The new bovid species from the Middle Awash, at just older than 1.9 Ma, represents another exciting but poorly represented find of an African Plio-Pleistocene fossil caprin. Fortunately, the only known specimen is a partial cranium well-enough preserved to allow for some level of taxonomic diagnosis and phylogenetic analysis. The posterior cranium of Capra wodaramoya is slightly larger than those of a male Ethiopian ibex (C. walie), but the horns of the fossil species are simply massive, approaching the basal proportions seen in a male argali (Ovis ammon). The horns would have coursed upwards and backwards like in the living ibex, and were probably very impressive when complete. This large fossil caprin joins a range of other ‘supersized’ antelopes recorded from the African early Pleistocene, including Megalotragus kattwinkeli Hippotragus gigas, Tragelaphus strepsiceros gigas and Pelorovis oldowayensis. Leakey (1965) noted a period of early Pleistocene gigantism in particular among the fossil taxa of Bed II at Olduvai Gorge. This is a subject area ripe for further research. The general rarity of fossil caprins in the deposits of the eastern African Rift Valley is probably related to their preference for mountainous terrains far from the depositional axis. Their occasional presence, however, probably indicates some tenuous link with nearby mountainous terrain and, in the case of Capra wodaramoya, with the abutting Ethiopian highlands.
The Bayesian analysis of the combined molecular and morphological supermatrix produces a tree (Fig. 2) that is well resolved and reflects a phylogeny more in line with the total evidence than those derived from either data set alone. Separate analyses of the morphological and molecular characters reveal several areas of conflict between the two data sets (Figs. 3, 4), whereas optimization of the morphological characters on the tree from the combined analysis (Fig. S2) reveals areas of consensus. Analyses using parsimony produce trees that are similar to those resulting from Bayesian analysis but often with less resolution or with relationships that are atypical (Fig. 4, Fig. S1).
A common problematic area among all the analyses is that of basal relationships within Caprini. While these appear resolved in the morphological parsimony tree (Fig. 4a), none of the nodes have bootstrap support and the nested position of Pantholops violates caprin monophyly. A lack of resolution at the base of Caprini has plagued most phylogenetic studies to date, leading to suggestions of rapid adaptive radiation shortly after the tribe's origins in the Miocene (Hassanin et al., 1998; Ropiquet & Hassanin, 2005b). We propose that incorporation of more fossil taxa into the phylogenetic framework – especially Miocene caprins (Gentry, 2000) – might help resolve basal caprin relationships through improved morphological character optimization for this part of the tree.
Our Bayesian analysis of the combined molecular and morphological data (Fig. 2) revalidates the sister-group relationship of Pantholops hodgsonii to Caprini, united by possession of a small central incisor, among other characters (Fig S2). Pantholops lacks the key character of shortened metacarpals, which we here take to be diagnostic of Caprini. The chiru has been shown to further differ from caprins in numerous phenotypic, including behavioural, characters (Vrba & Schaller, 2000), and so, while recognizing their sister-clade relationship, we prefer to keep Pantholops and Caprini separate in what is surely a more ecologically meaningful taxonomy.
Lalueza-Fox et al. (2005) found the extinct subfossil Myotragus balearicus to be closely related to Ovis, although with low node support (mostly <50%), and a phylogeny requiring polyphyly of the Caprina. Our Bayesian analyses only recognized clades with ≥50% support, and so we did not recover a similar result. In our analyses, the position of Myotragus is relatively unresolved, forming part of the polytomy at the base of Caprini. Long molecular and morphological branch lengths (Fig. 2) reflect the fact that Myotragus is very highly derived, and its closest relatives among living species may not be easy to recognize.
It is satisfying to see the placement of the Pliocene fossil takin Budorcas churcheri from Hadar (Gentry, 1996) as the sister taxon to the living takin. The presence of a takin – an animal today associated with high altitudes of the Himalayan Plateau – in the late Pliocene of Ethiopia remains curious. Budorcas churcheri indicates that the living takin is a geographical relict, the last remaining of a once more widespread Budorcas clade. The Budorcas clade itself here takes part in the large polytomy at the base of Caprini. Other molecular analyses, however, have sometimes placed the takin closer to Capra (Hassanin et al., 2009), closer to Ovis (Groves & Shields, 1997; Hassanin et al., 1998) or more towards the base of the Caprini (Ropiquet & Hassanin, 2005b).
The morphology-only analyses also recovered a clade uniting Budorcas spp. and Ovibos moschatus. This clade is supported by 2 unambiguous character state changes (29:0-1, horn cores arising behind orbit, and 40:0–1, horn sheath forming a basal boss) in characters that are otherwise homoplastic, and has bootstrap and posterior probability support values that are relatively high (Fig. 4). The concept of a monophyletic Budorcas–Ovibos clade has been effectively buried (Gentry, 1992; Groves & Shields, 1997; Hassanin & Douzery, 1999), and it is interesting to see it resurface here on the basis of morphological apomorphies. Hassanin et al. (2009) used the name Ovibovina for a clade comprising Ovibos+Capricornis+Naemorhedus, which is also recovered here in both the molecular and combined analyses (Figs 2, 3). Morphologically, Ovibovina is supported by a single unambiguously optimized character (lack of horn core compression, which reverts in Ovibos, Fig. S2).
Although its composition has changed, Caprina (traditionally ‘Caprini’) is one of the few traditional subclades of Caprini (traditionally ‘Caprinae’) to have survived recent systematic shakeups. Caprina is here recovered in the morphological and combined analyses, but not in that of the cytochrome b data alone. Morphological support for Caprina is high, with no less than eight unambiguously optimized synapomorphies (Fig. S2). Caprina is the largest resolved subclade of Caprini, comprising the living goats (Capra spp.), sheep (Ovis spp.) and close relatives (Ammotragus, Pseudois, Hemitragus). Hassanin et al. (2009) analysis found support for inclusion of Oreamnos, Rupicapra and Budorcas within Caprina as well.
