Maternal-fetal resource allocation: Co-operation and conflict
Introduction
In eutherian mammals, pregnancy is an apparently highly co-operative interaction between the mother and fetus which, at best, leads to delivery of viable offspring with little detriment to the future health or fecundity of the mother [1]. Through a variety of morphological and physiological adaptations, the fetus demands resources from the mother that support its growth in utero, and generally, a larger well-resourced fetus is more likely to survive at birth and onto reproductive age. The mother benefits from the investment in her offspring because it contributes to the transmission of her genes to future generations [2]. However, inevitably, maternal investment in the current fetus will leave fewer resources for future reproduction. Because the fetus inherits only half of its genes from its mother and shares, at most, half of its genes with its mother's future offspring, there is a conflict between the mother and fetus because the fetus will demand more resources from the mother than may be in her long term reproductive interests to supply [1]. Several lines of evidence suggest that interactions between maternal and fetal genes can occur in determining the level of maternal investment in individual pregnancies. Inter- and intra-specific crosses between breeds of several species show that the mother can constrain the fetal genetic drive for growth and that, conversely, the fetal genome can influence the mother with consequences for fetal growth and pregnancy outcome [3], [4], [5], [6]. Similarly, more direct manipulation of the fetal genome by gene deletion or disruption is known to alter the metabolic and endocrine adaptations of the mouse dam to pregnancy [7], [8], [9]. However, much less is known about the nature of the interactions between maternal and fetal genes in the context of normal pregnancy.
If, as predicted by Kinship Theory, maternal-fetal conflict over the level of maternal investment in the fetus is the norm, it is likely to be particularly relevant in late gestation when the fetus is growing most rapidly in absolute terms or when resources are scarce, for example, due to undernutrition during pregnancy or to a low pre-pregnancy body mass index (BMI) of the mother [10], [11]. Similarly, the importance of conflict will vary with the mating system of the species, particularly the degree of polyandry, and perhaps the size of the conceptus(es) in relation to maternal mass [1], [10]. There are wide inter-species differences in fetal growth rates and in the proportion of maternal weight that is accounted for by the gravid uterus in late gestation (Table 1). Therefore, conflict in nutrient allocation during pregnancy may be more significant in rodents and other species in which total conceptus mass accounts for 20% or more of maternal weight than in higher order primates, in which the gravid uterus is only 6–9% of maternal mass at term (Table 1). Increased litter size leading to direct inter-sibling rivalry and an increased total fetal demand for nutrients may also heighten potential conflict between mother and fetuses in determining nutrient allocation ([5], [6], [11] and Table 1).
With strict monogamy which occurs rarely in mammals [12], the mother and current offspring are equally related to her future offspring and this provides a constraint on the magnitude of maternal-fetal conflict. From Hamilton's rule (Fig. 1), the current offspring will demand resources from the mother as long as the fitness benefit to itself is twice the fitness cost to future offspring [1]. However, in the more common polyandrous mating systems where females mate with more than one male during their reproductive life, conflict is potentially more intense as the differing paternal contributions to the fetal genomes of half-sibs will be less constrained in demanding resources from the mother to the detriment of half-sibs (Fig. 1). Maternal-fetal conflict under polyandry results in differential selection on maternally and paternally inherited alleles in the fetus, with paternal alleles promoting increased maternal investment in the fetus and maternal alleles evolving expression patterns that counteract the effects of ‘greedy’ paternal alleles [2]. The resulting biased expression pattern of the parental alleles is manifested as genomic imprinting [13].
Section snippets
The placenta and maternal-fetal nutrient allocation
As the site of nutrient transfer, the placenta is pivotal in the tug-of-war between mother and fetus over resource allocation [14]. It is the interface where cooperation and conflict coexist and responds to both fetal signals of nutrient demand and maternal signals of nutrient availability in optimising the distribution of available nutrients. To achieve this, the placenta adapts its phenotype in response to a wide range of environmental conditions by changing its surface area for nutrient
Imprinted genes in maternal-fetal nutrient allocation
Imprinted genes, which are expressed in a parent-of-origin manner, have an important role in resource allocation across species and are believed to have evolved in mammals in response to the conflict between parental genomes in transplacental nutrient transfer [13], [53]. These genes are expressed preferentially in the placenta and, in general, paternally expressed genes increase placental and fetal growth while maternally expressed genes have the reverse effects [13], [33], [53]. Indeed, key
Conclusions
Many aspects of gestation, including components of the control of maternal-fetal nutrient allocation, may be largely co-operative processes mutually beneficial to mother and fetus. It is in late gestation when the fetus begins to growth rapidly that conflict over maternal investment may become particularly intense. Especially when nutrients are scarce or conceptus mass is unusually high, some constraint on maternal investment is likely, even if only to ensure sufficient reserve for lactation
Conflict of interest statement
Neither author has any conflicts of interest.
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