Among the 166 HN and FL muscle characters recognized in our earlier phylogenetic studies6, 7, there were 16 character state differences between common chimpanzees and modern humans (Figs 1 and 2; see SI). The new HL data added 12 more differences: the usual absence in modern humans of a psoas minor, ischiofemoralis, adductor minimus, opponens hallucis, contrahentes pedis, opponens digiti minimi, and of tendons of flexor hallucis longus to digits 3–4, and the presence of a fibularis tertius, of digit 2 as the interossei axis of the foot, and of fibularis longus-medial cuneiform, soleus-tibia and flexor digitorum brevis-digit 5 attachments (see Fig. 3 and refs 11, 15). Therefore, since the chimpanzee-human split c.8 Mya, the divergence rate for striated muscle gross morphology has been c.3.5 characters per million years (Ma). In comparison, across the body there are seven differences in muscle morphology between common chimpanzees and bonobos (Figs 1 and 3; SI). This divergence rate of c.3.5 muscle characters per Ma since common chimpanzees and bonobos split c.2 Ma is similar to the divergence rate for common chimpanzees and modern humans. Interestingly, only one of the common chimpanzee/bonobo differences involves HN muscles: bonobos have a single belly of the omohyoideus, compared to the two bellies that are usually present in both common chimpanzees and modern humans (Fig. 1). Three of the differences are in the FL: (1) the intermetacarpales and flexores breves profundi muscles in the hand of bonobos fuse to form dorsal interossei, a shared feature with modern humans; (2) bonobos have a stout tendon of the flexor digitorum profundus attaching to digit 1, and (3) an attachment between the pectoralis minor and the coracoid process of the scapula (Fig. 2). In the HL, bonobos retain a scansorius and have popliteus-fibula and extensor hallucis longus-proximal big toe phalanx attachments: all these features are missing in common chimpanzees and modern humans (Fig. 3).

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. Full size image

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. Full size image

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. Full size image

Importantly, of the seven common chimpanzee/bonobo differences only two, the presence of dorsal interossei and scansorius in bonobos, concern major differences (i.e., presence/absence of muscles). This contrasts with the 20 major differences between common chimps and modern humans (13 for HN-FL + 7 for HL). The seven common chimpanzee modern human HL muscle absence/presence differences were listed within the 12 HL differences listed in paragraph above. The 13 HN-FL differences are: the presence in modern humans of the HN muscles temporoparietalis, risorius and arytenoideus obliquus (these two latter muscles are only present as variants in chimpanzees) and of the FL muscles rhomboideus minor, flexor pollicis longus, adductor pollicis accessorius, extensor pollicis brevis; presence in common chimpanzees of the FL muscles levator claviculae, dorsoepitrochlearlis, epitrochleoanconeus, contrahentes to digits 4 and 5, and intermetacarpales (Figs 1, 2 and 3 and refs 11, 15). The number of major bonobo-human muscle absence/presence differences is exactly the same, i.e. 13, because bonobos and modern humans do not have distinct intermetacarpales (Fig. 2), but bonobos are different from modern humans in having a scansorius (Fig. 3). Thus, although the overall common chimpanzee/bonobo vs. modern human, and common chimpanzee vs. bonobo divergence rates are similar overall, in terms of major changes the common chimpanzee vs. bonobo divergence rate (two character state differences in c.2.0 Ma) is strikingly (>2.5 times) lower than the common chimpanzee vs. modern human divergence rate of 20 major changes in c.8 Ma. The rate for the bonobo vs. modern human divergence is also higher (>1.6 times) than the bonobo vs. common chimp divergence concerning major changes, because there are also 13 major differences between the musculature of bonobos and modern humans. This is because in the FL bonobos and modern humans have dorsal interossei in contrast to common chimpanzees (Fig. 2), but in the HL bonobos differ from modern humans and common chimpanzees because they retain a scansorius (Fig. 3). Remarkably, all seven differences between common chimpanzees and bonobos are features that are shared by one of the two panin species and modern humans. Moreover, the analysis of these differences reveals a mosaic evolution across the three lineages. Different anatomical regions are evolving in markedly different ways in different taxa: the four features shared between common chimpanzees and modern humans concern the HN and HL muscles, whereas the three bonobo-modern human similarities concern the FL muscles. It will be interesting to investigate whether the four former features are under the control of the approximately three per cent of the modern human genome that is more closely related to the common chimpanzees, and the three later features are linked with the three per cent of our genome that is shared with the genome of bonobos4.

The relatively small number of changes in striated muscle morphology in the panin clade compared to the human clade is particularly evident when the data for P. paniscus are included in a phylogenetic analysis of the 166 HN and FL muscle characters used in our previous studies6, 7 (Fig. 4 and SI). Importantly, the inclusion of these data affected the distribution of synapomorphies at two thirds (6/10) of the nodes in the tree (Fig. 4), including the one leading to modern humans, relative to the tree obtained in our previous analyses (see refs 6, 7). Firstly, there was a removal of the 0 –> 1 change of char. 112 (CS1 vestigial tendon of long flexor to distal phalanx of digit 1) from the node leading to great apes + humans and of the 1 –> 0 change of this character from the human lineage, as the presence of a non-vestigial tendon in bonobos now makes it equally parsimonious to have CS1 acquired in great apes + humans and then reverted in humans and bonobos or an independent acquisition of CS1 in common chimpanzees, gorillas and orangutans (3 steps). Secondly, the 0 –> 1 change in char. 66 (CS1 intermediate tendon of omohyoideus present) was removed in the node leading to panins + humans, as the absence of tendon in bonobos now makes it equally parsimonious to have acquisition of the tendon in this node and subsequent loss in bonobos or an independent acquisition in P. troglodytes and modern humans (2 steps). Thirdly, two of the features that were previously seen as Pan synapomorphies (concerning char. 140: CS1 intermetacarpales not present as separate muscles; and char. 83: CS1 pectoralis minor going to coracoid process) are now assigned to P. troglodytes, i.e. reversion to CS0 in both characters. Thus, the Pan clade thus now has only two synapomorphies (reversion to CS0 in char. 120: CS1 not having a distinct epitrochleoanconeus; and in char. 131: CS1 contrahentes digitorum missing). These changes emphasize the importance of taking information about bonobos into account in studies on human evolution.

