Phylogenetic position of palaeomerycids within the Pecora

The Palaeomerycidae is a monophyletic group of pecorans diagnosed by the presence of a single forked occipital appendage formed by the elongation of the supraoccipital and the nuchal plane, presence of nuchal fossa, Palaeomeryx-fold in the lower molars, and a laterally-oriented expansion of the nuchal crest. As we will discuss later, our phylogenetic hypothesis reconstructs the presence of ossicones as a basal feature of all the giraffomorphs. We define the Palaeomerycidae as the least inclusive clade of pecorans containing Triceromeryx and Ampelomeryx. Much has been written on the Palaeomeryx-fold, also known by the more ‘neutral’ name of external post-protocristid [71], as a primitive and unique structure that disappears in the more advanced forms within the different pecoran lineages. Our present work helps to reject this pre-conception and show the Palaeomeryx-fold (or better said the different Palaeomeryx-folds, because several morphologies of this post-protocristid fold exist) as a structure that has appeared several times within different unrelated lineages of pecorans (e.g. palaeomerycids and moschids) and has also been secondarily lost in others (e.g. cervids). The Palaeomeryx-fold is not the only known dental structure of pecorans that secondarily appears in a given lineage. The case of the metastylids and other dental structures of the moschid Hispanomeryx andrewsi [45] perfectly pictures how plastic the pecoran dentition can be, and how supposedly ‘primitive’ and previously lost dental structures can be ‘regained’ into a clade of relatively derived pecorans. Palaeomerycids are also characterized by a highly modified occipital area. The nuchal fossa and the expansion of the nuchal crest were never described before and are related with an extension of the surface area for the insertion of the neck musculature, both longitudinally (nuchal fossa) and laterally (expansion of the nuchal crest). The latter allows for a more pronounced lateral bounding of the head. As commented in the description of Xenokeryx, the nuchal fossa receives the insertion of the extensors muscles rectus capitis dorsalis, semispinalis capitis and the rectus capitis dorsalis minor. As such, the longitudinal expansion of all these muscle packs would allow for a more powerful head extension. Also, as noted by Astibia et al. [24] the neck musculature probably climbed the most basal part of the occipital appendage acquiring a relatively pronounced angle in its occipital insertion, thus helping in the enhanced head extension of palaeomerycids. These neck-head modifications resulted in powerful lateral and dorsal movements of the head although their exact purpose is not known, and both ecological and behavioral morpho-functional hypotheses could be suggested (e.g. male intraspecific fighting is an obvious one) but we have no data to back up any of them.

We support the hypothesis of a very close relationship between palaeomerycids and giraffoid pecorans (the clade that includes Giraffa and Prolibytherium, their more recent common ancestor and all of its descendants). The Giraffomorpha is defined here as the least inclusive clade containing Giraffa and Triceromeryx. We reject the assignment of Prolibytherium to the Palaeomerycidae proposed by several authors [10,27,29], and confirm its arrangement within the Giraffoidea [11, 26]. However, Prolibytherium does not cluster with the Climacoceratidae, so we also reject our previously proposed hypothesis of a sister-group relationship between Prolibytherium and the true climacoceratids such as Orangemeryx [26].

