Born this way: Does variation in perinatal limb bone morphology predict adult locomotor repertoire in primates?

Abstract

Primates show a high degree of locomotor diversity that engenders similar variance in limb bone cross-sectional geometry and bending strength: leaping primates have stronger hindlimb bones whereas suspensory species have stronger forelimb bones. Prior studies have asserted that such differences in limb bone properties are due to variation in bone loading during postnatal life. We investigate whether some of this limb bone variation could be developmentally canalized, such that predictable differences in forelimb-hindlimb bone strength are already present at birth. Our infant sample included 17 primate species (including strepsirrhines, monkeys, and apes) and one tree shrew species, encompassing a wide variety of locomotion, including leaping, brachiation, and habitual quadrupedalism. We tested how well two benchmarks of adult positional behavior-leaping prevalence and intermembral index (i.e., IMI; typically ≪100 in leapers and ≫100 in suspensory primates) predict perinatal interlimb variation in limb bone length (e.g., IMI), cross-sectional resistance to bending, and material stiffness. As predicted, we found that perinatal IMI and forelimb-hindlimb ratios of limb bone cross-sectional geometry significantly decreased with adult leaping frequency and increased with adult IMI. The influence of adult positional behaviors on forelimb-hindlimb ratios of bone material stiffness was more equivocal, though we found that primates that leap more frequently as adults have relatively stiff femoral bone as infants. Some of the previously documented variation in adult primate interlimb bone strength must be developmentally canalized in prenatal life, well before substantial interlimb variance in bone loading has taken place.