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. Full size image

As can be seen in Fig. 4, the rate of HN and FL muscle evolutionary changes in the human clade (4 in 8 Ma, i.e. 0.5 per Ma) is twice that in the chimpanzee clade (8 in 8 Ma, i.e. 1 per Ma). Moreover, all the four changes in the chimpanzee clade are reversions to the ancestral state, i.e. there is not even a single acquisition of a derived muscle feature within that clade, whereas in the human clade there are several examples of muscles that are not part of the normal phenotype in any other primate (i.e., they are autapomorphies). A similar picture also applies to the striated musculature of the hindlimb, in that all of the 12 differences in HL muscles between common chimpanzees/bonobos vs. modern humans are due to derived changes in the lineage leading to modern humans (Fig. 3)15. Furthermore, since the split between common chimpanzees and bonobos c.2 Mya the only two changes that occurred in the chimpanzee clade are within the lineage leading to common chimpanzees. That is, within all the 124 HN and FL muscles of bonobos (Table S2) there is not a single minor change - even including a simple site of origin or attachment, or a fusion, of a muscle - in the 2 Ma of evolution of the bonobo lineage. This is a striking example of evolutionary stasis.

To put these results in perspective, it is useful to compare them with those of our previous paper focusing specifically on the comparison of primate morphological (muscle) and molecular evolutionary rates13. This is because the phylogenetic analysis, terminal taxa and muscle characters that were used as a basis for that paper are exactly the same as those used for the present paper, with the difference that we now include bonobos as an additional terminal taxon (see SI and Fig. 4). It should be noted that for the earlier paper the muscle rates were calculated taking into account both the split between clades and the time of appearance of each terminal taxon (genus) calculated by taking into account genetic data available for various species within a genus. Figure 4 of this genus (as they are shared by different gorilla species) were assumed to have been acquired during 7.1 Ma, i.e. a rate of 0.28 (2/7.1) changes per Ma. Using the same methodology, in that paper the muscle rate leading to the genus Pongo was 0.51 changes per Ma. As explained in detail in that paper, these muscle evolutionary rates are very slow when compared with the rates leading to other hominoid terminal taxa such as Hylobates (rate of 2.72) and Homo (rate of 1.77; for more details, see that paper). So, if we were to use the same methodology in order to compare those rates in a systematic way with the results obtained for chimpanzees in the cladistic analysis of the present paper and thus set the chimpanzee/human split at 7.5 Mya and the origin of the genus Pan at c. 3 Mya as we did in that paper, instead of using respectively the 8 Mya and 2 Mya dates suggested in more recent genetic studies (see above) the rate leading to Pan in the cladogram of Fig. 4 would be only 4.4 muscle changes per Ma (2 muscle changes in 4.5 MMa). This results in a rate even lower than the very slow rate of 0.51 leading to the genus Pongo, for instance. Moreover, within all the hominoid genera, Pan is the only one that lacks a unique feature/muscle character state - or even a derived character - as a synapomorphy. The only two muscles changes acquired are reversions to the plesiomorphic state and, even more remarkably, there we no muscle changes, major or minor, leading to P. paniscu﻿s, as noted above.

These new bonobo data are also relevant to two major ongoing debates in biological sciences. The first is whether bonobos or common chimpanzees are a better model for the last common ancestor (LCA) of chimpanzees, and of chimpanzees and modern humans. Zihlman and colleagues have suggested that, within the two extant chimpanzee species, bonobos make a more suitable model for the two LCAs21,22,23,24, but others have proposed that bonobos are highly derived chimpanzees, being for instance adapted to unique ecological conditions that selected for a specialized locomotor habits25. Our data do not support the latter suggestion because bonobos do not display a single muscle or muscle feature that is unique within primate, or even hominoid, evolution. In fact, it is now becoming increasingly accepted that the bonobo-common chimpanzee divergence was likely mainly due to the barrier to gene flow created by the formation of the Congo River c.1.5–2.5 Mya. Since then relatively little hybridization has occurred between bonobos and common chimpanzees on opposite sides of this river4. This scenario can therefore help to explain why the anatomical differences between the two Pan species are so minor when compared to the striking anatomical differences between them and humans. The second debate is about hypothesized differences in the ontogenetic trajectories of common chimpanzees and bonobos. Some have argued that bonobos are more paedomorphic than chimpanzees26, but more recently Bolter and Zihlman27 suggested that skeletal development in common chimpanzees is slower than that of bonobos, an idea also partially supported in a recent study linking phenotypic development and genotypic variation in common chimpanzees and bonobos28. One of the two major (presence/absence) muscle differences between these two species is consistent with the hypothesis that the musculoskeletal development of common chimps is slower than that of bonobos. This is because early in human ontogeny the intermetacarpales are distinct muscles (as they remain in adult common chimpanzees), and only in the later stages of human development do they become fused with the flexores breves profundi to form the dorsal interossei (as they are in adult bonobos)29, 30. These discussions emphasize how the study of the soft tissues of bonobos and other apes is crucial for a comprehensive and integrative understanding of the evolution and biology of chimpanzees, other apes, and primates, and ultimately of our own human lineage.