Mothers determine offspring size in response to own juvenile growth conditions

Through non-genetic maternal effects, mothers can tailor offspring phenotype to the environment in which young will grow up. If juvenile and adult ecologies differ, the conditions mothers experienced as juveniles may better predict their offspring's environment than the adult environment of mothers. In this case maternal decisions about investment in offspring quality should already be determined during the juvenile phase of mothers. I tested this hypothesis by manipulating juvenile and adult maternal environments independently in a cichlid fish. Females raised in a poor environment produced larger young than females raised without food limitations, irrespective of the feeding conditions experienced during adulthood. This maternal boost was due to a higher investment in eggs and to faster larval growth. Apparently, mothers prepare their offspring for similar environmental conditions to those they encountered as juveniles. This explanation is supported by the distribution of these fishes under natural conditions. Juveniles live in a different and much narrower range of habitats than adults. Therefore, the habitat mothers experienced as juveniles will allow them to predict their offspring's environment better than the conditions in the adult home range.     

Affinity towards maternal odour and offspring dispersal in the common lizard

Kin competition is known to strongly influence the spacing behaviour of juveniles in the common lizard, a species which is only weakly social and has no parental care. We examined whether variation in offspring dispersal propensity was associated with variation in their ability to discriminate odours of their mothers versus unknown females. We caught pregnant females in two populations and reared them in the laboratory until parturition. Just after birth, we recorded the juvenile response to the odour of either their mother or an unrelated female. Mothers and offspring were then released at the mother's last capture point, and juvenile movement was monitored by recapture for 2 years. Philopatric individuals were more attracted to the odour of their mother and more repulsed by the odour of an unrelated female than dispersers. In this species, ability to discriminate maternal cues appears to be implied in the spacing behaviour of juveniles. Since juvenile males and females reacted in the same way, the main role of mother discrimination is likely to be the avoidance of kin competition by promoting juvenile dispersal. This does not necessary require mother discrimination to imply mother recognition, or not to be implied in other functions such as inbreeding avoidance. Further research is needed to clarify these points. We suggest that context-dependent kin discrimination may be involved in the spacing behaviour of a large number of species, even for those species where other social functions for kin discrimination have been proposed.     

Persistent maternal effects on juvenile survival in North American red squirrels

Maternal effects can have lasting fitness consequences for offspring, but these effects are often difficult to disentangle from associated responses in offspring traits. We studied persistent maternal effects on offspring survival in North American red squirrels (Tamiasciurus hudsonicus) by manipulating maternal nutrition without altering the post-emergent nutritional environment experienced by offspring. This was accomplished by providing supplemental food to reproductive females over winter and during reproduction, but removing the supplemental food from the system prior to juvenile emergence. We then monitored juvenile dispersal, settlement and survival from birth to 1 year of age. Juveniles from supplemented mothers experienced persistent and magnifying survival advantages over juveniles from control mothers long after supplemental food was removed. These maternal effects on survival persisted, despite no observable effect on traits normally associated with high offspring quality, such as body size, dispersal distance or territory quality. However, supplemented mothers did provide their juveniles an early start by breeding an average of 18 days earlier than control mothers, which may explain the persistent survival advantages their juveniles experienced.     

Post‐birth separation affects the affiliative behaviour of kin in a pitviper with maternal attendance

The relatedness of individuals can have pronounced effects on behavioural interactions, as engaging in mutually beneficial behaviours with kin can increase inclusive fitness. Parental care can be particularly important for kin discrimination in birds and mammals, but similar studies have not been conducted on species exhibiting more rudimentary forms of care. Maternal attendance of young is ubiquitous among viviparous temperate pitvipers, but the adaptive value of this behaviour has received little attention. We sought to determine if being deprived of a maternal attendance period as neonates altered how cottonmouths (Agkistrodon piscivorus Lacépède), a common North American pitviper, responded to kin vs. non‐kin. We measured the affiliative behaviour of related and unrelated juvenile–juvenile and mother–juvenile pairs that had been allowed a maternal attendance period or had been separated since birth. We found that maternal attendance was not required for sibling or mother–offspring recognition, but did enhance female affiliative behaviour overall, and particularly that of sisters. In contrast, related juveniles that were separated at birth showed a reversal of the sex‐specific affiliative behaviour observed in maternally attended juveniles. Post‐birth separation had only a modest effect on mother–juvenile affiliative behaviour, and no effect on the strong affiliation between mothers and daughters. The patterns of affiliative behaviour observed in maternally attended snakes corresponded to patterns that have emerged from previous captive and field studies of pitvipers; however, the behaviour of juveniles separated at birth was atypical. Thus, it is possible that maternal attendance plays some role in the development of adaptive sex‐specific and kin‐directed affiliative behaviour in pitvipers.     

