Placentation

Placental development differs greatly among members of different taxa. Not only does blastocyst attachment take place at different times, the penetration of trophoblast varies considerably. From an epitheliochorial relationship between fetus and mother to the hemochorial placentation of taxa, such as the higher primates, the trophoblast becomes increasingly exposed to maternal immune recognition which may be one cause of rejection in interspecific embryo transfers or hybridization. Shape of uterus and endometrium and genetic factors govern the morphologic form of the placenta. The paper reviews ungulate placentation, successes and failures of interspecific embryo transfers, and the scant knowledge of genetic determinants in primate placentas.     

The maternal recognition of pregnancy in mammals

Progesterone secreted by the corpora lutea stimulates uterine secretion of nutrients required for embryonic growth. But progesterone also blocks maturation of ovarian follicles and oestrous behaviour. When conception fails, therefore, the corpora lutea must lyse, in order to allow a second ovulation and oestrus, while in pregnancy the corpora lutea must be maintained. A number of different endocrine mechanisms exist to ensure the corpora lutea are controlled appropriately depending on pregnancy status; among the best studied of these are the secretion by the developing conceptus of interferons (in ungulates) or chorionic gonadotropins (in primates). These and other mechanisms are reviewed.     

Olfactory regulation of maternal behavior in mammals

In mammals, olfactory cues are extensively used in many aspects of maternal care to ensure the coordination of mother-infant interactions and consequently the normal development of the offspring. Outside the period of parturition and lactation, when the young are not a behavioral priority, olfactory cues play an inhibitory role on maternal responsiveness since in most mammalian species studied so far, nonpregnant females find the odor of young aversive. On the contrary at the time of parturition, a shift in the hedonic value of infantile odors occurs so that the young now become a very potent stimulus and this sensorial processing constitutes an important part of the maternal motivational system. Moreover, infants' odors provide a basis for individual recognition by their mothers and some species (ungulates) have developed highly specialized mechanisms for processing of the infant signals. Perception of the smell of the young also regulates various aspects of maternal behavior. Dodecyl propionate, a compound released by of pup's preputial glands, has been shown to influence anogenital licking behavior, a fundamental pattern of maternal behavior in rodents. While there is no functional specificity of either the main or the accessory olfactory systems in the development of maternal behavior amongst species, it appears that only the main olfactory system is implicated when individual odor discrimination of the young is required. Neural structures, such as the main olfactory bulb, undergo profound changes when exposed to offspring odors at parturition. These changes in synaptic circuitry contribute both to maternal responsiveness to these odors, to their memorization, and to effects of long-term maternal experience.     

Nutrition, fertility and maternal investment in primates

While the energetics of reproduction have been intensively investigated among women, studies of mother-offspring relationships among non-human primates have tended to neglect the effect of nutrition of the mother on lactational performance and on growth and survival of offspring. Typically fertility has been compared between populations under different nutritional regimes. In this paper, the relations between suckling frequencies, the time of weaning, the survivorship of offspring, the contraceptive effects of lactation and the quality of maternal diets are outlined. Energy transfer from mother to offspring in the form of milk is proposed as a measurable component of maternal investment, and the behavioural causes and consequences of lactational anoestrus are explored using data from free-ranging vervet monkeys. It is suggested that nutrition of the mother is most important during the early phase of rapid infant growth, because at that time the energetic requirements of lactation are high; and that a mother's ability to assess her infant's demands and needs for nutrition for growth leads to alterations in suckling frequencies which result in variation in female fertility.     

Mechanisms of activation of maternal behaviour in mammals

In mammals, the activation of maternal behaviour depends on internal maternal factors related with parturition. The nature of these factors may vary between species, although oestradiol, foetus expulsion and intracerebral oxytocin are the most commonly encountered. They induce a period of specific receptivity to some sensory cues provided by the neonate. These cues (tactile, olfactory, auditory, ...) also vary between species. The interactions between the mother and her progeny during this period, known as the sensitive period, facilitate the maintenance of maternal responsiveness beyond the initial phase of activation by the factors internal to the mother. The ability of mothers to display a well-adapted maternal behaviour is also modulated by maternal experience gained at the first parturition. Furthermore, this capacity is also influenced by the nature of the interactions experienced in infancy with the own mother of the female, which can lead to a non-genomic transmission of some individual characteristics of maternal behaviour or sensitivity to stress across generations.     

