A Gliriform Tooth from the Eocene of the Erlian Basin (Nei Mongol, China) and the Premolar Morphology of Anagalidan Mammals at a Crossroads

Abstract

The middle Eocene in Nei Mongol (China) was an interval of profound faunal changes as regards the basal Glires and gliriform mammals in general. A major diversification of rodent lineages (ctenodactyloids) and more modern small-sized lagomorphs was accompanied by a decline of mimotonids (Gomphos and Mimolagus) and anagalids. The latter was an enigmatic group of basal Euarchontoglires endemic to China and Mongolia. Here, we describe the first anagalid tooth (a P4) from the Huheboerhe classic site in the Erlian Basin. The tooth, characterized by its unique morphology intermediate between mimotonids and anagalids is semihypsodont, has a single buccal root typical of mimotonids, a large paracone located anteriorly, and a nascent hypocone, characteristic of advanced anagalids. The new finding of neither an abundant nor speciose group suggests a greater diversity of anagalids in the Eocene of China. This discovery is important because it demonstrates the convergent adaptations in anagalids, possibly of ecological significance.

1. Introduction

Glires (rodents and lagomorphs) is the most numerous clade of Euarchontoglires which, in turn, is one of the four main clades of placental mammals, recognized on the basis of molecular and morphological data—e.g., [1,2,3]. The “basal Glires” is an operational term for a paraphyletic group of primitive members of the clade, which do not display clear rodent or lagomorph synapomorphies. However, this group can be partitioned into simplicidentates (Eurymylidae) and duplicidentates (Mimotonidae), based on the number of incisors [4,5,6]. The basal Glires usually cluster in the phylogenetic analyses with Anagalidae [4,7], an enigmatic grouping of basal Euarchontoglires. The concept of “Anagalida” was proposed originally by Szalay and McKenna [8] as including Anagalidae, Pseudictopidae, Zalambdalestidae, and possibly, Didymoconidae; later emended by the addition of Macroscelida and Lagomorpha [9]. Macroscelida in the light of molecular data are considered Afrotheria [10]; thus, the Anagalida sensu McKenna [9] are now disproved. Meng and Wyss [11] defined the term “Gliriformes” as all taxa are phylogenetically closer to Glires than to any other Recent placental group—a notion endorsed, e.g., by Missiaen and Smith [12].

Whether Anagalidae themselves form a monophyletic group or are also a paraphyletic group is still a matter of debate [13]. Nevertheless, with respect to the cranial and especially dental morphology, they can be viewed as a morphological transitional zone in the morphospace between the basal primates and scandentians on one side and basal Glires on the other, but they are closer to the last group [13].

All representatives of Anagalidae and almost all early Glires are known exclusively from the Paleogene of Asia (mainly from China) with the only exception of the rodentiaform Alagomyidae lineage which is also known from North America [14]. Most anagalid taxa are restricted spatio-temporally to the Paleocene of southern and central China [13,15]. The Eocene representatives were confined to northern China and Mongolia [13,16,17,18] and their findings are scarce. Thus, any new discovery of this enigmatic group is of considerable interest to our understanding of evolution of gliriform mammals.

Here we present an upper premolar of an unknown genus and species of the anagalid branch of the Euarchontoglires from the middle Eocene (Irdinmanhan Asian Land Mammal Age) Huheboerhe locality in the Erlian Basin, Nei Mongol, China. The specimen shows strong similarities both to Eocene representatives of basal Glires and some more evolved Anagalidae.

2. Materials and Methods

The isolated gliriform premolar (IVPP V26960) is housed in the collection of the Institute of Vertebrate Paleontology and Paleoanthropology of the Chinese Academy of Sciences, Beijing, China (IVPP). The tooth was examined with a scanning microscope JSM 6100 (at the IVPP). Terminology of dental structures follows Meng and Wyss [11].

