Diversification rates in Ctenodactylidae (Rodentia, Mammalia) from Mongolia

Gundis, or comb rats, are rodents of the family Ctenodactylidae. Extant gundis are restricted to Africa and represent a vestige of the diversity that the ctenodactylids attained at both palaeoecological and palaeobiogeographical levels. Here, we present an updated review of the Ctenodactylidae from the Valley of Lakes, Mongolia, based on the study of large collections now available. We have recognised 13 valid species of ctenodactylids grouped into five genera: Karakoromys, Huangomys, Tataromys, Yindirtemys, and Prodistylomys. The ctenodactylids show an initial burst in diversification in the early Oligocene followed by a sequential generic extinction of Karakoromys, Huangomys, and Tataromys. A maximum richness peak at the late Oligocene was followed by a profound diversity crisis. Yindirtemys, the only surviving genus, persisted into the Miocene, joining three Prodistylomys species. These last representatives of the group disappeared coinciding with the late Xiejian faunal reorganisation (Mongolian biozone D).


Introduction
The Valley of Lakes is one of the Pre-Altai depressions of Central Mongolia. It is situated within the Gobi Altai Mountains in the south and the Khangai Mountains in the north. This depression is formed by a Proterozoic to Paleozoic basement filled with terrestrial sediments ranging in age from the Cretaceous to the Quarternary. The areas of study are the Taatsiin Gol and Taatsiin Tsagaan Nuur where the exposed sediment sequence of the Hsanda Gol and Loh Fms. are very rich in Oligocene and Miocene fossils (Fig. 1). These Cenozoic sediments are interfingered with basalts. 40 Ar/ 39 Ar datings of the basalt flows define at least two groups of Oligocene basalts (basalt I, 31.5 M.a.; basalt II, 27-28 M.a.) and a middle Miocene basalt (basalt III, ∼13 M.a.; Daxner-Höck et al. 1997;Höck et al. 1999). Over eight field seasons, between 1995 and 2012, a Mongolian-Austrian team has collected in the Valley of Lakes. Eight informal local biozones have been defined according to their rodent assemblages and lithostratigraphic positions. These are A, B, C, C1, D, D1/1, D1/2, and E (Daxner- Höck and Badamgarav 2007;Daxner-Höck et al. 2013). The combination of these local mammal biozones and basalt ages provide a complete biochronology for the studied area (Daxner- Höck and Badamgarav 2007;Daxner-Höck et al. 2010, 2015. Ctenodactylid rodents are an important part of mammal assemblages in Asia (Gomes Rodrigues et al. 2014). In the Oligocene and early Miocene of Mongolia, the family is represented by 13 species, which is 19% of the total number of rodent species (Fig. 2). The morphological characters of Ctenodactylidae are: a hystricomorphous skull and a sciurognathous mandible, well-developed lower masseteric crest and incisor enamel with multiserial microstructure and small premolars, and the upper P4 lacking metacone and hypocone. Ctenodactylidae have their first occurrence in Asia during the Paleogene. The group is divided into four subfamilies: Kakaromyinae Wang, 1994, Tataromyinae Lavocat, 1961, Distylomyidae Wang, 1994, and Ctenodactylinae Gervais, 1853. The Tataromyinae diversified and flourished during the Oligocene, spreading from East to Central Asia.
The subfamily Distylomyinae firstly occurred in the late Oligocene of China, spreading to Mongolia and diversifying in the early Miocene. Both Tataromyinae and Distylomyinae disappeared before the middle Miocene. In contrast, the subfamily Ctenodactylinae survived and diversified, reaching western Asia, Mediterranean islands, and Africa. Nowadays, Ctenodactylids are restricted to four living genera distributed along North Africa.
In the last 10 years, several works of the ctenodactylids of the Valley of Lakes have been conducted Oliver and Daxner-Höck 2017;Oliver et al. 2016). However, these papers are mainly focused on the systematic of the different taxa, not in the overall diversity dynamics of the group. Therefore, this work updates the systematic of the Ctenodactylidae from the Valley of Lakes and emphasises the diversification trends (palaeobiostratigrapy and palaeobiogeography).

