New proviverrines (Hyaenodontida) from the early Eocene of Europe ...

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Zoological Journal of the Linnean Society, 2014, 171, 878–917. With 13 figures

New proviverrines (Hyaenodontida) from the early Eocene of Europe; phylogeny and ecological evolution of the Proviverrinae FLORÉAL SOLÉ1,2*, JOCELYN FALCONNET2 and LAURENT YVES3,4 1

Earth & Life History O.D., Department of Paleontology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000 Brussels, Belgium 2 Département Histoire de la Terre, Muséum National d’Histoire Naturelle, UMR 7207 CR2P: Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements, CP 38; 8 rue Buffon; F-75005, Paris, France 3 Association Paléontologique du Sud-Ouest (APSO), 13 chemin des Telles, F-31360 Roquefort-sur-Garonne, France 4 Muséum d’Histoire Naturelle de Toulouse, 35 allées Jules Guesde, F-31000 Toulouse, France Received 10 October 2013; revised 17 March 2014; accepted for publication 17 March 2014

We describe six proviverrine species from the Early Eocene of France. Three species are new: Minimovellentodon russelli sp. nov. from Mutigny [mammal palaeogene (MP)8 + 9], Boritia duffaudi sp. nov. from La Borie (MP8 + 9), and Leonhardtina godinoti sp. nov. from Grauves (MP10). We describe new specimens and propose new generic combinations for three species from MP10: Protoproviverra palaeonictides, Matthodon menui, and Oxyaenoides lindgreni. We also propose a new generic combination for the primitive Eoproviverra eisenmanni (MP7). Matthodon menui was previously considered as a possible oxyaenodontan, but the new fossils clearly support its reference to Hyaenodontida. Leonhardtina godinoti and Ma. menui are the oldest occurrences for these genera, which were previously unknown before the Middle Eocene. Moreover, the discovery of the proviverrine Mi. russelli in Mutigny implies that the Proviverrinae dispersed in Northern Europe between biozone Palaeocene-Eocene (PE) III (Abbey Wood) and biozone PE IV (Mutigny). This also supports a homogenization of the European faunas during the Early Eocene. The dispersal is concomitant with the disappearance of the oxyaenodontans, arfiines, and sinopines (Hyaenodontida) from Europe. The proviverrines may have filled the ecological niches left vacant by the disappearance of the other carnivorous mammals. With 20 genera and over 30 species, proviverrines were successful in Europe. We performed the first phylogenetic analysis comprising almost all the Proviverrinae. Our analyses indicate that the Proviverrinae diversified greatly during the Early Eocene Climatic Optimum and show a general trend towards specialization throughout the Eocene. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 171, 878–917. doi: 10.1111/zoj.12155

ADDITIONAL KEYWORDS: hypercarnivory – palaeoecology.

INTRODUCTION As discussed in Solé, Gheerbrant & Godinot (2011, 2013a), carnivorous mammals provide interesting arguments for discussing the palaeobiogeography of Europe during the Early Eocene. The European *Corresponding author. E-mail: [email protected]

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hyaenodontidans are represented in the Early Eocene by nine species referred to three distinct subfamilies: (1) Proviverrinae: ‘Proviverra’ eisenmanni [Rians, mammal palaeogene (MP)7], Parvagula palulae (Palette, MP7), Morlodon vellerei (Avenay and Saint-Agnan, MP8 + 9/MP10), Francotherium lindgreni (Mancy, MP10); (2) Sinopinae: Prototomus minimus (Dormaal and Abbey, MP7/MP8 + 9), Prototomus girardoti (Dormaal, Pourcy,

© 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 171, 878–917

EVOLUTION OF THE PROVIVERRINAE Soissons, and Abbey Wood, MP7/MP8 + 9), Galecyon morloi (Dormaal, MP7), Galecyon galus (Rians, MP7); (3) Arfiinae: Arfia gingerichi (Dormaal and Try, MP7) (Rich, 1971; Godinot, 1981; Godinot et al., 1987; Smith & Smith, 2001; Hooker, 2010; Solé, 2013; Solé et al., 2013a). The specimens described here are all referred to the Proviverrinae. This subfamily is considered to be endemic to Europe, where it underwent a radiation (Solé, 2013). In contrast to the Proviverrinae, the Arfiinae and Sinopinae rapidly disappeared from Europe (Solé et al., 2013a). Moreover, the Arfiinae and Sinopinae are mostly restricted to the Paris Basin, whereas the Proviverrinae are recorded throughout Europe. The new specimens are from the two European provinces defined by Marandat (1997) for the earliest Early Eocene: the Northern Province and the Mesogean (= Southern) Province. The Northern Province localities studied here are all located in the Paris Basin: Mutigny (MP8 + 9), Chavot, Monthelon, Cuis, Mancy, and Grauves (MP10) (Fig. 1). Only one locality from the Southern Province – La Borie – provided a new specimen (Fig. 1). It is worth remembering that Marandat et al. (2012) showed the importance of the

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southern French localities for understanding the palaeobiogeography of Europe during the earliest Eocene. In this framework, the description of the hyaenodontidan from La Borie appears to be important and will allow comparisons with contemporaneous European localities. Finally, in order to investigate the interrelationships of Proviverrinae and to understand the evolution of this group, we performed the first phylogenetic analysis dealing with almost all its representatives.

NOMENCLATURE JUSTIFIED

EMENDATIONS

Solé (2013) subdivided the former ‘Proviverrinae’ into three distinct subfamilies: the Proviverrinae Schlosser, 1886 sensu stricto and the new Sinopaninae Solé, 2013 and Arfianinae Solé, 2013. The formation of the last two names has since proved to be incorrect and their spelling must therefore be emended, following Article 32.2 of the Code (ICZN, 1999). The type genus of the Sinopaninae is Sinopa Leidy, 1871, after a Niitsítapi (or ‘Blackfoot’) word for the

Figure 1. Map showing Early Eocene hyaenodontidan-bearing localities (A), with focus on the Paris Basin (France) (B). MP7: 1, Dormaal (Belgium); 2, Abbey Wood (England); 3, Rians, Palette (France). MP8 + 9: 4, La Borie (France); 5, Chavot, Cuis, Mancy, Monthelon, Grauves (France); 6, Try, Condé-en-Brie, Saint-Agnan (France); 7, Mutigny, Avenay (France); 8, Sézanne-Broyes (France); 9, Le Quesnoy (France). Data from the present paper, Godinot (1981), Godinot et al. (1987), Smith and Smith (2001), Hooker (2010), Solé (2013), Solé et al. (2013a). A, retrieved and modified from http:// commons.wikimedia.org/wiki/File:European_Union_relief_laea_location_map.svg. B, retrieved and modified from http:// commons.wikimedia.org/wiki/File:Topographic_map_of_the_Seine_basin.svg. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 171, 878–917

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kit fox Vulpes macrotis Merriam, 1888. As this name is neither a Greek nor a Latin word, Article 29.3.3 applies: ‘the stem for the purposes of the Code is that adopted by the author who establishes the new familygroup taxon, either the entire generic name [. . .], or the entire generic name with the ending elided, or the entire generic name with one or more appropriate linking letters incorporated in order to form a more euphonious family-group name’ (ICZN, 1999). The formation of Sinopaninae corresponded neither to the first nor to the second case. Regarding the third case, the first author confirms that he did not aim to make the subfamily name euphonious when he added an ‘n’ between the stem and the subfamily suffix. The name Sinopaninae was therefore not formed in accordance with Article 29.3, in which case Article 29.5 might apply to maintain the spelling that is in prevailing usage. As it was founded very recently, however, this is impossible. Hence, following Article 32.5.3, Sinopaninae is an incorrect original spelling that must be corrected. There are several options, as stated by Article 29.3.3: ‘Sinopainae’, with the whole genus name, or ‘Sinopinae’, with elision of the terminal vowel. As seen before, there is no need to add linking letters to obtain a euphonious subfamily name. In addition to be easier to pronounce in several languages, the second version is congruent with the current hyaenodontid subfamilial names. For these reasons, the second spelling is preferred as the correct original spelling. The original spelling of the subfamily based on Sinopa Leidy, 1871, is therefore corrected from Sinopaninae Solé, 2013, to Sinopinae Solé, 2013 (ICZN, 1999). By contrast, the Arfianinae Solé, 2013, were named after Arfia Van Valen, 1965. This genus name was founded on the onomatopoetic ‘arf’, which represents the sound made by a barking dog, with the addition of the feminine Latin suffix -ia, frequently used to form adjectives from nouns. In this case, Arfia falls under Article 29.3.1: ‘the stem for the purposes of the Code is found by deleting the case ending of the appropriate genitive singular’ (ICZN, 1999). Thus, the correct stem formed from Arfia is not ‘arfian-’ but ‘arfi-’. As the name Arfianinae was formed after 1999 from a genus name ending with a Latin suffix, Article 29.4 states that: ‘its original spelling must be maintained as the correct original spelling, provided [29.4.1] it has a correctly formed suffix [Art. 29.2], and [29.4.2] its stem is formed from the name of the type genus as though it were an arbitrary combination of letters [Art. 29.3.3]’ (ICZN, 1999). Although the subfamilial suffix ‘-inae’ is correct, the stem would have been ‘arfia-’ if the type genus name had been an arbitrary combination of letters. The requirements of Article 29.4 are therefore not fulfilled. As in the case of ‘Sinopaninae’, Article 29.5 cannot apply either, because there is no

current prevailing usage. Thus, following Article 32.5.3, Arfianinae is an incorrect original spelling that must be corrected. In accordance with Article 29.3.1, the correct original spelling of the subfamily founded upon the genus Arfia Van Valen, 1965 is therefore Arfiinae Solé, 2013.

AGREEMENT

IN GENDER

The ending of the species name Tinerhodon disputatum Gheerbrant, 1995 is incorrect. It corresponds indeed to the neuter nominative ‘-um’. As the specific epithet is a Latin word, which is neither based on a personal nor on a geographical name, it must agree with the gender of the genus name according to Article 31.2 (ICZN, 1999). As the presence of the classical Greek word ‘odon’ indicates that Tinerhodon Gheerbrant, 1995, is masculine, the correct spelling is Tinerhodon disputatus Gheerbrant, 1995.

MATERIAL AND METHODS INSTITUTIONAL AND

COLLECTION ABBREVIATIONS

The Association Paléontologique du Sud-Ouest (APSO) carried out the fieldwork in the fossiliferous locality of La Borie. They collected specimens from seven distinct fossiliferous sites, which are numbered SP0 to SP6 (Laurent et al., 2010). The holotype of Boritia duffaudi comes from SP5 and is housed in the Muséum d’Histoire Naturelle de Toulouse (Haute-Garonne, France). The specimens referred to Oxyaenoides lindgreni, Protoproviverra palaeonictides, and Leonhartina godinoti are housed in the Muséum National d’Histoire Naturelle (Paris). The material ascribed to Matthodon menui is kept in the Muséum National d’Histoire Naturelle (Paris) and Naturhistorisches Museum Basel. The specimen assigned to Minimovellentodon russelli belongs to the Musée des Confluences (Lyon). MNHN, Muséum National d’Histoire Naturelle (Paris); MNHN.F.L-x-Ma, collection Louis from Mancy; MNHN.F.L-x-GR, collection Louis from Grauves; MNHN.F.Ma, collection from Mancy; MNHN.F.1939x, palaeontological collections; MNHN.F.Cui, collection from Cuis; MNHN.F.CHO, collection from Chavot; MNHN.F.Al, collection Lemoine, ‘Agéien’. T.S., Naturhistorisches Museum Basel. MHNT.PAL: Muséum d’Histoire Naturelle de Toulouse, Paleontological collection; MHNL, Musée des Confluences (Lyon). L: left; R: right.

DENTAL

TERMINOLOGY AND MEASUREMENTS

The Proviverrinae generally possess the primitive eutherian dental formula: three incisors, one canine,


EVOLUTION OF THE PROVIVERRINAE four premolars and three molars. We follow the dental terminology of Van Valen (1966) and Ginsburg (1999) for molars and premolars, respectively. Regarding upper premolars, we prefer to use the term ‘postmetacrista’ rather than ‘metastyle’. The measurements (length × width in mm) follow Gingerich & Deutsch (1989). The statistical parameters are the observed range (OR) and mean (M).

PALAEOECOLOGY Numerous authors (e.g. Van Valkenburgh, 1988, 2007; Wang, Tedford & Taylor, 1999) have created categories to describe the dietary habits of carnivorous mammals. The most significant categories are: (1) hypercarnivory (= diet composed of at least 70% meat); (2) mesocarnivory (= diet composed of 50–70% meat, with the balance made up of nonvertebrate foods); (3) hypocarnivory (= diet > 70% nonvertebrate foods). These categories are not entirely discrete and grade into one other in extant carnivorous mammals. Therefore, we only use the term hypercarnivorous for taxa that possess molars without a metaconid and have a strongly reduced or absent talonid on the lower molars (e.g. Oxyaenoides). Werdelin (1989) and Van Valkenburgh (2007) distinguished (1) bone-cracking taxa (e.g. hyenas) that use their premolars to break bones and (2) bone-crushing taxa (e.g. wolves) that use their postcarnassial molars instead. Morlo (1999) quantitatively showed that some hyaenodontidans had a durophagous diet. These hyaenodontidans probably broke bones with their premolars because their carnassial teeth are located very distally and because their molars display wear facets (notably wear facet 2) that are related to a shearing function. They thus may be considered bone-cracking predators. Diet is usually estimated qualitatively on the basis of morphofunctional studies (e.g. Denison, 1938; Butler, 1946; Van Valen, 1969). These estimations are based on comparisons with extant mammals. Nevertheless, some authors have proposed dental and cranial measurements to estimate the diet of extinct species. For carnivorous mammals, we cite Van Valkenburgh (1988) and Biknevicius, Van Valkenburgh & Walker (1996). As their methodologies were established for carnivoramorphan taxa, some adjustments were made by Morlo (1999) in his study of the palaeoecology of the ‘creodonts’. We followed his methodology and categories: meat, meat/bone and meat/nonvertebrates. We estimated diets only for the taxa here described; the diets of the other proviverrines are from Morlo (1999). However, we estimated that Matthodon possessed a meat/bone diet rather than a meat one, based on the enlargement of the premolars.

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Several methods have been proposed to estimate the body mass of extinct taxa, all based on comparisons with extant taxa. Gingerich (1990), Van Valkenburgh (1990), Anyonge (1993), and Egi (2001) based their estimates on postcranial elements. This method is inadequate for the proviverrines that are described below because their postcranium remains unknown. Another method relying on dental measurements instead was proposed by Morlo (1999). It can be easily applied to ‘creodonts’, including the material described in this study. We thus used this latter methodology.

SYSTEMATIC PALAEONTOLOGY MAMMALIA LINNAEUS, 1758 PLACENTALIA OWEN, 1837 FERAE LINNAEUS, 1758 HYAENODONTIDA LEIDY, 1869 Diagnosis Same as for the only family.

Distribution Africa, Asia, Europe, and North America; Selandian (Palaeocene) to Serravallian (Miocene).

Family Hyaenodontidae Leidy, 1869.

Note The Hyaenodontida is traditionally placed in the extinct order Creodonta together with the Oxyaenidae. Noting the possible paraphyly or polyphyly of Creodonta, several recent works have assigned Hyaenodontidae to a monotypic order, Hyaenodontida (Grohé et al., 2012; Solé, 2013; Solé et al., 2013b; Morlo et al., 2014).

HYAENODONTIDAE LEIDY, 1869 Diagnosis Elongate, narrow skulls with narrow basicrania and high, narrow occiput; frontals concave between orbital regions; tritubercular to sectorial molars with carnassial blades in P4, M1, M2, and M1, M2, and M3 (except in Limnocyoninae and Machaeroidinae); M3 present in most taxa; M 3 generally present; manus and pes mesaxonic, ranging from plantigrade to digitigrade; fibula articulated with calcaneum; astragalar−cuboid articulation reduced or absent; terminal phalanges compressed and fissured at tip; central, scaphoid, and lunar unfused (except perhaps for the hyainailourine Pterodon).


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Distribution Africa, Asia, Europe, and North America; Selandian (Palaeocene) to Serravallian (Miocene). Subfamilies Apterodontinae Szalay, 1967; Arfiinae Solé, 2013; Hyaenodontinae Leidy, 1869; Hyainailourinae Pilgrim, 1932; Indohyaenodontinae Solé et al., 2013b; Koholiinae Crochet, 1988; Limnocyoninae Wortman, 1902; ?Machaeroidinae Matthew, 1909; Proviverrinae Schlosser, 1886; Sinopinae Solé, 2013; Teratodontinae Savage, 1965. Note The systematic position of the sabre-toothed Machaeroidinae amongst ‘Creodonta’ is presently uncertain (see Gunnell, 1998).