Alloparental Care in the African Striped Mouse Rhabdomys pumilio is Age‐Dependent and Influences the Development of Paternal Care

Alloparents contribute to offspring care and alleviate the workload of breeders. The help provided varies with the age and/or experience of helpers, but it is not known whether breeders vary their investment based on the age of helpers by adjusting the parental care they provide. We studied the alloparental care provided by juvenile and subadult philopatric daughters in biparental African striped mice Rhabdomys pumilio with and without the mother as a measure of alleviation of maternal workload. We showed in a previous study that alleviation of maternal workload directly affects the development of paternal care in their sons, so we studied the expression of paternal care in young males raised by helpers as a proxy of the long‐term consequences of helping. Both juvenile and subadult daughters provided care but the level of alloparental care and concomitant alleviation of maternal care was age‐dependent. In the absence of the mother, juvenile daughters provided just 6% of care compared with 24% of subadult daughters. Sons raised by mothers and juvenile helpers displayed the expected exaggerated levels of care also observed when mothers raise litters on their own. While our results show the direct value of subadult daughters, juvenile daughters could contribute indirectly (e.g. nest maintenance) to alleviating maternal workload. The development of paternal care indicates that mothers do distinguish between the care provided by different aged helpers. Overall, the type of alloparental care provided by female striped mice is expected to change over their lifetimes, resulting in increased inclusive fitness through caring for siblings and acquisition of parenting skills.     

Nonlinear maternal effects on personality in a rodent species with fluctuating densities

Consistent among individual variation in behavior,or animal personality,is present in a wide variety of species.This behavioral variation is maintained by both genetic and environmental factors.Parental effects are a special case of environmental variation and are expected to evolve in populations experiencing large fluctuations in their environment.They represent a non-genetic pathway by which parents can transmit information to their offspring,by modulating their personality.While it is expected that parental effects contribute to the observed personality variation,this has rarely been studied in wild populations.We used the multimammate mouse Mastomys natalensis as a model system to investigate the potential effects of maternal personality on offspring behavior.We did this by repeatedly recording the behavior of individually housed juveniles which were born and raised in the lab from wild caught females.A linear correlation,between mother and offspring in behavior,would be expected when the personality is only affected by additive genetic variation,while a more complex relationship would suggests the presence of maternal effects.We found that the personality of the mother predicted the behavior of their offspring in a non-linear pattern.Exploration behavior of mother and offspring was positively correlated,but only for slow and average exploring mothers,while this correlation became negative for fast exploring mothers.This may suggests that early maternal effects could affect personality in juvenile M.natalensis,potentially due to density-dependent and negative frequency-dependent mechanisms,and therefore contribute to the maintenance of personality variation.     

Long-term evaluation of body mass at weaning and postweaning survival rates of Weddell seals in Erebus Bay, Antarctica

Variability in juvenile survival rate is expected to be an important component of the dynamics of long-lived animal populations. Across a range of species, individual variation in juvenile body mass has been shown to be an important cause of variation in fates of juveniles. Our goal in this paper was to estimate age-specific apparent survival rates for Weddell seals ( Leptonychotes weddellii ) in Erebus Bay, Antarctica, and to investigate hypotheses about relationships between body mass at weaning and apparent survival rate for juveniles. Mark–resighting models found average apparent juvenile survival rate (survival from weaning to age 3) was similar between males and females, and revealed positive relationships between body mass at weaning and apparent juvenile survival rate. The effects of body mass on juvenile survival rate differed between the sexes and the relationship between body mass and survival rate was stronger in males. These results indicate that the magnitude of energy transferred from mother to pup during lactation likely has important consequences on offspring survival rate and maternal fitness.     

