Metabolic hypothesis for human altriciality

Abstract

The classic anthropological hypothesis known as the "obstetrical dilemma" is a well-known explanation for human altriciality, a condition that has significant implications for human social and behavioral evolution. The hypothesis holds that antagonistic selection for a large neonatal brain and a narrow, bipedal-adapted birth canal poses a problem for childbirth; the hominin "solution" is to truncate gestation, resulting in an altricial neonate. This explanation for human altriciality based on pelvic constraints persists despite data linking human life history to that of other species. Here, we present evidence that challenges the importance of pelvic morphology and mechanics in the evolution of human gestation and altriciality. Instead, our analyses suggest that limits to maternal metabolism are the primary constraints on human gestation length and fetal growth. Although pelvic remodeling and encephalization during hominin evolution contributed to the present parturitional difficulty, there is little evidence that pelvic constraints have altered the timing of birth.

Fig. 1.

Maternal investment in hominoids. Among the great apes, humans have relatively long gestation lengths, large-brained infants, and large-bodied infants. For further explanation, see Fig. S2.

Fig. 2.

Hip abductor mechanics. (A) To maintain equilibrium about the hip during single leg stance, the hip abductors must generate torque (multiple of muscle force, F_m × abductor moment arm, r) equal to the external torque rotating the pelvis away from the stance side. Previous mechanical models assumed the external ground reaction force (GRF) passes nearly vertically through the body midline; therefore, the body weight moment arm could be approximated as equal to one-half biacetabular width. However, external torque is properly measured as the multiple of joint reaction force (JRF) at the distal segment of the femur and the JRF moment arm (R). This calculation accounts for the mediolateral component of the external force and the inertial and gravitational moments acting on the more distal segments of the limb. These forces cause the resolved JRF to move away from the joint center of rotation during single leg stance. (B) As a result, there is no relationship between one-half biacetabular width and the external moment arm at the hip (R) in the coronal plane during walking. Results are similar for running (see SI Text and Table S1).

Fig. 3.

Metabolic constraint on gestation length and fetal size. Fetal energy demands (black circles, kcal/d) increase exponentially during gestation. Maternal energy expenditure (gray squares) rises during the first two trimesters but reaches a metabolic ceiling in the third, as total energy requirements approach 2.0× BMR. Projected fetal energy requirements for growth beyond 9 mo (dashed line) quickly exceed the maximum sustainable metabolic rates for human mothers. After parturition (arrow), infant energy demands (black circles) increase more slowly, and maternal energy requirements do not exceed 2.1× BMR. Required maternal energy expenditure for a fetus developmentally similar to a chimpanzee newborn (7-mo-old infant; symbol with asterisk) would entail maternal energy requirements greater than 2.1x BMR. Data are from refs. – (Table S2).

Fig. 4.

Schematic of OD and EGG hypotheses. (A) Early hominins, like living apes, have little difficulty in parturition; the neonatal brain is small relative to the pelvic outlet. (B) As hominin brain size expands, neonatal brain and pelvis size become tightly coupled. (C) The OD hypothesis proposes that further neonatal brain expansion is constrained by selection acting on pelvic width: the female pelvis cannot expand further because of selection on locomotor economy. (D) The EGG hypothesis proposes that further neonatal brain expansion is constrained by the limits of maternal energy supply: larger neonatal brain and body sizes would exceed the mother’s capacity to provide energy to the fetus (Fig. 3).