PROVIVERRINAE SCHLOSSER, 1886, SENSU SOLÉ, 2013 Diagnosis Proviverrines differ from sinopines in exhibiting a combination of apomorphic features such as developed paraconid and wider talonid on P2, P3, and P4, developed entoconid on P3 and P4, developed parastyle on P4, a metacone more developed than the paracone on M 1 and M 2 (except in the primitive Eoproviverra eisenmanni), and a reduced metacingulum; and plesiomorphic features such as the presence of an entoconid on P4, and the retention of a bulbous entoconid on molars in the majority of the genera. Moreover, this clade has a double-rooted P1 (apomorphic feature); only Matthodon differs in having secondarily developed a single-rooted P1. Distribution Europe; Ypresian (Eocene) to Priabonian (Eocene). Genera Alienetherium Lange-Badré, 1981; Allopterodon Ginsburg et al., 1977; Boritia gen. nov.; Cynohyaenodon Filhol, 1873; Eoproviverra gen. nov.; Eurotherium Polly & Lange-Badré, 1993; Leonhardtina Matthes, 1952; Lesmesodon Morlo & Habersetzer, 1999; Matthodon Lange-Badré & Haubold, 1990; Minimovellentodon gen. nov.; Morlodon Solé, 2013; Oxyaenoides Matthes, 1967; Paenoxyaenoides Lange-Badré, 1979; Paracynohyaenodon Martin, 1906; Parvagula Lange-Badré, 1987 in Godinot et al., 1987; Praecodens Lange-Badré, 1981; Prodissopsalis Matthes, 1952; Protoproviverra Lemoine, 1891; Proviverra Rütimeyer, 1862; Quercytherium Filhol, 1880.

and high on molars, protoconid narrow, increasing in size from M1 to M3, protoconid one-third taller than paraconid, postprotocristid developed in the upper part, a short and crestiform talonid, reduced on M3, an M1 longer and narrower than M2, metacone taller and longer than paracone on M1 and M2, parastyle well developed, notably on M2, metastyle as long as paracone and metacone, projected distally and underlined by a cingulum, connate paracone and metacone, and metaconule absent. Synonymy Francotherium Rich, 1971 (subjective junior synonym; this study). Type species Oxyaenoides bicuspidens Matthes, 1967. Referred species Oxyaenoides schlosseri (Rütimeyer, 1891); Oxyaenoides lindgreni (Rich, 1971) comb. nov. Type locality MP11, Geiseltal (Germany). Distribution MP10, Mancy (France); MP11, Geiseltal (Germany), Poudingues de Palassou (France); MP13−14, Egerkingen (Switzerland).

OXYAENOIDES

(RICH, 1971) (FIG. 2)

LINDGRENI

COMB. NOV.

Emended diagnosis (modified from Rich, 1971) Oxyaenoides lindgreni is characterized by premolars that are compressed labiolingually and elongated mesiodistally with low and poorly individualized paraconid on P3 and P4, entoconid on P4, M1 smaller than M2 and M3, absence of metaconid, elongated molars, short and narrow talonid with no distinction between the cusps, labial part of talonid taller than lingual part, paracone reduced compared with metacone, and an elongated and distally shifted postmetacrista. Oxyaenoides lindgreni differs from Oxyaenoides bicuspidens by a smaller size and numerous plesiomorphic features such as a shallower mandible, lower hypoconid on P4, less individualized paraconid on P4 and larger paracone on M1.

OXYAENOIDES MATTHES, 1967

Chresonymy 1971: Francotherium lindgreni in Rich, pp, 20–23, fig. 6.

Emended diagnosis (reformulated from Lange-Badré & Haubold, 1990) Proviverrine of large size characterized by a P3 shorter than P4, molars without metaconid, paraconid short

Holotype MNHN.F.L-49-Ma, right mandible with P4, M1, and M3, and alveoli of P1, P2, P3, and M1.


EVOLUTION OF THE PROVIVERRINAE

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Figure 2. Oxyaenoides lindgreni (Rich, 1971) comb. nov. A, B, MNHN.F.L-23-Cuis, LM1. A, occlusal view; B, labial view. C−E, MNHN.F.L-49-Ma (holotype), right dentary bearing P4, M2, and M3, and alveoli of C1−P3 and M1. C, labial view; D, lingual view; E, occlusal view. F−H, MNHN.F.Ma14826, right dentary bearing P3 and P4 and alveoli of P2 and M1. F, occlusal view; G, labial view; H, lingual view. Scale bar = 10 mm. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 171, 878–917

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Referred specimens MNHN.F.Ma14826, right mandible with P3 and P4, posterior alveolus of P 2 , and anterior root of M 1 ; MNHN.F.Ma14833, RM2; MNHN.F.L-23-Cuis, LM1. Type locality MP10, Mancy (France). Additional distribution MP10, Cuis (France). Measurements See Table 1. Description The enamel is crenulated. The paracone and metacone, which are connate, are high and pointed. The base of the metacone is larger than that of the paracone; metacone and paracone of similar height on MNHN.F.L23-Cuis, but because the apex of the metacone is worn, the latter was probably taller than the paracone. The postmetacrista is aligned mesiodistally and is as long as the paracone and metacone together. The parastyle is very reduced and short, suggesting that MNHN.F.L23-Cuis corresponds to an M1. The stylar shelf is also very reduced. The protocone, which is missing on MNHN.F.L-23-Cuis, was probably very small and shifted mesially, as in Oxyaenoides bicuspidens. Table 1. Measurements (in mm) of the specimens of Oxyaenoides lindgreni (Rich, 1971) comb. nov. Locus M1 P1 P2 P3 P4 M1 M2 M3 MD

L W L W L W L W L W L W L W L W H

N

OR

1 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

11.49 – > 8.66* > 2.99* > 7.73* > 3.20* 9.40 3.56 11.53 4.88 10.74 5.53 11.21 4.66 10.59 4.92 21.88

Weight = 9.714 kg† *Estimated on the basis of the roots. †Weight estimated after Morlo (1999). N, number of specimens; OR, observed range.

Diastemata are present between the canine, P1, P2, and P3. P3 and P4 are close. The mandible is deep and its depth is constant. Foramina are present below P1 and P3. The symphysis reaches the distal root of P2. P1 and P2 are only known by their alveoli. The two teeth are two-rooted. The premolars lengthen mesiodistally from P1 to P4. The preserved premolars are mesiodistally elongated and are symmetrical in lateral view. The enamel is crenulated on P3 and P4. On P3, a paraconid is present mesially, but is low and poorly individualized. The protoconid is high, with a rather blunt apex. The talonid is low and short, being wider than long. It is as wide as the protoconid. The hypoconid is high and located labially. The entocristid is low and bears no cusp. Only a poorly developed postcingulid is present. The P4 is similar in morphology to the P3. In comparison, the paraconid is slightly more individualized, but is as low as on P3. The talonid is short, although as wide as the protoconid. As on P3, the talonid is wider than long. The hypoconid is labially located as on P3, but is taller. A very small and low entoconid is present. A small postcingulid is visible. There is no precingulid. The M1 is presently unknown. However, the holotype MNHN.F.L-49-Ma shows that the M1 is clearly smaller than the two other molars. The specimen MNHN.F.Ma14833 is identified as an M2 based on a comparison with the holotype MNHN.F.L-49-Ma. The molars are sharpened and simplified compared with those of earlier hyaenodontidans. There is no metaconid on the M2 and M3. The paraconid is shifted mesially. The protoconid is distinctly taller than the paraconid. The talonid is shorter and narrower than the trigonid. The talonid cusps are poorly individualized except for the hypoconid, which is clearly visible. There is no entocristid; the postfossid is thus fully opened lingually. The labial part of the talonid is distinctly taller than the lingual part. Discussion As the teeth on the holotype (Fig. 2C–E) are very worn, the new specimens described here provide new information concerning one of the largest hyaenodontidans from the Early Eocene of Europe – only Matthodon menui (Rich, 1971) is larger than Oxyaenoides lindgreni (see below). The new lower teeth described here all agree with the holotype described by Rich (1971): the P4 of MNHN.F.L-49-Ma and MNHN.F.Ma14826 are almost equal in size. MNHN.F.Ma14833 perfectly fits in size and morphology with the M2 of MNHN.F.L-49-Ma. The presence of a two-rooted P1 and a developed entoconid on P4 supports the referral of the Mancy specimens to the Proviverrinae. They display numerous features that are plesiomorphic for Proviverrinae, such as diastemata separating premolars and a narrow


EVOLUTION OF THE PROVIVERRINAE talonid on the molars. By contrast, they show apomorphic characters such as a mesially located paraconid, absence of a metaconid, and a simplified talonid. These features represent specializations towards a sectorial dentition. Rich (1971) noted the morphological similarity between O. lindgreni and Propterodon irdinensis Matthew & Granger, 1925, from the Middle Eocene of Mongolia. He also noted that O. lindgreni might represent an ancestor of the Hyaenodon−Pterodon complex. Morlo & Habersetzer (1999) referred O. lindgreni to Hyaenodontinae s.l. However, as demonstrated by Polly (1996), the development of a sectorial dentition occurred several times amongst the Hyaenodontida. The similarities between O. lindgreni and the other hypercarnivorous hyaenodontidans could therefore result from convergent evolution. Oxyaenoides lindgreni has recently been referred to the Proviverrinae (Solé, 2013); this referral is here supported. The European species is distinguished from Propterodon by the presence of an entoconid on P4 and the development of the paraconid on premolars, which are characteristic features of Proviverrinae. Thus, Propterodon and O. lindgreni evolved independently towards hypercarnivory. The remains of O. bicuspidens from MP11 of Geiseltal are closest to the species from Mancy. The two species share the absence of a metaconid and entoconid, as well as the presence of mesiodistally elongated premolars and molars, a mesially well-projecting paraconid on molars, a narrow and short talonid, a high labial part of the talonid, a lingually open postfossid, a metacone larger than the paracone, and a long and distally shifted postmetacrista. The morphology of the P3 and P4 are very similar to what is known in O. bicuspidens: the P3 and P4 are mesiodistally elongated and have a low and mesially elongated paraconid. Finally, the Mancy specimens and O. bicuspidens share a constant depth along the mandible; this is an apomorphic feature compared with the hyaenodontidans Prototomus (Sinopinae) and Parvagula (Proviverrinae). The P4 (MNHN.F.Ma14826) found in Mancy differs from that of O. bicuspidens in having a wider talonid, a lower and narrower hypoconid, and a lower and less individualized paraconid. The talonid of MNHN.F.Ma14826 is less sectorial than that of O. bicuspidens. The paracone on M 1 is larger in O. lindgreni than in O. bicuspidens. By comparison, all the features of the Mancy P4 and Cuis M1 can be regarded as plesiomorphic. The Mancy mandibles are slightly shallower than the mandible of O. bicuspidens; this is a plesiomorphic feature. Finally, O. bicuspidens is larger than the fossils from the MP10 localities. Despite the several differences between the fossils from MP10 and those of O. bicuspidens, they clearly share a common pattern characterized by hypercarnivorous adaptations (e.g. loss of entoconid and

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metaconid, reduced paracone). We see no reason for referring the MP10 material to a genus distinct from Oxyaenoides. The features that distinguish the former from the latter are plesiomorphic and only justify a specific distinction. We thus propose a new combination for the taxon because Francotherium appears to be a junior synonym of Oxyaenoides. Consequently, the hypercarnivorous hyaenodontidan Oxyaenoides was present in Europe during the Early Eocene. Oxyaenoides is clearly more specialized than the other proviverrines from the Early to earliest Middle Eocene (M7−MP13). Only Matthodon displays similar hypercarnivorous features (e.g. loss of metaconid), but differs in having enlarged premolars (see below). Finally, together with Matthodon menui, O. lindgreni represents the largest carnivorous mammal of MP10, with a mass of about 10 kg.

MATTHODON LANGE-BADRÉ & HAUBOLD, 1990 Emended diagnosis (reformulated from Lange-Badré & Haubold, 1990) This large proviverrine, which is slightly smaller than Prodissopsalis eocaenicus, is characterized by short, robust premolars bearing a large mesial cusp, which increases in size from P1 to P4, and a semicircular talonid, which bears thick folds of enamel, a singlerooted P1, very small (vestigial on M3) metaconid, protoconid as long as paraconid, mesially located paraconid, convex lingual face of protoconid separating paraconid and metaconid, very short and narrow talonid bearing poorly individualized cusps, talonid on M3 shorter than that of M2 and filled in by folds of enamel, lingually located hypoconid, M1 longer than P4, two-rooted P3, three-rooted P4, metacone taller than paracone, large stylar shelf and reduced protocone on molars; dental formula 2,1,4,3. Type species Matthodon tritens Lange-Badré & Haubold, 1990. Referred species Matthodon menui (Rich, 1971) comb. nov. Type locality MP11, Geiseltal (Germany). Distribution MP10, Chavot, Monthelon, Cuis, Mancy and Grauves (France); MP11, Geiseltal (Germany).

MATTHODON

(RICH, 1971) (FIGS 3–4, 13A–B)

MENUI

COMB. NOV.

Emended diagnosis (modified from Rich, 1971) Matthodon menui is smaller than Ma. tritens by 12%. It differs from Ma. tritens in retaining plesiomorphic


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Figure 3. Matthodon menui (Rich, 1971) comb. nov. A−C, MNHN.F.L-68-GR, left dentary with M1 and roots of P2 to P4 and M2. A, occlusal view; B, lingual view; C, labial view. D, E, MNHN.F.CHO14799, right dentary with canine, P2 to M2, and root of P1. D, labial view; E, lingual view; F, occlusal view. G−I, T.S. 374, right dentary with complete P2−P4, and M3, fragmentary M1 and M2, and root of P1. G, labial view; H, lingual view; I, occlusal view. Scale bar = 10 mm. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 171, 878–917

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Figure 4. Matthodon menui (Rich, 1971) comb. nov. A, B, TS 914, right maxillary with P3 and P4. A, labial view; B, occlusal view. C, D, MNHN.F.Ma14832, RP4. C, labial view; D, occlusal view. E, F, MNHN.F.L-58-Ma, RM2. E, labial view; F, occlusal view. Scale bar = 10 mm.

features such as narrower and less robust premolars, less developed paraconid on P2 and P3, metaconid on molars larger and more individualized, slightly longer talonid on molars, M3 longer than M2.

Table 2. Measurements (in mm) of the specimens of Matthodon menui (Rich, 1971) comb. nov.

Chresonymy 1971: Oxyaena menui in Rich, pp. 25–29, fig. 9; 1971: Oxyaenoidea or Hyaenodontoidea in Rich, pp. 30–33, fig. 11.

P3

Holotype MNHN.F.1939-586, left mandible with M3 and roots of M2 and distal root of M1.

C1

Referred specimens MNHN.F.Cui14838, LP4; MNHN.F.CHO14799, right mandible with canine, P2 to M2, and alveolus of P1; T.S. 914, right maxillary with P3 and P4; T.S. 374, right mandible with complete P2-P4, and M3, fragmentary M1 and M2, and alveolus of P1; MNHN.F.Ma 14832, RP4; MNHN.F.L-68-GR, left mandible with M1 and alveoli of P2 to P4 and M2; MNHN.F.L-58-Ma, RM2.

P2

Locus

P4 M2

P1

P3 P4 M1 M2

L W L W L W L W L W L W L W L W L W L W L W H

Type locality MP10, Cuis (France).

M3

Additional distribution MP10, Chavot, Monthelon, Mancy, and Grauves (France).

