The first Asian record of the mouse-deer Afrotragulus (Ruminantia, Tragulidae) reassess its evolutionary history and offers insights on the influence of body size on Afrotragulus diversification

Locality, geological setting and age

Both Babri Wala and B 51 sites (Figure 2) belong to the Chinji Formation of the Lower Siwaliks Group (14.070–11.146 Ma, late Middle Miocene; see Barry et al. Citation2013 for chron designation), which has been classically divided into lower, middle and upper sections. A recent calibration (Barry et al. Citation2013) of the Siwaliks palaeomagnetic data (Sheikh Citation1984; Johnson et al. 1085; Johnson et al. Citation1988; McRae Citation1990; Kappelman et al. Citation1991) with the Magnetic Polarity Time Scale of Ogg and Smith (Citation2004) have resulted in a calculated age for the three Chinij Formation sections of 13.608–14.070 Ma for the Lower Chinji Fm (chrons C5AB-C5ACn), 12.735–13.363 Ma for the middle Chinji Fm (chrons C5Ar-C5AA) and 11.146–12.174 Ma for the upper Chinji Fm (chrons C5r-C5An; see Barry et al. Citation2013).

The area (locally known as Kund) of locality B 51 lies within the administrative boundaries of Chinji village. This area also represents the type section of Chinji Formation mentioned by Shah (Citation1977, 2009). McRae (Citation1990) described the lithological details of B 51 in his KR-4 (Kundal Rainbow Sandstone-4) section (later redrawn by Barry et al. Citation2013, fig. 15.3). Located 25 m above the base level, B 51 is composed of conglomerates, sandstone, siltstone, mudstone (predominant) and paleosols (McRae Citation1990). Paleomagnetically, B 51 fall in chron C5ACn, dating 14.070–13.739 Ma (Barry, pers. comm. 2019; Barry et al. Citation2013, fig. 15.3), which includes it in the lower Chinji Fm.

Babri Wala site is located ca. 1.6 km northeast of B 51 within the administrative boundaries of Kohtehra (Lat. 32° 42’ 57.25” N, Long. 72° 23’ 35.95” E and altitude 694.33 m), a small village about 2.41 km northeast of Chinji town (Lat. 32° 42’ 33.95” N, Long. 72° 22’ 09.32” E and altitude 698.3 m; Figure 2). The site is heavily eroded and with the upper part missing, with dimensions of about 4.5 m high, 2.74 m long and 1.5 m wide, and showing prevalent red mudstones with iron concretions and less abundant grey sandstones (Figure 3a). Like Chinji town, Kohtehra is located on the sandstones of the Nagri Formation. However, outcrops of the Chinji Formation (part of the Chinji Fm stratotype) are well exposed about 2.41 km south of Kohtehra village. According to Shah (Citation1977, 2009), the type section of the Chinji Fm lies in the administrative boundaries of Kohtehra. Johnson et al. (Citation1985), (Citation1988), Willis (Citation1993) and Badgley et al. (Citation1998) designated a 12 km long area as the Chinji Fm stratotype, ranging from Chinji Rest House and Chinji (locality 430 and 41) up to the area of Bhilomar (locality 495). The studied area of the Kohtehra village outcrops belonging to the Chinji Fm range between the K2-K5 sections of Johnson et al. (Citation1988) and part of a long section that includes the localities Y-GSP 693 and Y-GSP 732 (Badgley et al. Citation1998). Babri Wala site does not currently appear in the database of Yale-Geological Survey of Pakistan (Barry, pers. comm. 2019), constituting a new addition to the list of fossil productive sites of the Chinji stratotype, lying between the two unnumbered sites of Badgley et al. (Citation1998). Lithological comparison with the section KR-2 of McRae (Citation1990) reveals that Babri Wala correlates well with the upper half of this section located ca. 130 metres above the base level. The lithological features of the site indicate that it belongs to the middle Chinji Formation, with an approximate age of 12.6 Ma. (Johnson et al. Citation1988; McRae Citation1990). The associated fauna of the site and adjacent area include bovids (Miotragocerus gluten and Gazella sp.), stem-giraffids (Giraffokeryx punjabiensis), rhinoceroses (Gaindatherium browni) and rodents (Rodentia indet.).