Geological setting: The tooth was found at the Huheboerhe locality (Figure 1), which lies ca. 37 km SW of Erenhot (Nei Mongol, China), close to the China/Mongolia boundary [19]. The site is located at the “Huhebolhe Cliff” (sensu Russell and Zhai [20]) and is also known as “Huhe Bulak” or “locality 7 mi west and southwest of Camp Margetts”, as marked during the Central Asiatic Expedition (CAE) led by the American Museum of Natural History (AMNH) in 1930 [19]. Paleogeographically, Huheboerhe is located in the Erlian Basin [21,22], one of non-marine basins of late Mesozoic origin in northeastern China. The Huheboerhe section includes three sediment series divided by upper and lower hiatuses: the “upper beds”, consisting of a lower part of the Irdin Manha Formation (IM-1) and underlying upper beds of the Arshanto Formation (AS), the “middle beds” including deposits of the Arshanto Formation, and the “lower beds” consisting of the upper Nomogen Formation sediments of the Bumbanian Asian Land Mammal Age [23].

The fossil mammal fauna of Huheboerhe is rich; the lower beds yielded many Gomphos specimens [25], the Arshantan sediments include numerous remains of perissodactyls [19,23], and the Irdinmanhan deposits yielded, among others, artiodactyls, primates, cricetids, ischyromyids, many ctenodactyloids, lagomorphs, and the mimotonid Mimolagus aurorae [19,23,24,26,27,28].

3. Systematic Paleontology

• Mammalia Linnaeus, 1758
• Euarchontoglires Murphy et al., 2001
• Anagalida Szalay and McKenna, 1971
• Anagalidae Simpson, 1931
• Gen. et sp. indet.
• (Figure 2)

Referred material: An isolated left P4 (IVPP V26960) with a complete tooth crown, and broken buccal and lingual roots.

Locality and age: Huheboerhe, Erlian Basin, Nei Mongol, lower Irdinmanhan beds (IM-1) of the Irdin Manha Formation, middle Eocene (Irdinmanhan ALMA).

Description and Comparisons

IVPP V26960 is a left P4 with two clearly marked roots, with a semicircular cross-section; the buccal root was smaller than the main one, which is typical of the semihypsodont upper premolars. Similar to large Eocene mimotonids, such as Gomphos and Mimolagus [17,24,25], it has only one buccal root. However, overall morphology of the crown (a squarish outline, the paracone located anterobuccally, and an incipient hypocone) more closely resembles that of larger anagalids (such as Anagale, Anagalopsis, and Hsiuannania); thus, comparisons with both groups seem relevant for this study. The tooth size is close to that of large mimotonids (Mimolagus) and middle-sized anagalids such as Anaptogale; it is smaller than the P4 of Anagalopsis, Eosigale, Hsiuannania, and Qipania, but larger than that of Diacronus. The crown is distinctly bilaterally hypsodont, with the lingual side almost twice as high (3.6 mm) as at the buccal one (2.16 mm), which is another feature characteristic of both Mimotonidae and Anagalidae [5,29,30].

The occlusal surface is almost square in outline, with the parallel anterior and posterior margins (the distal one shorter) oriented perpendicularly to the buccal margin. Such arrangement forces the lingual margin of the tooth to be placed askew, with the protocone being the lingual-most prominent element. The total width of the tooth is 4.32 mm and the maximum anteroposterior length is 3.24 mm. Morphologically, the tooth is most similar to that of Anagale or Anagalopsis, which are, however, more square (Figure 2). It differs from the P4 of Eosigale and Diacronus where the outline of the occlusal surface is subtriangular, and from Hsiuannania tabiensis and Qipania yui with a less squarish P4 outline, closer to a trapezoid (Figure 2). The anterior and posterior sides of the tooth are not parallel in Hsiuannania but angled to each other, whereas in Qipania they are parallel but not at the right angle with the buccal margin. In both genera (Hsiuannania and Qipania) the buccal and lingual margins are positioned askew to the parasagittal axis. On the other hand, the P3 and P4 in Gomphos and Mimolagus are much more oval in outline than IVPP V26960 and have somewhat tapered lingual margins [24,25], not flattened ones.