As we already commented, the systematics and phylogenetic relationships of palaeomerycids were controversial. Many authors [4,5,13,27,29,34,35,72] considered the Palaeomerycidae as members of the Cervoidea (the pecoran forms more related to cervids than to another of the extant ruminant families). Janis & Scott [27], which offered an extensive revision of the Cervoidea, supported the cervoid affinities of palaeomerycids on the presence of distally closed metatarsal sulcus (a character widely used by other authors as well), presence of Palaeomeryx-fold in the lower molars, sabre-like upper canine in males, and presence of plantar metatarsal tuberosity in the metatarsal III-IV. However, palaeomerycids and giraffoids form a well-supported clade of giraffomorph pecorans in our phylogenetic tree (PP = 0.93). The hypothesis of relationship of palaeomerycids and giraffoids was already proposed by several authors mainly on the basis of the presence in both groups of ossicones and a suite of cranial, dental and postcranial characters [15,21,36]. However Janis & Scott [27] dismissed this hypothesis arguing that all these characters (including the presence of ossicones) were convergences, but Solounias [10] again resurrected the presence of ossicones as a feature that probably related palaeomerycids and giraffoids. In the meantime, Ginsburg [28] related palaeomerycids with dromomerycids and this group with giraffids and bovids, including all of them in the Bovoidea. That work was a good example of how almost all possible hypotheses of relationship were suggested for palaeomerycids. The reconstructed synapomorphies that link palaeomerycids with giraffoids in our tree include both cranial (morphology of the retroarticular process; contact between the retroarticular process and the external acoustic tube; laterally enclosed temporal canal; well-marked lateral margin of the infratemporal fossa; and presence of ossicones) and postcranial features (central plantar column of the metatarsal III-IV; absence of supraarticular fossetes in the metatarsal III-IV; and presence of a well-developed crest in the planto-medial area of the navicular-cuboid that does not reach the proximal region of the planto-medial process). The distribution of the condition of the metatarsal sulcus among pecorans cannot be used alone to link cervids with other groups. Palaeomerycids display a ‘moschid-type’ disposition of the sulcus for the common digital artery [26], which is the most common state among pecorans. When the digital artery is of moschid-type (superficial but not as superficial as in crown bovids), both conditions of the sulcus, open and closed, are expected to appear (e.g. the case of the Moschidae is archetypical of this). The true cervoid condition (see character 53) is the presence of a deep sulcus (cervid-type) that runs through the very middle of the shaft and fixes the distally closed condition of the gully. Hence, as occurs with moschids [26] the distal closing of the gully (character 58) is a parallelism between palaeomerycids and the inclusive clade that contains cervoids and their stem hornless forms (node E; Fig 9). Also, as in [26] the presence of a metatarsal tuberosity (character 56) does not appear in this work as a unique condition of cervoids since it is also present as a parallelism in other non-cervoid groups (e.g. moschids). In addition, in palaeomerycids and their closest sister-group Propalaeoryx this proximo-plantar tuberosity in the metatarsal III-IV is not as developed as in cervids, dromomerycids and moschids. Regarding the enlarged sabre-like canines of males, palaeomerycids had a moschid-type canine (with a characteristic double curvature;[26]), being this morphology basal and widespread among pecorans. Moreover, cervids (with the exception of the secondarily ‘fanged’ Hydropotes) possess a derived kind of enlarged canines that lack the double curvature of the moschid-type (cervid-type). The morphology of the plantar surface of the navicular-cuboid appears to be of the upmost importance for grouping the giraffomorphs together in our phylogenetic tree. This is also the case with the bovidomorphs, that show a characteristic featureless plantar surface of the navicular-cuboid, but this group is not to be discussed here. Giraffomorphs possess a well-developed crest that rise from the distal part of the planto-medial surface of the navicular-cuboid but does not reach the proximal border. This feature (character 62) becomes very exaggerated in giraffids, the navicular-cuboid of which has a complete crest. Also, the canal that runs laterally to this crest is more developed, with a marked concavity, in the Giraffoidea. Giraffomorphs are also characterized by the absence of supra-articular fossetes in the metatarsal III-IV (character 57). Analogous structures to the supra-articular fossetes of pecoran ruminants have been described in other ‘ungulate’ groups and related to improved running abilities [42] due to the augmented extension capability of the phalanges that enhance the elastic charge of the interosseus and flexor tendons that run on the plantar side of the feet. However this is difficult to quantify and we do not know the influence of the presence / absence of supra-articular fossetes in the biomechanics and running capabilities of pecorans. Nevertheless, it seems that the absence of these structures is a fairly good phylogenetic signal for giraffomorphs. Interestingly enough, the presence of ossicones (character 13) is recovered as a basal feature for the Giraffomorpha and not as a parallel development in giraffids and palaeomerycids. This phylogenetic reconstruction establishes an evolutionary hypothesis that implies a basal homology of the appendages of Prolibytherium and climacoceratids with the ossicones despite their disparate external morphologies, both coded here as different character states [2,12]. This is a very interesting question that could only be fully answered through a comparative histologic analysis of the supra-orbital cranial appendages present in every giraffomorph group from which these cranial structures are known.