Weight = 11.9 kg†

Measurements See Table 2. Description The P3 is two-rooted and very robust. Its enamel is crenulated. The parastyle is very low and poorly

MD

N

OR

M

1 1 2 2 1 1 1 1 2 1 2 2 2 2 3 3 2 2 2 2 2 2 3

10.02 7.44 10.96–11.08 7.48–9.51 8.73 10.76 15.17 9.51 > 3.29*–> 5.84* > 3.99* 8.5–8.63 5.35–5.76 8.92–9.77 6.02–6.33 10.24–12.47 6.41–7.14 10.67–11.06 6.54–6.87 11.43–12.59 6.76–7.52 11.89–11.97 7.07–7.67 25.98–30.57

– – 11.02 8.5 – – – – > 4.57* – 8.57 5.56 9.35 6.18 11.3 6.79 10.87 6.71 12.01 7.14 11.93 7.37 28.64

*Estimated on the basis of the roots. †Weight estimated after Morlo (1999). M = mean; N, number of specimens; OR, observed range.

individualized, the paracone is wide, and the postmetacrista is short and low. The P4 is threerooted. The parastyle is as small as on P3, the paracone is robust, and the postmetacrista is longer and taller


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than on P3. The protocone, which is slightly shifted mesially, is individualized and elongated transversally. A small cingulum is present labially. The parastyle is large on MNHN.F.L-58-Ma. A notch is present between the paracone and parastyle. The postmetacrista is longer than the preparacrista, but it is aligned transversally. The paracone and metacone are partially fused. The metacone is taller than the paracone. The protocone, which is short and narrow, is slightly shifted mesially. The parastyle, paraconule, and protocone are aligned. No metaconule is visible. The ectoflexus is pronounced, and the stylar shelf is wide. We think that MNHN.F.L-58-MA is an M2 because of the presence of a strong parastyle. What is known of the mandible shows that it is very deep, wide, and robust, and that it was apparently short. The depth of the mandible is constant. The symphysis is high and extends under the P3. Mental foramina are present below P2 and the anterior root of P4. The premolars are very close together. The P1 is unknown, but based on MNHN.F.CHO14799, this tooth is single-rooted. The three other premolars are tworooted. The P2 is shorter and smaller than P3 and P4. The mesial part of the tooth is wide, but there is no individualized paraconid. The protoconid is asymmetric in lateral view. The talonid is shallow and bears no individualized cusp. However, the distal part of the tooth is distally elongated and is only slightly narrower than the mesial part. The P3 is less asymmetric than the P2. The mesial part is more developed than on P2, but no real paraconid is visible. The protoconid is robust. The talonid is short. The lingual part of the talonid is broken, but is larger than the mesial part. A very small cusp (hypoconid?) is present labially. The P4 is more symmetrical than the P2 and P3. The protoconid is high and pointed. It is developed but the paraconid is small, low, and poorly individualized. The talonid is wide. A large and high hypoconid is present labially. An entoconid is present lingually. A lingual wear facet is visible on the entoconid. Thanks to the several specimens housed in European museums, the three molars of the taxon are known. The M 1 is only slightly shorter than the M2. The M3 is almost the same size as the M2. The trigonid of the M1 is worn, as usually observed in hyaenodontidans. The metaconid and paraconid are fully separated. The paraconid is taller than the metaconid. The latter is very reduced. The paraconid is projected mesially, and the paracristid is more elongated mesiodistally than transversally. The metaconid is more distal than the protoconid. The protoconid is distinctly taller than the paraconid. The talonid is short but as wide as the trigonid. The postfossid is narrow (the hypoconid is weakly located labially), deep, and closed both labially and lingually. The different cusps are weakly individualized. The distal part of the talonid

is taller than the lingual part. The hypoconid is strongly truncated by wear facet 3. Only a short precingulid is present. The less worn M2 trigonid still presents distinct and pronounced wear facets 1 and 2. The metaconid is taller than on M1, but remains small. The paraconid is sectorial and projected mesially. The M2 talonid is shorter than on M1, but similar in morphology: the postfossid is narrow and closed, the talonid is wide, and the cusps are not individualized. The wear facet 3 is large. The M3 is known thanks to the holotype (MNHN.F.1939-586) and a referred specimen from Monthelon (T.S. 374). The paracristid is more sectorial than on M2. The wear facets are similar. The metaconid is more reduced than on M2. The talonid is more reduced (length and width) than on M2. The talonid cusps are not separated.

Discussion Rich (1971) described MNHN.F.1939-586 as an Oxyaenidae because he considered that only two molars were present. He referred it to a new species of the genus Oxyaena, as Oxyaena menui, founded on the peculiar morphology of its M2. In the same study, Rich (1971) also referred MNHN.F.L-68-Gr to either an Oxyaenoidea or a Hyaenodontoidea. Gunnell & Gingerich (1991) established the similarity of these two specimens and proposed to refer them to the hyaenodontine Propterodon. This genus is only known from the ?Middle Eocene of northern China. It is similar to Matthodon in several features, such as the reduction of the metaconid, but differs in having less robust premolars and less developed paraconid and entoconid on the premolars. Thus, the similarities shared by the two genera (e.g. absence of a metaconid) probably result from adaptations to the consumption of vertebrate flesh. Few proviverrines from the Early Eocene and earliest Middle Eocene display molars characterized by reduced metaconids and entoconids. This condition is present in Oxyaenoides and Matthodon from Geiseltal (Middle Eocene, MP11) and the ‘Francotherium’ – here synonymized with Oxyaenoides (see above) – from the Paris Basin (Early Eocene, MP10). Matthodon differs from Oxyaenoides in having premolars that are robust and tightly packed and molars on which the postfossid is closed lingually by the entocristid. The material collected from Cuis, Chavot, Monthelon, Mancy, and Grauves (MP10) is clearly reminiscent of that of Ma. tritens (Middle Eocene). Matthodon menui shares with Ma. tritens the presence of a compressed lower dentition (no diastema between the premolars), a large canine, a single-rooted P1, wide premolars, and a reduced metaconid and talonid on molars. Moreover, the mental foramina in both Matthodon species are more distal than in other proviverrines: they are below the anterior root of P2 and anterior root of P4. Finally, the


EVOLUTION OF THE PROVIVERRINAE dentary symphysis of the MP10 specimens extends to the level of the P3, as in Ma. tritens. Matthodon menui possesses the typically robust premolars of the genus Matthodon, although they are less robust and narrower than in Ma. tritens. In the lower molars, the metaconid is less reduced than in Ma. tritens. Matthodon menui therefore represents a new species that is close to, but less specialized than Ma. tritens. Matthodon tritens is only known from its lower dentition (Lange-Badré & Haubold, 1990). A maxillary fragment with roots of I2 to P3 from Geiseltal has been referred to cf. Matthodon sp. by Lange-Badré & Haubold (1990); the upper dentition of Matthodon has thus remained poorly known. Nevertheless, amongst the material that we examined during the course of this study, we were able to refer one P 3 , two P 4 (T.S. 914, MNHN.F.Ma14832), and one M2 (MNHN.F.L-58-Ma) to Ma. menui, as they fit in size and morphology with the P3, P4, and M2 that are available for this species. As indicated above, Matthodon displays features that are also known in the hypercarnivorous genus Oxyaenoides: a reduced metaconid and cusps and a mesially projecting paraconid. These apomorphic features are adaptations towards a sectorial dentition. Interestingly, the postfossid of Matthodon is closed lingually by the entocristid, a plesiomorphic feature compared with what is seen in Oxyaenoides. Moreover, Matthodon also differs from Oxyaenoides by the posterior location of the mental foramina, the tightly packed, wider, and more robust premolars, the single root of the P1, and a postmetacrista on M2 that is less distally shifted. To us, the numerous differences between Matthodon and the hypercarnivorous Oxyaenoides

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suggest a possible convergence in hypercarnivorous specialization. The enlargement of the premolars in Matthodon indicates that it probably had a durophagous diet. This feature is combined with a specialization of the molars (e.g. strong reduction of the metaconid). As a result, the dentition of Matthodon species reminds one of that of extant scavengers such as the striped hyena. The discovery of Ma. menui is crucial because it supports a close relationship between the Early Eocene MP10 of the Paris Basin and the Middle Eocene MP11 of Geiseltal where Ma. tritens was found. It is now clear that there was a continuity between Early and Middle Eocene proviverrine faunas.

PROTOPROVIVERRA LEMOINE, 1891 Diagnosis Same as for the type and only species. Type species Proviverra palaeonictides Lemoine, 1880. Type locality MP10, Épernay area, ‘Agéien’ (France).

PROTOPROVIVERRA

PALAEONICTIDES

(LEMOINE, 1880)

(FIG. 5) Emended diagnosis This small proviverrine is characterized by a P4 bearing an individualized paraconid and two distinct cusps on the talonid, an open trigonid on the M1, which has a

Figure 5. Protoproviverra palaeonictides (Lemoine, 1880). A−C, MNHN.F.Al5155 (holotype), right dentary with P4 and M1, posterior alveolus of P2, and alveolus of M1. A, labial view; B, occlusal view; C, lingual view. Scale bar = 10 mm. © 2014 The Linnean Society of London, Zoological Journal of the Linnean Society, 2014, 171, 878–917

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mesially located paraconid that is lower than the metaconid, and three distinct cusps on the talonid. Chresonymy 1880: Proviverra palaeonictides in Lemoine, p. 587; 1881: Provivera pralaeonictides [sic] in Lemoine & Aumonier, p. 613; 1891, Protoproviverra pomelii in Lemoine, p. 265, pl. X, fig. 10; 1891: Protoproviverra palaeonictides in Lemoine, p. 272, pl. X, fig. 10; 1921: Proviverra pomeli in Teilhard, p. 50; 1965: Prototomus palaeonictides in Van Valen, p. 639. Synonymy Protoviverra pomelii Lemoine, 1891 (objective junior synonym). Holotype MNHN.F.Al5155, right mandible bearing P4 and M1, posterior alveolus of P3, alveoli of M2, and isolated P2. Type locality MP10, ‘Agéien’ (France). Measurements See Table 3. Description The mandible of MNHN.F.AL5155 is deep, but not very robust. The posterior part is only slightly taller than the anterior part. The mandible was probably narrower anteriorly than posteriorly. A mental foramen is present under the posterior root of P3. Ventrally, there is a mental canal. Morlo & Habersetzer (1999: fig. 15d) considered the isolated premolar housed with the fragmentary mandible MNHN.F.AL5155, as a P1. Its height and its pointed apex are more reminiscent of P2 than P1 – the P1 is usually lower and more mesiodistally elongated than the P2. The tooth is high and sharply pointed thanks to the protoconid. There is no paraconid. A short but wide talonid is present. It is worn, so no cusp is visible. The P4, which is present on the mandible, is elongated mesiodistally. A paraconid is present. It is Table 3. Measurements (in mm) of MNHN.F.Al5155, holotype of Protoproviverra palaeonictides (Lemoine, 1880) Locus P4 M1 MD

L W L W H

N

OR

1 1 1 1 11.1

5.29 2.71 5.13 3.10

N, number of specimens; OR, observed range.

individualized, low, and elongated mesially. The protoconid is triangular and pointed in lateral view. The talonid is slightly narrower than the protoconid. The postfossid is deep. A high hypoconid is present labially. The hypoconulid, which is located distally, is lower than the hypoconid and not projected distally. A very low entoconid can be seen lingually. A short notch separates the entoconid from the hypoconulid. On the M1, there is a very low paraconid that projects slightly mesially. The protoconid is low. The metaconid is taller and longer than the paraconid but is only slightly lower than the protoconid. The metaconid has a strong base; it is elongated mesiodistally. Its apex is projected lingually. It is slightly more distal than the protoconid. The trigonid is robust except for the paraconid. The talonid is slightly narrower than the trigonid. The cristid obliqua is not very oblique (distally shifted labially). The postfossid is narrow and distinctly shorter than the trigonid. The three cusps are located distally. They are high and the postfossid is deep. The hypoconulid is slightly more distal, but is not well projected distally. The hypoconid is equidistant from the hypoconulid and entoconid. The hypoconid is as high as the entoconid; the hypoconulid is lower because of its wear. The cristid obliqua and entocristid are slightly oblique. The precingulid, which is located mesially, is short. This is the sole labial cingulid present on M1. The alveoli of M2 are visible on MNHN.F.AL5155; they indicate that this tooth is distinctly larger than the M1. Discussion The ‘agéienne’ fauna was defined and described by Lemoine (1891). This fauna was distinguished from the older and more primitive Cernaysian fauna. The original ‘agéienne’ mammal fauna was collected in the area of Ay, between Reims and Epernay. However, the exact locality of the samples is unknown. Lemoine probably collected fossils in similar facies, but not of identical age (Laurain et al., 1983; Escarguel, 1999). The majority of the taxa resemble the Cuisian mammals of the ‘Falun à Unios et Térédines’ of Avenay, whereas the remaining ones are more similar to those of the ‘Sables à Unios et Térédines’ sensu stricto. The fragmentary mandible MNHN.F.AL5155 has been assigned to the MP10 reference level (Morlo & Habersetzer, 1999). The species Protoproviverra palaeonictides was originally referred to Proviverra by Lemoine in 1880, before he moved it to a new genus, Protoproviverra, in 1891. The validity of this genus was questioned by Teilhard (1921), who synonymized Protoproviverra with Proviverra. After he examined the holotype, Van Valen (1965) transferred Protoproviverra palaeonictides to Prototomus. However, it clearly differs from the other species of the genus Prototomus because its holotype


EVOLUTION OF THE PROVIVERRINAE MNHN.F.AL5155 has a large paraconid and entoconid on its P4 and a wide talonid bearing an entoconid on its M1. These features strongly support its referral to the Proviverrinae. The M1 of MNHN.F.AL5155 differs from that of Proviverra by a combination of plesiomorphic (less developed cingulids) and apomorphic (more opened prefossid, mesially located paraconid) features. The same combination also distinguishes Protoproviverra palaeonictides from Lesmesodon, Allopterodon, and Leonhardtina. The mesial position of the paraconid and metaconid, which results in an open prefossid, the wide and basined talonid, and the deep mandible are similar to the earliest Middle Eocene genera Cynohyaenodon, which is unusual amongst small proviverrines in having a sectorial dentition (Lange-Badré, 1979), and Eurotherium. The oldest species of Eurotherium is Eurotherium matthesi, which is recorded in MP11 of Geiseltal (Lange-Badré & Haubold, 1990). The P 4 of Protoproviverra palaeonictides and Eu. matthesi are similar in bearing an individualized paraconid and two talonid cusps. However, the M1 of Protoproviverra palaeonictides importantly differs from that of Eu. matthesi in having a separated hypoconulid and entoconid – the closeness of the entoconid and hypoconulid is characteristic of Eurotherium (Lange-Badré & Haubold, 1990). The genus Cynohyaenodon is known by two species from the Middle Eocene: Cynohyaenodon trux (MP12−14) and Cynohyaenodon ruetimeyeri (MP13−14) – the latter being the larger and more specialized (Lange-Badré & Haubold, 1990) – and in the Late Eocene also by two species: Cynohyaenodon cailuxy (MP16−17a) and Cynohyaenodon lautricensis (MP16). The MP10 material is intermediate in size between the two Middle Eocene Cynohyaenodon species. The P4 is especially interesting because it enables the distinction of the two Geiseltal species. The P4 of MNHN.F.AL5155 is more robust and is taller than in Cy. trux, but also narrower than in Cy. ruetimeyeri. Its M1 is also less sectorial than in Cy. ruetimeyeri: the paraconid is less mesially located and the metaconid is more developed. These two features are significant because the mesial projection of the paraconid and the reduction of the metaconid increased during the evolution of the genus Cynohyaenodon (Lange-Badré, 1979). To summarize, ‘Proviverra palaeonictides’ represents a valid species of Protoproviverra that is morphologically close to Eurotherium and Cynohyaenodon. These relationships have been confirmed by our phylogenetic study (Fig. 9B). Amongst species of Cynohyaenodon, Protoproviverra palaeonictides is closer to Cy. ruetimeyeri than to Cy. trux. Moreover, Protoproviverra exemplifies the diversity of the ecological niches occupied by proviverrines during the MP10.

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LEONHARDTINA MATTHES, 1952 Emended diagnosis (modified from Lange-Badré & Haubold, 1990) This proviverrine genus is characterized by low premolars without cingulids, P3 longer than P4, presence of two cusps on the talonid of P3 and P4, molars with a closed prefossid, equally developed paraconid and metaconid except on M3 where the metaconid is lower, protoconid narrow and slightly elevated, talonid short and wide with a long hypoconulid, which is equidistant from the entoconid and the hypoconid – the latter being the highest cusp –, P3 large, P4 as long as wide, with large and isolated parastyle, large and sharply pointed protocone on molars, paracone as long as the metacone but taller, paracone and metacone completely separated, long parastyle, small metacone, and parastyle as long as the protocone area on M3. Type species Leonhardtina gracilis Matthes, 1952. Referred species Leonhardtina godinoti sp. nov. Type locality MP12−13, Geiseltal (Germany). Distribution MP10, Grauves (France); MP12−13, Geiseltal (Germany).

LEONHARDTINA

GODINOTI SP. NOV.

