Rapid Onset of Maternal Vocal Recognition in a Colonially Breeding Mammal,the Australian Sea Lion

Background

In many gregarious mammals, mothers and offspring have developed the abilities to recognise each other using acoustic signals. Such capacity may develop at different rates after birth/parturition, varying between species and between the participants, i.e., mothers and young. Differences in selective pressures between species, and between mothers and offspring, are likely to drive the timing of the onset of mother-young recognition. We tested the ability of Australian sea lion mothers to identify their offspring by vocalisation, and examined the onset of this behaviour in these females. We hypothesise that a rapid onset of recognition may reflect an adaptation to a colonial lifestyle.

Principal Findings

In a playback study maternal responses to own pup and non-filial vocalisations were compared at 12, 24 and every subsequent 24 hours until the females'' first departure post-partum. Mothers showed a clear ability to recognise their pup''s voice by 48 hours of age. At 24 hours mothers called more, at 48 hours they called sooner and at 72 hours they looked sooner in response to their own pup''s vocalisations compared to those of non-filial pups.

Conclusions

We demonstrate that Australian sea lion females can vocally identify offspring within two days of birth and before mothers leave to forage post-partum. We suggest that this rapid onset is a result of selection pressures imposed by a colonial lifestyle and may be seen in other colonial vertebrates. This is the first demonstration of the timing of the onset of maternal vocal recognition in a pinniped species.     

Maternal Oxytocin Is Linked to Close Mother-Infant Proximity in Grey Seals (Halichoerus grypus)

Maternal behaviour is a crucial component of reproduction in all mammals; however the quality of care that mothers give to infants can vary greatly. It is vital to document variation in maternal behaviour caused by the physiological processes controlling its expression. This underlying physiology should be conserved throughout reproductive events and should be replicated across all individuals of a species; therefore, any correlates to maternal care quality may be present across many individuals or contexts. Oxytocin modulates the initiation and expression of maternal behaviour in mammals; therefore we tested whether maternal plasma oxytocin concentrations correlated to key maternal behaviours in wild grey seals (Halichoerus grypus). Plasma oxytocin concentrations in non-breeding individuals (4.3 ±0.5 pg/ml) were significantly lower than those in mothers with dependent pups in both early (8.2 ±0.8 pg/ml) and late (6.9 ±0.7 pg/ml) lactation. Maternal plasma oxytocin concentrations were not correlated to the amount of nursing prior to sampling, or a mother’s nursing intensity throughout the dependant period. Mothers with high plasma oxytocin concentrations stayed closer to their pups, reducing the likelihood of mother-pup separation during lactation which is credited with causing starvation, the largest cause of pup mortality in grey seals. This is the first study to link endogenous oxytocin concentrations in wild mammalian mothers with any type of maternal behaviour. Oxytocin’s structure and function is widely conserved across mammalian mothers, including humans. Defining the impact the oxytocin system has on maternal behaviour highlights relationships that may occur across many individuals or species, and such behaviours heavily influence infant development and an individual’s lifetime reproductive success.     

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.     

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.     

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.     

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.     

FEMALE PROMISCUITY AND MATERNALLY DEPENDENT OFFSPRING GROWTH RATES IN MAMMALS

Conflicts between family members are expected to influence the duration and intensity of parental care. In mammals, the majority of this care occurs as resource transfer from mothers to offspring during gestation and lactation. Mating systems can have a strong influence on the severity of familial conflict—where female promiscuity is prevalent, conflict is expected to be higher between family members, causing offspring to demand more resources. If offspring are capable of manipulating their mothers and receive resources in proportion to their demands, resource transfer should increase with elevated promiscuity. We tested this prediction, unexplored across mammals, using a comparative approach. The total durations of gestation and lactation were not related to testes mass, a reliable proxy of female promiscuity across taxa. Offspring growth during gestation, however, and weaning mass, were positively correlated with testes mass, suggesting that offspring gain resources from their mothers at faster rates when familial conflict is greater. During gestation, the relationship between offspring growth and testes mass was also related to placenta morphology, with a stronger relationship between testes mass and growth observed in species with a less invasive placenta. Familial conflict could have a pervasive influence on patterns of parental care in mammals.     