The Eurasian palaeomerycids share a common ancestor with the Miocene African pecoran Propalaeoryx. Remains of this genus have been found in both South and East Africa [11, 30, 48, 72]. It was accepted that Propalaeoryx was a member of the Giraffoidea [11,27,30,48] with some authors regarding it as a climacoceratid within giraffoids [11,48], an exclusively African family that contains forms such as Orangemeryx, included in this work. Propalaeoryx appears with a high support as the closest sister-group to the Palaeomerycidae (PP = 0.91), and hence we reject the hypothesis of Propalaeoryx belonging to both the Climacoceratidae and the Giraffoidea. Apart from postcranial features such as the distally closed metatarsal gully and the previously commented small version of the metatarsal tuberosity, the most intriguing of the derived traits shared by palaeomerycids and Propalaeoryx is the presence of a deep dorso-ventral rectilinear groove located between the caudal part of the temporal fossa and the nuchal plane (character 25). The function of this groove is unknown, although it strongly resembles a robust superficial vascular canal. The close relationship of palaeomerycids and Propalaeoryx probably implies a vicariance event that took part in the Oligocene / Miocene boundary (~24 Ma) that split-off the original common lineage into two branches, African and Eurasian. Thus, the evolutionary history of giraffoids-giraffomorphs (and of palaeomerycids themselves) results more complicated than previously thought. Whereas palaeomerycids preserved a more primitive type of dentition, Propalaeoryx shows a mosaic pattern of derived dental traits (more flattish and higher-crowned cuspids) with primitive features as the retention of the p1 [11,30]. As of today, there is no evidence of cranial appendages in Propalaeoryx, and resolving this issue with future discoveries should clarify the pattern of evolution of the supra-orbital appendages of giraffomorphs.

A clade containing dromomerycids and cervids placed within a more inclusive clade well differentiated from giraffomorphs is well supported in our phylogenetic tree (P = 1.0), thus corroborating the hypothesis of dromomerycids and palaeomerycids not being sister groups or even closely related into a major inclusive clade. We reject the proposals of Janis & Scott [27] and Prothero & Liter [29] that regarded the frontal appendages of palaeomerycids and dromomerycids as ‘labile and variable’ within a ‘family Palaeomerycidae’ that contained both ‘palaeomerycines’ and ‘dromomerycines’. Dromomerycids have supra-orbital appendages that never show the macroscopic features and suture with the skull roof associated with giraffid and palaeomerycid ossicones. They probably represent apophyseal structures [1], but a histological study of these supra-orbital appendages is needed to comprehend their true nature. The occipital appendage of dromomerycids is also completely different in morphology and probably in origin. First of all, it is not universally present in the Dromomerycidae, whereas all known cranial remains of male palaeomerycids with preserved occipital area present the occipital appendage. In dromomerycids this element is a sub-cylindrical structure that grows up from the supra-occipital (at the end of the sagittal line of the cranium) creating a single, non-forked rod. In palaeomerycids the occipital appendage not only involves a more or less vertical growth of the supra-occipital area, but also a lateral expansion that results in the integration of areas belonging to the occipital crest and in the development of an appendage that is not the cylindrical rod of dromomerycids but a laterally expanded structure that becomes broad and elliptical or flattish in cross-section [24]. Also, the nuchal plane gets reorganized, extending upwards and forming the well-developed pit that we name here as the nuchal fossa. However, in dromomerycids this kind of reorganization does not occur and the nuchal plane presents the rectilinear and concave morphology (with a subtle crest in the sagittal plane) typical of ruminants. Apart from the cranial appendages, dromomerycids are set apart from palaeomerycids by a huge set of cranial, dental and postcranial derived features (Nodes E, F and G; Table 3, Fig 9).