A mother’s legacy: the strength of maternal effects in animal populations

Although mothers influence the traits of their offspring in many ways beyond the transmission of genes, it remains unclear how important such ‘maternal effects’ are to phenotypic differences among individuals. Synthesizing estimates derived from detailed pedigrees, we evaluated the amount of phenotypic variation determined by maternal effects in animal populations. Maternal effects account for half as much phenotypic variation within populations as do additive genetic effects. Maternal effects most greatly affect morphology and phenology but, surprisingly, are not stronger in species with prolonged maternal care than in species without. While maternal effects influence juvenile traits more than adult traits on average, they do not decline across ontogeny for behaviour or physiology, and they do not weaken across the life cycle in species without maternal care. These findings underscore maternal effects as an important source of phenotypic variation and emphasise their potential to affect many ecological and evolutionary processes.     

Causes and consequences of variation in offspring body mass: meta‐analyses in birds and mammals

Early survival is highly variable and strongly influences observed population growth rates in most vertebrate populations. One of the major potential drivers of survival variation among juveniles is body mass. Heavy juveniles are better fed and have greater body reserves, and are thus assumed to survive better than light individuals. In spite of this, some studies have failed to detect an influence of body mass on offspring survival, questioning whether offspring body mass does indeed consistently influence juvenile survival, or whether this occurs in particular species/environments. Furthermore, the causes for variation in offspring mass are poorly understood, although maternal mass has often been reported to play a crucial role. To understand why offspring differ in body mass, and how this influences juvenile survival, we performed phylogenetically corrected meta‐analyses of both the relationship between offspring body mass and offspring survival in birds and mammals and the relationship between maternal mass and offspring mass in mammals. We found strong support for an overall positive effect of offspring body mass on survival, with a more pronounced influence in mammals than in birds. An increase of one standard deviation of body mass increased the odds of offspring survival by 71% in mammals and by 44% in birds. A cost of being too fat in birds in terms of flight performance might explain why body mass is a less reliable predictor of offspring survival in birds. We then looked for moderators explaining the among‐study differences reported in the intensity of this relationship. Surprisingly, sex did not influence the intensity of the offspring mass–survival relationship and phylogeny only accounted for a small proportion of observed variation in the intensity of that relationship. Among the potential factors that might affect the relationship between mass and survival in juveniles, only environmental conditions was influential in mammals. Offspring survival was most strongly influenced by body mass in captive populations and wild populations in the absence of predation. We also found support for the expected positive effect of maternal mass on offspring mass in mammals (r_pearson = 0.387). As body mass is a strong predictor of early survival, we expected heavier mothers to allocate more to their offspring, leading them to be heavier and so to have a higher survival. However, none of the potential factors we tested for variation in the maternal mass–offspring mass relationship had a detectable influence. Further studies should focus on linking these two relationships to determine whether a strong effect of offspring size on early survival is associated with a high correlation coefficient between maternal mass and offspring mass.     

Postweaning mass gain in juvenile alpine marmots Marmota marmota

The effects of several environmental factors on the postweaning growth of wild Alpine marmots were investigated. Factors considered were year of birth, sun exposure in the home range, litter size, and sex of young. Components of growth were juvenile mass at emergence from the natal burrow (as a result of preweaning growth) and postweaning growth rate. We also considered the length of the active season during which growth occurs. Mass at emergence and postweaning growth rate varied according to year of birth, were higher in south-facing than in north-facing home ranges, and were higher in small litters. Mass at emergence was higher for males than for females. We suggest that environmental factors affected the juvenile growth pattern through influences on maternal body condition. Our results support Trombulak's hypothesis that mothers maintain as many young as physiologically possible. We suggest that mothers in poor condition sacrificed the mass of their offspring rather than their number. A body mass sexual dimorphism of juveniles occurred at emergence, suggesting that mothers may provide more care for their male than their female offspring. Received: 9 June 1997 / Accepted: 22 September 1997     

Life-stage specific environments in a cichlid fish: implications for inducible maternal effects