(FIG. 6)

Diagnosis Leonhardtina godinoti differs from Leonhardtina gracilis in its smaller size (15–20% smaller) and a taller P3, less mesially projected paraconid, and longer talonid on M3. Chresonymy 1971: Prototomus cf. Protoproviverra palaeonictides in Rich, pp. 11–15. Etymology Dedicated to Prof. Marc Godinot, who has greatly contributed to the knowledge of Early Eocene European mammals. Holotype MNHN.F.L-195-Gr, right mandible with P3, talonid of M1, and M2−M3, and alveoli of C, P1−P2, and roots of P4. Type locality MP10, Grauves (France). Measurements See Table 4. Description MNHN.F.L-195-Gr is a right mandible, which bears P3, M2, and M3. The mandible is very shallow. Its ventral


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Figure 6. Leonhardtina godinoti sp. nov. A−C, MNHN.F.L-195-Gr (holotype), right dentary bearing P3, talonids of M1, M2−M3, roots of C1−P2, P4, and mesial root of M1. A, labial view; B, lingual view; C, occlusal view. Scale bar = 10 mm.

margin is bowed ventrally. The symphysis extends below the mesial root of P2. Two mental foramina are present, one between P 1 and P 2 , the other below P 3 . The masseteric fossa and angular process are rather low. The mental canal is visible ventrally on the anterior part of the specimen; it is more dorsally located on the distal part. The coronoid crest is broken; however, its mesial part indicates that the structure was probably close to the vertical, as seen in L. gracilis. The premolars are close to each other; there is only a tiny diastema between the P2 and P3. All premolars are two-rooted. The P2 is larger than the P1 and was probably high, as in L. gracilis. The P3 ends with a pointed apex. At its base, there is a tiny but distinct paraconid. A short talonid with two

cusps (hypoconulid and entoconid) is also present. The P3 is longer than the P4. The M1 is broken on MNHN.F.L-195-Gr but the M1 and M2 appear morphologically similar even though the former is smaller than the latter. The morphology of M2 is characterized by a sharply pointed and mesiodistally compressed trigonid. The metaconid is located slightly mesially relative to the protoconid. The paraconid is slightly smaller than the metaconid. The paracristid is long but is aligned transversally. The trigonid is a bit longer and wider than the talonid. The postfossid is very wide and deep. It is surrounded by three individualized cusps, of which the hypoconid is the highest. The hypoconulid is slightly projected distally. The cristid obliqua is oblique (labially shifted


EVOLUTION OF THE PROVIVERRINAE Table 4. Measurements (in mm) of MNHN.F.L-195-Gr, holotype of Leonhardtina godinoti sp. nov. Locus P1 P2 P3 P4 M1 M2 M3 MD

L W L W L W L W L W L W L W H

N

OR

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

> 3.54* > 1.23* > 4.72* > 2.22* 5.69 2.12 > 5.46* > 2.38* 5.13 3.13 5.89 3.50 5.96 3.49 8.84

Weight = 990 g† *Estimated on the basis of the roots. †Weight estimated after Morlo (1999). N, number of specimens; OR, observed range.

distally). The talonid of the M3 is more elongated mesiodistally than on previous molars. The hypoconulid is projected distally. The entoconid is individualized. The postfossid is not narrow. The precingulid is distinct. Discussion The holotype of Leonhardtina godinoti, MNHN.F.L195-Gr, was previously referred by Rich (1971) to Prototomus cf. palaeonictides, but the re-evaluation of the latter species shows that it actually belongs to the genus Protoproviverra – which is close to Cynohyaenodon and Eurotherium (see above). Leonhardtina godinoti displays several plesiomorphic features amongst the Hyaenodontida, such as a shallow mandible, a distinct entoconid on the molars, a weak mesial projection of the paraconid, and a slightly reduced metaconid. Nevertheless, the holotype also displays apomorphic features, amongst which are closely placed premolars, a symmetric P3 in lateral view, a developed paraconid on P3, an entoconid on P3, a P3 longer than P4, and a wide talonid on the lower molars. Some of these features (e.g. P3 paraconid developed, wide talonid on molars) are shared with the small Middle Eocene proviverrines Cynohyaenodon, Lesmesodon, Proviverra, Allopterodon, and Leonhardtina. MNHN.F.L-195-Gr differs from Cynohyaenodon in its mesiodistally compressed and sharply pointed trigonid on M2. This latter morphology is found in the other small Middle Eocene proviverrines. Moreover, MNHN.F.L-195-Gr displays a

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P 3 that is longer than P 4 , as also observed in Leonhardtina, Proviverra, and Allopterodon. In contrast, it differs from the latter two genera and from Lesmesodon in having less developed cingulids on the premolars and molars and a narrower talonid on P3. The morphology of MNHN.F.L-195-Gr therefore lacks the apomorphic characters of Proviverra and Allopterodon. The M1 of MNHN.F.L-195-Gr is larger than those of Proviverra typica and Allopterodon torvidus, close in size to those of Lesmesodon edingeri and Allopterodon bulbosus, and smaller than those of Lesmesodon behnkeae and Allopterodon minor. Finally, the morphology of the fossils from Grauves is very similar to that of Leonhardtina gracilis from Geiseltal (MP12−13). They share the presence of a closed prefossid on molars and the lack of cingulids on premolars and molars. A P3 that is longer than the P4 is also notable. The premolars and molars of MNHN.F.L-195-Gr are smaller than those of Leo. gracilis (15–20% smaller); MNHN.F.L-195-Gr is distinguished by a P3 that is taller than long, a less mesially projected paraconid, and a longer talonid on M3. All these features are plesiomorphic amongst Proviverrinae. The fossil from Grauves appears similar to that of the Middle Eocene Leo. gracilis, but represents a distinct species that lacks some of the apomorphic features of the latter. We propose naming this new species Leonhardtina godinoti sp. nov. This discovery provides evidence for the presence of the genus Leonhardtina in MP10 of the Paris Basin, which significantly increases its stratigraphical range. This genus was previously restricted to the Middle Eocene of Geiseltal (MP12−13). Our study thus allows us to root this genus in the Early Eocene of Europe.

BORITIA

GEN. NOV.

Diagnosis Same as for the genus and only species. Etymology From ‘La Borie’ (type locality) and ‘-itia’ (Latin) = pertaining to. Type species Boritia duffaudi sp. nov. Type locality MP8 + 9, La Borie (France).

BORITIA

DUFFAUDI SP. NOV.

(FIG. 7)

Diagnosis The proviverrine genus Boritia is characterized by the presence of mental foramina located below the P1 and P3, a reduced P1, premolars with a wide talonid and a paraconid developed on P4, a poorly sectorial trigonid (paraconid poorly projected mesially, metaconid aligned


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Figure 7. Boritia duffaudi gen. et sp. nov. A−D, MHNT.PAL.2010.19.1 (holotype), right dentary bearing P3, P4, M1, M2, and M3 and alveoli of C1−P2. A, labial view; B, lingual view; C, occlusal view; D, occlusal close-up view. Scale bars = 10 mm.

transversally with the protoconid), and a short and narrow talonid on the molars. Boritia differs from the contemporaneous Morlodon by having a less reduced P1, more separated premolars, less robust premolars, less oblique cristid obliqua, and longer talonid on the molars. Etymology Dedicated to Dr Sylvain Duffaud, who discovered the holotype.

Holotype MHNT.PAL.2010.19.1, right dentary bearing P3, P4, M1, M2, and M3 and alveoli of C1−P2. Type locality MP8 + 9, La Borie (France). Measurements See Table 5.


EVOLUTION OF THE PROVIVERRINAE Table 5. Measurements (in mm) of MHNT.PAL.2010.19.1, holotype of Boritia duffaudi gen. et sp. nov. Locus P1 P2 P3 P4 M1 M2 M3 MD

L W L W L W L W L W L W L W H

N

OR

1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

> 4.75* > 3.02* ? > 3.07* 6.27 2.59 7.27 3.11 6.94 3.94 7.79 5.04 7.58 4.32 13.53

Weight = 2.58 kg† *Estimated on the basis of the roots. †Weight estimated after Morlo (1999) N, number of specimens; OR, observed range.

Description Two large foramina are present below the distal roots of P1 and P3, respectively. Very small foramina are also present below the mesial root of P2, and below the distal root of P2. The ventral margin of the dentary is slightly slanted posteriorly, which results in a posterior deepening of the mandible along the tooth row. The symphysis is shallow and extends below the distal root of P2. The beginning of the coronoid crest is vertical. The dorsal part of the coronoid crest is more oblique. The condyle is robust, but has a weak transverse extension. Although the P1, P2, and P3 are separated by diastemata, there are none between the P3 and the P4. The premolars increase in size anteroposteriorly. According to the alveoli, the P1 and the P2 are tworooted, but the first differs in the partial fusion of the roots. There are also two roots for the P3 and the P4. The P2 seems longer than the P3, but its length is probably overestimated because of the reconstruction. The P 3 is lower crowned than the P 4 . It is elongated mesiodistally and is slightly asymmetrical in lateral view. A slightly developed and high paraconid is present, although weakly individualized. The talonid is elongated distally, and larger than the protoconid. The little cusp that is present lingually may represent the entoconid. The P4 differs from the P3 in having a less asymmetrical morphology, a taller talonid, and a paraconid that is lower but more elongated mesially and individualized. The lingual cusp (entoconid) is present and is more developed than on P3. The talonid

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is wider than the protoconid. The talonid crest is labially located as on P3. The two cusps that are on the labial crest of the talonid are either the hypoconid and the protostylid or the hypoconid and the hypoconulid. The M2 is the largest molar, M1 the smallest one. The M3 represents the lower carnassial tooth (= most sectorial tooth) as usually observed in specialized Hyaenodontida. In all molars, the protoconid is distinctly sharper and taller than the other cusps of the trigonid. The paraconid is a bit smaller than the metaconid. It is slightly projected mesially. Moreover, the paracristid is elongated. The metaconid is located mesially (aligned with the protoconid). From M1 to M3 the metaconid becomes more reduced, is shifted more distally, and the paracristid becomes narrower transversally. The distal segment of the paracristid is aligned mesiodistally, whereas the protocristid crest is transverse. The base of the paraconid expands slightly lingually, but is less developed than the base of the metaconid. Although the contact between the metaconid and paraconid is large at the base, their apices are divergent. The metaconid is also slightly fused to the protoconid. Its apex is straight instead of being projected lingually as in Eoproviverra. In all molars, the talonid is shorter and only slightly narrower than the trigonid. The postfossid is closed lingually by the entocristid. On M1 and M2, the hypoconid, hypoconulid, and entoconid are clearly separated by notches, even if their apices are poorly developed. The hypoconid is slightly taller than the entoconid and hypoconulid. The entoconid is reduced and fuses partially with the hypoconulid. The entocristid forms a sectorial crest. The cristid obliqua is slightly oblique (distally shifted labially). The hypoconulid is narrow and projected distally. The M3 differs in having a narrower, shorter talonid and postfossid, and a lower talonid. The apices of the hypoconulid and hypoconid are worn, but they were probably poorly developed. The entoconid has no real apex. The entocristid and cristid obliqua are nearly aligned mesiodistally and are only slightly oblique, as on M1 and M2. Shallow notches separate the three cusps. The molars exhibit only the precingulids, which are short and vertical. The hypoflexid is deep, but not very pronounced on M1 and M2. Discussion MHNT.PAL.2010.19.1 is one of the best-preserved hyaenodontidan mandibles from the Early Eocene of Europe. The coronoid crest of the earliest members of this group is poorly known. We therefore compared this structure with that of the better-known hyaenodontidan from the Geiseltal Formation (Lange-Badré & Haubold, 1990). The coronoid crest is more vertical in Boritia than in the genera Oxyaenoides and Matthodon. The condyle is robust and bulbous, but with a weak transverse expansion as in the oldest hyaenodontidans. Jaw


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movement in Boritia thus appears to have been less restricted transversally than in the Middle Eocene Oxyaenoides and Matthodon. The presence of an entoconid on the molars, a tworooted P1, and an entoconid on P4 allows us to refer MHNT.PAL.2010.19.1 to the Proviverrinae as recently redefined by Solé (2013). The earliest proviverrines and the sister taxa of all other proviverrines are from southern France: Eoproviverra eisenmanni (Rians, MP7) and Parvagula palulae (Palette, MP7). Boritia shares several plesiomorphic features with Pa. palulae and Eo. eisenmanni, such as an oblique talonid (which is distally shifted labially) and diastemata between P1, P2, and P3. Pa. palulae and Eo. eisenmanni retained plesiomorphic proviverrine characters such as small size, and an M1 and M2 with narrower talonids bearing well-developed entoconids. MHNT.PAL.2010.19.1 has a less specialized trigonid than Eo. eisenmanni: the paraconid is less projected mesially and the metaconid is more mesially located. However, the smaller lingual projection of the apex of the metaconid of Boritia compared with Eo. eisenmanni is an apomorphic feature. In contrast to the trigonid, the talonids of the molars on MHNT.PAL.2010.19.1 differ from those of Eo. eisenmanni in their more derived morphology: talonid shorter and wider, and entoconid less bulbous and individualized (more crestiform and less pronounced apex). MHNT.PAL.2010.19.1 is more plesiomorphic than Pa. palulae in the narrowing of the anterior part of the mandible. The resemblance of MHNT.PAL.2010.19.1 to European hypercarnivorous proviverrine Oxyaenoides also necessitates a few comments. The premolars of Boritia are similar in the following traits: (1) mesiodistally elongated occlusal outline; (2) P3 and P4 that are symmetrical in lateral view; (3) P 3 and P 4 with a small paraconid; (4) P3 distinctly lower than the P4; (5) P4 with a high, distally elongated talonid, a labially located hypoconid, and an entoconid. This morphology corresponds to a mosaic of characters that are either plesiomorphic (4, 5) or apomorphic (1, 2, 3) amongst the Proviverrinae. The P 3 and P 4 of MHNT.PAL.2010.19.1 nevertheless differ from those of Oxyaenoides in the stronger development of the paraconid and talonid (which underlines the proviverrine trend towards a more robust dentition), a more developed paraconid, and a wider talonid. The lower molars of Boritia also differ from Oxyaenoides in retaining the plesiomorphic configuration of the postfossid, which is closed lingually by the entocristid. In Oxyaenoides, the postfossid is fully opened lingually, which is a common characteristic of hypercarnivorous hyaenodontidans. MHNT.PAL.2010.19.1 also differs from Oxyaenoides in displaying a larger metaconid and a shorter paracristid

(plesiomorphic features). Thus, the less sectorial, plesiomorphic lower molars and the robust, derived premolars are distinctive features of MHNT.PAL.2010.19.1 with respect to Oxyaenoides. The morphology of MHNT.PAL.2010.19.1 is similar to that of the recently described Morlodon vellerei (Avenay, Condé-en-Brie, MP8 + 9; Solé, 2013). In particular, they share apomorphic features related to the acquisition of a robust dentition such as the reduced P1, the wide premolar talonid, the developed paraconid on P3 and P4, and the reduction of the entoconid. By contrast, they also share plesiomorphic features that allow us to distinguish them from the older Eo. eisenmanni and Pa. palulae. The peculiar shape of the dentary is also unique to MHNT.PAL.2010.19.1 and Mo. vellerei in becoming anteriorly shallow, in contrast to what can be seen in the two species of Oxyaenoides. MHNT.PAL.2010.19.1 differs from Mo. vellerei in retaining numerous plesiomorphic features: clearly tworooted P1, narrower and less tightly packed premolars, less developed paraconid on P4, narrower postfossid, and longer and more oblique talonid. It thus appears that MHNT.PAL.2010.19.1 and Mo. vellerei represent two distinct species. We propose to refer MHNT.PAL.2010.19.1 to Boritia duffaudi sp. nov. The fossil locality of ‘La Borie’ has revealed a unique fauna from the Early Eocene of southern France (Laurent et al., 2010). Based on the presence of the mammals Lophiaspis, Dissacus, Plesiesthonyx, and of the groundbird Diatryma, an age close to the MP 8 + 9 reference level has been proposed. This age has been confirmed by the study of the Pachynolophus sp. from La Borie (Danilo et al., 2013). It is important to note that this is the first mammal locality known from southern France for this period. Indeed, the other French localities are located in the Paris Basin (e.g. Mutigny, Avenay).

MINIMOVELLENTODON

GEN. NOV.

Diagnosis Same as for the type and only species. Etymology ‘Minimus’ (Latin) = small, ‘velle¯ns’ (Latin) = scraping, ‘odon’ = tooth (Greek). Type species Minimovellentodon russelli sp. nov. Type locality MP8 + 9, Mutigny (France).

MINIMOVELLENTODON

RUSSELLI SP. NOV.

(FIG. 8)

Diagnosis Minimovellentodon differs from Eoproviverra and Parvagula in its larger size, deeper mandible, a



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Figure 8. Minimovellentodon russelli gen. et sp. nov. A−C, MHNL 20269998 (holotype), right dentary with P3−M3 roots of P2. A, occlusal view; B, labial view; C, lingual view. Scale bar = 10 mm.

metaconid that is lower than the paraconid (apomorphic feature), and in some primitive features such as a paraconid that is less projected mesially or the transverse alignment of the metaconid with the protoconid. It differs from Morlodon and Boritia in its smaller size, longer and narrower talonid, and larger metaconid on molars. Etymology Dedicated to Dr Donald Russell who has greatly contributed to our knowledge of Palaeocene and Eocene mammals. Holotype MHNL 20269998, right mandible bearing P3−M3, and roots of P2.

