Bonobo anatomy reveals stasis and mosaicism in chimpanzee evolution, and supports bonobos as the most appropriate extant model for the common ancestor of chimpanzees and humans

Abstract

Common chimps and bonobos are our closest living relatives but almost nothing is known about bonobo internal anatomy. We present the first phylogenetic analysis to include musculoskeletal data obtained from a recent dissection of bonobos. Notably, chimpanzees, and in particular bonobos, provide a remarkable case of evolutionary stasis for since the chimpanzee-human split c.8 Ma among >120 head-neck (HN) and forelimb (FL) muscles there were only four minor changes in the chimpanzee clade, and all were reversions to the ancestral condition. Moreover, since the common chimpanzee-bonobo split c.2 Ma there have been no changes in bonobos, so with respect to HN-FL musculature bonobos are the better model for the last common ancestor (LCA) of chimpanzees/bonobos and humans. Moreover, in the hindlimb there are only two muscle absence/presence differences between common chimpanzees and bonobos. Puzzlingly, there is an evolutionary mosaicism between each of these species and humans. We discuss these data in the context of available genomic information and debates on whether the common chimpanzee-bonobo divergence is linked to heterochrony.

Figure 1

Differences between head muscles of common chimpanzees, bonobos and modern humans. There are no major consistent differences concerning the presence/absence of muscles in adult common chimpanzees (left) and bonobos (center), the only minor difference (shown in grey in the common chimpanzee scheme) being that the omohyoideus has no intermediate tendon in bonobos, contrary to common chimpanzees (and modern humans). In contrast, there are many differences between bonobos and modern humans (right) concerning the presence/absence of muscles in the normal phenotype (shown in colors and/or with labels in the human scheme). See text for more details.

Figure 2

Differences between forelimb muscles of common chimpanzees, bonobos and modern humans. The only consistent difference between bonobos (center) and common chimpanzees (left) concerning the presence/absence of muscles (shown in colors in the common chimpanzee and bonobos schemes) is that in the former the intermetacarpales 1–4 are usually fused with the flexores breves profundi 3, 5, 6 and 8 to form the dorsal interossei muscles 1–4 (* in bonobo) figure, as is the case in modern humans. In contrast, there are many differences between bonobos and modern humans (right) concerning the presence/absence of muscles (shown in colors and/or with labels in the human scheme; muscles present in chimpanzees and not in humans are shown in black, in chimpanzees). See text for more details.

Figure 3

Differences between hindlimb muscles of common chimpanzees, bonobos and modern humans. The only consistent difference between bonobos (center) and common chimpanzees (left) concerning the presence/absence of muscles (shown in colors in the common chimpanzee scheme) is that the latter usually lack the scansorius, as is the case in humans. In contrast, there are many differences between bonobos and modern humans (right) concerning the presence/absence of muscles (shown in colors and/or with labels in the human scheme; muscles present in chimpanzees and not in humans are shown in black, in chimps). See text for more details.

Figure 4

Cladogram showing evolutionary changes in head-forelimb musculature in hominoids. Single most parsimonious tree (L = 303, CI = 57, RI = 75) obtained in our phylogenetic analysis; for a key of the characters and character state changes show in the cladogram, see text and SI. Note how node leading to LCA of two Pan species has only two changes; P. troglodytes then accumulated two changes, with no changes in the bonobo lineage (for more details, see text). Note that the phylogenetic software converts P. paniscus and P. troglodytes into P. Paniscus and P. Troglodytes.