Material and methods
We constructed a dataset of Mongolian ctenodactylid occurrence data from the early Oligocene to the early Miocene of the Valley of Lakes recorded at the species level. The resulting list includes 13 species grouped in 5 genera (see Table 1). The table also includes the localities, the codes of the fossil layers/assemblages, the Mongolian biozones, and the number of specimens studied in this work. Here, we followed the calculation of geochronologic ages of the Mongolian biozones/letter zones A, B, C, C1, and C1-D (Daxner- Höck et al. 2017: Figs. 30-31). The stratigraphic ranges of Ctenodactylidae species are drawn as lines between the first and last occurrence within the Mongolian biozones (lower or upper part). The ranges do not show the number of assemblages and specimens occurring in the respective interval. Singleton occurrences are figured as circles (see Fig. 3).
The bulk of the material is stored in the Natural History Museum in Vienna (Austria). Additional fossil material is stored in the collection of the Institute of Palaeontology and Geology of the Mongolian Academy of Sciences in Ulan Bator (Mongolia).
The measurements have been taken using Discovery V20 and Carl Zeiss software Axiocam MRc5.
We have estimated the species richness through time using lower and upper part of the biozones. Richness was obtained as the sum of species' presence in each biozone, assuming the range between first and last occurrences (Fig. 4).

Geographic distribution: Valley of Lakes (Mongolia), Ulantatal area (Inner Mongolia, China).
Remarks: Huangomys frequens occurred in two regions of the Valley of Lakes: Hsanda Gol in the localities of SHG-C/1-2 and SHG-A15-20; and Taatsiin Gol in the localities of TGR-B/1, TGR-AB/21, and TGR-AB/22 (see Table 1). This genus is one of the most common ctenodactylids from Mongolia with ∼180 specimens recovered.
Genus Tataromys Matthew and Granger, 1923 Type species: Tataromys plicidens Matthew and Granger, 1923  The table includes locality names, the codes of fossil layers/assemblages, the Mongolian biozones, the names and number of specimens of the different species. The assemblages stem from fossil layers of different sections, which were correlated with the type sections (Daxner- Höck et al. 2017: figs. 30-31) Tataromys sigmodon Matthew and Granger, 1923 Synonymy: Tataromys sigmodon Matthew and Granger, 1923: 6. Teilhard de Chardin and Leroy 1942: 25, 89. Mellet, 1968: 6, 10. Kowalski 1974. Wang et al. 1981: 27, 29-30. Wang, 1994 fig. 3C. Wang, 1997: 18-22, 88. Höck et al. 1999 Diagnosis : Smaller than T. plicidens and greater than T. minor; dp4/DP4 more bunodont than molars and slightly wider than P4/p4; asymmetrical P4, flattened anteriorly and rounded posteriorly; anteroloph reduced or absent, variable connections between metacone and posteroloph; general increase of length from lower p4/dp4 to m3, and from P4/DP4 or M2; great size variation of M3; on upper molars, mesosyncline L-shaped and posterosyncline short, metaloph strongly curved, reaching posteroloph on M1 and M2, posteriorly oblique and joining posteroloph on M3: morphotypes B, C, and E; on lower molars, trigonoid relatively long, usually with a relatively wide and closed basin, generally closed lingually, but sometimes superficially open on moderately worn teeth; hypoconulid usually joining arm of hypoconid; Size close to that of Alashania tengkoliensis; differs from Alashania by the shape of the dentary and the location of the foramen mentale; the development of a trigonoid basin, a short hyposinusid due to the direct junction between hypoconulid and hypoconid; metaloph joining the posteroloph (generally morphotypes B and C).
Stratigraphic range in Mongolia: Early Oligocene (upper part of biozone B) to late Oligocene (biozone C and lower part of biozone C1); Hsanda Gol Fm. (see Fig. 3).
Tataromys minor (Huang, 1985) Tataromys minor longidens Diagnosis: Of the size of Tataromys minor minor but molars more elongated, which is particularly discernable in the upper teeth; P4 larger transversally than the M1; trigonoid of the lower molars more frequently reduced.