Type locality MP8 + 9, Mutigny (France). Measurements See Table 6. Description Two mental foramina are present: between P1 and P2, and below P3. The P1, P2, and P3 are separated by diastemata. The anterior margin of the coronoid crest rises at an angle close to 70°. The mandible is deep under the molars but narrows anteriorly. The preserved teeth are all worn. The premolars are all transversally compressed (mesiodistally elongated). The P2 is two-rooted and shorter than the P3. There is a small, low, and short paraconid on P3. The P4 is


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Table 6. Measurements (in mm) of MHNL 20269998, holotype of Minimovellentodon russelli gen. et sp. nov. Locus P2 P3 P4 M1 M2 M3 MD

L W L W L W L W L W L W H

N

OR

1 1 1 1 1 1 1 1 1 1 2 1 1

> 4.21* > 1.64* 4.52 1.70 5.48 2.27 5.81 3.02 5.90 3.62 6.16 3.15 12.57

Weight = 1.18 kg† *Estimated on the basis of the roots. †Weight estimated after Morlo (1999). N, number of specimens; OR, observed range.

the longest premolar. It bears a paraconid, which is more developed than in the P3 but nevertheless remains low. The tooth is almost as long as the M1. The M1 is noticeably shorter than the M2 and M3. Their morphology is similar. The trigonid is compressed mesiodistally. The paracristid is short, and the paraconid is shifted mesially. The metaconid is aligned transversally with the protoconid. There is a wide contact between the paraconid and the metaconid. The protoconid is high and pointed. The talonid is oblique (distally shifted labially) and is elongated mesiodistally so that it appears narrower than the trigonid. The postfossid is narrow. The developed entoconid area indicates that this cusp was not crestiform as observed in sinopines, but was more cuspidate. The entocristid and cristid obliqua are oblique as the postfossid. The hypoconulid is projected distally. Only a short precingulid can be observed. The M3 differs in its a narrower talonid. The talonid is more elongated mesiodistally than on M1 and M2. Its paracristid is also longer and the paraconid is more mesially located. Discussion The mandible MHNL 20269998 displays features that are reminiscent of the oldest hyaenodontidans, such as the presence of three molars – the M3 being the largest, the second foramen located below P3, the deep mandible, the large paraconid on P4 and especially on the molars, and the presence of an important wear facet 2 on the molars – this latter feature indicates that the shearing function of the dentition was prominent. These

features clearly allow referral of MHNL 20269998 to hyaenodontidans. The position of the mental foramina, the close P3 and P4, the less asymmetrical premolars, the more developed paraconid on P4, and the shorter talonid on the molars of Minimovellentodon show that it differs significantly from the Palaeocene Tinerhodon, but agrees well with Eoproviverra and Parvagula. Minimovellentodon russelli has a plesiomorphic trigonid compared to Eoproviverra eisenmanni: the paraconid is not projected mesially and the metaconid is not distally located as in the latter species. The morphology of the trigonid of Minimovellentodon is close to that of Tinerhodon; it is clearly less sectorial than that of Eo. eisenmanni. The talonid of MHNL 20269998 is worn, but was apparently narrow and shorter than the trigonid. This plesiomorphic morphology was also retained by Eoproviverra. By contrast, Mi. russelli differs from Parvagula and Prototomus minimus (Dormaal) in its deeper mandible. Finally, the strong development of the paraconid on P 3 and P 4 also distinguishes Mi. russelli from the Dormaal Prototomus spp., Eoproviverra, and Parvagula. The distinctive morphology of Mi. russelli, which is a combination of plesiomorphic and apomorphic features when compared with Eoproviverra and Parvagula, justifies the erection of a new genus and species for the taxon of Mutigny. In conclusion, it is worth remembering that Minimovellentodon, Eoproviverra, and Parvagula have several apomorphic characters in common. However, the presence of a mesially located metaconid and weakly projected paraconid, as in the plesiomorphic Tinerhodon, indicates that Minimovellentodon is not directly related to Eoproviverra. Besides, in spite of its greater age, Eo. eisenmanni has a more sectorial dentition than Minimovellentodon. By contrast, the increase in the depth of the mandible of MHNL 20269998 suggests that Minimovellentodon is more closely related to Morlodon. Both these species have a deep mandible [(mandibular depth/M1 length) > 2; see Table 7]. Nevertheless, Minimovellentodon differs from Morlodon in having narrower premolars, a distinctly less mesially located paraconid (which results in a closed prefossid) on the molars, a narrower talonid and a more developed entoconid on the molars, and a longer talonid, notably on M3. All these features are plesiomorphic amongst Hyaenodontida and support the generic distinction. The proviverrine Minimovellentodon from Mutigny represents the oldest record of this subfamily in the Northern Province [sensu Marandat, (1997)]. It implies that the Proviverrinae were present in the Paris Basin since biozone PE IV of Hooker (1998) (Fig. 11; Table 8).



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Table 7. Comparison of the mandibular depth (MD) divided by the M1 length (M1 L) in several hyaenodontidan species from the Early Eocene of Europe MP level

Taxon

MD

M1 L

MD/M1 L

MP7

Prototomus minimus Parvagula palulae Minimovellentodon russelli Boritia duffaudi Morlodon velleri Matthodon menui Oxyaenoides lindgreni Protoproviverra palaeonictides Leonhardtina godinoti

7.1 4.5 12.6 13.5 14.1 29.4 21.9 10.2 8.84

3.95 3 5.8 6.9 6.7 10.7 10.7 5.13 5.13

1.8 1.5 2.2 1.9 2.1 2.8 2 1.99 1.72

MP8 + 9

MP10

Table 8. Hypothetical correlations between the two mammalian successions of the Northern and Southern European provinces during the earliest Eocene with indications of the faunal events that occurred between PE III and PE IV biozones. Adapted from Marandat et al. (2012: table 3) Ma

ELMA

Biozones

MP

Standard locality

Northern Province

Southern Province

Neustrian

PE V 8+9 Avenay Avenay La Borie PE IV Mutigny Faunal turnover: disappearance of the Oxyaenodonta, Sinopaninae (Hyaenodontida), Coryphodontidae Dispersal from Mesogean Province to Northern Province: Proviverrinae (Hyaenodontida), Lophiaspis (Perissodactyla) Dispersal from Northern Province to Mesogean Province: Plesiesthonyx (Tillodontia) 55.12 PE III Abbey Wood, Pourcy Rians/Fournes ? PE II Meudon, Soissons, Sinceny Fordonnes/Palette/ Le Clot ? 55.8 PE I 7 Dormaal Sotteville-sur-Mer, Try, Erquelinnes, Silveirinha ? Suffolk Pebble Beds, Le Quesnoy ELMA, European Land Mammal Ages; MP, mammal palaeogene; PE, Palaeocene-Eocene.

EOPROVIVERRA

GEN. NOV.

Diagnosis Same as for the type and only species. Etymology From the Greek ‘Eos’ meaning literally ‘dawn’ and figuratively ‘old’, ‘ancient’. Refers to the proximity of this taxon to the origin of proviverrines.

than metacone (plesiomorphic features). It also differs from Parvagula, Boritia, and Morlodon in having a more mesially located paraconid (an apomorphic feature). It differs from Oxyaenoides and Matthodon in having a more bulbous entoconid (a plesiomorphic feature). Chresonymy 1981: Proviverra eisenmanni in Godinot, pp. 64–67, fig. 8, pl. II 12, 14–17.

Type species Eoproviverra eisenmanni (Godinot, 1981) comb. nov.

Holotype MNHN.F.RI400, LM2?.

Type locality MP7, Rians (France).

Type locality MP7, Rians (France).

EOPROVIVERRA

EISENMANNI

(GODINOT, 1981)

COMB. NOV.

Diagnosis Eoproviverra eisenmanni differs from other proviverrines (except Parvagula) in its smaller size, larger metaconid and narrower talonid on molars, and paracone taller

Referred specimens MNHN.F.RI401, LM 1 ; MNHN.F.RI362, LM 2 ; MNHN.F.RI203, RM3; MNHN.F.RI204, right mandible bearing M1 and M2. Measurements See Godinot (1981).


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Description The specimens referred to this species were described by Godinot (1981). Discussion Godinot (1981) erected Proviverra eisenmanni for specimens found in the French locality of Rians – this locality is dated to the earliest Eocene of France. He referred the specimens to the genus Proviverra, which is considered to be one of the most primitive hyaenodontidans and so of the proviverrines (Polly, 1996), based on overall similarity. However, he noted that these specimens differ only from those of the type species, Proviverra typica (Middle Eocene). In fact, the Early Eocene specimens differ in having a narrower talonid, less mesiodistally compressed trigonid, and less developed cingulids on the molars, more labially located parastyle, and paraconule more separated from the paracone on M1, less separated paracone and metacone, larger stylar shelf on the molars and less developed cingulae on the molars. Consequently, the two taxa differ in numerous features, as noted by Morlo & Habersetzer (1999) and Solé (2013), and the Early Eocene species does not show the typical features of Proviverra typica. Except for the mesiodistal extension of the trigonid, the features of the taxon from Rians are plesiomorphic amongst proviverrines. Owing to the numerous differences, we erect a new genus, Eoproviverra gen. nov., for the Rians species.

FIRST DETAILED PHYLOGENETIC ANALYSIS OF THE PROVIVERRINAE AIM OF THE PHYLOGENETIC ANALYSIS The recent study of Solé (2013), which focused on the earliest hyaenodontidans, clarified the systematics of the Laurasian ‘Proviverrinae’. At that time, the first author proposed separating the ‘Proviverrinae’ into three groups: the Proviverrinae, the Sinopinae, and the Arfiinae. The subfamily Proviverrinae is endemic to Europe, whereas the Sinopinae and Arfiinae, which are recorded in Europe from Dormaal, Le Quesnoy, and Abbey Wood (Smith & Smith, 2001; Hooker, 2010; Solé et al., 2013a), rapidly disappeared from this continent (Solé et al., 2013a). The seven taxa described or discussed in the present study belong to the Proviverrinae. In order to determine their relationships, a phylogenetic analysis of the subfamily was conducted. Although the phylogeny of the Proviverrinae has already been addressed in the literature (e.g. Lange-Badré, 1979; Crochet, 1991; Solé, 2013), this analysis is the first for the whole subfamily and will therefore serve as a new basis for discussion of proviverrine evolution. Our analysis includes 31 proviverrine taxa, dated from the Early to Late

Eocene (Supporting Information Appendix S1). Only Praecodens from Bouxwiller (MP13, France) has not been included, because it is represented by only a single upper tooth.

MATERIAL AND

METHODS

The phylogenetic analysis focused on dental characters; the cranium and postcranium are lacking for most of the studied taxa. The character matrix was derived from those of Egi et al. (2005), Wible et al. (2009), and Solé (2013), with new character additions and/or definitions. The data matrix consists of 37 taxa, including two outgroup and 35 ingroup taxa (31 proviverrine species), which have been scored for 59 dental characters, including 47 binary characters and 12 multistate characters (Appendix S2). The treatment of characters is detailed below. As ‘Creodonta’ is surely diphyletic (Polly, 1994, 1996; Solé, 2013), oxyaenodontans are not suitable as an outgroup for hyaenodontidans. Instead, the outgroup used here consists of the early eutherians Eomaia and Cimolestes. Following Lillegraven (1969), Cimolestes magnus is considered as the closest to the ancestral morphotype of the Hyaenodontida. In order to test the monophyly of the Proviverrinae, representatives of closely related subfamilies were added to the data set, such as the Palaeocene Tinerhodon, because it is currently considered as the sister taxon to all other members of the Hyaenodontida (Gheerbrant, 1995; Gheerbrant et al., 2006; Solé, 2013; Solé et al., 2013b), the koholiine Boualitomus, the sinopine Prototomus, which is the oldest and most primitive representative of its subfamily, and the arfiine Arfia. The data matrix (Appendix S3) was assembled with WinClada 1.00.08 (Nixon, 1999) and the parsimony analysis was performed with TNT 1.1 (Goloboff, Farris & Nixon, 2008). The software was set up to keep up to 10 000 trees in memory, perform 1000 replications, and collapse trees after the search using ‘rule 1’ (minimum length = 0). Other options were set to default values. After the analysis, each node of the strict consensus tree was assigned a Bremer support calculated with TNT for ten supplementary steps and a bootstrap value obtained using WinClada (1000 replications, ten searches, one starting tree per replication). Finally, we performed a stratocladistic analysis with TNT 1.1 in order to study the effect of the stratigraphical distribution of the proviverrines on their phylogeny. To do so, we added a new character, which has been treated as additive (see Appendix S4).

RESULTS In the first analysis, all taxa were included and the characters were treated as unordered. The analysis



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Figure 9. Strict consensuses of the shortest trees resulting from the phylogenetic analyses of the Proviverrinae: A, first analysis, length (L) = 139, consistency index (CI) = 0.390, and retention index (RI) = 0.694; B, second analysis, L = 168, CI = 0.422, and RI = 0.754. Bremer support and bootstrap values are indicated above and below each node, respectively.

yielded 450 equally parsimonious trees of which the strict consensus has a length of 139 steps for a consistency index (CI) of 0.390 and a retention index (RI) of 0.694 (Fig. 9A). Higher taxonomic units can be recognized. The first clade recovered is that of the Proviverrinae, which includes the genera Matthodon and Oxyaenoides, and subclades that are centred around Allopterodon, Eurotherium, and Cynohyaenodon, but not Parvagula. This genus appears less closely related to the main proviverrine clade than Prototomus and Arfia are (see below). Finer interspecific relationships remain poorly resolved. A closer look at the topologies showed that this lack of resolution is partly caused by the erratic behaviour of Protoproviverra palaeonictides. Depending on the topology, this species is found as the sister group of either Clade P or Clade U (= Cynohyaenodon clade; Fig. 9B), two positions that are incompatible. However, we think that Protoproviverra is more probably at the root of Clade

U (= Cynohyaenodon clade) because, as discussed above, the P4 and M1 of Protoproviverra show similarities with those of the species of Cynohyaenodon. A second analysis was then performed in order to improve the resolution of the proviverrine phylogeny. Firstly, Protoproviverra palaeonictides was removed from the analysis because its presence blurs the phylogenetic signal in Proviverrinae. Secondly, the 12 multistate characters were here treated as additive because each of them corresponds to a linear transformation series, a morphocline. This analysis resulted in only nine parsimonious trees. Their strict consensus is 168 steps long and has a CI of 0.422 and a RI of 0.754 (Fig. 9B). Its topology is very similar to that of the first analysis. Clades centred around the genera Matthodon, Oxyaenoides, Allopterodon, Eurotherium, and Cynohyaenodon were recovered. The resolution of the consensus is much better than in the previous analysis, although some relationships remain uncertain. The


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most important difference between the first and the second strict consensus trees is that the Proviverrinae are no longer monophyletic: the relationship between Arfia, which represents the Arfiinae, and the supposedly proviverrine Clades F and I is now unresolved. The only interesting contribution of the stratocladistic analysis (172 trees; strict consensus: L = 203, CI = 0.38; RI = 0.71) is the exclusion of L. godinoti from the remainder of the Leonhardtina clade. Although this result was expected given the earlier occurrence of L. godinoti, it was not supported by the previous cladistic analyses. Further material is therefore required to better understand the relationship of L. godinoti to other members of the Leonhardtina clade.

RELATIONSHIPS AND

MORPHOLOGICAL EVOLUTION

Tinerhodon is the sister taxon of all the other hyaenodontidans in this analysis, with which it forms Clade A. This agrees with both its age (Late Palaeocene) and morphology (Gheerbrant, 1995; Gheerbrant et al., 2006). The Early Eocene species Boualitomus (Node B) is closer to proviverrines than to Tinerhodon. Node B is supported by a compressed transversally P4 and a keeled paraconid on molars [20(1), 25(1)]. However, the taxa Prototomus (Sinopinae) and Arfia (Arfiinae) are closer to the other proviverrines than Parvagula. The position of Prototomus is supported by a P1 with closely located roots [6(1)], narrower premolars [23(0)], paracone smaller than metacone [48(1)], metacone present on M3 [51(1)], and the existence of a prefossa/ postfossid shear [58(0)]. This is surprising, because these features are probably plesiomorphic for the Hyaenodontida (Solé, 2013). Node C, which unites Arfia and all proviverrines – except Parvagula – is supported by the absence of the protostylid [17(0)] and the presence of an individualized and mesially located protocone on P4 [42(1), 43(1)]. The paraphyly of the Proviverrinae may be the result of the present taxonomic sampling and our current lack of knowledge regarding the upper dentition of Parvagula palulae; nodes D and E are, in fact, supported by characters related to the upper dentition. The monophyly of the Proviverrinae was previously proposed by Morlo & Gunnell, (2003) and Peigné et al. (2007), and supported by the phylogenetic analysis of Solé (2013), but crucial proviverrine synapomorphies could not be scored for Parvagula, including characters 17, 42, 43, 48, 51, 53, or 59, which are synapomorphies for Clades D, E, F and I (= other proviverrines). Some of the synapomorphies of the clade Proviverrinae are also highly convergent, as emphasized by Solé (2013). Two proviverrine clades were recovered by the second analysis. The first, Clade F, includes the small MP10 to MP19 proviverrines Leonhardtina, Proviverra,

Lesmesodon, and Allopterodon. For this reason, Clade F will also be called the Allopterodon clade. It is supported by a two-rooted P1 [6(0)], the presence of a paraconid on P2, P3, and P4 [7(1), 10(1), 15(2)], a P3 longer than the P2 [9(1)], a P3 smaller than the P2 and P4 [13(1)], a P4 shorter than the P3 [14(2)], the presence of two cusps on the P3 and P4 talonids [12(1), 21(1)], a wide talonid on the molars [32(1)], the presence of an ectocingulid on the molars [35(1)], a P3 longer than the P2 [38(1)], the presence of conules on P4 [44(1)], separated paracone and metacone [50(2)], and a short metacingulum [53(1)]. This combination of features is related to the increasing role of the premolars – notably of the P3, which is smaller but distinctly longer than P2 and P4 – probably in catching prey, and of the crushing structures on premolars and molars (protocone and talonid) in crushing the aliments (probably mostly nonvertebrates). It is worth noting that relationships within the Allopterodon clade remain poorly understood in the present analysis, except for the eponymous genus. The monophyly of the genus Allopterodon is established here (Node G), a result that agrees with the relationships proposed by Lange-Badré & Mathis (1992). As noted by Mathis (1985), the genus Allopterodon is distinguished from Proviverra and Leonhardtina by its more developed premolar cingulids [19(2)]. The following features distinguish Allopterodon from Proviverra, Lesmesodon, and Leonhardtina: P4 shorter than P3 and M1 [22(1)], protocone triangular [45(1)] and postmetacrista low on P4 [46(1)], longer postmetacrista on molars [47(1)], and shorter parastylar area [49(1)]. Allopterodon minor and A. torvidus are grouped (node H) by the presence of a short parastylar area [49(2)] compared with that of A. bulbosus. The reduction in the parastylar area and elongation of the postmetacrista occurred several times in Proviverrinae according to the present topology. Proviverra typica is characterized by the development of the molar cingulids and cingulae [36(1), 56(1), 57(1)]. It is worth noting that Eo. eisenmanni and Proviverra typica are distantly related and that the creation of a new genus name for the Rians species is supported by the phylogenetic analysis. The second proviverrine clade is Clade I, which is supported by a deeper dentary [3(1)], a coronoid process that is more tilted distally [5(1)], the presence of a paraconid on P3 [10(1)], metastyle elongated on molars [47(1)], shorter parastylar area [49(1)], and shorter metacingulum on molars [53(1)]. The features that are displayed by the molars represent adaptations to a more sectorial dentition. The development of the paraconid on the molars is typical of the Proviverrinae. Clade I consists of a polytomy between the MP7 Eo. eisenmanni and MP8 + 9 Mi. russelli and Clade J. Eoproviverra eisenmanni is characterized by a metacone smaller than the paracone [49(2)], a feature