Maternal protectiveness and response to the unfamiliar in vervet monkeys

Vervet monkeys (Cercopithecus aethiops sabaeus) show individual differences in approach-avoidance behavior when faced with an unfamiliar and potentially threatening situation. Prior research from our colony demonstrated that juveniles who had experienced high levels of early maternal protectiveness were more cautious in response to novelty, compared to juveniles who had had less protective mothers. The research reported here was designed to verify this result in a paradigm that experimentally varied maternal protectiveness through the introduction of new breeding adult males. Mothers responded to the presence of new males by increased maternal protectiveness toward infants born in the year following the introductions. Individual differences in response to the unfamiliar were later evaluated by measuring the latency to approach within 1 m of novel food containers placed into the home enclosure of four naturally composed social groups. Infants approached with the same latency and in the same order as their mothers. Juveniles approached sooner than, and independent of, their mother's current behavior, but their latency to approach could be predicted by the experimentally induced variation in maternal protectiveness they had experienced as infants. Immatures who had been born in New Male years, when maternal protectiveness was high, were more cautious and had significantly longer latencies to approach the novel stimulus compared to immatures who had been born in Resident Male years. © 1993 Wiley-Liss, Inc.     

The ecology of lizard reproductive output

Aim We provide a new quantitative analysis of lizard reproductive ecology. Comparative studies of lizard reproduction to date have usually considered life‐history components separately. Instead, we examine the rate of production (productivity hereafter) calculated as the total mass of offspring produced in a year. We test whether productivity is influenced by proxies of adult mortality rates such as insularity and fossorial habits, by measures of temperature such as environmental and body temperatures, mode of reproduction and activity times, and by environmental productivity and diet. We further examine whether low productivity is linked to high extinction risk. Location World‐wide. Methods We assembled a database containing 551 lizard species, their phylogenetic relationships and multiple life history and ecological variables from the literature. We use phylogenetically informed statistical models to estimate the factors related to lizard productivity. Results Some, but not all, predictions of metabolic and life‐history theories are supported. When analysed separately, clutch size, relative clutch mass and brood frequency are poorly correlated with body mass, but their product – productivity – is well correlated with mass. The allometry of productivity scales similarly to metabolic rate, suggesting that a constant fraction of assimilated energy is allocated to production irrespective of body size. Island species were less productive than continental species. Mass‐specific productivity was positively correlated with environmental temperature, but not with body temperature. Viviparous lizards were less productive than egg‐laying species. Diet and primary productivity were not associated with productivity in any model. Other effects, including lower productivity of fossorial, nocturnal and active foraging species were confounded with phylogeny. Productivity was not lower in species at risk of extinction. Main conclusions Our analyses show the value of focusing on the rate of annual biomass production (productivity), and generally supported associations between productivity and environmental temperature, factors that affect mortality and the number of broods a lizard can produce in a year, but not with measures of body temperature, environmental productivity or diet.     

Paternal levels of DNA damage in spermatozoa and maternal parity influence offspring mortality in an endangered ungulate

Understanding which factors influence offspring mortality rates is a major challenge since it influences population dynamics and may constrain the chances of recovery among endangered species. Most studies have focused on the effects of maternal and environmental factors, but little is known about paternal factors. Among most polygynous mammals, males only contribute the haploid genome to their offspring, but the possibility that sperm DNA integrity may influence offspring survival has not been explored. We examined several maternal, paternal and individual factors that may influence offspring survival in an endangered species (Gazella cuvieri). Levels of sperm DNA damage had the largest impact upon offspring mortality rates, followed by maternal parity. In addition, there was a significant interaction between these two variables, so that offspring born to primiparous mothers were more likely to die if their father had high levels of sperm DNA damage, but this was not the case among multiparous mothers. Thus, multiparous mothers seem to protect their offspring from the deleterious effects of sperm DNA damage. Since levels of sperm DNA damage seem to be higher among endangered species, more attention should be paid to the impact of this largely ignored factor among the viability of endangered species.     

Maternal investment in relation to sex ratio and offspring number in a small mammal – a case for Trivers and Willard theory?

1.  Optimal parental sex allocation depends on the balance between the costs of investing into sons vs. daughters and the benefits calculated as fitness returns. The outcome of this equation varies with the life history of the species, as well as the state of the individual and the quality of the environment.
2.  We studied maternal allocation and subsequent fecundity costs of bank voles, Myodes glareolus , by manipulating both the postnatal sex ratio (all-male/all-female litters) and the quality of rearing environment (through manipulation of litter size by −2/+2 pups) of their offspring in a laboratory setting.
3.  We found that mothers clearly biased their allocation to female rather than male offspring regardless of their own body condition. Male pups had a significantly lower growth rate than female pups, so that at weaning, males from enlarged litters were the smallest. Mothers produced more milk for female litters and also defended them more intensively than male offspring.
4.  The results agree with the predictions based on the bank vole life history: there will be selection for greater investment in daughters rather than sons, as a larger size seems to be more influencial for female reproductive success in this species. Our finding could be a general rule in highly polygynous, but weakly dimorphic small mammals where females are territorial.
5.  The results disagree with the narrow sense Trivers & Willard hypothesis, which states that in polygynous mammals that show higher variation in male than in female reproductive success, high-quality mothers are expected to invest more in sons than in daughters.     