Figure 3. a, lithological column of the site of Babri Wala showing the two Afrotragulus-yielding mudstone levels; b, lithological column of the site of Hasnot-6, showing the upper conglomerate level from which PUPC 13/323 was recovered.

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The locality of Hasnot 6 (Figures 2, 3b; Lat. 32° 50’ 42.8” N and Long. 73° 17’ 51.5” E, elevation 359.89 m) belongs to the upper Dhok Pathan Formation of the Middle Siwaliks Subgroup, located over the locality B117 (Colbert Citation1935). Locality B117 has a palaeomagnetic age of 7.360 to 7.083 Ma (Barry et al. Citation2002) and it lies slightly below the fossiliferous levels of Hasnot 6, which is in turn situated about fifteen metres below the Tatrot Formation caps yielding Anancus sivalensis fossils (Abbas Citation2018). Hasnot 6 was once part of a larger locality that was cut away for the construction of the Padhri to Hasnot road. Lithostratigraphically, the topmost layer of Hasnot 6 is composed of a conglomerate fossiliferous bed. Below this uppermost level, there is a thick stratum of light grey coloured fine-grained non-fossiliferous sandstone, and below it there is a layer of loose conglomerate with light pink coloured clay and dark back coloured small sized pebbles. This layer is the most fossiliferous one and the level from which PUPC 13/323 was collected. The locality has yielded remains of Hippohyus cf. sivalensis, Propotamochoerus hysudricus, Gazella lydekkeri and Tragoportax punjabicus (Babar Citation2017). According to Pickford (Citation1988), Hippohyus sivalensis lived from ca. 5–2 Ma, which would correspond to latest Miocene to early Pleistocene. However, Barry et al. (Citation2002) consider the oldest occurrence of H. sivalensis around 6 Ma. According to Badgley et al. (Citation2008), Gazella lydekkeri ranged from 10.2 to 6.1 Ma, Tragoportax punjabicus ranged from 8.2 to 6.2 Ma and Propotamochoerus hysudricus ranged from 10.2 to 6.5 Ma. Hence, the estimated age for Hasnot 6 is roughly 6.5 Ma.

Material

The tragulid fossils from the Siwaliks described in this paper are curated by the AMNH (AMNH 19310, lower Chinji Fm) and the Dr. Abu Bakr Fossil Display and Research Centre, Department of Zoology, University of the Punjab, Lahore (PUPC 19/58, PUPC 19/59, PUPC 19/60, PUPC 19/61, middle Chinji Fm; and PUPC 13/323, Dhok Pathan Fm).

Data from the taxa included in the phylogenetic analysis come from Dorcabune anthracotherioides (originals AMNH); Dorcabune welcommi (cast MNCN, also publication); Dorcatherium crassum (Sansan originals MNHN and MNCN casts, photographs from Guzmán-Sandoval Citation2018, Mennecart et al. Citation2018); D. namaquensis (originals GSN); D. pigotti (originals NHM, casts MNCN, NMK); D. iririensis (original UM); D. guntianum (photographs SMNS); D. naui (original NHM, original from Los Valles de Fuentidueña, MNCN); Hyemoschus aquaticus (AMNH, MNCN); Siamotragulus sanyathanai (casts MNCN); S. bugtiensis (casts MNCN); S. songhorensis (originals NHM, UM); Yunnanotherium simplex (original publication Han 1986); Tragulus javanicus (AMNH, MNCN, MAUV); Moschiola memmina (AMNH, MNCN). All Afrotragulus studies were based on originals, with the exception of the mandible KNM-SO 1345 of A. parvus (Geraads Citation2010) from Songhor (photographs).

