Introduction

The aim of this review is to compare the results presented by palaeontologists and geneticists who investigated the phylogenetic relationship of the Rhizomyinae and the Spalacinae. In spite of the progress made in both disciplines during the last decade, conclusions remain conflicting.

In the classification of extant mammals by Wilson and Reeder (2005), the fossorial rodents Myospalacinae, Rhizomyinae (including the Tachyoryctinae) and Spalacinae are united into the family Spalacidae, separate from all other Muridae, thus returning to the classical arrangement of Thomas (1896). This view is supported by recent genetic studies which unanimously suggest that the Rhizomyinae and Spalacinae represent the same early branch of the Muridae (in the Muroidea).

The fossil record, however, suggests that the muroid ancestor of each of these subfamilies was different and that their ancestors adapted to a fossorial mode of life during a different period and in a different geographical area. Most palaeontologists therefore interpret the adaptations to a fossorial mode of life shared by these subfamilies to have developed independently (e.g. Flynn et al. 1984; Sen and Sarica 2011). The classification of McKenna and Bell (1997), which includes fossil genera, follows this view and considers the Myospalacinae, Rhizomyinae and Spalacinae to be separate subfamilies of the family Muridae. Other subfamilies of the Muridae containing fossorial species are the extant Arvicolinae and Sigmodontinae and the extinct Anomalomyinae and Tachyoryctoidinae (McKenna and Bell 1997).

The geographic distribution of the extant Myospalacinae, Rhizomyinae and Spalacinae shows that each of the three subfamilies occupies its own geographical area, the Myospalacinae in eastern Asia (mainly China and Mongolia), the Rhizomyinae in south and southeastern Asia (Rhizomys and Cannomys) and in the eastern part of Africa (Tachyoryctes) and the Spalacinae in southeastern Europe and Anatolia (Figs. 1 and 2).

Fig. 1
figure 1

Sketch maps of present day Eurasia and North Africa showing the major occurrences of the genera and species of the Rhizomyinae and Spalacinae during the late Oligocene and early Miocene. 1 Vetusspalax progressus, Banovići, Bosnia and Herzegovina (De Bruijn et al. 2013), 2 Prokanisamys kowalskii, Zinda Pir Dome, Pakistan (Lindsay 1996), 3 Prokanisamys arifi, Banda daud Shah, Pakistan (De Bruijn et al. 1981), 4 Prokanisamys arifi and P. major, Gaj River, Pakistan (Wessels and De Bruijn 2001), 5 Prokanisamys sp., Jebel Zelten, Libya (Wessels et al. 2003), 6 Heramys eviensis, Aliveri, Greece (Klein Hofmeijer and De Bruijn 1985), 7 Heramys sp., Sibnica, Serbia (Marković 2003), 8 Debruijnia arpati, Keseköy, northeast Anatolia (Ünay 1996), 9 Debruijnia sp., Söke, Dededag, western Anatolia (Sen and Sarica 2011), 10 Pliospalax sp., Karydia, northeastern Greece (Theocharopoulos 2000); 11 Pliospalax sp., Antonios, northeastern Greece (Vasileiadou and Koufos 2005), 12 Pliospalax sp., Çatalarkaç, central Anatolia (not published)