Trans-Generational Effect of Maternal Lactation during Pregnancy: A Holstein Cow Model

Epigenetic regulation in mammals begins in the first stages of embryogenesis. This prenatal programming determines, in part, phenotype expression in adult life. Some species, particularly dairy cattle, are conceived during the maternal lactation, which is a period of large energy and nutrient needs. Under these circumstances, embryo and fetal development compete for nutrients with the mammary gland, which may affect prenatal programming and predetermine phenotype at adulthood. Data from a specialized dairy breed were used to determine the transgenerational effect when embryo development coincides with maternal lactation. Longitudinal phenotypic data for milk yield (kg), ratio of fat-protein content in milk during first lactation, and lifespan (d) from 40,065 cows were adjusted for environmental and genetic effects using a Bayesian framework. Then, the effect of different maternal circumstances was determined on the residuals. The maternal-related circumstances were 1) presence of lactation, 2) maternal milk yield level, and 3) occurrence of mastitis during embryogenesis. Females born to mothers that were lactating while pregnant produced 52 kg (MonteCarlo standard error; MCs.e. = 0.009) less milk, lived 16 d (MCs.e. = 0.002) shorter and were metabolically less efficient (+0.42% milk fat/protein ratio; MCs.e.<0.001) than females whose fetal life developed in the absence of maternal lactation. The greater the maternal milk yield during embryogenesis, the larger the negative effects of prenatal programming, precluding the offspring born to the most productive cows to fully express their potential additive genetic merit during their adult life. Our data provide substantial evidence of transgenerational effect when pregnancy and lactation coincide. Although this effect is relatively low, it should not be ignored when formulating rations for lactating and pregnant cows. Furthermore, breeding, replacement, and management strategies should also take into account whether the individuals were conceived during maternal lactation because, otherwise, their performance may deviate from what it could be expected.     

HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING

Two explanations for species differences in neonatal brain size in eutherian mammals relate the size of the brain at birth to maternal metabolic rate. Martin (1981, 1983) argued that maternal basal metabolic rate puts an upper bound on the mother's ability to supply energy to the fetus, thereby limiting neonatal brain size. Hofman (1983) proposed that gestation length in mammals is constrained by maternal metabolic rate, implying an indirect constraint on neonatal brain size. Since individuals of precocial species have much larger neonatal brain sizes and are gestated longer for a given maternal body size than individuals of altricial species, Martin's and Hofman's ideas also require that mothers of precocial offspring have higher metabolic rates for their body sizes than mothers of altricial offspring. Data on 116 mammal species from 13 orders show that neither neonatal brain size nor gestation length is correlated with maternal metabolic rate when maternal body-size effects are removed. For a given maternal size, there is no difference in metabolic rates between precocial and altricial species, despite a two-fold difference between them in average neonatal brain size. However, neonatal brain size is strongly correlated with gestation length and litter size, independently of maternal size and metabolic rate. Analyses conducted within orders replicated the findings for gestation length and suggested that neonatal brain size may be at best only weakly related to metabolic rate. Differences in neonatal brain size appear to have evolved primarily with species differences in gestation length and litter size but not with differences in metabolic rate; large-brained offspring are typically produced from litters of one that have been gestated for a long time relative to maternal size. We conclude that species differences in relative neonatal brain size reflect different life-history tactics rather than constraints imposed by metabolic rate.     

Testing hypotheses for maternal effects in Daphnia magna

Maternal effects are widely observed, but their adaptive nature remains difficult to describe and interpret. We investigated adaptive maternal effects in a clone of the crustacean Daphnia magna, experimentally varying both maternal age and maternal food and subsequently varying food available to offspring. We had two main predictions: that offspring in a food environment matched to their mothers should fare better than offspring in unmatched environments, and that offspring of older mothers would fare better in low food environments. We detected numerous maternal effects, for example offspring of poorly fed mothers were large, whereas offspring of older mothers were both large and showed an earlier age at first reproduction. However, these maternal effects did not clearly translate into the predicted differences in reproduction. Thus, our predictions about adaptive maternal effects in response to food variation were not met in this genotype of Daphnia magna.     