Tragulid fossil material assigned to ‘D’. parvum and ‘D’. moruorotensis different from that described from Rusinga (including that of Whitworth Citation1958) and Moruorot (Pickford Citation2001) when the genus Afrotragulus was first erected (Sánchez et al. Citation2010) was cited from other East African sites (Pickford Citation2001, Citation2002; Geraads Citation2010), potentially expanding the chronostratigraphic range of the genus Afrotragulus in Africa (as effectively proposed by Geraads Citation2010). This material mostly consists of isolated postcranial fragments/bones (e.g. astragali) that preclude their unambiguous attribution to Afrotragulus, except, apparently, by size. However, size alone is not a trustworthy tool on tragulid systematics (see Sánchez et al. Citation2010 for the discussion on this topic), as evident by the larger-bodied Asian Afrotragulus described here. Hence, until part or all of these fossils are properly described and unambiguously assigned to Afrotragulus, we choose to be conservative and limit our sample to the African Afrotragulus material originally described in Sánchez et al. (Citation2010) plus all additional materials that can be unambiguously assigned to Afrotragulus, like the hemimandible KNM-SO 1345 from Songhor (Kenya, 20 Ma) included by Geraads (Citation2010) in D. parvum. The tragulid ankle KNM-RU 15136 from Rusinga (Kenya) was assigned by Geraads (Citation2010) to Dorcatherium cf. parvum. It has a free malleolar bone and the cubonavicular is fused with the ectomesocuneiform (Geraads Citation2010). Also the astragalus length appears similar (from the scale in the picture) to that of A. parvus from Rusinga (see Sánchez et al. Citation2010). However, until direct examination of this specimen is possible, we prefer to exclude it from the morphological/cladistic analysis.

Measurements

We follow the set of measurements proposed by Sánchez and Morales (Citation2008). All measurements of the new dental material were taken with digital calipers. The diminutive lower dentition of the Afrotragulus moruorotensis Mor1ʹ2000 holotype (see the original odontometrics in Pickford Citation2001) was measured again using a Nikon Measuroscope 5 10x microscope with an incorporated micrometre of 0.025 mm accuracy. The detailed odontometrics are presented as supplementary information.

Nomenclature and anatomical definitions

We use the general terminology of Azanza (Citation2000) for nomenclature of the ruminant dentition (English version in Sánchez and Morales Citation2008). The Dorcatherium-fold is the fold that occurs on the linguo-distal side of the metaconid (Figure 4). The Tragulus-fold is the fold situated on the distal side of the protoconid, usually linked to the post-protocristid (sometimes to the conid itself; Figure 4). Combined, both the Dorcatherium-fold and the Tragulus-fold form the M-structure (Figure 4d; see also e.g. Janis Citation1987; Geraads et al. Citation1987), a unique trait of the lower dentition that diagnoses the Tragulidae (see e.g. Métais et al. Citation2001; Sánchez et al. Citation2015a; Guzmán-Sandoval and Rössner Citation2019). The inter-lobular bridge is the rectilinear bridge of enamel that connects the anterior and posterior lobes in an Afrotragulus-type lower molar (Figure 4; Sánchez et al. Citation2010). The Zhailimeryx-fold is a fold of enamel that originates from the anterior part of the entoconid, the development of which is highly variable amongst tragulids (from well-developed to absent). The Dorcatherium-platform is the mesial semicircular structure of the lower molars formed by a hyper-developed pre-protocristid that turns lingually to contact a very small pre-metacristid (Figure 4; see also Sánchez et al. Citation2010; Morales et al. Citation2012).

Figure 4. Occlusal anatomical elements of tragulid lower molars. a, Afrotragulus moruorotensis, m2 of the holotype CMK Mor 1ʹ2000; b, Dorcatherium naui, m2, right hemimandible of the specimen BMNH M40432 from the type locality Eppelsheim; c, Moschiola meminna, left m2 (private collection Jan van der Made, Madrid); d, ‘Dorcatherium’ crassum, left m2 of neotype hemimandible Sa 9950 from Sansan (Morales et al. Citation2012), mirrored for comparison purposes. Taken from Sánchez et al. (Citation2015a); e, schematic depiction of the three types of mesial morphology in tragulid molars. From left to right: very large pre-protocristid which turns lingually and contacts a very small pre-metacristid, forming the Dorcatherium-platform; large rectilinear pre-protocristid that meets a smaller pre-metacristid, with no Dorcatherium-platform; straight pre-protocristid and pre-metacristid which are subequal in length, meeting parasagitallly and forming a triangular mesial outline of the teeth. All images by IMS.

