Functional significance of distal calcaneal elongation in primates
The functional significance of distal calcaneal elongation in particular groups when compared with others, when size-scaling effects are taken into account, is a controversial question. However, distal calcaneal elongation has been related to locomotor adaptations by interpreting it in terms of preference for leaping (Anemone and Covert 2000; Covert 1988; Dagosto 1986, 1988, 1990; Gebo 1986, 1993; Gebo et al. 2000a; Martin 1972, 1979, 1990). However, this explanation is unlikely because extant primates as a group display a distal calcaneus relatively elongated to some degree compared to non-primate mammals, in spite of the fact that primates as a whole show variable degrees of commitment to leaping and some do not leap at all (Ford 1988; Gebo 1987).
The fact that distal calcaneal elongation cannot be merely interpreted in the light of leaping abilities alone is further illustrated by additional sources of evidence: the distally elongated calcanei of lorisids and orangutans (Fig. 3), even though they never leap; or the situation close to the strepsirrhine regression of taxa with a low incidence of leaping (Fig. 3), such as the quadrupedal aye-aye and Cebus apella (Curtis and Feistner 1994; Gebo 1989a, b, respectively), or the suspensory Ateles and Hylobates; the similar degree of distal calcaneal elongation displayed by groups with different leaping frequencies, such as lemurids when compared with indriids and lepilemurids (Gebo and Dagosto 1988); and the wide spectrum of leaping frequencies displayed among closely related taxa with similar calcaneal proportions, such as cheirogaleids (Martin 1979). On the other hand, the marked degree of distal calcaneal elongation displayed by galagos and tarsiers clearly differs from the generalized proportions displayed by indriids, in spite of the fact that both groups are equally committed to leaping (>40% of their locomotor behaviours; Gebo 1987, 1988; Gebo and Dagosto 1988). These differences are attributable to a compromise with other types of locomotion (especially climbing), a biomechanically different type of leaping (thigh-powered instead of foot-powered), and differences in body size (Demes et al. 1996; Gebo 1988; Rollinson and Martin 1981). Considering these facts, it is highly unlikely that a moderate lengthening of the distal portion of the calcaneus can be interpreted as reflecting a higher emphasis on leaping, as argued by previous authors (Dagosto 1988, 1990; Gebo 1986; Covert 1988; Gebo et al. 2000a; Martin 1972, 1979, 1990).
Morton (1924) described two types of foot in primates, on the basis of the habitual position of the fulcrum: the ‘metatarsi-fulcrumating’ foot, typical of anthropoids and many non-primate mammals, with the fulcrum situated on the metarsal heads; and the ‘tarsi-fulcrumating’ foot, typical of prosimians, with the fulcrum situated on the distal tarsal bones, with the hallux and the other digits performing a tightly clasping action, while the metatarsals act passively as a span (Fig. 5). For our analysis of calcaneal proportions, the ‘tarsi-fulcrumating’ model of Morton (1924) is important because it allows identifying an important effect of the grasping adaptation of the foot: the posterior shifting of the fulcrum and its locomotor consequences.
The foot works as a second-class lever, in which the muscular force is applied to the tuber calcis (gastrocnemius, in-force), raising the load (partial body mass, out-force) at the ankle joint through rotation at the fulcrum (metatarsals or phalanges in generalized mammals and tarsus in most primates) (Fig. 5). Biomechanically, the distal calcaneus and consecutive segments such as the distal tarsals and metatarsals (depending on the species) are the load arm and their length permit the leverage action necessary to move the body. The degree of lengthening determines velocity (space covered by unit of time) (Hall-Craggs 1965; Demes and Günther 1989). The grasping adaptation of the primate foot implies, as an immediate biomechanical consequence, that the load arm is dramatically reduced, because the weight is transmitted to the branch by means of the webbing between digits one and two. The more proximal position of the fulcrum on this type of foot would imply an increase in the mechanical advantage of the muscle force, but a concomitant reduction in velocity. In a tarsi-fulcrumating foot, the leverage action that non-primate mammals accomplish with the metatarsals must necessarily be carried out by the tarsal segment of the foot, posterior to the new fulcrum position. Thus, the reduction of the load arm of the foot needs to be compensated by a lengthening of the tarsus (mainly the calcaneus) in all grasping primates, but particularly in the tarsi-fulcrumating prosimians, where the metatarsals are not involved in propulsion at all. In fact, this interpretation of Morton’s model contrasts with other views that admit that “the lengthening of the tarsus is an adaptation to increase the effective length of the hind limb so that a more powerful leap can be produced” (Dagosto 1988). The current belief that the lengthening of the tarsus indicates leaping adaptations largely stems from the latter interpretation.
