Adaptations towards herbivory in the carnivoran skull
Our results demonstrate that skull shape correlates with feeding behaviour. PCA of mandibles and crania suggest that, with the only exception of the bushy-tailed olingo (B. gabbi), all herbivorous species of Procyonidae (P. flavus), Ailuridae (A. fulgens) and Ursidae (A. melanoleuca and T. ornatus) share a set of common traits in their craniodental anatomy and specially for those morphological aspects recovered from the first two PCs in the case of the mandible and from PCI and PCIII in the case of the crania (Fig. 3a,d). These features relate to the capacity to exert high bite forces and include a stoutly built mandible with a deep mandibular corpus, an enlarged coronoid and well-developed lower post-carnassial molars, as well as a deep brachycephalic cranium with well-developed zygomatic arches, a short neurocranium and enlarged upper molars (Fig. 3). On the one hand, an elongated coronoid and an enlarged angular process are indicators of long lever arms for the temporalis and masseter muscles, respectively (Fig. 1c–e), and thus can be used as proxies for the input moment arms of these masticatory muscles (Turnbull, 1970; Van Valkenburgh & Ruff, 1987; Bicknevicius & Van Valkenburgh, 1996; Van Valkenburgh et al., 2003; Christiansen & Adolfssen, 2005; Palmqvist et al., 2007; Figueirido et al., 2010). On the other, a brachycephalic cranium reduces the output moment arms of the masticatory muscles (Fig. 1c–e), increasing the load exerted with the carnassials or the canine teeth (Christiansen & Adolfssen, 2005; Wroe et al., 2005; Christiansen, 2007; Christiansen & Wroe, 2007). In addition, a high cranium with a deep mandibular body is better suited for dissipating the high torsional forces generated in the parasagittal plane when the herbivorous carnivorans chew on tough foods with their enlarged molar teeth (Bukland-Wrigth, 1971, 1978; Werdelin, 1989; Biknevicius & Ruff, 1992). These results agree with the findings of Christiansen & Wroe (2007), who showed that the carnivorans that feed on fibrous plants have higher bite forces than those species of similar size that are specialized insectivores, omnivores or even carnivores that take small prey. In fact, only those carnivores that prey upon ungulate prey much larger than themselves and those specialized in the consumption of vertebrate carrion (e.g. the wolverine, Gulo gulo) parallel the bite force of herbivorous carnivorans (Christiansen & Wroe, 2007).
We have identified a set of common functional traits in the carnivoran skull that allow specializing on an herbivorous diet. As a result, we identify these morphological traits as common adaptations towards herbivory in the carnivoran skull, except in the bushy-tailed olingo.
Evolutionary constraints in the skull of herbivorous carnivorans
In this study, we have shown that skull shape does correlate not only with feeding behaviour but also with phylogenetic legacy. As stated earlier, all the adaptations of the carnivoran skull towards herbivory have been interpreted as functional traits that allow exerting high bite forces and such traits are similar to those of the hypercarnivorous species that subdue large vertebrate prey (Christiansen & Wroe, 2007). At first sight, this fact seems to be counterintuitive if we do not pay attention to historical contingency.
All the herbivorous carnivorans evolved from a generalized carnivorous mammal (Van Valkenburgh, 2007), with a body plan early established in the phylogeny of Carnivora. Therefore, the remarkable morphological resemblance of the skull among the herbivorous carnivorans was most probably driven by extrinsic factors (e.g. natural selection) as well as by intrinsic ones (e.g. a shared developmental pathway) and the latter may have posed constraints (sensuAlberch, 1982) on the direction of skull shape evolution towards herbivory. Thus, the adaptations of herbivorous species for exerting high bite forces are constrained functional solutions that were reached in a process driven by natural selection within the set of possibilities allowed by phylogenetic legacy.