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Fig. 2
figure 2

Sketch maps of present day Eurasia and northern Africa showing the major occurrences of the genera and species of the Rhizomyinae and Spalacinae during the middle Miocene and late Miocene–early Pliocene. 13 Kanisamys indicus and K. potwarensis, Potwar plateau, Pakistan (Wood 1937; Flynn 1982), 14 Prokanisamys benjavuni, Li Basin, Thailand (Mein and Ginsburg 1985), 15 Pronakalimys andrewsi, Fort Ternan, Kenya (Tong and Jaeger 1992), 16 Pliospalax sp., Vracevići, Serbia (Marković 2003), 17 Pliospalax, div. species, diverse localities, Anatolia (Ünay et al. 2003, Sen and Sarica 2011), 18 Eicooryctes, Kanisamys, Miorhizomys, Protachyoryctes, Rhizomyides, Potwar Plateau, Pakistan (Flynn 1982; López-Antoňanzas et al. 2012), 19 Kanisamys, Miorhizomys, Protachyoryctes, Rhizomyides, Haritalyangar and Bilaspur, India (Flynn 1982), 20 Tachyoryctes makooka, Digiba Dora, Ethiopia (Wesselman et al. 2009), 21 Miorhizomys nagrii, M. tetrachorax, Lufeng, China (Flynn and Qi 1982; Flynn 2009), 22 Nakalimys lavocati, Nakali, Kenya (Flynn and Sabatier 1984), 23 Rhizomyides carbonelli, Pul-e Charki, Afghanistan (Brandy 1979), Rhizomyides mirzadi, Bamian Basin, Afghanistan (Lang and Lavocat 1968), 24 Brachyrhizomys shajius, Yushe Basin, China (Flynn 1993), Brachyrhizomys shansius, Yushe Basin, China (Teilhard de Chardin 1942), 25 Heramys anatolicus, Sinap, Anatolia; Pliospalax incliniformis, Sinap, Anatolia, Pliospalax sinapensis, Sinap, Anatolia (Sarica and Sen 2003), 26 Pliospalax complicatus, Amasya, Anatolia (Sen and Sarica 2011), 27 Pliospalax, div sp., div. localities Anatolia (Ünay 1996; Sen and Sarica 2011), 28 Pliospalax macovei, Beresti, Malusteni, Romania (Kormos 1932), 29 Spalax odessanus, Odessa, Ukraine (Topachevski 1969), 29a Spalax odessanus, Kara Burun, Greece (De Bruijn 1984), 30 Pliospalax sotirisi, Rhodes, Greece (De Bruijn et al. 1970), 31 Pliospalax compositodontus, Andriivka, Ukraine (Topachevski 1969)

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Here, we restrict the discussion to the Rhizomyinae and Spalacinae because these two subfamilies are represented by many living species, and both have an exceptionally good fossil record. An overview of the genera and species included in each of these subfamilies is given in Table 1. Author names are provided for in this table, but are omitted in the text. The taxonomic levels applied are family, subfamily, genus and species, following McKenna and Bell (1997) for the Muridae. We neither use tribe, subgenus nor subspecies. Therefore, the Rhizomyinae, as used here, includes the Asian as well as the African genera. Furthermore, we include Sinapospalax into Pliospalax because the differences in dental pattern of the cheek teeth of the species in these genera are very subtle (Figs. 3, 4, 5 and 6). Eumyarion kowalskii, a species which plays an important role in our discussion, has been transferred by Wessels and De Bruijn (2001) to Prokanisamys because its cheek teeth lack the, for Eumyarion characteristic, strong anterior arm of the protocone in the M1 as well as the posterior arm of the hypoconid in the m1 (Figs. 4 and 6). Since this transfer has been ignored by some authors (e.g. Flynn et al. 2013) we explicitly state that we adhere to our earlier generic allocation. For the sake of comparison, the tooth rows are depicted as if they are of the same size (Figs. 3, 4, 5 and 6).

Table 1 The genera and species of the Rhizomyinae and Spalacinae
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Fig. 3
figure 3

Upper molars (M1, M2, M3), occlusal and lingual view. a Heramys eviensis, Aliveri, Greece (Klein Hofmeijer and De Bruijn 1985), b Debruijnia arpati, Keseköy, Anatolia (Ünay 1996), c Vetusspalax progressus, Banovići, Bosnia and Herzegovina (De Bruijn et al. 2013). The specimens are not to scale

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Fig. 4
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Upper molars (M1, M2, M3), occlusal and lingual view. a Kanisamys indicus, Gaj River, Pakistan (Wessels and De Bruijn 2001), b Prokanisamys arifi, Gaj River, Pakistan (Wessels and De Bruijn 2001). The specimens are not to scale

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Fig. 5
figure 5

Lower molars (m1, m2, m3), occlusal and labial view. a Heramys eviensis, Aliveri, Greece (Klein Hofmeijer and De Bruijn 1985), b Debruijnia arpati, Keseköy, Anatolia (Ünay 1996), c Vetusspalax progressus, Banovići, Bosnia and Herzegovina (De Bruijn et al. 2013). The specimens are not to scale