Through environmentally induced maternal effects females may fine-tune their offspring’s phenotype to the conditions offspring will encounter after birth. If juvenile and adult ecologies differ, the conditions mothers experienced as juveniles may better predict their offspring’s environment than the adult females’ conditions. Maternal effects induced by the environment experienced by females during their early ontogeny should evolve when three ecological conditions are met: (1) Adult ecology does not predict the postnatal environmental conditions of offspring; (2) Environmental conditions for juveniles are correlated across successive generations; and (3) Juveniles occasionally settle in conditions that differ from the juvenile habitat of their mothers. By combining size-structured population counts, ecological surveys and a genetic analysis of population structure we provide evidence that all three conditions hold for Simochromis pleurospilus, a cichlid fish in which mothers adjust offspring quality to their own juvenile ecology. In particular we show (1) that the spatial niches and the habitat quality differ between juveniles and adults, and we provide genetic evidence (2) that usually fish of successive generations grow up in similar habitats, and (3) that occasional dispersal in populations with a different habitat quality is likely to occur. As adults of many species cannot predict their offspring’s environment from ambient cues, life-stage specific maternal effects are likely to be common in animals. It will therefore be necessary to incorporate parental ontogeny in the study of parental effects when juveniles and adults inhabit different environments.     

Interacting maternal and spatial cues influence natal – dispersal out of social groups

Proximate cues for animal dispersal are complex and varied. Multiple cues may provide information about different aspects of habitat quality, and these aspects may interact with each other, as well as with population density in different ways. We examined how individuals incorporate multiple cues in their decisions to emigrate and immigrate in the colonial orb‐weaving spider, Cyrtophora citricola. We manipulated maternal feeding as a cue for prey abundance and measured the size of the maternal web, which provides a limited space for philopatric offspring and a second potential dispersal cue. In addition, we recorded all immigration events to determine dispersal distances and the cues juveniles may use in settlement. Dispersal increased when mothers were poorly fed, web sizes were small and clutch sizes were large. In addition to these overall effects, maternal feeding also interacted with web size, indicating that offspring from well‐fed mothers were more tolerant of high sibling densities. We also detected a threshold for the effect of clutch size on dispersal for the first egg sac: below 20 offspring, there was no effect of clutch size, but dispersal increased with clutch size for larger clutches. Dispersal distances were often short, and immigrants preferred sheltered trees and those occupied by adult females. Dispersal not only depended on multiple cues, but these cues interacted, and the importance of web size suggested that saturation of the natal web might force dispersal, at least for spiders with poorly‐fed mothers. How one aspect of habitat quality influences dispersal can therefore depend on the state of other aspects of habitat quality. In particular, some natal resources, such as a nest or territory, may become saturated and limit group size, but this limit will also depend on other factors, such as prey availability.     

Habitat exploration and use in dispersing juvenile flying squirrels

1. Variation in behaviours involved in habitat selection is important for several evolutionary and ecological processes. For example, habitat use during dispersal may differ from breeding habitat use, and for dispersers the scale of habitat familiarity is determined by exploratory behaviour. We studied habitat use and exploration of 56 radio-collared juvenile flying squirrels Pteromys volans L. within natal home range and during dispersal, and compared habitat use between juveniles and 37 adults within breeding home range. 2. Before dispersal, young flying squirrels actively moved around the natal site. Surprisingly, long-distance dispersers explored less than short-distance dispersers, but philopatric individuals explored similar distances as dispersers. Females explored less than males, although females are the more dispersive sex in flying squirrels. 3. For most of the individuals the settlement area was unfamiliar due to long dispersal distance. Consequently, direction and distance of exploration were not very strong predictors of settlement location. However, individuals familiar with the settlement area concentrated exploration to that area. Exploration did not correlate with short-term survival. 4. Dispersers preferred breeding habitat while dispersing, but were found more often in matrix habitat than juveniles within natal, or adults within breeding, home ranges. 5. We conclude that familiarity does not determine settlement as much as, for example, availability of the habitat for flying squirrels. Based on our results, it also seems clear that data on adult habitat use are not enough to predict habitat use of dispersing individuals. In addition, our results support the recent view that short- and long-distance dispersers may need to be analysed separately in ecological and evolutionary analyses.     