Terminal reproductive effort in a marsupial

Life-history theory predicts that as organisms approach the end of their life, they should increase their reproductive effort (RE). However, studies on mammals often find that measures of RE do not vary with maternal age. This might be because offspring have some control over energy transfer which may constrain adaptive variation in RE by mothers, particularly in eutherian mammals where placental function is primarily controlled by offspring. However, in marsupials, energy transfer is primarily by lactation and under maternal control, leaving marsupial mothers free to vary RE. Here, we provide the first analysis, to our knowledge, of age-specific RE in a marsupial, the common brushtail possum. RE, measured as the proportion of maternal mass lost during lactation, was strongly correlated with offspring mass as a yearling. Older females had higher RE, gave birth earlier in the season and were more likely to produce two offspring in a year. Females with high RE in one year were lighter at the beginning of the next breeding season. These results provide the clearest support yet for terminal RE in a mammal.     

Maternal condition and facultative sex ratios in populations with overlapping generations

Facultative investment in offspring sex is related to maternal condition in many organisms. In mammals, empirical support for condition-dependent sex allocation is equivocal, and there is some doubt as to theoretical expectations. Much theory has been developed to make predictions for condition-dependent sex ratios in populations with discrete generations. However, the extension of these predictions to populations with overlapping generations (OLGs; e.g., mammals) has been limited, leaving doubt as to the specific prediction for maternal-condition-dependent sex ratios in mammals. We develop a population genetics model that incorporates maternal effects on multiple offspring fitness components in a population with OLGs. Using a rare-gene and evolutionarily stable strategy approach, we demonstrate that sex ratio predictions of this model are identical to those for equivalent discrete generations models. We show that the predicted sex ratios depend on the sex-specific ratio of R(o) (offspring lifetime fitness) for offspring of good and poor mothers. This offspring lifetime fitness rule indicates that empirical research on conditional sex ratios should consider all three components of offspring R(o) (juvenile survival, adult life span, and fertility).     

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.     

Primary productivity can affect mammalian body size frequency distributions

Frequency distributions of mammal body sizes in large‐scale assemblages have often been found to show a positive skew. In an attempt to explain this pattern, a model has been put forward which incorporates energetic constraints on fitness and thereby predicts optimal body sizes corresponding to the mode of the distribution. A key assumption of the model is that energy is unlimited. However, if energy is limited, the input of energy into a herbivorous mammal community should influence the shape of the frequency distribution. Thus, I propose that increases in primary productivity will decrease the variation of body size and increase the mean body size in a distribution. So, in low‐productivity environments we should see a predominance of small‐sized species, but with a great variation of body sizes due to limitations of resources (energy). I tested this hypothesis using the herbivorous mammal fauna (rodents, bats and marsupials) in seven biomes of Australia. Because herbivorous marsupials generally are fairly large‐bodied while rodents and bats are small‐sized and because marsupials also have a different mode of reproduction from placental mammals, the hypothesis was also tested on placental mammals and marsupials separately. There was no clear mode for the entire assemblage in any biome, but as primary productivity increased, the variation of body masses decreased and the mean body mass of the distribution increased. Body mass distributions of both placental mammals and marsupials displayed clear modes. Placental mammals also showed an increase in mean body mass. The variation in body mass of marsupials was highest for the intermediately productive biomes. Primary productivity does seem to have some effect on mammalian body mass in this case, but the results here need to be complemented with studies of other assemblages before any general conclusions can be drawn. It is also important to distinguish which taxa are affected in a heterogeneous assemblage like the Australian herbivorous mammal fauna.     

Effects of allometry,productivity and lifestyle on rates and limits of body size evolution

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow–fast life-history continuum, and the allometric scaling of generation time to predict a clade''s evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow–fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.     

Placental invasiveness and brain-body allometry in eutherian mammals

Brain growth is a key trait in the evolution of mammalian life history. Brain development should be mediated by placentation, which determines patterns of resource transfer from mothers to fetal offspring. Eutherian placentation varies in the extent to which a maternal barrier separates fetal tissues from maternal blood. We demonstrate here that more invasive forms of placentation are associated with substantially steeper brain-body allometry, faster prenatal brain growth and slower prenatal body growth. On the basis of the physiological literature we suggest a simple mechanism for these differences: in species with invasive placentation, where the placenta is bathed directly in maternal blood, fatty acids essential for brain development can be readily extracted by the fetus, but in species with less invasive placentation they must be synthesized by the fetus. Hence, with regard to brain-body allometry and prenatal growth patterns, eutherian mammals are structured into distinct groups differing in placental invasiveness.