Geographic distribution: Valley of Lakes (Mongolia).
Remarks: According to Schmidt-Kittler et al., 2006, this subspecies has only occurred in Mongolia, which is one of the most common ctenodactylids (∼150 specimens). The material of Tataromys minor longidens is from two regions: Taatsiin Gol in the localities of TGR-C/1 + 2, ABO-A/3, TAR-A/2, and TGW-A/2a + 2b; and Tatal Gol in the locality of TAT-055 (see Table 1).
Tataromys plicidens Matthew and Granger, 1923 Synonymy: Tataromys    Diagnosis: Comparable to Tataromys minor and Yindirtemys grangeri in its size; in the lower molars, mesoconid present but less voluminous than in the species grangeri; no vertical groove on the posterior wall of the protoconid separating it from the mesoconid developed; cones more rounded than in Tataromys minor but without selonodont tendency as in Yindirtemys grangeri; metaloph of upper molars mostly connected to the hypocone, corresponding to pattern type B.  Table 1).

Stratigraphic range in
Yindirtemys aff. ulantatalensis (Huang, 1985) Synonymy: Tataromys  buno-selenodont molars, with high cusps, swollen at their bottom and acute at their top; weakly expressed and low lophs and lophids; on lower molars, high and crescentic mesoconid, at midline of the teeth; mesoconid limited by two vertical grooves, the anterior drawing a clear sinus between metaconid and mesoconid; wide trigonoid basin; additional crests present; on upper molars, anterocone high, short antesinus; clear posterosinus; morphotypes A and B most frequently observed (A: Metaloph curved forward and directly connected to the protocone; hypocone linked to the metaloph by its anterior arm; short posteroloph connected to the posterior arm of the hypocone; morphotype B: Metaloph curved backward and connected to the posteroloph-anterior arm of the hypocone junction); additional crests mainly on M3 (crochet, anti-crochet, and double junction anterocone-protocone-protoloph).
Remarks: The material of Yindirtemys aff. ulantatalensis from the Valley of Lakes has been recovered in the region of Taatsiin Gol, in the locality of TAR-A/2 (see Table 1). Schmidt-Kittler et al. (2006) assigned this scarce material (only three specimens recovered), to the species Yindirtemys aff. ulantatalensis. These authors considered that the morphological characters of the Mongolian species were identical to Yindirtemys ulantatalensis from Ulantatal. However, the size of the Mongolian species was within the inferior part of the size variation.
Emended diagnosis (this paper): Medium-sized species of Yindirtemys; more complicated dental pattern than older Yindirtemys; swollen and bulky molars; upper molars with a distinct anterocone; labial anteroloph medium or long; M3 with deflexus structure; sinus transverse and deep.

Geographic distribution: Valley of Lakes (Mongolia) and North Aral region (Kazakhstan).
Remarks: The maxilla of Yindirtemys birgeri from the locality of TAT-051/2, in the Tatal Gol region, is the only specimen recovered in Mongolia (see Table 1).
Diagnosis (Wang, 1997): Large species of Yindirtemys; upper cheek teeth having swollen cusps; P4 posterior cingulum developed; upper molars with transverse, nearly straight  (2017) were able to differentiate Y. suni from Y. deflexus since new fossil material is available from several localities of the Valley of Lakes. The material of Y. suni from the Valley of Lakes is relatively scarce (∼50 specimens recovered) and belongs to the two regions: Tatal Gol, in the locality of TAT-E/32, and Taatsiin Gol, in the localities of HTS-056/3, HTE-009, HTE-008, HTE-014-018, and UNCH-A/3 + 4 (see Table 1).
Geographical range: Valley of Lakes, Mongolia.

Remarks:
The description of this new species will be published in a forthcoming paper. Prodistylomys nov. spec. 1 is the largest Prodistylomys in the Valley of Lakes. This species occurred in the region of Taatsiin Gol (localities of HTE-003 and HTE-012; see Table 1). The recovered material is very scarce (about 10 specimens).
Geographical range: Valley of Lakes, Mongolia.