Mother-offspring associations in northern muriquis, Brachyteles hypoxanthus

Maternal care of offspring is ubiquitous among primates, but its duration varies across species due to factors such as dispersal patterns and social dynamics, which influence opportunities for and potential benefits of maternal investment in older offspring, respectively. We examined mother-offspring associations in wild northern muriquis (Brachyteles hypoxanthus), in which males are philopatric, females typically disperse before puberty, and social relationships among and between males and females are egalitarian. Associations were systematically recorded between ten mothers, each with two-six offspring in the study group, and all group members from August 2003-May 2004 at the RPPN-Feliciano Miguel Abdala in Minas Gerais, Brazil. Infants of both sexes received similarly high percentages of their mothers' association time. Mothers without infants also maintained strong associations with their youngest juvenile sons. Mothers did not spend consistently more time associating with either juvenile or adult sons than daughters. Our finding of non-preferential associations between muriqui mothers and their older male offspring suggests that extended maternal investment in offspring may be of minimal value in their egalitarian society compared with its value for species living in hierarchical societies.     

Larger female fish contribute disproportionately more to self-replenishment

While chance events, oceanography and selective pressures inject stochasticity into the replenishment of marine populations with dispersing life stages, some determinism may arise as a result of characteristics of breeding individuals. It is well known that larger females have higher fecundity, and recent laboratory studies have shown that maternal traits such as age and size can be positively associated with offspring growth, size and survival. Whether such fecundity and maternal effects translate into higher recruitment in marine populations remains largely unanswered. We studied a population of Amphiprion chrysopterus (orange-fin anemonefish) in Moorea, French Polynesia, to test whether maternal size influenced the degree of self-recruitment on the island through body size-fecundity and/or additional size-related maternal effects of offspring. We non-lethally sampled 378 adult and young juveniles at Moorea, and, through parentage analysis, identified the mothers of 27 self-recruits (SRs) out of 101 recruits sampled. We also identified the sites occupied by each mother of an SR and, taking into account variation in maternal size among sites, we found that females that produced SRs were significantly larger than those that did not (approx. 7% greater total length, approx. 20% greater biomass). Our analyses further reveal that the contribution of larger females to self-recruitment was significantly greater than expected on the basis of the relationship between body size and fecundity, indicating that there were important maternal effects of female size on traits of their offspring. These results show, for the first time in a natural population, that larger female fish contribute more to local replenishment (self-recruitment) and, more importantly, that size-specific fecundity alone could not explain the disparity.     

Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the common brushtail possum

The local-resource-competition hypothesis predicts that where philopatric offspring compete for resources with their mothers, offspring sex ratios will be biased in favour of the dispersing sex. This should produce variation in sex ratios between populations in relation to differences in the availability of resources for philopatric offspring. However, previous tests of local resource competition in mammals have used indirect measures of resource availability and have focused on sex-ratio variation between species or individuals rather than between local populations. Here, we show that the availability of den sites predicts the offspring sex ratio in populations of the common brushtail possum. Female possums defend access to dens, and daughters, but not sons, occupy dens within their mother's range. However, the abundances of possums in our study areas were determined principally by food availability. Consequently, in food-rich areas with a high population density, the per-capita availability of dens was low, and the cost of having a daughter should have been high. This cost was positively correlated with male bias in the sex ratio at birth. Low per capita availability of dens was correlated with male bias in the sex ratio at birth.     

Effects of prolactin deficiency during the early postnatal period on the development of maternal behavior in female rats: Mother's milk makes the difference

During early life, prolactin (PRL) ingested by the pups through the milk participates in the development of neuroendocrine, immunological and reproductive systems. The present study tested whether a deficiency in PRL in the dam's milk during early lactation affected the offspring in terms of the maternal responsiveness in the sensitization paradigm and behavioral response to a novel environment in the offspring. Thus, lactating rats were injected (sc) on postnatal days (PND) 2–5 with bromocriptine (125 μg/day), bromocriptine + ovine PRL (125 μg + 300 μg/day), or vehicle. As juveniles (at PND 24) or adults (PND 90–100), one female from each litter was exposed to 5 foster pups continuously for 8 days and their maternal responsiveness was recorded. Female offspring were also tested in an open field arena. Adult, but not juvenile, female offspring of bromocriptine-treated mothers showed an increased latency to become maternal, in comparison to latencies displayed by the offspring of control mothers. Furthermore, the proportion of adult, but not juvenile, offspring of bromocriptine-treated mothers that became maternal was lower than that showed by the offspring of vehicle-treated mothers. In comparison to female offspring of vehicle-treated mothers, female offspring of bromocriptine-treated mothers spent less time hovering over the pups (as juvenile females), body licking (as both juvenile and adult females), and in close proximity to pups (as adult females) during the maternal behavior test. Simultaneous administration of ovine PRL and bromocriptine reversed almost all the negative effects of bromocriptine. These data suggest that maternally-derived PRL participates during the early postnatal period in the development of neural systems that underlie the control of maternal behavior.     