EVOLUTION OF THE PROVIVERRINAE that is probably the plesiomorphic condition of the Hyaenodontida (Solé, 2013). Node J is supported by the following synapomorphies: shorter diastemata between the premolars [4(1), presence of a paraconid on P2 [7(1)], presence of two cusps on P3 [12(1)], taller paraconid on P4 [15(2)], M1 shorter than P4 [24(1)], wider talonid on molars [32(1)], and presence of prefossa/postfossid shearing [59(1)]. It is interesting to note that the features of the talonid of the premolars and molars appear convergently in the Allopterodon clade. The reduction of the diastemata between the premolars allowed for a shortening of the tooth row and jaws; thus increasing the bite force. One of the synapomorphies that was listed above – the prefossa/postfossid shearing [59(1)] – was also identified in Minimovellentodon, suggesting potential affinities between this genus and Clade J. Node K is supported by blunt premolars [23(1)], taller paraconid on molars [27(1)], less oblique cristid obliqua [34(2)], and prominent metaconule [54(1)]. The successive sister taxa of clades K and L are the MP8 + 9 Morlodon and Boritia. The first has a relatively opened trigonid [26(1)], as in Clade R, whereas the second is characterized by a short protocone on P4, as in Prototomus [43(0)], and the presence of a pre- and a postcingulum, [56(1)], as in Prototomus, Arfia, and Proviverra typica. The last two features may be plesiomorphic for hyaenodontidans (Solé, 2013). Nodes L to Y contain taxa that range from MP10 to MP18. The synapomorphies supporting Node L include a more open trigonid [26(2)], a paraconid that is taller than the metaconid [27(2)], a shortened talonid on M3 [37(1)], a very long postmetacrista on molars [47(2)], and a very reduced parastylar area [49(2)]. As indicated above, the latter features are convergent amongst Proviverrinae. The same can be said of the opening of the trigonid and the reduction of the metaconid. Node M gathers the two Matthodon species by the shared presence of distally located mental foramina [1(1), 2(1)], a single-rooted P1 [6(2)], and a P4 that is longer than the M1 [24(0)]. In short, the genus has a characteristically short but powerful dentition. Node N is only supported by a two-rooted P1 [6(0)], a feature also typical of both Parvagula and Clade F. As an aside, Morlo & Gunnell (2003), followed by Solé (2013), proposed a two-rooted P1 as the primitive condition for Proviverrinae. Their hypothesis is based on the anatomy of Parvagula, the oldest proviverrine for which premolars are available. The Oxyaenoides clade contains the species O. bicuspidens and O. schlosseri, as well as ‘Francotherium’ lindgreni (node O), a relationship that supports the new combination of the last species as O. lindgreni. The close affinities of these species are supported by the presence of diastemata between the

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premolars [4(0)], the presence of a single cusp on P3 [12(0)], narrower premolars [23(0)], the absence of the metaconid [28(1)], the reduction of the entoconid on the molars [29(1)], and a shallow postfossid and narrow talonid on molars [31(1), 32(0)]. The morphology of the molars involves a very sectorial dentition and a possibly hypercarnivorous diet. As a matter of fact, these features often characterize hypercarnivorous clades in Hyaenodontida (e.g. Hyainailourinae, Hyaenodontinae, Koholiinae). Node P is supported by a well-developed and crestiform entoconid on P4 [21(1)], the closeness of the hypoconid and entoconid [30(1)], a P3 longer than P2 [38(1)], the presence of a lingual bulge on P3 [39(1)], a three-rooted P3 [40(1)], a separation between the paracone and metacone [50(1)], and the reduction of the prefossa/postfossid shear [59(0)]. The most interesting features are the lengthening of the P3, with its three roots, and the separation of the metacone and paracone on the molars. The last feature is also known in the Allopterodon clade, but the separation is much wider in the latter clade. The hypercarnivore Paenoxyaenoides is characterized by several features, of which two are reminiscent of Oxyaenoides. The absence of a metaconid on the molars represents a synapomorphy of the latter genus [28(1)], whereas the very short talonid on M3 is only found in O. schlosseri [37(2)]. The third and last apomorphy of Paenoxyaenoides is the absence of a metacone on M3, a feature shared with Eu. matthesi [58(1)]. As in Oxyaenoides, these features support a hypercarnivorous diet for Paenoxyaenoides. Node Q is only supported by the presence of a welldeveloped metaconule [54(0)], a reversal toward the ancestral condition of hyaenodontidans. Clade R is supported by P3 longer than P4 [14(1)] and a slightly opened trigonid (36–49°), as in Boritia [26(1)]. This clade is subdivided into two subclades, one centred around Eu. matthesi, Clade S, and the other around Cynohyaenodon cayluxi, Clade U. The Eurotherium clade unites the Middle Eocene species Prodissopsalis eocaenicus, Alienetherium buxwilleri, and Eu. matthesi. The position of the latter suggests that the genus Eurotherium is diphyletic and that Eurotherium theriodis should be assigned to a genus of its own. In any case, node S is supported by an M1 longer than P4 [24(0)] and a paraconid and metaconid of equal height [27(1)]. Here, Eu. matthesi is closer to Alienetherium than to Prodissopsalis, forming Clade T with the former. This relationship is supported by the presence of diastemata between the premolars [4(0)] and the fact that the cristid obliqua is slightly oblique [34(1)]. The first condition is plesiomorphic for proviverrines, the second one for hyaenodontidans. The Cynohyaenodon clade includes the genera Quercytherium, Paracynohyaenodon, and, of course,


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Cynohyaenodon. Similar relationships have been suggested by Lange-Badré (1979), Crochet (1991), and Solé (2013). The monophyly of this clade is founded on the shared presence of a P2 as long as the P3 [9(1)], cingulids on premolars [19(1)], a separation between the hypoconid and entoconid on the molars [30(0)], large conules on P4 [44(1)], and a well-mesially located protocone on the molars [55(1)]. As stated previously, the first, second, and fourth transformations are convergent between the Cynohyaenodon and Allopterodon clades. Node V is supported by the reduction of the paraconid and talonid on the premolars [7(0), 8(1), 11(1), 12(0), 15(1)] and the reduction of the parastylar area, postmetacrista, and protocone on P4 [41(1), 42(0), 46(2)]. These features reflect the enlargement and simplification of the premolars observed in Quercytherium in particular. As hypothesized by Crochet, (1991), Cynohyaenodon lautricensis is closely related to the two species of Quercytherium. Amongst the Hyaenodontida, such an enlargement and simplification of the premolars is otherwise only recorded in the African Teratodon (Savage, 1965; Lewis & Morlo, 2010). The latter genus belongs to the Teratodontinae (Savage, 1965; Solé et al., 2013b), so the peculiar premolars of Quercytherium represent convergent adaptations. Clade W includes three species of Cynohyaenodon – including the type species – and the two species of Paracynohyaenodon. It is supported by a P3 longer than the P2 [38(0)] and the presence of prominent conules on P4 [44(2)]. It is worth mentioning that the presence of a long P3 is shared with Cy. lautricensis. This may either be the result of a convergent reversal toward the ancestral condition of hyaenodontidans or of a potential synapomorphy of the Cynohyaenodon clade, with another reversal to a short P3 in Quercytherium. To test this hypothesis, however, the phylogenetic position of Cy. lautricensis would need to be resolved, whereas the presence of both a short and a long P3 in Eu. matthesi shows that intraspecific variation must be taken into account. The grouping of Paracynohyaenodon, Cy. trux, and Cy. ruetimeyeri in Clade X is only supported by the shortening of the P3 compared to the P4 [14(0)]. Although the two species of Paracynohyaenodon are very closely related, there is no evidence for the monophyly of the genus. These species here form a polytomy with clade Y, that is, Cy. trux and Cy. ruetimeyeri. The latter node is supported by the presence of a paraconid that is as high as the metaconid [27(1)], a long talonid on M3 [37(0)] and long postmetacrista on molars [49(1)]. These features indicate development of the sectorial structures of the molars, as commonly observed in the youngest hyaenodontidans. It is worth mentioning that the paraphyly of the genus Cynohyaenodon – discussed by Crochet, (1991) – is supported by the present study.

Proviverrines show a remarkable trend toward the development of the anterior premolars. The size of the latter increases greatly in the youngest taxa. This is exemplified by the small to middle-sized proviverrines such as those belonging to the Allopterodon or Cynohyaenodon clades. The width of the talonid tends also to increase in the same clades, as well as in the Eurotherium clade. The most sectorial and specialized molars are present in the Oxyaenoides clade, the Matthodon clade, Paenoxyaenoides, and the Cynohyaenodon clade. Paenoxyaenoides differs from Oxyaenoides in the enlargement of the talonid, although both genera display a similar reduction of the metaconid and elongation of the paracristid. The cladogram that resulted from the second analysis agrees rather well with the stratigraphical distribution of the proviverrines (Fig. 10). However, it will be important in the near future to document the origin of the small to middle-sized proviverrines (Allopterodon, Cynohyaenodon, and Eurotherium clades) for a better understanding of the interrelationships of the Proviverrinae.

PALAEOECOLOGICAL EVOLUTION OF THE PROVIVERRINAE A FAUNAL

TURNOVER AND HOMOGENIZATION OF THE

EUROPE EARLY EOCENE

MAMMALIAN CARNIVORE FAUNA IN DURING THE

Hyaenodontidans first appeared in Europe in the earliest Eocene (Smith & Smith, 2001; Solé et al., 2013a). Probably originating in Africa, they dispersed with other mammals into Europe during the Palaeocene−Eocene Thermal Maximum (PETM), a migration also termed the Mammalian Dispersal Event. Marandat (1997) identified distinct mammal distributions close in age to MP7 in the Northern Province and the Mesogean Province (Fig. 11A). Gruas-Cavagnetto (1992) noted, on the basis of palaeobotanical data, the existence of a climatic barrier between the Northern and the Mesogean provinces. This intra-European provincialism may be related to the orogenesis of the Pyrenees and to the transgressions of the Aquitaine Sea (Plaziat, 1981). Marandat et al. (2012) recently suggested that there was a strong latitudinal temperature gradient in western Europe at least before and after the PETM (Fig. 11A). The recent studies of Solé et al. (2011, 2013a) have shown that the distribution of the Hyaenodontida and Oxyaenodonta support the intra-European provincialism suggested by Marandat (1997). The Sinopinae were present in both provinces, whereas the Proviverrinae are only recorded in the Mesogean Province, and the Arfiinae and Oxyaenodonta only in the Northern Province at that time (Fig. 11A).


Figure 10. Phylogeny of the Proviverrinae correlated with stratigraphy and with eustatic and climatic variations. The dashed time range of Paenoxyaenoides indicates that its age is poorly constrained. Stratigraphical scale, eustatic curve, and isotopic curves produced with TSCreator (Ogg & Lugowski, 2013) from the data compiled by Gradstein et al. (2012). ELMA, European Land Mammal Ages; MP, mammal palaeogene.



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Figure 11. Comparison of the European biogeography of placental carnivorous mammals during the earliest Eocene: A, between the MP7 and MP8 + 9 levels and B, during the MP8 + 9 level. A, the Northern Province is characterized by the presence of the hyaenodontidan Sinopinae and Oxyaenodonta, whereas the Mesogean Province is characterized by the presence of the hyaenodontidan Sinopinae and Proviverrinae. Proviverrinae occurred in Rians and Palette (France) and Silveirinha (Portugal). Sinopinae are identified at Dormaal (Belgium), Le Quesnoy, Pourcy, Soissons (France), and Abbey Wood (England). Oxyaenodonta are identified in Dormaal, Houdancourt (Belgium), Meudon, Sinceny, Muirancourt, Le Quesnoy (France), and Abbey Wood (England) (Hooker, 2010; Solé et al., 2011). Above the line: Northern Province; below the line: Mesogean Province. B, the provinces have been homogenized because of disappearances (e.g. Sinopinae and Oxyaenodonta) and faunal dispersals (e.g. Proviverrinae; see Table 8). The arrow symbolizes the dispersal of the Proviverrinae from the Mesogean to the Northern Province. Redrawn from Marandat et al. (2012: fig. 1).

Solé et al. (2011, 2013a) demonstrated the rapid disappearances of the Arfiinae, Sinopinae, and Oxyaenodonta from Europe during the Early Eocene. These groups are restricted to biozones PE I, PE II, and PE III of Hooker (1996, 1998) (Table 8). This faunal turnover probably affected both the Mesogean and Northern provinces because the Sinopinae also disappeared from the Mesogean area (Solé et al., 2013a). Solé (2014) showed an almost identical pattern in the evolution of the European carnivoraforms. Another group of mammals, the Coryphodontidae, which were the largest herbivorous mammals of the time, disappeared from Europe at the same time (Table 8).

Similarly, Chew (2009) showed the presence of biotic turnover events in the mammalian fauna of the Willwood Formation of Wyoming, USA. These events occurred during the earliest Eocene Wasatchian biozones Wa3 to Wa5, which are about 55 to 54 Mya in age. Chew (2009) reported increasing extinction rates, followed by a diversity crash, and a subsequent faunal reorganization. This extinction event coincided with a climate cooling (decrease in mean annual temperature of 5–8 °C) between PETM and the Early Eocene Climatic Optimum (EECO) as evidenced by Wing, Bao & Koch (1999). Thus far, however, this cooling has not been recognized in Europe. As the Abbey Wood (PE III) and Mutigny (PE


EVOLUTION OF THE PROVIVERRINAE IV) localities have been respectively dated to 55.12 Mya (Hooker, 2010) and 54–52 Mya (Neal, 1996; Duprat, 1997), the disappearance of Arfiinae, Sinopinae, Coryphodontidae, and Oxyaenodonta may represent the consequence of the global cooling evidenced by Wing et al. (1999) on the European mammalian fauna. This faunal turnover preceded a south−north dispersal of the Proviverrinae (Fig. 11B). The presence of Proviverrinae in the Northern Province is now undoubtedly dated to the PE IV zone (Mutigny) based on the discovery of Minimovellentodon. This discovery implies that Proviverrinae dispersed from the Mesogean to the Northern Province between PE III and PEIV (Table 8). It is worth mentioning that the perissodactyl Lophiaspis, which is recorded in the earliest Eocene of Palette and Silveirinha, in the Mesogean Province (Depéret, 1910; Godinot et al., 1987; Estravís, 2000), is also recorded in the Northern Province, but only starting from PE IV (Hooker, 1996, 1998). The Proviverrinae and Lophiaspis thus probably dispersed together from the Mesogean to the Northern Province (Fig. 11B; Table 8). Solé (2014) recently showed that the carnivoraform Quercygale first appeared in Europe in Mutigny (PE IV zone); this implies that the terrestrial connections between Europe and Asia may possibly have been active at this time. The arrival of this carnivoraform genus was probably favoured, as were the proviverrines, by the disappearance of competitors from the Northern Province (Oxyaenodonta, Sinopinae).