Remarks:
The description of this new species will be published in a forthcoming paper. Prodistylomys nov. spec. 2 is the commonest Prodistylomys species in the Valley of Lakes. However, in comparison with other ctenodactylids, the fossils recovered are relatively scarce (35 specimens). This mediumsized species occurred in the Taatsiin Gol region, in the localities of RHN-A/12, RHN-020, UNCH-A/3 + 4, and LOG-A/1 (see Table 1).
Geographical range: Valley of Lakes, Mongolia.
Remarks: The description of this species will be published in a forthcoming paper. Prodistylomys nov. spec. 3 is very scarce, only one specimen recorded in the locality of HTE-005 (Taatsiin Gol region).

Diversity and size changes of the Mongolian Ctenodactylidae
Four different groups have been defined according to the morphology and size of the Mongolian ctenodactylids: 1. Ctenodactylids from the early Oligocene (biozones A and B) and early late Oligocene (biozone C) as Kakaromys decessus, Huangomys frequens, Yindirtemys shevyrevae, and Tataromys minor longidens are typically small-sized. Additionally, these species show bunodont teeth, with relatively simple dental pattern. Furthermore, height of the crown is very low. 2. Part of the early late Oligocene (biozone C) ctenodactylids such as Yindirtemys aff. ulantatalensis, Tataromys sigmodon, and T. plicidens form the second group. These species retain a comparable dental morphology, but, are larger than the previous ones. 3. In contrast to the small early Oligocene forms, the ctenodactylids from late Oligocene (biozones C1, C1-D) and early Miocene (biozone D) are medium to large-sized (Fig. 3). These species are exemplified by the genus Yindirtemys (Y. birgeri, Y. deflexus, and Y. suni), whose dentition have a more complicated dental pattern and a higher degree of selenodonty and hypsodonty (i.e. the height of the crown is larger than previous).

4.
The last group is restricted to the genus Prodistylomys from early Miocene (biozone D) with the species Prodistylomys nov. spec. 1, Prodistylomys nov. spec. 2. and Prodistylomys nov. spec. 3. These forms are small to medium sized and stand out for their very simple dental pattern (bilophodont), prismatic crowns and hypsodonty.
Along the Oligocene and early Miocene, there is an increase in size among the different Yindirtemys species (Figs. 5 and 7). The oldest ones, Y. shevyrevae and Yindirtemys aff. ulantatalensis, are the smallest species, whereas the youngest, Y. deflexus and Y. suni, are the largest. Our studies on the Ctenodactilidae from Mongolia evidence that the subfamily Tataromyinae trends towards increasing size, crown height, and more developed crests, confirming previous studies Oliver and Daxner-Höck 2017). These modifications started in the early Oligocene (biozone A), continued in the heyday of the family in late Oligocene (biozone C), increased rapidly towards the latest Oligocene (biozone C1), and ended with the extinction of the genus in the early Miocene (biozone D).
Ctenodactylidae occurred for the first time in Central Mongolia in the early Oligocene (Mongolian biozone A). Three genera dominated this biozone, Karakoromys, Huangomys, and Yindirtemys (Figs. 3 and 4). During biozone B, these three genera remain constant, only Karakoromys disappeared during the lower part of biozone B. From biozone B onwards a relatively varied ctenodactylid assemblage persists in the region, and the genus Tataromys first was evidenced in the higher part of biozone B.
An important climatic disturbance took place at the beginning of the late Oligocene (biozone C; 27-28 M.a.), called the Mid-Oligocene Reorganization (Harzhauser et al. 2016), coinciding with the Oligocene Glacial Maximum. This significant climatic change forced two effects in the ctenodactylid assemblages. Firstly, the species Huangomys frequens (a typical component from early Oligocene) went extinct. Secondly, the stable assemblages recorded at the biozone B were replaced by short-termed changing faunas towards its maximum between 26 and 25 M.a. (late Oligocene; Fig. 4) dominated by Yindirtemys and Tataromys species. Up to five ctenodactylid species are recorded at this time in the Valley of Lakes (Fig. 3).
The richness' curve shows that the ctenodactylids experienced a drastic diversity drop towards the boundary between biozone C1 and C1-D (Fig. 4), defined as the Late Oligocene Extinction Event (Harzhauser et al. 2016), in which both Tataromys species and Y. birgeri went extinct. The genus Yindirtemys acted as a transitional component, being the only representative of the highly impoverished ctenodactylid faunas at the end of the late Oligocene. While Y. deflexus, the only survivor species from the crisis disappeared at the Oligo-Miocene boundary, Y. suni not only crossed it, but persisted up to the early Miocene (biozone D) as a relict of Tataromyinae. During the early Miocene, Y. suni was accompanied by three species of the genus Prodistylomys, the only genus of Distylomyinae in the area.

