offspring of treated mothers, as well as in the breeders themselves was also investigated. Pregnant mothers were fed 10% liquor through drinking water from 12th day of gestation till weaning of the progeny. Then offspring were allowed to live without further treatment and mothers continued to get liquor treatment. In long term bioassays, liquor caused 22% total tumor incidence in male BALB/c mice and 28% in male Swiss mice. In female Swiss mice and in hamsters, liquor did not show any pronounced effect on tumor incidence. Similar negative results were obtained in case of offspring of treated mothers, but the offspring of liquor treated mothers had higher mortality prior to weaning as compared to those of untreated mothers.     

Daphnia magna microRNAs respond to nutritional stress and ageing but are not transgenerational

Maternal effects, where the performance of offspring is determined by the condition of their mother, are widespread and may in some cases be adaptive. The crustacean Daphnia magna shows strong maternal effects: offspring size at birth and other proxies for fitness are altered when their mothers are older or when mothers have experienced dietary restriction. The mechanisms for this transgenerational transmission of maternal experience are unknown, but could include changes in epigenetic patterning. MicroRNAs (miRNAs) are regulators of gene expression that have been shown to play roles in intergenerational information transfer, and here, we test whether miRNAs are involved in D. magna maternal effects. We found that miRNAs were differentially expressed in mothers of different ages or nutritional state. We then examined miRNA expression in their eggs, their adult daughters and great granddaughters, which did not experience any treatments. The maternal (treatment) generation exhibited differential expression of miRNAs, as did their eggs, but this was reduced in adult daughters and lost by great granddaughters. Thus, miRNAs are a component of maternal provisioning, but do not appear to be the cause of transgenerational responses under these experimental conditions. MicroRNAs may act in tandem with egg provisioning (e.g., with carbohydrates or fats), and possibly other small RNAs or epigenetic modifications.     

Development of social grooming between mother and offspring in wild chimpanzees

Grooming between female chimpanzees and their offspring was studied in the Mahale Mountains, Tanzania. Infants under 2 years of age rarely groomed their mothers, and mostly groomed accessible parts of their mother's bodies, if they did so. Most older adolescents reciprocated grooming with their mothers almost equally. Daughters appeared to mature socially earlier than sons, judging from the earlier ages at which a female infant began to groom her mother, groom mutually with her, and groom others. Weaning infants groomed their mothers more when they were in oestrus than when they were not. Development of the use of grooming as a means of social manoeuvring is discussed.