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Phylogenetic analysis

We performed a cladistic analysis at the species-level to explore the phylogenetic relationships of the new studied Siwaliks tragulids using the TNT software (Goloboff and Catalano Citation2008). We chose Zhailimeryx jingweni as the outgroup (TNT only allows a single outgroup) since this taxon was previously used successfully for root tragulids (Métais et al. Citation2001; Sánchez et al. Citation2015a, Citation2018). As the ingroup, we chose the same terminals as in Sánchez et al. (Citation2018) with the addition of Siamotragulus bugthiensis, S. songhorensis, Yunnanotherium simplex and the three new Asian Afrotragulus. The morphological data matrix consists of an updated and extended version of the matrix presented in Sánchez et al. (Citation2015a), including 73 characters picked from the skull (11), upper dentition (6), lower dentition (32) and postcranial skeleton (24). We performed a run using a traditional search with 1000 replicates with TBR (Tree Bisection Reconnection) that recovered one most parsimonious tree (MPT) of 162 steps. The character/state distribution for the discussed nodes and terminals is presented in Table 1.

Body size estimates

We predict body mass (in kg) – as a measurement of body size – of fossil Afrotragulus spp. and Yunnanotherium simplex from the (occlusal) length measure of their molars (Table 2), as the correlation between this variable and the body size in a wide variety of living ruminants (including tragulids) has been successfully tested (Janis Citation1990a) and allowed accurate estimates of body mass for extinct forms (Janis Citation1990b; DeMiguel et al. Citation2012; DeMiguel Citation2016). We included Yunnantoherium into the calculations since it is part of the sister clade to Afrotragulus together with the extant Tragulus and Moschiola. The selection of craniodental remains for body mass estimation is due to the fact that these are the only (and most diagnostic) elements available in our fossil sample (except for a couple of astragali), though skeletal parts (and in particular those that play a role in body support – such as major limb bones) are much weight bearing (Gingerich Citation1990; Janis Citation1990a). We calculated the mean body mass for each specimen following regression equations by Janis Citation1990a (log(Y) 0 a + b log (X); Y = body mass in kg; a-b constants for each group; X = m1 m2 length in cm) and then for each species by averaging mean across individuals (Table 1). Only lower molars and adult specimens (in which the length growth is complete) were considered. When several specimens (i.e. different tooth positions) from the same individual were available, only the first molar was selected for analysis because m1 length results in better weight estimates.

Description

Upper permanent dentition. The upper dentition is represented in the sample by a single left M2. The anterior lobe is anteroposteriorly larger than the posterior lobe. The protoconal cingulum is well developed, a typical Afrotragulus feature (see Sánchez et al. Citation2010). The molar is markedly selenodont with well-developed cristae. The lingual ribs are strong and elongated. The post-protocrista is short but the pre-metaconulecrista is well developed, almost reaching the inner buccal wall.

Lower permanent dentition. The lower molars are narrow, although they do not have the elongated look of the molars of A. moruorotensis and A. megalomilos. Similarly, the cuspids are more bunoid than in clade B (see Discussion) Afrotragulus. Also, the cristids are high but not so horizontally extended as in A. moruorotensis and A. megalomilos. This condition is especially visible in the pre-hypocristid. The distal lobe of m1-m2 is distinctly larger than the mesial lobe. The third lobe of the m3 appears in a central position (character 18:1). The interlobular bridge is short in all three molars and has a relatively primitive aspect, with the distal end of some of the cristids still visible (Figure 5i). The post-hypocristid is long and curved, turning mesially to contact the entoconid, it is bifurcated with two small branches in the m3. The mesial cingulid is present, and the posterior cingulid is strong. The ectostylid is short although sometimes with a relatively broad base.

Afrotragulus moralesi sp. nov.