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Fig. 6
figure 6

Lower molars (m1, m2, m3, occlusal and labial view. a Kanisamys indicus Gaj River, Pakistan (Wessels and De Bruijn 2001), b Prokanisamys arifi Gaj River, Pakistan (Wessels and De Bruijn 2001). The specimens are not to scale

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Concise review of the molecular genetic studies

A number of molecular phylogenetic studies have been performed with the aim, among (many) other aims, of testing the hypothesis that the Rhizomyinae and the Spalacinae belong to the same early branch of the Muroidea. These studies are listed in Table 2. The results in general strongly indicate that the Rhizomyinae and the Spalacinae, together with the Myospalacinae, form a separate clade within the Muroidea (Jansa and Weksler 2004; Norris et al. 2004; Blanga-Kanfi et al. 2009; Jansa et al. 2009; Gogolevskaya et al. 2010). Michaux et al. (2001), Norris et al. (2004) and Steppan et al. (2004), on the basis of their data, proposed placing the Rhizomyinae and the Spalacinae in a separate family, Spalacidae, leaving the family name Muridae to all other members of the superfamily Muroidea. The close relationship between the Myospalacinae and Rhizomyinae and the Spalacinae has been confirmed in a study by Lin et al. (2014) based on the results of transcriptome sequencing. Cytogenetic studies comparing chromosomes of species of the Rhizomyinae and the Spalacinae (e.g. by comparative painting) have not been performed.

Table 2 Molecular genetic studies analyzing phylogenetic relationships among Muroidea including Rhizomyinae and Spalacinae
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Concise review of the fossil data

Most of the early fossil representatives of the Rhizomyinae and Spalacinae are known by dental remains only, so their life-style has to be inferred from the teeth, which introduces uncertainty. The development of dental similarity in these subfamilies as an adaptation to a fossorial life-style makes it difficult to distinguish grades from clades: the occurrence of the same morphologies in taxa does not necessarily mean that they are closely related as these morphologies can be derived independently (Wood 1965).

The Spalacinae Gray, 1821

The origin, taxonomy and phylogeny of the Spalacinae have been discussed by many authors (e.g. Petter 1961; De Bruijn et al. 1970; Fejfar 1972; De Bruijn 1984; Klein Hofmeijer and De Bruijn 1985; De Bruijn and Saraç 1991; Hugueney and Mein 1993; Ünay 1996; Sen and Sarica 2011). The genera Rhizospalax (now in the Castoridae) and Prospalax (now in the Anomalomyinae) have in the past been considered to be Spalacinae. Fejfar (1972) suggested that the origin of the Anomalomyinae and Spalacinae was in the Tachyoryctoidinae, while others defended the view that the Anomalomyinae, the Tachyoryctoidinae and the Spalacinae are not closely related (Klein Hofmeijer and De Bruijn 1985; De Bruijn and Saraç 1991).

The first fossil true spalacine was recognised by Kormos in 1932—Pliospalax macovei from the Pliocene of Romania. A number of Pliospalax species of middle Miocene to late Pliocene age (Europe, Turkey and Ukraine) have been described since, with the first record of the subfamily pushed back in time by such new finds as Heramys eviensis (early Miocene, MN4, Greece; Klein Hofmeijer and De Bruijn 1985), Debruijnia arpati (early Miocene, MN3, Anatolia; Ünay 1996) and Vetusspalax progressus (late Oligocene, MP30, Bosnia and Herzegovina; De Bruijn et al. 2013). The dentitions of these species share unmistakably spalacine characteristics, namely, (1) anterior wall of the protocone of the M1 being almost at right angles to the base of the crown; (2) fusion of the anterocone of the M1 into the anteroloph; (3) forward position of the metaconid of the m1 at the expense of the anteroconid. Heramys, Debruijnia and Vetusspalax do not represent one evolutionary lineage because the older Vetusspalax shows more derived characteristics than the younger Debruijnia (Figs. 3, 4, and 5). This points to an early radiation of the Spalacinae in southeastern Europe and the eastern Mediterranean area during the Oligocene. The fossil and extant geographical ranges of the Spalacinae roughly overlap (Figs. 1, 2), suggesting that the earliest spalacines recognised were already fossorial rodents because these are known to be limited in their dispersal abilities (Flynn 1982, 1990; Savič and Nevo 1990; Kryštufek and Griffiths 2002). The fossil record thus provides strong evidence that the Spalacinae developed a fossorial life-style much earlier than, and independently from, the Rhizomyinae.