The herbivorous carnivorans retain the simple stomach (i.e. without a caecum) and short gastrointestinal tract typical of carnivores, in contrast to the chambered stomachs and complex intestinal morphologies of ruminants and other mammalian herbivores (Roberts & Gittleman, 1984; Schaller et al., 1985; Johnson et al., 1988; Bleijenberg & Nijboer, 1989; Reid et al., 1991). Microbial digestion only plays a minor role in the digestive strategy of carnivorans, resulting in a low digestibility rate for cellulose and other complex carbohydrates (Wei et al., 1999, 2007; Senshu et al., 2007). Furthermore, all carnivores have a fixed temporomandibular joint (Ewer, 1973) which, together with their enlarged canine teeth, limits jaw movements to the vertical plane, with some lateral movements for grinding (Davis, 1964). This prevents the teeth from being occluded simultaneously for grinding tough foods, as in ungulates. As a result of these limitations, herbivorous carnivorans must eat huge quantities of food, which forces the development of the main muscles involved in mastication (i.e. masseter and temporalis), hence the capacity for exerting similar bite forces than those of carnivorous mammals that usually hunt prey much larger than themselves. The need in a carnivoran for high input moment arms for the temporalis and masseter muscles translates in the development of a long coronoid and an enlarged angular process, which precludes the development of a wide gape.
Constraints on digestive tract and craniomandibular morphology as a result of a basic body plan adapted to carnivory have resulted in a very different set of solutions in herbivorous carnivorans, compared to ungulates. Skull shape in herbivorous carnivorans evolved towards the capacity of exerting a high bite forces in a process that paralleled the evolution of hypercarnivores. The same adaptive solution (i.e. an increase in bite force) was taken for reaching two opposite feeding strategies (i.e. herbivory and hypercarnivory) through carnivoran evolution. This strongly suggests that not all possible adaptive solutions are under the domain of natural selection, which operates on the variability available by the phylogenetic legacy of each particular group.
The role of natural selection and historical contingency in shaping the skull design of herbivorous carnivorans
The combined effects of phylogenetic legacy and natural selection for shaping cranial design have led to repeated patterns of biomechanical homoplasy in the evolution of the carnivoran skull towards herbivory. In fact, in this study we identify several of these patterns. This is especially the case of jaw shape in the giant panda (A. melanoleuca), an ursid, and the red panda (A. fulgens), an ailurid (Fig. 4a; Fig. 5a), which both feed on bamboo (Table 1; Appendices S1 and S2). This result is also confirmed by the evidence from the fossil record. In fact, the earlier fossil remains of the Ailuropoda lineage (e.g. the Miocene Ailurarctos from China) have an incipient crushing dentition adapted for a durophagous diet and the late Pliocene Ailuropoda microta and Ailuropoda wulingshanensis have intermediate tooth morphologies between Ailurarctos and the living A. melanoleuca (Qiu & Qi, 1989; Hunt, 2004; Qi et al., 2006; Jin et al., 2007). Similarly, the fossil record of the most basal ailurids such as the species of Simocyon (Miocene of Europe and North America, Mio-Pliocene of Asia) and Amphictis (Oligo-Miocene of Eurasia) do not show the specialized skull morphology of the red panda, which suggests that their common ancestor was a generalized carnivore, not a bamboo feeder (Salesa et al., 2006). However, it is worth noting that Pristinailurus bristoli from the Mio-Pliocene of North America has intermediate mandibular and dental morphologies between the species of Simocyon and the living Ailurus (Wallace & Wang, 2007). Therefore, both the reconstructed evolutionary trajectories and the fossil evidence more robustly support the independent evolution towards bamboo feeding between the distantly related Ailurus and Ailuropoda. As a result, it is striking that two distantly related species that diverged > 40 Ma ago (Goldman et al., 1989; Ledje & Arnason, 1996; Flynn & Nedbal, 1998; Bininda-Emonds et al., 1999; Ginsburg, 1999; Flynn et al., 2000, 2005; Angarsson et al., 2010) have extremely similar mandibles. This indicates the strong role of the phylogenetic legacy (i.e. the existence of a shared and stable developmental path established early in the evolutionary history of the carnivorans) as well as the consequences of the biomechanical limitations for shaping jaw design. However, this pattern could be also explained by a remarkable evolutionary plasticity and/or a strong effect of natural selection.
