Fibre type composition in the lumbar perivertebral muscles of primates: implications for the evolution of orthogrady in hominoids

Abstract

The axial musculoskeletal system is important for the static and dynamic control of the body during both locomotor and non-locomotor behaviour. As a consequence, major evolutionary changes in the positional habits of a species are reflected by morpho-functional adaptations of the axial system. Because of the remarkable phenotypic plasticity of muscle tissue, a close relationship exists between muscle morphology and function. One way to explore major evolutionary transitions in muscle function is therefore by comparative analysis of fibre type composition. In this study, the three-dimensional distribution of slow and fast muscle fibres was analysed in the lumbar perivertebral muscles of two lemuriform (mouse lemur, brown lemur) and four hominoid primate species (white-handed gibbon, orangutan, bonobo, chimpanzee) in order to develop a plausible scenario for the evolution of the contractile properties of the axial muscles in hominoids and to discern possible changes in muscle physiology that were associated with the evolution of orthogrady. Similar to all previously studied quadrupedal mammals, the lemuriform primates in this study exhibited a morpho-functional dichotomy between deep slow contracting local stabilizer muscles and superficial fast contracting global mobilizers and stabilizers and thus retained the fibre distribution pattern typical for quadrupedal non-primates. In contrast, the hominoid primates showed no regionalization of the fibre types, similar to previous observations in Homo. We suggest that this homogeneous fibre composition is associated with the high functional versatility of the axial musculature that was brought about by the evolution of orthograde behaviours and reflects the broad range of mechanical demands acting on the trunk in orthograde hominoids. Because orthogrady is a derived character of euhominoids, the uniform fibre type distribution is hypothesized to coincide with the evolution of orthograde behaviours.

Keywords: autochthonous; epaxial; great ape; hypaxial; lesser ape; skeletal musculature.

Figure 1

Preparation and tissue sampling in example of the epaxial musculature from the female bonobo. (a) Dorsal perspective of the embalmed cadaver to illustrate the preparation for sampling by marking the mid-vertebral levels. The epaxial musculature on the right had already been removed. (b) Division of the left musculature into histologically manageable tissue blocks. The light sutures served as indicators for the mid-vertebral levels, the dark ones indicated the medial and dorsal edges of the block. Grid size: 30 mm.

Figure 2

Results of the immunohistochemical protocol in example (a) of the cross-section at the vertebral level L4/5 for the mouse lemur. (b) Magnification of the complementary staining results. (a,b) Left: labelling with the primary anti-fast antibody (i.e. fast fibres are brown), right: labelling with the primary anti-slow antibody (i.e. slow fibres are brown). (c) Schematic illustration of the segregation of slow and fast fibres (colour-coded as indicated in the legend) to allow for the interspecific comparison illustrated in Fig. 5. Muscle abbreviations: ilc, m. iliocostalis; im, mm. intermammillares (et mammilloaccessorii); is, mm. interspinales; lo, m. longissimus lumborum; m, m. multifidus; pmj, m. psoas major; pmn, m. psoas minor; q, m. quadratus lumborum; r, mm. rotatores; s, m. sacrocaudalis.

Figure 3

Distribution pattern of muscle fibre types in the lumbar regions of (a) mouse lemur (M) and the brown lemur (E), (b) the gibbon (G) and the orangutan (O), (c) the bonobo (B) and the female chimpanzee (C1) and (d) the two male chimpanzees (C2, C3). The percentage of slow fibres is illustrated by a grey scale (see colour code on the bottom). Note that the percentage of fast fibres is complementary to that of slow fibres. The muscles grouped together as the dorsomedial, dorsolateral and the ventral tracts, respectively, are surrounded by thicker lines. Because the right side was reconstructed from the tissue blocks, the lines separating the muscles do not perfectly match the lines on the left, which were drawn after the CT scans. Muscle abbreviations: il, m. iliacus; ilc, m. iliocostalis; im, mm. intermammillares (et mammilloaccessorii); is, mm. interspinales; lo, m. longissimus lumborum; m, m. multifidus; pmj, m. psoas major; pmn, m. psoas minor; r, mm. rotatores; sc, m. sacrospinalis.

Figure 4

Frequency plots of the proportion of slow fibres in the three lumbar muscle tracts studied: (a) dorsomedial, (b) dorsolateral, (c) ventral of the mouse lemur (M), brown lemur (E), gibbon (G), orangutan (O), bonobo (B) and the three chimpanzees (C1, C2, C3) (from top to bottom). The proportions of slow fibres were divided into classes of 10% for each lumbar level and the frequency of their occurrence in a given tract and level was plotted. Numbers in the top right corner of each graph represent means ± SD (first line) as well as minimum and maximum (second line) of the slow fibre proportions observed at the respective vertebral level. Numbers to the left of each row indicate mean ± SD of the percentage of slow fibres for all lumbar levels investigated.

Figure 5

Hypothesized evolutionary transformation of the fibre distribution pattern in the perivertebral muscles in primates. Data were assembled from various studies (Kojima & Okada, ; Schilling, ; Hesse et al. ; this study) and mapped onto a simplified phylogenetic hypothesis (based on Crompton et al. 2008). The regionalized fibre distribution symplesiomorphic for non-primate mammals and primates is indicated by an open square. The homogeneous pattern suggested as a derived character for euhominoids and hypothesized to be associated with the evolution of orthograde behaviours is indicated by a filled square. Illustrated cross-sections from the following mid-lumbar levels: L2: Pan; L3: Hylobates, Pongo; L4: Monodelphis, Tupaia, Macaca, Homo; L5: Microcebus, Eulemur.