The new tooth shows cuspo-lobate morphology with a large, conical paracone, low and partly worn protocone, and two tiny style-like cuspules at the buccal margin of the tooth, distal to the paracone (Figure 2); whether both are stylar cusps or one of them is a minuscule metacone remains unclear. The paracone is the most prominent feature of the tooth. It is as eminent in the new specimen as in other anagalid genera, although it does not cover as much area of the occlusal surface as in Anaptogale and Eosigale, being more constricted at the base (1.68-mm width and 1.1-mm length). It resembles Anagalopsis and Hsiuannania more closely in the overall proportions of cusp size relative to the whole dental surface. In Gomphos, the paracone, or the “central cusp” sensu Meng et al. [25], is placed centrally at the tooth occlusal surface in both P3 and P4, and is surrounded by the pre- and postprotocrista originating at a poorly distinguished protocone. Such topography of the occlusal structures is different from that of IVPP V26960. The P4 in Mimolagus is poorly known, although the strongly worn tooth of the holotype of M. rodens indicates the centro-buccal position of the paracone (see also [17]). The P4 of Mimolagus aurorae is not known, but the P3 is similar to that of Gomphos in general morphology [24].

IVPP V26960 lacks the paraconule, similarly to Anagalopsis and Gomphos, but unlike in Hsiuannania and Qipania, which have small paraconules. The preprotocrista in the new specimen is long and goes straight anteriorly to the anterior side of the paracone, where it ends, defining the anterior margin of the tooth. In this way, the protocrista is complete in the new specimen, not interrupted by the paraconule as in Hsiuannania. In Anaptogale, however, the preprotocrista is poorly developed and very short, and in Hsiuannania and Qipania the preprotocrista ends at the paraconule. Gomphos does not have the paraconule at P4, and its occlusal structure is relatively simple. The heavily worn upper dentition of Mimolagus rodens (IVPP RV51002.1) does not show any additional cusps, apart from the paracone and remains of the protocone.

The postprotocrista in the new specimen is smooth and meets the posterior margin of the tooth, which can be regarded as the postcingulum. The tooth shows no sign of the anterior cingulum present in Anaptogale, Diacronus, Eosigale, Hsiuannania, and Qipania, and has no buccal cingulum, unlike Diacronus and Eosigale.

There is no clear indication of conules; nevertheless, a wear surface of the protocone (and the posterior part of the protocristae) bears a circular extension, indicating a small cusp distally to the protocone, what may be interpreted as a weakly expressed metaconule.

The joining point of the postprotocrista and the posterior tooth margin also indicates the position of a nascent hypocone. It forms a minute shelf slightly dorsal to the occlusal surface. In this feature the tooth resembles that of Hsiuannania tabiensis (IVPP V4274; Figure 2), and differs markedly from both Gomphos and Mimolagus, which do not have a hypocone on the premolars.

There is no parastyle, whereas such a structure is well-expressed in Anagale and also as a minute cusp in Gomphos (Figure 2). There is no marked hypostria at the shaft between the protocone and the hypocone but the shaft wall shows a shallow groove-like concavity descending along the shaft. Posteriorly and lingually to the paracone there is a large, flat-bottomed basin, which is interpreted as the trigon basin.

4. Discussion

Since the middle Eocene onward, mammalian faunas in central Asia experienced major faunal turnovers coupled with climate cooling and aridification [31,32,33,34]. Specifically, on the Mongolian Plateau, the basal Glires lineages identified with mimotonids and eurymylids gave way to rodents and lagomorphs of a modern aspect; both groups underwent diversification between the middle-to-late Eocene and the early Oligocene [21,24,26,27,28]. The demise of archaic gliriform taxa such as Anagalidae, and ischyromyid rodents [35] coincided with the advent of numerous small perissodactyls [19], primates [36], and tree-shrews [37].