Another incipient pattern of jaw homoplasy can be reported for the kinkajou (P. flavus), a procyonid, and the spectacled bear (T. ornatus) (Fig. 4a,d; Fig. 5a), which both are mainly frugivores (Table 1; Appendices S1 and S2). Although in this case the pattern of homoplasy is not as evident as in the case of pandas, again the evidence from the fossil record of Potos and Tremarctos confirms the independent evolution of similar morphologies. In fact, the earlier tremarctine known from the fossil record is the early Miocene, North American Plionarctos, which retains a primitive tremarctine mandible without a premasseteric fossa (Tedford & Martin, 2001). The Tertiary record of procyonids shows that some primitive procyonids like the Miocene Broiliana from Europe has a mesocarnivorous dentition (Baskin, 1982, 2004). Furthermore, Parapotos tedfordii from the Miocene of North America (Baskin, 2003) shows intermediate mandible features between Broiliana and the extant frugivorous P. flavus (F.J. Serrano-Alarcón, personal observations).
Strikingly, the specific patterns of homoplasy reported for the evolution of jaw morphology towards frugivory or bamboo feeding did not arise in the evolution of cranial shape (Figs 4d and 5b). In our opinion, this probably reflects the greater evolutionary plasticity of the mandible compared with the cranium (Barone, 1986). Jaw morphology is mainly related to food acquisition and processing, whereas cranial shape is the result of conflicting demands between different functions (e.g. feeding, olfaction, vision and brain processing; Figueirido et al., 2009). For this reason, although a set of functional cranial traits can be identified as common adaptations towards herbivory in carnivorans, no specific mechanical adaptation towards frugivory or bamboo feeding is evident. In contrast, these adaptations are reflected in the morphology of the mandible, giving rise to repeated patterns of homoplasy among frugivores, on the one hand, and among bamboo feeders, on the other. This strongly suggests that studies of morphological integration between mandible and cranial shape are necessary for understanding the correlated evolution of these two structures that conform the skull.
Patterns of biomechanical homoplasy among carnivorans have been exemplified in a number of studies on the evolution of hypercarnivory (including bone-cracking adaptations) in distantly related lineages (e.g. Werdelin, 1989; Van Valkenburgh, 1991, 2007; Holliday & Steppan, 2001; Van Valkenburgh et al., 2003; Wroe & Milne, 2007; Wroe et al., 2007). In spite of the fact that herbivorous carnivorans represent also an excellent choice for exploring the role and limits of natural selection and historical contingency in sorting phenotypic variation, patterns of evolution towards herbivory remain largely unexplored. Our findings show that several skull traits that allow increasing bite force have been shaped in the carnivorans as adaptations for an herbivorous diet. Several evolutionary constraints arising from the peculiar phylogenetic legacy of the carnivoran skull have limited the range of adaptive possibilities that natural selection could follow. This fact indicates that few adaptive solutions allow a carnivoran to behave as a strict herbivore. As a result, phylogenetic legacy and natural selection have interplayed during the evolutionary history of carnivorans, giving rise to repeated patterns of biomechanical homoplasy. In this regard, we have recognized the three types (or levels) of homoplastic patterns proposed by Stayton (2006) within our skull shape data. In fact, we have found type II pattern of homoplasy (i.e. partial convergence) in all herbivores: although their shapes are not identical, these species show similar deviations from their sister groups and, as a result, are more similar to other herbivorous carnivorans than to their closest relatives (Fig. 3a,d). In contrast, a type I pattern (i.e. complete convergence) has emerged in the nearly identical mandibles of the two bamboo feeders (Fig. 4a) and type III (i.e. parallel evolution) most probably has taken place in the mandibles of frugivores, as they show some parallel changes from their sister groups (Fig. 4a).
Homoplasy is a key concept in evolutionary theory. Quantitative documentation of homoplasy has provided new advances for the study of adaptation (e.g. Wroe & Milne, 2007), constraints (e.g. Herrel et al., 2004) and paleobiology (e.g. Van Valkenburgh, 1991), providing support for a better understanding of the evolutionary history of phenotypes (Stayton, 2006). As a result, the quantification of the homoplastic patterns carried out in this article could ultimately be performed to other taxa and ecological niches. Our findings clearly demonstrate the importance of incorporating historical approaches in morphometric analyses for understanding the role and limits of natural selection and historical contingency in sorting morphological and ecological diversity as key elements of evolutionary theory.