The Rhizomyinae Winge, 1887

Hypothetically the earliest rhizomyine is supposed to have been a non-fossorial cricetine from the late Oligocene of southeast Asia (Wessels et al. 2003, 2008). Prokanisamys kowalskii from the earliest Miocene of Pakistan is the oldest record of the Rhizomyinae recognised. Prokanisamys has a wide geographical range in southeast Asia and reached North Africa during the early Miocene (Fig. 1; Wessels et al. 2003; Wessels 2009). Although the postcranial skeleton of Prokanisamys is not known, it is assumed that the species of that genus were not fossorial (Flynn 1982, 1985), an assumption supported by its wide geographical range. The adaptation to a fossorial life-style in the rhizomyines of southeast Asia seems to have taken place during the early late Miocene, and in the tachyoryctines of northeast Africa during the late Miocene and the Pliocene (Flynn 1982, 1990; Flynn and Sabatier 1984; Tong and Jaeger 1992; Wesselman et al. 2009). The rather poor fossil record of the African rhizomyines—there is no record of the group between the early Miocene Prokanisamys sp. from Libya and the late middle Miocene Pronakalimys from Kenya—does not confirm hypothesised explanations for the multiple migrations of Rhizomyinae from Asia to Africa as interpreted in López-Antoňanzas et al. (2012). From a biological point of view, a long-distance migration of fossorial, territorial rodents is unlikely (Kryštufek and Griffiths 2002), so our working hypothesis is that the non-fossorial Prokanisamys migrated from Asia to Africa where it developed a fully fossorial mode of life independent of its Asian counterparts.

The lower incisors of the Spalacinae and Rhizomyinae

The lower incisors of many species of Spalacinae and Rhizomyinae show two longitudinal ribs in combination with the derived type ten or eleven microstructure of the enamel (Kalthoff 2000). This need not necessarily mean that these two groups are closely related, because the same traits of the lower incisors occur in a number of other subfamilies of the Muridae, such as in the late Oligocene and Miocene Eumyarioninae and Cricetodontinae. Apparently, this combination of characteristics of lower incisors developed a number of times in different subfamilies.

The evolutionary dynamics of the Rhizomyinae and Spalacinae

Table 3 summarises the numbers of genera and species of the Rhizomyinae and the Spalacinae in the four time slices defined in Figs. 1 and 2. The Spalacinae show a generic decline during the middle Miocene which is almost certainly an artefact due to the paucity of studies on the collections from the middle Miocene of Anatolia. Their representation in terms of numbers of genera and species (Table 3) during the late Miocene/early Pliocene probably reflects reality. The Rhizomyinae play a modest role until the late Miocene, when they became very diverse, in particular in the northern part of the Indian subcontinent. This radiation may well correlate with the development of a fossorial life-style, which may have enhanced a mosaic type of evolution.

Table 3 The number of genera and species of the Rhizomyinae and Spalacinaea
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Conclusions

The discrepancy between the opinions of geneticists and palaeontologists on the relationship of the Rhizomyinae and Spalacinae is intriguing and not understood. Explanations may perhaps be sought in the restrictions inevitably connected with the methods used in the genetic studies of Table 2 and in the incompleteness inherent to the fossil record. New insights may be obtained through the application of advanced molecular genetic techniques (genome and transcriptome sequencing) such as those which have already been used for rhizomyine and spalacine species by Zhao et al. (2013), Fang et al. (2014) and Lin et al. (2014).

Although the fossil record of the Rhizomyinae and Spalacinae is relatively good, it is clear that much of the earliest history of these subfamilies is not documented. The oldest spalacine known, Vetusspalax from the late Oligocene of southeast Europe, has a much too derived dentition to be ancestral to all later ones. The radiation of the Spalacinae must thus have occurred earlier in the Oligocene. The oldest rhizomyine known, the non-fossorial Prokanisamys from the earliest Miocene of the Indian subcontinent, can not yet be traced to a specific muroid ancestor.

Until the differences in opinion between geneticists and palaeontologists are resolved, we propose to classify the Rhizomyinae and the Spalacinae as separate subfamilies within the Muridae.