After the middle Eocene the number of known anagalids dropped to three monotypic genera. Anagalopsis kansuensis from Gansu (northern China) and Zofiagale ergilinensis (Mongolia) are known solely from their type material [13,17], while Anagale gobiensis from Nei Mongol (China) is represented by two specimens, each of them consisting of the cranium and associated postcranial remains [16,18]. The only other Eocene finding ascribed to Anagalidae is one unilaterally hypsodont tooth of an unknown species from the Irdinmanhan beds at Wulanhuxiu, Nei Mongol, China [30]. The Eocene record of the basal Glires is slightly more diverse, with four species of Gomphos [25,30], and two of Mimolagus [17,24,38]; interestingly, they show the same pattern of size increase [24]. Thus, during the middle-to-late Eocene the representatives of large mimotonids and anagalids co-occurred in the Erlian Basin.

The dental morphology of IVPP V26960 is intermediate between that of large Eocene mimotonids and advanced anagalids. The outline and structure of the occlusal surface more closely resemble those of anagalids than mimotonids—in particular, Anagale and Anagalopsis, in the shape and cusp arrangement, and Hsiuannania in the presence of the small hypocone, situated on the shaft. On the other hand, the presence of a single buccal root is characteristic of the Eocene mimotonids (but not the Paleocene ones), whereas in most of the anagalid genera the P4 has double buccal roots. The premolar IVPP V26960 is slightly smaller than the corresponding teeth of Anagale, Anagalopsis, and Hsiuannania, but nearly equal in size to that of Mimolagus [24].

The evolution of the dentition in Euarchontoglires is highly mosaic, with frequent examples of convergence or evolutionary parallelisms in more distant or more closely related lineages, respectively [5]. However, the dentition of Anagalidae still lacks, typical of Glires, deletions in their premolar segment, and incisors (up to three pairs) are usually only slightly enlarged and semiprocumbent; their molars display distinct unilateral hypsodonty also typical of early Glires and the whole duplicidentate lineage. In some cases (e.g., Anagalopsis, Hsiuannania or Qipania) the crowns of the molars are higher than those in the co-occurring Glires (see e.g., [30]). Additionally, the molar occlusal surfaces, in most anagalids, show very heavy wear, which obliterates all cuspal pattern but the most buccal structures (see, e.g., [16,17]). Such extensive dental wear suggests an abrasive diet indicative of a high fiber content, demanding long chewing, as seen in duplicidentates—i.e., lagomorphs and larger mimotonids, such as Gomphos or Mimolagus [24].

That said, the taxonomic affiliation of IVPP V26960 is quite enigmatic. One might argue that, morphologically, the presence of a single buccal root advocates a Glires affiliation. However, the patterning mechanism of the root number in placental mammals is regulated developmentally and is highly plastic [39]; thus, a thorough modification of the tooth occlusal structure to resemble that of anagalids would probably require a greater number of the evolutionary transformations in mimotonids than merely the fusion of the buccal roots in anagalids. We are inclined to regard the new finding from the Irdinmanhan beds of Huheboerhe as a representative of a new genus and species of the derived anagalid lineage, probably related closely to Anagalopsis or Anagale. Its progressive characters are, apart from the root structure, the simplification of the occlusal crown pattern, the loss of the anterior and buccal cingula, and a nascent hypocone, indicating a trend towards molarization of the premolars, which parallels Glires [40]. Eventually, in the early Oligocene, the anagalids and basal Glires lost the ecological competition to radiating rodents and lagomorphs of a modern aspect, and small perissodactyls [24,31].

This study suggests that the increased sampling and better taxonomic resolution, especially from the Irdinmanhan and younger sediments, is needed to further address the question of morphological convergence and ecological specializations in late anagalids.