Figure 5(m–o)

LSID. – zoobank – 7FC6D555–D653–4632–A8BE–FCB4A88A8482

Etymology of name. Honouring Prof. Jorge Morales, for a life devoted to the study of ruminants.

Holotype. PUPC 13/323, left m3 (Figure 5m–o).

Paratypes. None.

Locality and age. Locality Hasnot 6, Dhok Pathan Formation (ca. 6.5 Ma), Upper Miocene.

Material. The same as the holotype, PUPC 13/323, left m3.

Diagnosis. Afrotragulus with prehypoconulid-cristid developed as a buccal wall that connects with the post-hypocristid in the upper half of the crown; posthypocristid bifurcated in the m3 with two small branches; almost aligned entoconid and hypoconid.

Differential diagnosis. Afrotragulus moralesi differing from its sister taxon A. akhtari in: prehypoconulid-cristid developed as a buccal wall that connects with the post-hypocristid in the upper half of the crown. Differing from A. parvus in: prehypoconulid-cristid developed as a buccal wall that connects with the post-hypocristid in the upper half of the crown; and posthypocristid bifurcated in the m3 with presence of two small branches. Differing from A. moruorotensis in: posthypocristid bifurcated in the m3 with presence of two small branches; non-aligned lingual cuspids; strong posterior cingulid; cristids developed but without the horizontal extension (webbing-like morphology) of clade B Afrotragulus. Differing from A. megalomilos in: posthypocristid bifurcated in the m3 with presence of two small branches; non-aligned lingual cuspids; strong posterior cingulid; cristids developed but without the horizontal extension (webbing-like morphology) of clade B Afrotragulus; and central position of the third lobe of the m3.

Description

Lower permanent dentition. The m3 of A. moralesi is shorter and more compact than that of A. moruorotensis, with less horizontally extended cristids, especially the pre-hypocristid. Nevertheless, the cristids are distinctively higher than those of A. akhtari. Typical of Afrotragulus, the anterior and posterior lobes are sub-equal in size, with very similar width. The M-structure is very reduced, and the interlobular bridge is short. The post-hypocristid is long and bifurcated, showing two small branches. The third lobe is located in a central position. The prehypoconulid-cristid is developed as a buccal wall that connects with the post-hypocristid in the upper half of the crown. This constitutes a parallelism with the A. megalomilos-A. moruorotensis clade and, together with the high cristids, easily differentiates A. moralesi from A. akhtari. The entoconid and hypoconid are aligned. There is a mesial cingulid, and the ectostylid is small.

Afrotragulus megalomilos sp. nov.

Figure 6(a–c)

Figure 6. Afrotragulus megalomilos sp. nov. holotype, with the holotype of its sister taxon A. moruorotensis (new CT SCAN images) added for comparison purposes. a–c, AMNH 19310, holotype, left hemimandible with m1-m3. a, buccal, b, lingual and c, occlusal views; d–f, Afrotragulus moruorotensis holotype CMK Mor 1ʹ2000, left hemimandible with m1-m3. d, buccal, e, lingual and f, occlusal views.

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1935 Dorcatherium minus Colbert: 309.

2019 Dorcatherium dehmi Guzmán-Sandoval and Rössner: 13, 20,

Body mass estimates

Body mass in Afrotragulus spp. (Table 2) ranges from approximately 1.5 kg in A. moruorotensis to 23 kg in A. moralesi (though this latter inference is based on a single m3, which provides higher size estimates). Afrotragulus parvus and A. akhtari are small species (2.3–3 kg) and A. megalomilos is an intermediate-sized species (13 kg). Body mass for Yunnanotherium simplex was determined as approximately 5.5 kg (Table 2).

