Locomotor play drives motor skill acquisition at the expense of growth: A life history trade-off

Abstract

The developmental costs and benefits of early locomotor play are a puzzling topic in biology, psychology, and health sciences. Evolutionary theory predicts that energy-intensive behavior such as play can only evolve if there are considerable benefits. Prominent theories propose that locomotor play is (i) low cost, using surplus energy remaining after growth and maintenance, and (ii) beneficial because it trains motor skills. However, both theories are largely untested. Studying wild Assamese macaques, we combined behavioral observations of locomotor play and motor skill acquisition with quantitative measures of natural food availability and individual growth rates measured noninvasively via photogrammetry. Our results show that investments in locomotor play were indeed beneficial by accelerating motor skill acquisition but carried sizable costs in terms of reduced growth. Even under moderate natural energy restriction, investment in locomotor play accounted for up to 50% of variance in growth, which strongly contradicts the current theory that locomotor play only uses surplus energy remaining after growth and maintenance. Male immatures played more, acquired motor skills faster, and grew less than female immatures, leading to persisting size differences until the age of female maturity. Hence, depending on skill requirements, investment in play can take ontogenetic priority over physical development unconstrained by costs of play with consequences for life history, which strongly highlights the ontogenetic and evolutionary importance of play.

Keywords: Developmental origins of health and disease; human evolution; juvenile risk hypothesis; motor training hypothesis; phenotypic plasticity; resource allocation; surplus resource hypothesis.

Fig. 1. Energy trade-off between locomotor play and growth.

Red, female; blue, male. Residual plots of the individual values for the whole study period (Pearson partial correlations controlled for average food availability and lactation category; n = 12). ¹Residuals are translated into deviations from average in percentage. (A) Growth rate over locomotor play (r = −0.889, P < 0.001); additionally controlled for sex (no figure): r = −0.785, P = 0.002; additionally controlled for average play intensity (no figure): r = −0.895, P < 0.001. (B and C) Growth rate (r = 0.612, P = 0.060) and locomotor play (r = −0.759, P = 0.011) over resting time. (D and E) Growth rate (r = −0.037, P = 0.919) and locomotor play (r = 0.155, P = 0.668) over feeding time.

Fig. 2. Sex-specific investment in growth and locomotor play with increasing food availability.

Red, female; blue, male. (A) Growth rate over food availability: with increasing food availability, female immatures invested in increased growth rates (model significance P = 0.003 compared to null model, R² = 0.251, n = 52), whereas male immatures did not (model significance P = 0.07, R² = 0.065, n = 48; all: P < 0.001, R² = 0.171). (B) Locomotor play over food availability: male immatures invested energy from increased food availability in locomotor play (model significance P = 0.021, R² = 0.360, n = 109), whereas female immatures did not (model significance P = 0.084, R² = 0.321, n = 119; all: P = 0.95, R² = 0.032; all model predictor variables were z-transformed).

Fig. 3. Latencies of motor skill acquisition are predicted by the interaction between the amount and the intensity of locomotor play before the acquisition.

Estimates ± SD of the z-transformed variables predicting latency of motor skill acquisition of 16 skills (LMM, n = 184). Random factor: motor skill labels; model significance: P = 0.014, R² = 0.715; intercept: estimate 8.2 ± 0.4. *Before/after the respective age of motor skill acquisition. Sex of the infant was not significant and thus excluded from the model.

Fig. 4. Sex differences in growth rates over age.

(A) Male body size index over age (break point = 4.2 ± 0.15 years, adjusted R² = 0.952, P < 0.0001; slopes different at P < 0.0001; n = 278; ‡ open blue circles: exact birth date unknown, excluded from regression). (B) Female body size index over age (break point = 4.0 ± 0.15 years, adjusted R² = 0.935, P < 0.0001; slopes different at P < 0.0001; n = 331; ♦ open red circles and lower scattered line: female with low age (5.0 years) at first birth, excluded from regression). (C and D) Before growth spurt, female growth rate was 11.1% higher than male growth rate (GLM: interaction age × sex, P < 0.01), resulting in an average body size difference of 13.0% at age 3.6 to 4.1 years. Adult individual averages set to the age of 9.5 years, the estimated full-grown age of males.