However, our allometric analysis clearly reveals, in agreement with some views (Dagosto 1990; Martin 1990) but in strong contrast to others (Gebo 1986; Gebo et al. 2000a; Morton 1924), that the ‘metatarsi-fulcrumating’ primates (anthropoids) also display a relatively elongated distal portion of the calcaneus, although to a lesser degree than prosimians. The adaptation of the foot to grasping in both prosimians and anthropoids therefore explains the higher relative distal calcaneal length of primates as a whole when compared with other mammals, whereas the greater emphasis on grasping and the associated ‘tarsi-fulcrumating’ foot of prosimians explains their higher degree of distal calcaneal elongation (except in the slow-climbing lorisids) when compared with the more cursorial anthropoids. In spite of using their foot in grasping postures during locomotion, anthropoids frequently employ their metacarpal heads as a fulcrum during horizontal quadrupedalism. On the contrary, the foot of most prosimians is adapted to vertical clinging, therefore implying that the distal tarsal bones are much more frequently employed as a fulcrum when compared with anthropoids.
To sum up, the widely accepted hypothesis that distal calcaneal elongation, irrespective of its extent, is related to leaping improvement (Dagosto 1988; Martin 1993) is rejected by our analysis. Instead, grasping would act as a functional constraint determining that the tarsal segment must accomplish the leverage action of the foot. The moderate degree of distal calcaneal elongation displayed by primates as a whole when compared with other mammals might be simply related to the need to compensate for the reduction of the load arm due to grasping adaptations. The differences in calcaneal elongation between anthropoids and prosimians could be related to the different foot postures habitually employed by both groups. In this context, the anthropoid-like moderate elongation present in lorises might be explained by their adaptation to slow-cautious climbing, which does not require the same degree of lengthening than in other primates with more active locomotion. Our allometric analysis of calcaneal proportions in primates and other mammals thus clearly indicates that a moderate degree of calcaneal elongation cannot be interpreted as indicating a higher emphasis on leaping, but is merely a biomechanical compensatory remodelling required by the acquisition of a grasping foot. Under this perspective, only when the calcaneal proportions depart from the size-scaling relationships of non-specialized primate groups (prosimians and anthropoids), can leaping locomotion be inferred on the basis of distal calcaneal length.
Calcaneal proportions in Anchomomys and other fossil primates
The measurements of the Anchomomys calcaneal specimens analyzed in this paper (Fig. 2) have been reported in Table 1, whereas a succinct description is provided below. The calcanei from both localities are quite similar to one another, although that from Sant Jaume de Frontanyà is slightly larger than the one from Caenes, potentially reflecting interspecific differences. Morphologically, these calcanei are narrow and elongated, with a proportionally long distal portion and a short heel process. The posterior calcaneal facet is relatively long and proportionally narrow, especially in the specimens from Sant Jaume de Frontanyà. The section of the heel process is ovoid (mediolaterall compressed), and the section of the anterior part is triangular. The peroneal tubercle is moderately sized, while the calcaneocuboid joint is broad, fan-like, deep and plantarly open where the pivot is situated. There is a large distal plantar tubercle for the calcaneocuboid ligament. This association of features is somewhat peculiar, because in spite of the omomyoid-like appearance and proportions, the adapid affinities of the material can be readily recognized on the basis of the long and narrow posterior calcaneal facet, as well as the morphology of other postcranial elements from Sant Jaume de Frontanyà (Moyà-Solà and Köhler 1993).