Placentation in multiple births.

Outcomes of multifetal pregnancy in prenatal life are markedly affected by chorionicity. Several disease processes are found in monochorionic (MC) twins that do not occur in dichorionic (DC) twins. Improvements in prenatal outcomes will depend on reliable first trimester diagnosis of chorionicity, allowing early monitoring for complications of MC placentation. Particular structures and functions of MC twin placentas affect outcomes and can be targeted for specific treatments, especially in twin-twin transfusion. The causes of severe DC twin fetal growth discordance are clarified. In post-natal life, zygosity is a determining effect in genetic predisposition to many chronic diseases, including neoplasia. Few MC twins know that they are monozygotic (MZ). Few twin researchers realize that MZ twins may be genetically discordant. Abandonment of the word "identical" for MZ twins would assist in clarifying these issues of zygosity, concordance and discordance.     

Influence of maternal stress on metal-induced pre- and postnatal effects in mammals

Studies in rodents have shown that, during pregnancy, maternal stress from restraint, noise, light, and heat among other factors may be associated with adverse effects on embryo/fetal and postnatal development. Moreover, it is also well known that exposure to certain metal levels during gestation can also cause maternal and developmental toxicity. Because potentially, pregnant women may be concurrently exposed to metals and various types of stress, the influence of maternal stress on the metal-induced adverse pre-and postnatal effects has been investigated for a number of elements. This influence is reviewed here. It is concluded that maternal stress enhances the metal-induced embryo/fetal and developmental toxicity only at doses of the metal which are also clearly toxic to the dam.     

Changes in maternal investment in eggs can affect population dynamics

The way that mothers provision their offspring can have important consequences for their offspring's performance throughout life. Models suggest that maternally induced variation in life histories may have large population dynamical effects, even perhaps driving cycles such as those seen in forest Lepidoptera. The evidence for large maternal influences on population dynamics is unconvincing, principally because of the difficulty of conducting experiments at both the individual and population level. In the soil mite, Sancassania berlesei, we show that there is a trade-off between a female's fecundity and the per-egg provisioning of protein. The mother's position on this trade-off depends on her current food availability and her age. Populations initiated with 250 eggs of different mean sizes showed significant differences in the population dynamics, converging only after three generations. Differences in the growth, maturation and fecundity of the initial cohort caused differences in the competitive environment for the next generation, which, in turn, created differences in their growth and reproduction. Maternal effects in one generation can therefore lead to population dynamical consequences over many generations. Where animals live in environments that are temporally variable, we conjecture that maternal effects could result in long-term dynamical effects.     

Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.     

Sex-biased maternal investment in voles: importance of environmental conditions

Adaptive bias in sex allocation is traditionally proposed to be related to the condition of mothers as well as to the unequal fitness values of produced sexes. A positive relationship between mother condition and investment into male offspring is often predicted. This relationship was also recently found to depend on environmental conditions. We studied these causalities experimentally using a design where winter food supply was manipulated in eight outdoor-enclosed populations of field voles Microtus agrestis. At the beginning of the breeding season in spring, food-supplemented mothers seemed to be in a similar condition, measured as body mass, head width, body condition index and parasite load (blood parasite Trypanosoma), to non-supplemented mothers. Food supplements affected neither the litter size, the reproductive effort of mothers, nor the litter sex ratios at birth. However, food supplementation significantly increased the birth size of male offspring and improved their condition, as indicated by reduced parasite loads (intestinal Eimeria). Interestingly, mothers in good body condition produced larger male offspring only when environmental conditions were improved by food supplements. Although the adaptiveness of variation in mammalian sex ratios is still questionable, our study indicates that mothers in good condition bias their investment towards male offspring, but only when environmental conditions are favourable.     