Palaeobiological insights: the influence of body size in driving diversification and diet evolution of Afrotragulus

Other than its highly derived lower molars, what first caught the eye about African Afrotragulus was the very small size of both A. parvus and A. moruorotensis, a feature remarked by Pickford (Citation2001) and Whitworth (Citation1958) in the first description of ‘Dorcatherium’ moruorotensis and ‘D’. parvum respectively. The new Asian Afrotragulus provides interesting new data about body size in Afrotragulus, and hence offers an opportunity for the analysis of this feature, its evolutionary consequences, and its palaeobiological implications related to diet and habitat preferences. Body size (calculated as body mass) profoundly affects life history of living organisms, as it is directly related to morphology, energy needs, physiology and ecology (with clear implications on both food choice, and resource and habitat partitioning; Demment and Van Soest Citation1985; Clauss et al. Citation2013; DeMiguel et al. Citation2014 and references therein). Body size estimates are essential for inferring the palaeobiology of extinct organisms (Campione and Evans Citation2012) and also underlie the diversity of feeding niches and digestive capacity in the Ruminantia (Demment and Van Soest Citation1985; Clauss et al. Citation2013; DeMiguel et al. Citation2014). In general, larger ruminants are able to meet their energetic requirements by eating more abundant foods of lower quality such as twigs or stems because they can process those in large quantities. By contrast, smaller ruminants require higher-quality parts (e.g. forbs, leaves, seeds or fruits) that are easier and quicker to digest in order to meet their energetic requirements (Clauss et al. Citation2013).

Extant tragulids (ranging 1.5–16 kg; Meijaard Citation2011) are all selective feeders that pick leaves, shoots, flowers and fruits from the forest floor. Unlike pigs and some ruminants (e.g. moschids and certain bovids), tragulids cannot rise on their hind limbs to reach food at a certain height level, restricting them to look for fallen fruits and leaves and to nip low-growing shoots (Meijaard Citation2011). Extant tragulids are mostly frugivorous (with additional browsing behaviour) that prefer forested habitats in which fruit is available more or less year round (Meijaard Citation2011; Clauss and Rössner Citation2014). Living tragulid density correlates with fruit abundance (Heydon and Bolloh Citation1997). For example, the lesser mouse deer Tragulus kanchil, one of the smallest living forms (1.5–2.5 kg; Figure 9) is mostly frugivorous, consuming seeds, shoots and mushrooms (Meijaard Citation2011). The African chevrotain Hyemoschus supplements its mostly frugivorous diet (approximately 70% of its food intake) with a small amount of animal protein, hunting for ants and small crabs, and eating carrion and fish. Animal protein appears to play no role in the Asian living species (Meijaard Citation2011). It is possible that the more primitive dentition (with more pointed cuspids) of the African chevrotain is better suited for processing small occasional animal prey than the fully selenodont molars of its Asian relatives. Some researchers argued that fossil tragulids exploited a wider trophic spectrum than extant forms, ranging from pure browsing to mixed feeding (Kaiser and Rössner Citation2007; Ungar et al. Citation2012). One hypothesis posits that after flourishing in the first half of the Miocene, in the middle Miocene tragulids could not compete against the rapidly radiating pecorans due to their different digestive physiology and reproductive life history (Clauss and Rössner Citation2014). As a result, tragulids only survived in tropical forested relic areas in which a mostly frugivorous diet is possible year round, places where the advantages of pecorans were not so decisive. This hypothesis proposes that the mostly frugivorous feeding habits of living tragulids do not represent the ancestral condition but a secondary adaptive constraint (Ungar et al. Citation2012; Clauss and Rössner Citation2014).

Our body size estimates show two different classes of Afrotragulus species. Although originally considered very small forms, Afrotragulus body size range is larger than the entire size spectrum of living tragulids (Figure 9). Afrotragulus moruorotensis, A. parvus and A. akhtari were tiny – A. moruorotensis is smaller than the smallest living ruminant, the lesser mouse deer (and is instead similar to smallest species of macropods such as the nabarlek Peradorcas concinna). Afrotragulus parvus and A. akhtari are similar in size to the three smallest Tragulus (T. javanicus, T. kanchil and T. versicolor) and to Moschiola chevrotains (Figure 9; size values from Meijaard Citation2011). At the other end of the range, Afrotragulus megalomilos and A. moralesi are larger forms similar in size to Hyemoschus aquaticus and the bovid Cephalophus dorsalis. Additionally, Yunnanotherium simplex may be considered as a very small species, similar to the bovid Cephalophus monticola and slightly larger than Yunnanotherium sister group, the living Asian tragulids (Figure 9). Contrary to Afrotragulus, the clade containing the extant Asian forms apparently developed a small body size constraint early on at the root of the lineage, never producing larger forms. Other than Yunnanotherium and the two living genera, additional Miocene forms potentially belonging to this clade, namely the previously mentioned ‘D’. minimus and at least one undescribed form from the Siwaliks (AMNH collection, IMS pers. obs.), are also diminutive. If they indeed belong to the Yunnanotherium + ‘extant Asian’ clade, that adds support to the hypothesis of a synapomorphic basal small size constraint in the entire lineage of the living Asian tragulids.