A DIVERSIFICATION

DRIVEN BY THE

EECO

Morlo (1999) and Morlo, Gunnell & Nagel (2010) compared the niche structure and evolution of carnivore guilds in the Eocene of Europe and North America. When comparing the European MP11−13 faunas and the North American Bridgerian NALMA (Br)-2 faunas, they noted the higher diversity of the North American fauna, the limited body mass variation of the European carnivores, and the differing ecological importance of hyaenodontidans between the continents. Indeed, these studies showed ‘a highly diverse ecomorphological pattern within the subfamily Proviverrinae’ (Morlo et al., 2010: 275) in Europe. Morlo (1999: 302) also stated that ‘the different ecological importance of the proviverrines on the two continents might be explained by the competition they were confronted with in North America from other groups’, namely, the Oxyaenodonta, Limnocyoninae, Viverravidae, and the other Carnivoraformes. The observations of Morlo (1999) indicate that the disappearances of the Oxyaenodonta and Sinopinae from Europe probably favoured the diversification of the Proviverrinae. It is because of the extinction of their ecological com-

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petitors during the Early Eocene that the Proviverrinae radiated and became the top mammalian predators in Europe, a classical phenomenon known as ‘ecological replacement’. A better understanding of the diversification of the proviverrines can only be obtained by a detailed characterization of how their ecological and morphological diversity evolved throughout the Eocene. The present study focuses on the body mass and diet of proviverrines, which had a fundamental role in their evolution. These two ecological characters have been plotted on the timecalibrated strict consensus tree obtained in the previous analysis (Fig. 10). The resulting figure clearly shows a diversification of the proviverrines during the Early Eocene. Indeed, we have now recorded four genera in the MP10 reference level (Matthodon, Oxyaenoides, Protoproviverra, Leonhardtina) vs. three in the MP8 + 9 reference levels (Minimovellentodon, Morlodon, Boritia) and two in the MP7 reference level (Eoproviverra, Parvagula). Moreover, the MP10 genera represent distinctive proviverrine groups that are known in the Middle Eocene: the Matthodon clade (Matthodon menui), the Oxyaenoides clade (Oxyaenoides lindgreni), and the Allopterodon clade (L. godinoti); Protoproviverra palaeonictides is phylogenetically close to both the Eurotherium and the Cynohyaenodon clades. It is worth noting that the body masses of the proviverrines increased greatly between the MP7 and MP10 reference levels: Oxyaenoides and Matthodon weighed about 10 kg, whereas the earliest proviverrines weighed less than 1 kg. Finally, Oxyaenoides and Matthodon represent two highly specialized ecomorphotypes: Oxyaenoides was hypercarnivorous, whereas Matthodon was a durophagous and hypercarnivorous predator. As a consequence, the proviverrines increased in diversity and specialization during the Early and earliest Middle Eocene. A similar diversification occurred in other groups of mammals, such as Perissodactyla and Artiodactyla, during the Early Eocene (e.g. Sudre & Erfurt, 1996); it therefore reflected a global trend of the European mammalian fauna during the Early Eocene. This period, which includes the MP8 + 9 and MP10 reference levels, seems to have been a time of stabilization and diversification for mammals (Russell, 1975). It corresponds to the EECO (∼53–50 Mya; Fig. 10), a short period that saw the highest mean ocean temperature of the Cenozoic (Zachos et al., 2001; Zachos, Dickens & Richard, 2008) and witnessed an increase in tropicality as well as floral diversity. An increase in diversity is also observed for mammals in North America (Woodburne, Gunnell & Stucky, 2009). The lack of competitors probably favoured the diversification of the Proviverrinae in this warm period (Fig. 10). This diversification contrasts with that reconstructed for the European carnivoraforms (Solé, 2014).


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Figure 12. Values of Ln(body mass) of oxyaenodontidans and hyaenodontidans from MP7 to MP17b. Values given in Table 10.

In conclusion, the Early Eocene diversification of the Proviverrinae in Europe was probably caused by both (1) the lack of competitors and (2) the EECO.

THE

Table 9. Comparison between the largest carnivorous mammals (based on diet, locomotion, and body mass) of the MP7 and MP10 reference levels MP7

MP10

Oxyaena woutersi • Meat diet • Generalized (terrestrial) • 7.4 kg

Oxyaenoides lindgreni • Meat diet • Cursorial* • 9.88 kg

Palaeonictis gigantea • Meat/bone diet • Generalized (terrestrial) • 12.3 kg

Matthodon menui • Meat/bone diet • Semifossorial* • 12.4 kg

RELATIVELY ‘SMALL SIZE’ OF THE

PROVIVERRINAE

Comparison of the carnivorous mammals of MP7 and MP10 indicates that some taxa belonged to the same ecomorphospace. This phenomenon is well illustrated by the MP7/MP10 couples (1) Oxyaena and Oxyaenoides, which were hypercarnivorous (= exclusive meateaters) and weighed almost 10 kg, and (2) Palaeonictis and Matthodon, which were durophagous and hypercarnivorous predators and were slightly heavier than 10 kg (Fig. 12, Table 9). This clearly shows that the oxyaenodontans were ecologically replaced by some large proviverrine species after their extinction. We also note that the Proviverrinae from MP10 were more specialized than the oxyaenodontans from MP7. Oxyaenoides was a cursorial taxon (Morlo, 1999), whereas Oxyaena woutersi from Dormaal and Le Quesnoy was a generalized terrestrial species (Solé et al., 2011). Moreover, the metaconid had disappeared from the molars of Oxyaenoides, whereas it was still present in Oxyaena. Matthodon differs from Palaeonictis in its more reduced metaconid and by more advanced adaptations towards semifossoriality. However, it is probable that the latter two genera hunted prey of similar size on the ground.

*Locomotor types are inferred based on that of their closest relatives according to our phylogenetic analysis of the proviverrines.

A crucial point here is that the largest proviverrines from MP10 did not exceed the size of the MP7 oxyaenodontans. Moreover, as noted by Carbone et al. (1999), extant carnivorous mammals that weigh below 21.5–25 kg generally hunt prey that are smaller than themselves. Hence, Oxyaena, Palaeonictis, Matthodon, and Oxyaenoides would not have hunted large mammals such as Lophiodon, but would have rather been feeding on small artiodactyls and perissodactyls. As the beginning of the Bridgerian and the MP10 localities are dated to 51–50 Mya (Escarguel, Marandat


EVOLUTION OF THE PROVIVERRINAE & Legendre, 1997; Escarguel, 1999; Woodburne et al., 2009), we consider that the Br-1 and MP10 carnivorous faunas are contemporaneous. A comparison between them is therefore relevant. The detailed guild analysis performed by Morlo (1999) on the Br-1 assemblage allows for adequate comparisons with the new data provided here on MP10 proviverrines. The largest taxa are especially interesting. To start with, the MP10 and Br-1 localities share taxa with a similar ecology, such as Oxyaenoides and Patriofelis, both of which had a meat diet and cursorial locomotion. By contrast, Matthodon and Ambloctonus had a meat/bone diet, but belonged to distinct ecomorphospaces; Matthodon was characterized by a semifossorial mode of life, whereas Ambloctonus was terrestrial, as was its sister genus Palaeonictis. The body masses of the two North American oxyaenodontans were between 30 and 100 kg, according to Morlo (1999), whereas the body masses of their European hyaenodontidan counterparts approached only 10 kg. Thus, Patriofelis and Ambloctonus were much larger than Matthodon and Oxyaenides. The upper limit of the body mass range of carnivorous mammals was therefore much higher in North America than in Europe at that time. This difference persisted in the Middle Eocene (see Morlo et al., 2010). In conclusion, we think that the faunal turnover between the MP7 and MP8 + 9 levels, which is marked by the extinction of European Oxyaenodonta, may have delayed the appearance of very large carnivorous mammals in Europe. The first proviverrines with a body mass close to 20 kg appeared in MP11. It is interesting to note that this corresponds to the upper limit of the body mass range of proviverrines, despite their endemic evolution and the lack of competitors (Fig. 12, Table 10). As a result, European carnivorous mammals remained clearly smaller than their North American counterparts during the entire Eocene. The environment in which North American and European carnivorous mammals lived – an interior continental setting of mixed landscapes in North America vs. an archipelago in Europe – might have favoured differences in ecology, including mass, diet, locomotion, and mode of life.

THE BRIDGERIAN CRASH AND THE FIRST INTRA-EOCENE MAMMALIAN TURNOVER During an interval ranging from Br-1b to Br-3 there was a major reorganization of the North American mammalian fauna, termed the ‘Bridgerian Crash’ (Woodburne et al., 2009). This phenomenon is illustrated by the stark contrast between the low number of first appearance datums and the high number of last appearance datums. According to Woodburne et al. (2009), these extinctions were probably influenced by the coeval return to cooler and more seasonally arid conditions after the

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EECO. This climatic deterioration had a major impact on floras and thus on mammalian communities. North American carnivorous mammals show a marked decline in diversity, seen in hyaenodontidans (limnocyonines and sinopines), oxyaenodontans, carnivoraforms, and viverravids. It should be mentioned that oxyaenodontans disappeared from North America at the end of the Bridgerian, whereas hyaenodontidan sinopines disappeared during the Uintan. Coryphodontids disappeared during the Bridgerian. By contrast, there is no evidence for a ‘crash’ in proviverrines. The MP10 and MP11 proviverrines are in fact very similar taxonomically and ecologically. This is best illustrated by the two largest proviverrines, Oxyaenoides and Matthodon, which persisted in MP11 although they were represented by different species. By contrast, Protoproviverra became extinct, but was replaced by its close relatives Cynohyaenodon, Alienetherium, and Eurotherium. A bit heavier, they nevertheless retained the same meat-based diet. Finally, Leonhardtina did disappear in MP11, but was replaced by its relative Lesmesodon before it reappeared in the fossil record in MP12 – although the monophyly of the genus Leonhardtina needs to be investigated further. There is therefore no striking modification in diversity and ecology in proviverrines after the end of the EECO. According to Collinson, Fowler & Boutler (1981), the forests that were mostly tropical and paratropical during the Ypresian underwent major floristic changes as the climate became cooler and drier from the end of the Ypresian to the Lutetian. These data confirm that the European environments changed after the EECO, just as in North America. The floristic turnover highlighted by Collinson et al. (1981) is probably the main cause behind the first intra-Eocene mammalian turnover that occurred in Europe, as discussed by Franzen (2003) and Badiola et al. (2009). This turnover particularly affected mammals found in the MP12 and MP13 reference levels, as illustrated by the artiodactyls and perissodactyls of the Geiseltal area. Study of these groups showed a replacement, step by step, of Early Eocene taxa by others that were more adapted to highly abrasive food, typical of drier environments. Franzen (2003) believed that this turnover was probably driven by the northward shift in climate, and thus vegetation zones; the new taxa that appeared during the Geiseltalian may have originated in the Iberian Peninsula and migrated northward, following the environments that they were adapted to. The Geiseltalian proviverrines persisted through the disappearance of the durophagous and hypercarnivorous Matthodon, the appearance of the genus Cynohyaenodon, and the return of Leonhardtina in the fossil record between the MP11 and MP12 reference levels. The presence of Leonhardtina in MP10 in the Paris Basin and in Geiseltal in MP12


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Table 10. Mean tooth measurements and body mass estimations. Estimations for the M2 and M3 of Protoproviverra based on comparisons with Cynohyaenodon trux; M1 of Leonhardtina gracilis based on comparisons with molars of Proviverra typica; M1 of Allopterodon torvidus based on comparisons with molars of Proviverra typica; M3 of Paracynohyaenodon magnus based on comparisons with Paracynohyaenodon schlosseri. Measurements of specimens of the MP12 and MP13 levels were combined for Proviverra typica and Cy. trux. We used the means provided by Lange-Badré (1979) for Allopterodon bulbosus, Allopterodon minor, Paracynohyaenodon schlosseri, Quercytherium simplicidens, Quercytherium tenebrosum, and Cynohyaenodon cayluxi

MP

Species

Taxon

(M1−M3)L (mm)

Mass (kg)

LnMass

References

7

Oxyaena woutersi Palaeonictis gigantea Galecyon morloi Prototomus girardoti Prototomus minimus Arfia gingerichi ‘Proviverra’ eisenmannae Parvagula palulae Boritia duffaudi Minimovellentodon russelli Morlodon vellerei Leonhardtina godinoti Matthodon menui Oxyaenoides lindgreni Protoproviverra palaeonictides Eurotherium matthesi Oxyaenoides bicuspidens Matthodon tritens Cynohyaenodon trux Leonhartina gracilis Prodissopsalis eocaenicus Proviverra typica Cynohyaenodon trux Leonhartina gracilis Prodissopsalis eocaenicus Proviverra typica Allopterodon torvidus Cynohyaenodon rutimeyeri Cynohyaenodon trux Eurotherium theriodis Oxyaenoides schlosseri Prodissopsalis eocaenicus Proviverra typica Allopterodon bulbosus Allopterodon minor Cynohyaenodon cailuxy Paenoxyaenoides liguritor Paracynohyaenodon magnus Paracynohyaenodon schlosseri Quercytherium tenebrosum Allopterodon bulbosus Allopterodon minor Cynohyaenodon cayluxi Paenoxyaenoides liguritor Paracynohyaenodon schlosseri Paracynohyaenodon magnus Quercytherium simplicidens Quercytherium tenebrosum Allopterodon bulbosus

O O S S S A P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P P

19.33 23.20 14.71 13.58 11.34 19.58 6.35 7.80 22.31 17.87 21.46 16.98 34.48 32.54 16.60 28.98 36.25 39.48 19.35 19.92 39.86 14.00 19.35 20.35 38.80 14.00 14.60 20.40 17.80 29.50 38.12 38.80 13.30 15.55 21.03 19.90 38.80 24.99 23.21 23.04 15.55 21.03 19.90 38.80 23.21 24.99 23.55 23.04 15.55

6.480 12.296 0.598 0.452 0.240 1.633 0.031 0.065 2.582 1.185 0.526 0.990 11.904 9.714 0.915 6.468 14.191 19.149 1.567 1.735 19.803 0.503 1.567 1.870 18.016 0.503 0.583 1.886 1.169 6.885 16.931 18.016 0.420 0.727 2.098 1.729 18.016 3.845 2.967 2.891 0.727 2.098 1.729 18.016 2.967 3.845 3.122 2.891 0.727

8.776 9.417 6.394 6.114 5.481 7.398 3.445 4.167 7.856 7.077 7.720 6.898 9.385 9.181 6.819 8.775 9.560 9.860 7.357 7.459 9.894 6.221 7.357 7.534 9.799 6.221 6.368 7.542 7.064 8.837 9.737 9.799 6.041 6.589 7.649 7.455 9.799 8.255 7.995 7.969 6.589 7.649 7.455 9.799 7.995 8.255 8.046 7.969 6.589

Smith & Smith, 2001; Solé et al., 2011 Smith & Smith, 2001; Solé et al., 2011 Smith & Smith, 2001 Smith & Smith, 2001; Solé et al., 2013a Smith & Smith, 2001 Smith & Smith, 2001 Godinot, 1981 Godinot et al., 1987 Present paper Present paper Solé, 2013 Present paper Present paper Present paper Present paper Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990; Van Valen, 1965 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990; Van Valen, 1965 Van Valen, 1965 Van Valen, 1965 Van Valen, 1965 Van Valen, 1965 F. Solé (unpublished data) Lange-Badré & Haubold, 1990 Lange-Badré & Haubold, 1990; Van Valen, 1965 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Crochet, 1991 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979 Crochet, 1991 Lange-Badré, 1979 Lange-Badré, 1979 Lange-Badré, 1979

8+9

10

11

12

13

14

16

17a

17b

A, Arfiinae; O, Oxyaenodonta; P, Proviverrinae; S, Sinopainae. (M1−M3)L, M1 to M3 length.


EVOLUTION OF THE PROVIVERRINAE seems to support the northward migration during the first intra-Eocene faunal turnover of the proviverrines, but the relationship of L. gracilis and L. godinoti needs to be confirmed. The appearances of Prodissopsalis and Proviverra in MP12 of Geiseltal could also have been the result of this northward migration. Our results thus agree with the existence of the first intra-Eocene mammalian faunal turnover, as proposed by Franzen (2003) for Central Europe.

THE

EXTINCTION OF THE

PROVIVERRINAE

Proviverrine species were still numerous in the MP17a reference level, with at least seven species recorded (Fig. 10). Moreover, proviverrines remained ecologically diverse, as exemplified by Quercytherium, which is characterized by unusually large premolars. The presence of the large and hypercarnivorous Paenoxyaenoides shows that the Proviverrinae remained the top mammalian predators at this time. However, by the end of this period, we see a progressive decline and disappearance of the Proviverrinae: the small MP 17b A. bulbosus and MP 18 to MP 19 A. minor persisted to the end of the Late Eocene (Lange-Badré, 1979; Morlo & Habersetzer, 1999; Fig. 10). The Proviverrinae were extinct by the end of the Eocene. The abrupt decline and later extinction of the proviverrines might have resulted from the climatic deterioration that characterized the end of the Eocene (Fig. 10). This global cooling and drying was the main driver of the second Eocene floristic turnover recorded in Europe, mostly during the Bartonian and Priabonian (Collinson et al., 1981). The proviverrines may also have suffered because of the appearance of new competitors during the second intra-Eocene mammalian turnover, described by Franzen (2003). The hyainailourines Paroxyaena and Pterodon, which originated in Africa (Solé et al., 2013b), appeared in the MP16 and MP18 reference levels, respectively, whereas the first hyaenodontines, which probably came from Asia (Lange-Badré, 1979), appeared in the MP17a reference level (BiochroM’97, 1997). Moreover, the first carnivoran (Cynodictis lacustris) appeared in Europe in MP18 (BiochroM’97, 1997). All these new immigrants, which show a wide range of adaptations and sizes (Lange-Badré, 1979), would have ecologically competed with and/or replaced the proviverrines before the end of Late Eocene.