The Effects of Birth Weight and Maternal Care on Survival of Juvenile Steller Sea Lions (Eumetopias jubatus)

Steller sea lions were listed as endangered following a collapse of the western distinct population beginning in the late 1970s. Low juvenile survival has been implicated as a factor in the decline. I conducted a multistate mark-recapture analysis to estimate juvenile survival in an area of the western population where sea lions are showing signs of recovery. Survival for males and females was 80% between 3 weeks and 1 year of age. Approximately 20% of juveniles continued to be nursed by their mothers between ages 1 and 2 and 10% between ages 2 and 3. Survival for juveniles that suckled beyond 1 year was 88.2% and 89.9% to ages 2 and 3, respectively. In contrast, survival for individuals weaned by age 1 was 40.6% for males and 64.2% for females between ages 1 and 2. Birth mass positively influenced survival for juveniles weaned at age 1 but had little effect on individuals continuing to suckle. Cumulative survival to age 4 was double that estimated during the population decline in this region. Evidence suggests that western Steller sea lions utilize a somewhat different maternal strategy than those in the eastern distinct population. Western adult females generally invest more in their pups during the first year but wean offspring by age 1 more often. This results in better survival to age 1, but greater mortality between ages 1 and 3 compared to the eastern population. Different maternal strategies may reflect density dependent pressures of populations at opposite levels of abundance.     

Offspring size and parental fitness in Daphnia magna

Variation in offspring size and number has been described for a wide range of organisms. Many theoretical models predict that in a given environment, the production of one single offspring size would yield the highest parental fitness. In most planktonic cladocerans, however, offspring size has been found to increase with size and age of the mother, and as individuals of variable size often co-occur within a population, offspring of variable sizes can be produced simultaneously. In this study, I investigated the relationship between age of the mother and size of her offspring to assess at what age of the mother the optimal offspring size was produced. Optimal offspring size was defined as that size of the offspring yielding the highest parental fitness, which translates to a definition of optimal offspring size as the one having the highest juvenile fitness per unit effort put in these juveniles. I observed that the youngest females produced offspring with the highest juvenile fitness per unit effort, and hence concluded that offspring produced by these females were of optimal size. Larger offspring produced by older females were estimated to yield only 70% of the potential fitness of optimally sized offspring.     

Maternal Separation in Guinea-Pigs: A Study in Behavioural Endocrinology

The aim of this study was to elucidate the modulation of behaviour and endocrine stress responses of guinea‐pig pups by social and spatial factors in a maternal separation paradigm. The animals were kept in two colonies (each colony: nine males, 13 females and their offspring; enclosure size: 6 m²). Blood samples were taken from the ear vessels of eight male and eight female pups (aged 13–14 d) immediately before and 2 h after they were removed from their colony and were placed singly into a novel environment. Furthermore, eight male and eight female pups were tested in their home colony before and after 2 h of sepration from their mothers. Blood samples were taken from control animals (eight male and eight female pups) which remained in the home colonies together with their mothers. Additionally, the behaviour of 16 male and 16 female pups was recorded in their home colonies when their mothers were either present or absent. Male and female pups separated from their mothers showed a significantly higher locomotor activity, with females showing higher frequencies of distress calls, than pups whose mothers were present. The mother's absence did not cause a significant increase in serum cortisol concentrations in the male or the female offspring. This result is entirely different from the endocrine stress response of pups that were placed singly in an unknown environment. These animals showed a significant increase in their serum cortisol concentrations after 2 h of separation from their mothers. The absence of the mother led to distinct changes in the behaviour of the guinea‐pig pups. However, staying in the familiar social and spatial environment buffered the endocrine stress response that normally occurs because of maternal separation.