Somewhat surprisingly, the calcaneus of A. frontanyensis has, in spite of being an adapoid, omomyoid-like overall proportions. However, the allometric analysis reported in this paper clearly shows that, when size-scaling considerations are taken into account, the calcaneal proportions of A. frontanyensis (Fig. 2; Table 1) are the expected ones for a primate with a ‘tarsi-fulcrumating’ foot of its small size (Figs. 3, 4). Omomyoids are customarily considered more specialized leapers, whereas adapoids are usually interpreted as more generalized quadrupedal animals with more restricted leaping adaptations. We show here, however, that the apparently peculiar calcaneal proportions of A. frontanyensis merely result from size-scaling effects, so that they do not indicate any particular emphasis on leaping behaviours. This agrees with other postcranial features of this taxon, such as the long and narrow (adapoid-like) proximal calcaneal facet, the general morphology of the talus—including the talofibular joint that gently slopes laterally and the lateral position of the groove for the tendon of the flexor hallucis longus (Moyà-Solà and Köhler 1993)—and even the femoral anatomy, which shows a generalized quadrupedal pattern without specific leaping features (SMS, unpublished data). This does not mean that A. frontanyensis never leaped, but merely that this taxon lacks the high degree of leaping specialization that is displayed by extant tarsiers and galagos. This is confirmed by the overall postcranial anatomy of the former, which fits well the pattern of a quadrupeal and climbing prosimian with low incidence of leaping. Hence, when size-scaling effects are taken into account, the calcaneal proportions of A, frontanyensis, apparently unusual for an adapoid, are best interpreted as the expected proportions for a small-bodied primate with a grasping and a prosimian-like foot with a proximally-placed fulcrum, adapted to vertical clinging, but with no particular emphasis towards leaping.
With regard to other fossil primates, no significant departure from the expected calcaneal proportions for a primate with a ‘tarsi-fulcrumating’ foot of their size are found in fossil galagids (Komba and Progalago from the Miocene of East Africa), omomyids or eosimiids, contrary to what would be expected if they were committed leapers (Figs. 3, 4). This fact does not imply that leaping adaptations cannot be confidently inferred from of other skeletal features in these taxa (Dagosto 1988; Walker 1970; Gebo 1987, 1988, 1989a, b; Gingerich 1981). Rather, it merely means that, on the basis of calcaneal proportions, no special adaptations to leaping can be inferred. Eosimiids, which are considered putative stem anthropoids (Beard et al. 1994, 1996), display anthropoid-like calcaneal proportions, which contradicts previous inferences of leaping adaptations on the basis of a moderate calcaneal elongation (Gebo et al. 2000a, b), but agrees with the frequent use of horizontal foot postures that has been inferred from several pedal elements (Gebo et al. 2000b), as in extant anthropoids. In this regard, eosimiids resemble the larger-bodied, stem anthropoids from Africa (propliopithecoids). To sum up, the previous interpretation of calcaneal elongation in omomyoids and eosimiids as a leaping adaptation is not supported by our analysis. On the contrary, the high ACL/TCL length ratio in Eosimias is merely a consequence of its small body size, as in A. frontanyensis.
On the other hand, some adapines (Adapis and Leptadapis) from the Eocene of Europe display a shorter ACL than expected on the basis of BM (even shorter than in lorisids), displaying an intermediate condition between anthropoids and non-primate mammals. Their calcaneal proportions are unusual for a primate with a grasping foot (Martin 1979, 1990), particularly as judged on the basis of the long, robust and abductable hallux (Dagosto 1983). This led to different interpretations, suggesting either that these calcanei had been misidentified as primate (Martin 1979), that they represent a secondary reversal to the ancestral euprimate condition (Dagosto 1983), and/or that they reflect an adaptation to slow arboreal locomotion (Martin 1993). The proportions of the adapine calcaneum, with very short ACL, together with other morphological similarities to lorisids (Dagosto 1983), suggest that, like the latter group, adapines probably never leaped and had a very slow-moving locomotion, therefore confirming previous suggestions (Dagosto 1983; Martin 1993) that fossil European adapines were specialized slow-quadrumanous climbers similar to the extant Nycticebus (Dagosto 1983, 1993).