Hemitragus is by all accounts polyphyletic (Ropiquet & Hassanin, 2005a). Although the three included species are morphologically similar, even our morphology-only analysis did not succeed in creating a Hemitragus clade. Our morphological and combined analyses place Hemitragus jemlahicus as the sister taxon to a monophyletic Capra clade, and not sister to Capra sibirica as found by the cytochrome b analysis. This replicates the results of other studies where mitochondrial phylogenies returned a polyphyletic Capra (Ropiquet & Hassanin, 2005a; Pidancier et al., 2006). Interestingly, these studies also investigated nuclear genes and found that nuclear DNA phylogeny supports monophyly of Capra, consistent with morphological observations.
Similarly, analysis of mitochondrial DNA indicates that ibexes (C. ibex, C. nubiana, C. pyrenaica, C. walie) form a paraphyletic grouping. Nuclear DNA, in contrast, supports monophyly of the ibexes including C. caucasica and C. cylindricornis (Pidancier et al., 2006), again in accordance with our morphological observations (Fig. 4). Our supermatrix analysis (Fig. 2) reflects cytochrome b ibex paraphyly, but is swayed enough by the morphological characters to separate C. sibirica and Hemitragus jemlahicus and recover a monophyletic Capra. Close mtDNA relationships are found between the two African ibexes and also between the two European species.
Monophyly of the genus Capra is well supported by ten unambiguous cranial characters and high bootstrap and posterior probabilities in all analyses. The new Ethiopian fossil species is nested deep within the Capra clade. The affinities of Capra wodaramoya appear to lie specifically with the Eurasian ‘bezoar-type’ goats and not the African or Eurasian ibexes, with biogeographical implications discussed below.
Molecular clock calibration and diversification times
At 1.76 Ma, Capra dalli from the Pleistocene of Georgia (Bukhsianidze & Vekua, 2006) already provided indications of the minimum age of the Capra clade. Now, Capra wodaramoya marginally extends this age further to 1.9 Ma, providing an updated minimum-age datum point that may be used for molecular clock calibration and divergence estimation. Similarly, Budorcas churcheri provides a minimum age of around 3 Ma for the takin lineage.
Lalueza-Fox et al. (2005) produced molecular clock–derived clade divergence estimates for Caprini. Their analysis was based on the mitochondrial cytochrome b and 12S genes and the nuclear 28S rDNA gene and was calibrated using the age of isolation of the Myotragus lineage on the Balearic islands, presumed to be with the end of the Messinian Salinity Crisis at 5.35 Ma. Their estimates provide dates of around 1.5Ma for the origin of Capra and 6.2 Ma for the origin of Caprini+Pantholops, which are probably too young. Numerous caprins older than 6.2 Ma are recorded from late Miocene sites in China, Turkey and Europe (Gentry et al., 1999). Some of these taxa are very derived morphologically, certainly more so than Pantholops or basal caprins such as Capricornis, making it likely they belong inside the crown group. One reason for Lalueza-Fox et al.'s results might be the use of the Myotragus calibration point as a hard date rather than as a minimum date: the insular isolation of Myotragus may well have taken place at 5.3 Ma, but the most recent common ancestor of Myotragus and its living sister taxon may have lived millions of years prior to that. By comparison, Ropiquet & Hassanin's (2005a) divergence estimates of 10.4–7.5 Ma for Caprini and 11.9–8.7 Ma for Caprini+ Pantholops accord better with the fossil record.
Caprins are today represented in Africa by only three species: the aoudad or barbary sheep (Ammotragus lervia) with a North African and Saharan montane distribution, the Nubian ibex (Capra nubiana) in parts of north-eastern Africa and Arabia, and the Ethiopian ibex (Capra walie), found only in the Simien Mountains of Ethiopia.
This representation is meagre compared to the current diversity and range of caprins across Eurasia. The Neogene fossil record, however, documents numerous Plio-Pleistocene caprin species in sub-Saharan Africa, from Ethiopia to South Africa (refs. in Vrba, 1995), up into the Holocene (Brink, 1999). Our phylogenetic analysis suggests that the two fossil species we considered, Capra wodaramoya and Budorcas churcheri, were each the product of an independent dispersal event into Africa, separate from those of the Ethiopian ibex or aoudad lineages. Along with the living species, this indicates caprins dispersed from Eurasia into Africa on no less than four separate occasions since the Pliocene (Fig. 2). What is not immediately clear is whether African fossil caprins such as these were part of long-lived African lineages, or were short-lived immigrants from Eurasia. Vrba (1995) noted wide morphological disparity among Plio-Pleistocene African caprins, suggesting no close relationships among the different species. Accordingly, she proposed that the record of African caprins represents numerous separate immigration events into the continent from Eurasia, particularly timed at 2.7–2.5 Ma and 1.9–1.7 Ma. The age and phylogenetic position of Capra wodaramoya provides an additional data point in support of Vrba's observations. Because caprins tend to inhabit terrain not amenable to fossilization processes (high altitude, highly erosional terrains), the rare appearance of caprins in the African fossil record might equally be a function of biased taphonomic and fossilization processes. Outside of a phylogenetic approach, it might be difficult to favour dispersalist versus taphonomic explanations for the spotty African caprin record. Addition of the remainder of African fossil caprin taxa into the phylogenetic framework we have developed can further test to what degree the African fossil caprin record is (i) the product of a few poorly sampled but endemically successful and long-lived lineages (null hypothesis) or (ii) the product of numerous short-lived immigration events in from Eurasia (Vrba's hypothesis).