Growth, weaning and maternal investment from a comparative perspective

The process of weaning is related to a critical or threshold body weight attained by offspring among large-bodied mammals; the anthropoid primates, ungulates and pinnipeds. While weaning weight was allometrically related to maternal weight in interspecific comparisons, it was isometrically related to neonatal weight. When a neonate had grown to four times its birth weight, it was weaned. Differences between taxonomic groups were found only among the fasting phocids, where weanlings attained a lower, but proportional, weight. The duration of lactation was only weakly allometrically related to maternal or neonatal weight, and varied between individuals intraspecifically as a function of maternal condition. The time to weaning appears to be ecologically sensitive rather than to reflect interspecific life-history variation, in that, irrespective of the time to weaning, similar proportional weights appear to be attained. Interspecific similarities in threshold weaning weights are suggested to result from constraints on maternal abilities to meet energetic requirements of offspring through lactation after infants attain a threshold weight.     

Unequal maternal investment in offspring quality in relation to predation risk

Equal investment within broods does not always maximize parental reproductive value if the reproductive value of some of the young is low. We examined maternal investment in terms of offspring size in relation to the prospects of survival from predation within broods of the shield bug Elasmucha ferrugata Fabr. (Heteroptera; Acanthosomatidae). Shield bug females guard eggs and first instar nymphs against invertebrate predators by covering the clutch with their body and by behaving aggressively towards their enemies. Survival of eggs was not possible without maternal care. When females were allowed to guard their brood, eggs at the periphery were more vulnerable to predators than eggs at the centre. We found that females laid significantly larger eggs in the safest, central part of the clutch. There seems to be an advantage of large nymph size, since when nymphs were reared separately with low food resources, the larger ones were more likely to survive. Larger nymphs were also more likely to push themselves to the safest, central part of the clutch. Females seem to allocate their resources more to the offspring with the highest probability of avoiding predation. Thus our study supports unequal maternal investment within broods of E.ferrugata.     

Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals

Trivers and Willard's suggestion that natural selection favors maternal control of offspring sex ratio in relation to maternal condition has been much debated. The theoretical plausibility of the idea, under some conditions, is firmly established, and there is strong empirical support for conditional sex allocation in some taxa. However, the extent to which this hypothesis can be applied to mammals, particularly ungulates, has been more controversial. We used meta-analysis to review published studies of the Trivers-Willard hypothesis within ungulates and to assess the overall level of empirical support for the hypothesis. Overall, data from 37 studies of 18 species suggested a weak but significant positive correlation between maternal condition and sex ratio (r=+0.09). However, average effect size differed markedly between different categories of studies. Studies using measures of maternal condition that were taken preconception and on the basis of behavioral dominance provided strong evidence for a relationship between maternal condition and the sex ratio (r=+0.17-0.25). In contrast, studies that used morphological or physiological measures of condition that were measured postconception provided little or no evidence for a relationship between maternal condition and sex ratio (r=+0.05-0.06). There are several reasons to suggest that data collected postconception and relying on morphological measures of condition are less likely to capture variables that cause selection for biased sex allocation. In addition, we found that the relationship between sex ratio and maternal condition depended on life-history characteristics; relationships were stronger when sexual size dimorphism was more male biased and when gestation periods were longer. Overall, our analyses suggest that data from ungulates are consistent with the Trivers-Willard hypothesis but only when appropriate measures are used.     

An evolutionary perspective on the patterning of maternal investment in pregnancy

Pregnancy is thought to be a metabolically very expensive endeavor, yet investigations have produced inconsistent results concerning the responsiveness of human birth weight to maternal nutritional stress or nutritional intervention. These findings have led some researchers to conclude that fetal growth is strongly buffered against fluctuations in maternal energy balance, making the fetus in effect a “nearly perfect parasite.” This buffering would appear to be a reasonable adaptive response given the high risk of morbidity and mortality associated with low birth weight. However, a life-history approach leads to the prediction that maternal investment strategies in pregnancy should be geared toward maximizing lifetime reproductive success rather than simply the success of the current pregnancy, and by extension that maternal investment strategies should vary with reproductive value. The physiology of human pregnancy in fact appears to include a number of mechanisms that protect maternal energy resources from diversion to the fetus and preserve them for future reproductive events. These mechanisms include adjustment of blood flow to the uterus and perhaps minor adjustments in gestation length, although evidence for the latter is scant. Suggestions are made for ways of investigating these maternal options.