Figure 9. Body size (in terms of body mass) distribution in Afrotragulus spp. and its sister group, the extant Asian lineage (including its extinct member Yunnanotherium simplex). The African chevrotain Hyemoschus aquaticus is included here for comparison purposes between Afrotragulus spp. and all the living tragulids. The body size data of the extant forms come from Meijaard (Citation2011). The dashed boxes represent body mass ranges. Three living taxa have unknown body size and are not included here: Moschiola kathygre, Tragulus williamsoni and T. nigricans (Meijaard Citation2011). It is worth noting that the body size of A. moralesi was calculated using the only known m3 (PUPC 13/323), and this dental piece offers higher size estimations than the m1 does. Hence, a more realistic figure for the body mass of this species would fall within the 15–20 kg segment. Hyemoschus and Tragulus art by Marco Ansón. Composed image by IMS.

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Among extant ruminants, species with a similar body mass to that of Afrotragulus spp. and Yunnanotherium simplex are all browsers. Such small size might have acted as a serious physiological and energetic constraint on the smaller Afrotragulus, and may have limited this species’ ability to expand dietary niches (i.e. preventing transition from browsing to intermediate feeding), and subsequently live outside of habitats capable of delivering the necessary amount of fruit year round. Hence, at least the smallest forms (i.e. 1.5–3 kg) A. parvus, A. akhtari and (especially) A. moruorotensis were probably very limited by the time and energy requirements of finding scantier and unevenly distributed high-quality (easy-to-digest) foods required by a low digestive capacity, as observed in small animals (Demment and Van Soest Citation1985). The smaller species of Afrotragulus were probably highly frugivorous selective feeders consuming mostly small fallen fruits and seeds rather than typical browsers. Larger body sizes (>10 kg) were attained twice in parallel in both lineages of Afrotragulus by A. megalomilos (middle Miocene) and A. moralesi (late Miocene). This probably enabled larger Afrotragulus to escape the energetic constraints associated with very small body sizes, permitting these species to potentially exploit a broader (more mixed-feeder) diet, taking advantage of their derived molar dentition, which morphofunctionally mimicked that of pecorans. Increased plasticity in diet possibly facilitated these larger forms to adopt new lifestyles and enter new niche spaces to survive the climate-induced environmental changes of their respective epochs, A. megalomilos to the mid-Miocene cooling and A. moralesi to the drying and increased seasonality of the late Miocene (Quade and Cerling Citation1995), as occurred with some large-bodied cetartiodactyls in less productive habitats of North America (Pound et al. Citation2012). A previous analysis of dental texture of early Miocene small tragulid species from Kenya (included A. parvus; Ungar et al. Citation2012) found that they were mixed feeders apparently contrasting with our interpretation that the bulk of Afrotragulus spp. (A. moruorotensis, A. parvus and A. akhtari) had mainly frugivorous diets, but instead agree with the more opportunistic diets proposed for A. megalomilos and A. moralesi. Unfortunately, that study does not provide data for extant tragulid species, nor for that matter are individual modern species demonstrated in the study at all, making comparisons with individual modern species impossible. Also, the study does not include A. moruorotensis. While more research is needed to examine dietary adaptations in other Afrotragulus and other extinct tragulids, we agree with Ungar et al. (Citation2012) that extinct African tragulids exploited a broader spectrum of foods during the early Miocene, and our new discoveries demonstrate the same for extinct Asian Afrotragulus.