Ontogeny of food grasping in mouse lemurs: behavior, morphology and performance

Abstract

In primates, grasping constitutes a vital function involved in many behaviors. Anatomical specializations of the prehensile extremities originated early‐on in their evolution. However, the precise functional and ecological contexts that have driven this evolution remain unclear. Interspecific comparative studies show that a given morphology can induce different grasping behaviors and also that a given behavior can be performed using different morphological structures. In this context, an intraspecific ontogenetic approach offers the opportunity to describe the relations between patterns in grasping behavior and patterns of grasping morphology. We quantified manual grasping strategies and the associated morphometric (i.e. segments lengths) and performance (i.e. pull strength) traits for both limbs during the development of a small arboreal primate, the gray mouse lemur (Microcebus murinus). Our results show an early onset of grasping in young mouse lemurs. Moreover, younger individuals had relative longer hindlimbs (i.e. tibia and metatarsus) allowing them to have near‐maximal levels of grasping strength. This very fast development despite an incomplete neuromuscular development highlights the importance of this grasping function directly after birth.

An interdisciplinary approach to the evolution of grasping and manipulation

“…Their results show that ontogenetic declines in relative digit length may be a common mammalian trend that has been selected for in primates. The authors find support for this, their 'functional grasping theory' of primate hand and foot growth (Young & Heard-Booth, 2016), which is also discussed in another recent paper (Boulinguez-Ambroise et al, 2019).…”

Increased performance in juvenile baboons is consistent with ontogenetic changes in morphology

“…Also, longer forearms likely enhance the attachment surface for finger and hand flexors (Thomas et al, 2016), thus promoting stronger grip. Relatively longer limbs have consequently been observed to be related to high grasping performance in juvenile mouse lemurs (Boulinguez‐Ambroise et al, 2019). Furthermore, a greater anatomical mechanical advantage of the forearm extensors and flexors (i.e., triceps and biceps brachii) has been demonstrated in juvenile capuchin monkeys (Young, 2005) such that young individuals may produce greater output forces for a given amount of muscle force compared to adults.…”

“…As juveniles are not “miniature adults,” but rather experience concomitant changes in morphology and behavior during growth (Carrier, 1996; Herrel & Gibb, 2006; Young & Shapiro, 2018), studying ontogeny offers the opportunity to simultaneously and in “real‐time” explore the relations between behavior, performance, and morphology (Boulinguez‐Ambroise et al, 2019; Druelle, Young, & Berillon, 2017; Hurov, 1991; Russo & Young, 2011; Thomas et al, 2016). Such an approach might thus provide unique insights into the behavioral transitions that likely occurred during the evolution of the primate prehensile and locomotor systems.…”

“…Furthermore, a greater anatomical mechanical advantage of the forearm extensors and flexors (i.e., triceps and biceps brachii) has been demonstrated in juvenile capuchin monkeys (Young, 2005) such that young individuals may produce greater output forces for a given amount of muscle force compared to adults. Interestingly, previous studies have suggested different functional roles for the hind limb and the forelimb during primate locomotion, with grasping feet having a more substantial role in locomotion, freeing the forelimbs for other functions such as foraging (Boulinguez-Ambroise et al, 2019;Cartmill, 1974b;Chadwell & Young, 2015;Charles-Dominique, 1977;Patel et al, 2015). Recent studies on locomotor development have also revealed morphological or behavioral differences between the grasping functions of the hand and the foot.…”

The Forearm Musculature of the Gray Mouse Lemur (Microcebus murinus): An Ontogenetic Study

“…While ontogenetic patterns of forearm strength and flexibility are not widely reported either for M. murinus or for primates more generally, what little data exist would seem to suggest interesting developmental trends within this region. Immature mouse lemurs are reported to show relatively high grasping strength when adjusted for body mass (Boulinguez‐Ambroise et al ., ), while data on hand usage during food acquisition suggest that younger adults practice unimanual grasps more frequently than senescent individuals, suggesting some variation in forelimb use associated with aging (Le Brazidec et al ., ). However, as only experimentally derived in vivo measurements of grip strength are reported for this species, the myological changes which drive potential variation in forearm strength and flexibility during development remain unknown.…”