A unifying model for timing of walking onset in humans and other mammals

Abstract

The onset of walking is a fundamental milestone in motor development of humans and other mammals, yet little is known about what factors determine its timing. Hoofed animals start walking within hours after birth, rodents and small carnivores require days or weeks, and nonhuman primates take months and humans approximately a year to achieve this locomotor skill. Here we show that a key to the explanation for these differences is that time to the onset of walking counts from conception and not from birth, indicating that mechanisms underlying motor development constitute a functional continuum from pre- to postnatal life. In a multiple-regression model encompassing 24 species representative of 11 extant orders of placental mammals that habitually walk on the ground, including humans, adult brain mass accounted for 94% of variance in time to walking onset postconception. A dichotomous variable reflecting species differences in functional limb anatomy accounted for another 3.8% of variance. The model predicted the timing of walking onset in humans with high accuracy, showing that this milestone in human motor development occurs no later than expected given the mass of the adult human brain, which in turn reflects the duration of its ontogenetic development. The timing of motor development appears to be highly conserved in mammalian evolution as the ancestors of some of the species in the sample presented here diverged in phylogenesis as long as 100 million years ago. Fundamental patterns of early human life history may therefore have evolved before the evolution of primates.

Fig. 1.

The phylogenetic relatedness of species in the present sample illustrated by a chronogram based on divergence time estimates from phylogenomic analysis (48) complemented with mitogenomic analysis (49).

Fig. 2.

Continuous independent variables considered as predictors of time to walking onset. Time to walking onset, log(WO), is shown as a function of absolute adult brain mass, log(AbsBrM), neonatal brain mass, log(NeoBrM), gestation time, log(Gest), adult body mass, log(BoM), brain advancement at birth (neonatal brain mass/adult brain mass), log(BrAdv), and adult relative brain mass (adult brain mass/body mass), log(RelBrM). PC, postconception; g, grams; d, days. Sample is shown as in Tables S1 and S2. Double circle, humans; dotted circles (in BoM and RelBrM), nonhuman primates; solid lines, model II linear regression (reduced major axis) on all species. R² and P values for linear regressions are given in diagrams.

Fig. 3.

Residuals from regression analyses in Fig. 2. (Upper) Absolute values of residuals as a function of, from left to right, absolute adult brain mass, log(AbsBrM), neonatal brain mass, log(NeoBrM), and gestation time, log(Gest). (Lower) Based on the same data as Upper, but with means and 1.0 SD indicated by horizontal longer dashed lines and shorter solid lines, respectively. Data points from humans are indicated by arrows in all diagrams.

Fig. 4.

Absolute adult brain mass and hindlimb standing position as predictors of time to walking onset. (Left) Time to walking onset, log(WO), as a function of absolute adult brain mass, log(AbsBrM), and hindlimb standing position. Solid symbols and solid regression line represent species that can assume a plantigrade hindlimb standing position; open symbols and dashed regression line represent species that cannot assume a plantigrade hindlimb standing position (Table S2). Analysis of variance with covariance (ANCOVA) confirmed the overall robust main effect of adult brain mass as a covariate (F_(1,24) = 820.51, P < 0.0001, η² = 0.97) and revealed a main effect of hindlimb standing position as a grouping variable (F_(1,24) = 40.39, P < 0.0001, η² = 0.66). For the full model equation derived from multiple-regression analysis, R² values, and P values, see main text. The 95% confidence interval for R² was 0.95–0.99. (Right) The same as the Left panel, but with species indicated next to each data point for clarity. The Pearson correlation coefficient was 0.97 (two-tailed P < 0.0001; cf. Fig. S3). Axis units are as in Left but the x axis is expanded.