Life history trade-offs and the partitioning of maternal investment: Implications for health of mothers and offspring

Abstract

Lay Summary: This review sets out the hypothesis that life history trade-offs in the maternal generation favour the emergence of similar trade-offs in the offspring generation, mediated by the partitioning of maternal investment between pregnancy and lactation, and that these trade-offs help explain widely reported associations between growth trajectories and NCD risk. Growth patterns in early life predict the risk of non-communicable diseases (NCDs), but adaptive explanations remain controversial. It is widely assumed that NCDs occur either because of physiological adjustments to early constraints, or because early ecological cues fail to predict adult environmental conditions (mismatch). I present an inter-generational perspective on developmental plasticity, based on the over-arching hypothesis that a key axis of variability in maternal metabolism derives from life history trade-offs, which influence how individual mothers partition nutritional investment in their offspring between pregnancy and lactation. I review evidence for three resulting predictions: (i) Allocating relatively more energy to growth during development promotes the capacity to invest in offspring during pregnancy. Relevant mechanisms include greater fat-free mass and metabolic turnover, and a larger physical space for fetal growth. (ii) Allocating less energy to growth during development constrains fetal growth of the offspring, but mothers may compensate by a tendency to attain higher adiposity around puberty, ecological conditions permitting, which promotes nutritional investment during lactation. (iii) Since the partitioning of maternal investment between pregnancy and lactation impacts the allocation of energy to 'maintenance' as well as growth, it is expected to shape offspring NCD risk as well as adult size and body composition. Overall, this framework predicts that life history trade-offs in the maternal generation favour the emergence of similar trade-offs in the offspring generation, mediated by the partitioning of maternal investment between pregnancy and lactation, and that these trade-offs help explain widely reported associations between growth trajectories and NCD risk.

Keywords: lactation; life history strategy; maternal investment; non-communicable disease; pregnancy.

Figure 1.

(a) Growth in mass of fetus/infant up to 12 months post-partum, and placenta up to term. (b) Energy costs of pregnancy by trimester (T) and of lactation over the first 8 months post-partum. Data from refs. [7] and [8]

Figure 2.

Association between infant growth pattern and (a) weight and length z-scores at birth and (b) height and BMI z-scores at 5 years. Data (mean ± standard error) from ref. [23], reproduced with permission from ref. [17]

Figure 3.

Associations between maternal fat-free mass and offspring size in an Ethiopian birth cohort (n = 403), for (a) absolute birth weight and (b) birth weight as a percentage of maternal fat-free mass. Andersen, Friis, Kaestel, Wells, Girma, unpublished data

Figure 4.

Conceptual diagram illustrating life history trajectories and their associated risk of Non-Communicable Diseases (NCDs). Each trajectory demonstrates different trade-offs, shaping both metabolic capacity and load (traits relevant to the life-course emergence of NCD risk) and the somatic traits that underlie partitioning of maternal investment between pregnancy and lactation. Blue: high maternal investment in pregnancy favours energy allocation to growth/maintenance, promoting longevity and health. Green: low maternal investment in pregnancy is followed by post-natal energy constraint, preventing catch-up. This leads to small adult size but low NCD risk. Red: low maternal investment in pregnancy is followed by catch-up during lactation, continuing into childhood. The extra energy accelerates maturation and increases adiposity without benefitting adult size, thus increasing NCD risk. Each of these trajectories produces in adult women the traits that favour the same trajectory in the next generation. Redrawn with permission from ref. [17]