Between Scylla and Charybdis: renegotiating resolution of the 'obstetric dilemma' in response to ecological change

Abstract

Hominin evolution saw the emergence of two traits-bipedality and encephalization-that are fundamentally linked because the fetal head must pass through the maternal pelvis at birth, a scenario termed the 'obstetric dilemma'. While adaptive explanations for bipedality and large brains address adult phenotype, it is brain and pelvic growth that are subject to the obstetric dilemma. Many contemporary populations experience substantial maternal and perinatal morbidity/mortality from obstructed labour, yet there is increasing recognition that the obstetric dilemma is not fixed and is affected by ecological change. Ecological trends may affect growth of the pelvis and offspring brain to different extents, while the two traits also differ by a generation in the timing of their exposure. Two key questions arise: how can the fit between the maternal pelvis and the offspring brain be 'renegotiated' as the environment changes, and what nutritional signals regulate this process? I argue that the potential for maternal size to change across generations precludes birthweight being under strong genetic influence. Instead, fetal growth tracks maternal phenotype, which buffers short-term ecological perturbations. Nevertheless, rapid changes in nutritional supply between generations can generate antagonistic influences on maternal and offspring traits, increasing the risk of obstructed labour.

Keywords: adaptation; birthweight; encephalization; fistula; nutrition transition; obstetric dilemma.

Figure 1.

Long-term secular trends in (a) adult body mass and (b) adult cranial capacity over the past 1.2 Myr in the genus Homo. The trends do not match, indicating that the relationship between adult body mass and brain size has shifted during this period. This suggests that the obstetric dilemma may also have undergone renegotiation during the same period. Adapted from Ruff et al. [13].

Figure 2.

Schematic diagram illustrating how the obstetric dilemma emerges from the interaction between two traits, the maternal pelvis and offspring neonatal size, which are shaped by ecological stresses that are characterized by a one-generation time-lag in the timing of their exposure.

Figure 3.

Prevalence of special educational need (SEN) by gestation at delivery, showing an inverse dose–response association with the lowest level of detrimental outcome for offspring born at 41 weeks post-conception. Reproduced with permission from MacKay et al. [63].

Figure 4.

Estimates of heritability in weight and length/height in The Netherlands Twin Register study, with data from another study of late pregnancy added. Heritability of weight declines from approximately 50% at 25 weeks gestation to approximately 30% at birth, then increases to approximately 70% by 36 months. The post-natal pattern for length is very similar. Adapted from [93,95].

Figure 5.

(a) Odds ratio for giving birth to macrosomic infants (defined as above the 90th centile for birthweight in the population) according to maternal stature, obesity and diabetes, along with offspring sex, across 23 countries. Countries are grouped by region (Africa, Asia, Latin America), demonstrating similar risks. The data were adjusted for country, maternal age, size and metabolic status and offspring sex. (b) Odds ratios for maternal or perinatal morbidity and mortality arising from macrosomic offspring, adjusted for country, maternal age, size and metabolic status and offspring sex. Adapted from [124].