Implications for reconstructing the ancestral euprimate locomotor repertoire
For more than a half-century, two competing views on the reconstruction of the ancestral locomotor adaptations of earliest euprimates have been under discussion: the vertical clinging and leaping (VCL) (Napier and Walker 1967) and the nocturnal visual predation (NVP) (Cartmill 1972) hypothesis. Napier and Walker (1967) suggested VCL to constitute the ancestral locomotor behaviour of euprimates. Although still a matter of debate (Anemone and Covert 2000; Dagosto 2007; Demes and Günther 1989; Gebo 1986; Gebo et al. 2000a, b; Gingerich 1981; Lemelin and Schnidt 2007; Szalay and Dagosto 1988), this notion has not changed substantially since its initial proposal, and leaping has figured prominently in subsequent refinements of this hypothesis, as shown by definitions such as ‘hind limb dominated locomotion’ (Rollinson and Martin 1981) or ‘grasp-leaping’ (GL) (Dagosto 1988, 2007; Szalay and Dagosto 1980). In strong contrast, Cartmill (1972, 1974) proposed a slow moving quadrupedal ancestor with grasping extremities related to NVP as a model for the last common euprimate ancestor. On the basis of different sources of evidence, this hypothesis is supported by other authors (Anemone 1990; Ford 1988; Godinot 2007; Lemelin and Schnidt 2007; Schnidt and Lemelin 2002). In fact, the basic point of disagreement between both views is the role of leaping in earliest primates’ locomotion.
The hypothesis that leaping played an essential role in euprimate origins stems mainly (but not exclusively, see Dagosto 2007) from the distinctive elongation of the distal foot elements, such as the navicular, the neck of the talus and the cuboid and specially the calcaneus, in most Palaeogene primates and extant strepsirrhines. These euprimate traits, more accentuated in prosimians than in anthropoids (Ford 1988; Gebo 1986), have been considered a biomechanical innovation in the lever system of the foot enabling to increase the effective length of the hind limbs, so that a more powerful leap can be produced (Hall-Craggs 1965; Dagosto 1988, 2007). According to this hypothesis, euprimates would have resorted to lengthening their tarsal elements for leaping across large gaps within an arboreal environment, because their metatarsals are involved in grasping (Dagosto 1988; Morton 1924). Lengthening of the distal tarsals has been therefore considered a functional alternative to the lengthening of metatarsals, which is the normal condition in other specialised jumpers (e.g., Jacculus, kangaroos, rabbits etc.) (Dagosto 1988). This hypothesis played also an important role in the reconstruction of the ancestral morphotype of the Anthropoidea. The apparently somewhat elongated anterior calcaneus of Eosimias has been therefore interpreted as a primitive feature shared with omomyoids, a suggested sister-group of anthropoids (Gebo 1988), being interpreted as evidencing a leaping ancestry for anthropoids (Gebo et al. 2000b).
On the contrary, the alternative interpretation is presented here that the moderately elongated distal calcaneus and, by extension, tarsus of primates is a compensatory mechanism to recover the lost load arm (metatarsal length) when the foot adopts the grasping function, instead of a leaping adaptation. This interpretation has important implications for the discussion on earliest euprimates locomotion. Under our point of view, the moderately long tarsus of most primates merely stresses the significance of grasping as the original primate adaptation. The fact that, apart from Morton’s (1924) work, no attempt has been made to understand the mechanical consequences of the structural changes in the foot related to grasping (e.g., the posterior shift of the fulcrum) has led to overestimating the leaping signal of tarsal lengthening in primates, particularly because some extant forms showing a very long tarsus are strongly committed to leaping. Of course, an analysis of a single feature in a single bone, such as calcaneal proportions, is insufficient to make general conclusions on the locomotor morphotype of the earliest primates. Moreover, a reappraisal of all the features functionally related to leaping/quadrupedalism in primates is beyond the scope of this work. However, the fact that primates as a group display a relatively longer distal calcaneus when compared with other mammals emphasizes the fundamental role of grasping in primate origins. In particular, our results strongly indicate that the VCL hypothesis needs to be revised by taking into account that a moderate foot elongation cannot be used to infer leaping adaptations in earliest primates.