Composition of Ctenodactylidae palaeocommunities in Central Asia
We have compared the specific richness of the ctenodactylids from the Valley of Lakes to that from Ulantatal (Inner Mongolia). Both areas have well-known Oligocene deposits, as well as diverse mammal faunas (Huang 1982;Daxner-Höck et al. 2010). In the Valley of Lakes five genera and 13 species of Ctenodactylidae are evidenced (Fig. 3), whereas from Ulantatal nine genera and 16 species were described (Gomes Rodrigues et al. 2014, table 2).
In both regions, the early Oligocene is characterised by Karakoromys. The species Karakoromys deccesssus is known from Mongolia and China, K. cf decessus only from China.
Huangomys frequens is also common in both areas. In Mongolia it is restricted to the early Oligocene, but in China it persisted to the late Oligocene.
The genus Helanshania is only present in the early Oligocene of Ulantatal.
Yindirtemys and Tataromys also occurred in the early Oligocene, and developed different species. This development goes along with size increase and successively with more complicated dental pattern. In the Valley of Lakes five Yindirtemys species developed, two small-sized (Y. shevyrevae and Y. aff. ulantatalensis), one medium-sized (Y. birgeri) and two large-sized (Y. deflexus and Y. suni). In Ulantatal occurred also five species, four of small size (Y. shevyrevae, Y. aff. shevyrevae, Y. ulantatalensis and Y. bohlini) and Y. deflexus of large size. Three Tataromys species were evidenced in Mongolia and China. T. sigmodon and T. plicidens in both areas, T. minor in Ulantatal and the subspecies T. minor longidens in the Valley of Lakes.
The Ctenodactylidae disappeared in Ulantatal at the end of the Oligocene, however, in the Valley of Lakes the family persisted up to the early Miocene with Y. suni and the Prodistylomys species (Prodistylomys nov. spec. 1, Prodistylomys nov. spec. 2. and Prodistylomys nov. spec. 3). Distylomyinae are registered in China (Xinjiang and Nei Mongol) from late Oligocene (Distylomys qianlishanensis) to early Miocene (Wang 1997), and in Mongolia (Valley of Lakes) in the early Miocene.
The distribution of the ctenodactylids suggests that no physical barriers existed between Kazakhstan, Mongolia, and northern China throughout the Oligocene and early Miocene; the differences in the palaeocommunity are derived from different ecological niches and from different environments and/or different climatic conditions Bendukidze et al. 2009;Gomes Rodrigues et al. 2014;Oliver and Daxner-Höck 2017).

Conclusions
Our study shows the diversity of Mongolian ctenodactylids.
The pattern of the ctenodactylids shows three phases: A first starts as diversity burst at the early Oligocene. The second phase records an increment in the faunal replacement with higher extinction that lead to a diversity maximum in biozone C1 (at ∼26-25 M.a.; late Oligocene). We assume that the observed changes of ctenodactylid compositions are linked with the climatic instability in the course of the late Oligocene, called the Late Oligocene Extinction Event (Harzhauser et al. 2016).
Finally, the third phase is characterised by taxonomically impoverished ctenodactylid faunas of the early Miocene. The history of the Ctenodactylidae in Mongolia was influenced by palaeogeographic reorganisation (transformations of local palaeoenvironments) and by overall climate changes towards increasing aridity (see Harzhauser et al. 2016).