CONVERGENCES AMONGST PROVIVERRINAE The Proviverrinae lived almost 20 Myr in Europe, where they were the top mammalian predators. Although shortlived, they still succeeded in occupying a wide array of ecological niches over the course of the Eocene, with a great diversity of body masses and ecologies. Even

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so, it is not surprising that some of the anatomical features displayed by proviverrines are convergences. Two types of dietary-related convergence can be distinguished here: some are adaptations towards hypercarnivory and others towards durophagy. Hypercarnivorous mammals display very sectorial teeth, which are generally characterized by the reduction to loss of the metaconid on the molars. This type of diet appeared twice in the Proviverrinae, in the Early−Middle Eocene Oxyaenoides and in the Late Eocene Paenoxyaenoides (Fig. 10). The dental structures of these two genera are remarkably similar, although they belong to two different clades: Paenoxyaenoides differs from Oxyaenoides in having a wide talonid bearing three cusps, as in some of its relatives (e.g. Eurotherium and Prodissopsalis). Van Valkenburgh, Wang & Damuth (2004) noted that the evolution of large size in carnivores is generally associated with a dietary shift to hypercarnivory and a decline in species’ durations because of an increased vulnerability to extinction. Moreover, as observed by Holliday & Steppan (2004), hypercarnivores are more limited in subsequent morphological evolution than are less specialized forms, given that evolutionary reversals seem unlikely (= Dollo’s law). The replacement of Oxyaenoides by Paenoxyaenoides thus agrees with the observations of Van Valkenburgh et al. (2004) and Holliday & Steppan (2004). Durophagy is exemplified in proviverrines by Matthodon (Early to Middle Eocene) and Quercytherium (Late Eocene) (Figs 10, 13). As usually observed in bonecracking predators, the two genera have a very high mandible and large premolars. Matthodon differs from Quercytherium in having larger molars lacking a metaconid, and thus in being hypercarnivorous as well, whereas Quercytherium displays very large P2 and P3 (Fig. 13). These differences clearly support independent adaptation towards durophagy. The repeated, independent evolution of similar feeding morphologies in distinct clades has been often observed in carnivorous mammal groups. The case of the Proviverrinae is interesting because these independent acquisitions occurred in a short time (∼20 Myr). As noted by Van Valkenburgh (1999: 488), ‘there are a fairly limited number of ways to hunt, kill, and consume prey, and consequently, sympatric predators have tended to diverge along the same lines, no matter where or when they lived’. Van Valkenburgh (1999) discussed two hypothetical examples for explaining the replacement of one clade by a second one: ‘active/ competitive displacement’ or ‘passive replacement’ (Benton, 1987). Concerning the Proviverrinae, the rise of the second clade overlaps the fall of the first clade in time and space; the taxa closely related to Paenoxyaenoides and Quercytherium are contemporaneous with Oxyaenoides and Matthodon (Fig. 10). Thus,


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Figure 13. Comparison of two bone-cracking proviverrines. A, B, Matthodon menui, MNHN.F.CHO14799 (holotype), right dentary bearing canine, P2−M2, and root of P1. A, labial view; B, occlusal view. C, D, Quercytherium tenebrosum, MNHN.F.Qu8644 (holotype), left dentary bearing P2 to M3 and alveoli for C and P1. Mirrored views. C, occlusal view; D, labial view. Note the depth of the dentaries and the robustness of the premolars in both genera. Scale bar = 10 mm.


EVOLUTION OF THE PROVIVERRINAE competition as causal agent seems to have been involved in the evolution of proviverrines, in addition to replacement, as discussed above. Phylogenetic increase in body size over time, or Cope’s rule, is a common phenomenon in mammals. This phenomenon was discussed for carnivorous clades by Van Valkenburgh (2007). Body mass tended to increase in the Proviverrinae during the Eocene. The largest sizes evolved several times independently, in Oxyaenoides, Matthodon, Paenoxyaenoides, and Quercytherium. Surprisingly, the genus Allopterodon distinguishes itself by a small increase in body mass: A. bulbosus is only slightly heavier than 1 kg (Fig. 10). Lange-Badré & Mathis (1992) also remarked on the stability of the dentition of the species of Allopterodon. However, it is worth noting that A. bulbosus differs in having enlarged premolars (Lange-Badré, 1979). This genus conserved a more generalized morphology. As noted by Van Valkenburgh (1999), the smallest and more omnivorous carnivorous mammals are also those that are the least specialized, a characteristic that might favour persistence when environments change. Moreover, levels of interspecific competition are not likely to be as high as they are within the large predator guilds. The dental conservatism and small size of the species of Allopterodon may explain its survival up to the very end of the Eocene as the last of the Proviverrinae. Furthermore, as indicated above, the species of the Allopterodon clade differ from their proviverrine contemporaries of the Cynohyaenodon clade in their clearly less sectorial dentition and frequently also in their smaller size. Indeed, in the Allopterodon clade, the fact that the prefossid remained closed conferred a more puncturing function on the trigonid. The species of this clade also differ in having a narrow mandible and straight coronoid crest, in contrast to the condition seen in other proviverrines, in which the coronoid crest is generally distally tilted at an angle of 120°, vs. 100° in Allopterodon. The peculiar morphologies of the dentition and mandible of the species of Allopterodon are reminiscent of those of insectivorous bats (see Smith et al., 2007: fig. 1). It is therefore quite possible that Allopterodon fed mostly on nonvertebrates such as arthropods, unlike the contemporaneous Paracynohyaenodon and Cynohyaenodon. The peculiar features and ecological niche would have limited the size increase of Allopterodon. In any case, it is reasonable to think that it was the arrival of potential competitors, small carnivorans, in Europe since MP18 that brought the last proviverrine to extinction.

CONCLUSION The material described here provides crucial information concerning the radiation of the Proviverrinae. It allowed for the description of three new species and

913

modification of the generic assignment of four others. These new data greatly increase our knowledge of the diversity of this subfamily during the Early Eocene. The holotype mandible of Boritia duffaudi, found in La Borie, is one of the best-preserved hyaenodontidan mandibles known from the Early Eocene of Europe and therefore provides new and significant information on the oldest representatives of this clade from the Mesogean Province. However, as noted by Marandat et al. (2012), the faunal disparity that existed during the earliest Eocene makes correlations particularly difficult between the European and Mesogean provinces. The discovery of an MP8 + 9 locality, which provides evidence for the homogenization of the two provinces, thus represents a crucial element for establishing correlations between them. Such correlations will play a major role in understanding the faunal events that occurred during the earliest Eocene. The causes of the homogenization that occurred between the biozones PE III and PE IV in Europe remain unclear. It is probable that the strong latitudinal climatic gradient of the earliest Eocene decreased. Addressing this question will necessitate new investigations, including detailed comparison of the floral and faunal evolution of the European and Mesogean provinces. The new data also suggest that the radiation of the Proviverrinae was favoured by both the EECO and the local extinction of the Oxyaenodonta and the hyaenodontidan Sinopinae and Arfiinae from Europe as a whole. The Proviverrinae dominated the European carnivorous faunas until the Late Eocene, occupying a wide array of ecological niches over time, displaying a great diversity of ecomorphs and body size. The large hypercarnivorous and durophagous ecomorphs seen in the Proviverrinae are similar to what is known in North America at the same time. The evolution of the Proviverrinae entirely agrees with the schemes proposed by Van Valkenburgh (1999, 2007) and Van Valkenburgh et al. (2004) for carnivorous mammals.

ACKNOWLEDGEMENTS The photographs of Boritia duffaudi were taken by Laurent Yves. Other photographs were taken by C. Lemzaouda and P. Loubry (Muséum National d’Histoire Naturelle, Paris). We warmly thank the Société Terreal for having authorized access to the quarries, and especially L. Nathan (Directeur des Carrières Sud) for his assistance during the excavations. Many thanks to the people involved in the fieldwork in La Borie. We thank also F. Duranthon (Muséum d’Histoire Naturelle de Toulouse), L. Costeur (Naturhistorisches Museum Basel), D. Berthet (Musée des Confluences, Lyon), and C. Argot and P. Tassy (Muséum National


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d’Histoire Naturelle, Paris) for allowing access to the hyaenodontidan material housed in their respective institutions. This paper is a contribution to project MO/ 36/020, which is financially supported by the Federal Science Policy Office of Belgium. We warmly thank the anonymous referee and the Associate Editor for their constructive comments and corrections leading to improvements of the manuscript.

REFERENCES Anyonge W. 1993. Body mass in large extant and extinct carnivores. Journal of Zoology 231: 339–350. Badiola A, Checa L, Cuesta MA, Quer R, Hooker JJ, Astibia H. 2009. The role of Iberian finds in understanding European Eocene mammalian paleobiogeography. Geologica Acta 7: 243–258. Benton MJ. 1987. Progress and competition in macroevolution. Biological Review 62: 305–338. Biknevicius AR, Van Valkenburgh B, Walker J. 1996. Incisor size and shape: implications for feeding behaviors in sabertoothed ‘cats’. Journal of Vertebrate Paleontology 16: 510– 521. BiochroM’97. 1997. Synthèses et corrélations. In: Aguilar J-P, Legendre S, Michaux J, eds. Actes du colloque international de biostratigraphie BiochroM’97. Mémoires et Travaux de l’EPHE 21. Montpellier: Ecole Pratique des Hautes Etudes, Institut de Montpellier, 769–805. Butler PM. 1946. The evolution of carnassial dentitions in the Mammalia. Proceedings of the Zoological Society of London 116: 198–220. Carbone C, Mace GM, Roberts SC, Macdonald DW. 1999. Energetic constraints on the diet of terrestrial carnivores. Nature 402: 286–288. Chew AE. 2009. Paleoecology of the early Eocene Willwood mammal fauna from the central Bighorn Basin, Wyoming. Paleobiology 35: 13–31. Collinson ME, Fowler K, Boutler MC. 1981. Floristic changes indicate a cooling climate in the Eocene of southern England. Nature 291: 315–317. Crochet J-Y. 1988. Le plus ancien Créodonte africain: Koholia atlasense nov. gen., nov. sp. (Eocène inférieur d’El Kohol, Atlas saharien, Algérie). Comptes Rendus de l’Académie des Sciences, Paris 307: 1795–1798. Crochet J-Y. 1991. A propos de quelques Créodontes proviverrinés de l’Eocène supérieur du Sud de la France. Neues Jahrbuch für Geologie und Paleontologie Abhandlungen 182: 99–115. Danilo L, Remy JA, Vianey-Liaud M, Marandat B, Sudre J, Lihoreau F. 2013. A new Eocene locality in southern France sheds light on the basal radiation of Palaeotheriidae (Mammalia, Perissodactyla, Equoidea). Journal of Vertebrate Paleontology 33: 195–215. Denison RH. 1938. The broad-skulled Pseudocreodi. Annals of the New York Academy of Sciences 37: 163–257. Depéret C. 1910. Études sur la famille des Lophiodontidés. Bulletin de la Société Géologique de France 4: 558–567. Duprat M. 1997. Les faciès à mammifères (MP 6 à MP16)

dans le Nord-Est du Bassin de Paris (France): argumentation du modèle tectono-sédimentaire des dépôts paléogènes. In: Aguilar J-P, Legendre S, Michaux J, eds. Actes du colloque international de biostratigraphie BiochroM’97. Mémoires et Travaux de l’EPHE 21. Montpellier: Ecole Pratique des Hautes Etudes, Institut de Montpellier, 315–336. Egi N. 2001. Body mass estimates in extinct mammals from limb bones dimensions: the case of North American hyaenodontids. Palaeontology 44: 497–528. Egi N, Holroyd PA, Tsubamoto T, Soe AN, Takai M, Ciochon RL. 2005. Proviverrine hyaenodontids (Creodonta, Mammalia) from the Eocene of Myanmar and a phylogenetic of the proviverrines from the para-Tethys area. Journal of Systematic Paleontology 34: 337–358. Escarguel G. 1999. Les rongeurs de l’Éocène inférieur et moyen d’Europe occidentale. Systématique, phylogénie, biochronologie et paléobiogéographie des niveaux-repères MP7 à MP14. Palaeovertebrata 28: 89–351. Escarguel G, Marandat B, Legendre S. 1997. Sur l’âge numérique de quelques faunes de Mammifères de l’Éocène inférieur et moyen d’Europe occidentale. In: Aguilar J-P, Legendre S, Michaux J, eds. Actes du colloque international de biostratigraphie BiochroM’97. Mémoires et Travaux de l’EPHE 21. Montpellier: Ecole Pratique des Hautes Etudes, Institut de Montpellier, 443–460. Estravís C. 2000. Nuevos mamíferos del Eoceno Inferior de Silveirinha (Baixo Mondego, Portugal). Coloquios de Paleontología 51: 281–311. Filhol H. 1873. Sur les vertébrés fossiles des dépôts de phosphate de chaux de Quercy. Bulletin de la Société Philomatique de Paris 10: 85–89. Filhol H. 1880. Note sur des mammifères fossiles nouveaux provenant des phosphorites du Quercy. Bulletin de la Société Philomatique de Paris 7: 120–126. Franzen JL. 2003. Mammalian faunal turnover in the Eocene of central Europe. Geological Society of America Special Papers 369: 455–461. Gheerbrant E. 1995. Les mammifères paléocènes du Bassin d’Ouarzazate (Maroc) III. Adapisoriculidae et autres mammifères (Carnivora, ?Creodonta, Condylarthra, ?Ungulata et incertae sedis). Palaeontographica Abteilung A 237: 39– 132. Gheerbrant E, Iarochene M, Amaghzaz M, Bouya B. 2006. Early African hyaenodontid mammals and their bearing on the origin of the Creodonta. Geological Magazine 134: 475– 489. Gingerich PD. 1990. Prediction of body mass in mammalian species from the long bone lengths and diameters. Contributions from the Museum of Paleontology 28: 79–92. Gingerich PD, Deutsch HA. 1989. Systematics and evolution of Early Eocene Hyaenodontidae. Mammalia, Creodonta) in the Clarks Fork Basin, Wyoming. Contributions from the Museum of Paleontology 27: 327–391. Ginsburg L. 1999. Order Carnivora. In: Rössner GE, Heissig K, eds. The Miocene land mammals of Europe. München: Friedrich Pfeil, 109–148. Ginsburg L, Arques J, Broin F, Le Calvez Y, Mouton J, Obert D, Privé-Gill C, Rougan J. 1977. Découverte d’une


EVOLUTION OF THE PROVIVERRINAE faune de mammifères dans le Lutétien supérieur de La Défense, à Puteaux, près Paris (Hauts-de-Seine). Comptes Rendus de la Société Géologique de France 6: 311–313. Godinot M. 1981. Les mammifères de Rians (Éocène inférieur, Provence). Palaeovertebrata 10: 43–126. Godinot M, Crochet J-Y, Hartenberger J-L, LangeBadré B, Russel DE, Sigé B. 1987. Nouvelles données sur les mammifères de La Palette (Éocène inférieur, Provence). Münchner Geowissenschaftliche Abhandlungen A Geologie und Paläontologie 10: 273–288. Goloboff PA, Farris JS, Nixon KC. 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 774–786. Gradstein FM, Ogg JG, Schmitz M, Ogg G. 2012. The geologic time scale 2012, 2-volume set. Amsterdam: Elsevier. Grohé C, Morlo M, Chaimanee Y, Blondel C, Coster P, Valentin X, Salem M, Bilal A, Jaeger J-J, Brunet M. 2012. New Apterodontinae (Hyaenodontida) from the Eocene locality of Dur At-Talah (Libya): systematic, paleoecological and phylogenetical implications. PLoS ONE 7: e49054. Gruas-Cavagnetto C. 1992. Pollens et dinophycées de l’Ilerdien moyen (Eocène inférieur) de Fordones (Corbières, France). Cahiers de Micropaléontologie 6: 51–66. Gunnell GF. 1998. Creodonta. In: Janis CM, Scott KM, Jacobs LL, eds. Evolution of tertiary mammals of North America. Volume 1: terrestrial carnivores, ungulates, and ungulatelike mammals. Cambridge: Cambridge University Press, 91– 109. Gunnell GF, Gingerich PD. 1991. Systematics and evolution of Late Paleocene and Early Eocene Oxyaenidae (Mammalia, Creodonta) in the Clark’s Fork Basin, Wyoming. Contributions from the Museum of Paleontology 28: 141– 180. Holliday JA, Steppan SJ. 2004. Evolution of hypercarnivory: the effect of specialization on morphological and taxonomic diversity. Paleobiology 30: 108–128. Hooker JJ. 1996. Mammalian biostratigraphy across the Paleocene-Eocene boundary in the Paris, London and Belgian basins. In: Knox RW, Dunay RE, eds. Correlation of the Early Paleogene in Northwest Europe. Oxford, UK: Geological Society Publication, The Alden Press, 205–218. Hooker JJ. 1998. Mammalian faunal change across the Paleocene-Eocene transition in Europe. In: Aubry M-P, Lucas SG, Berggren WA, eds. Late Paleocene-Early Eocene climatic and biotic events in the marine and terrestrial records. New York: Columbia University Press, 419–441. Hooker JJ. 2010. The mammal fauna of the early Eocene Blackheath Formation of Abbey Wood, London. Monograph of the Palaeontographical Society, London 165: 1–162. ICZN. 1999. International code of zoological nomenclature, 4th edn. London: International Trust for Zoological Nomenclature. Lange-Badré B. 1979. Les créodontes (Mammalia) d’Europe occidentale de l’Éocène supérieur à l’Oligocène supérieur. Mémoires du Muséum National d’Histoire Naturelle 42: 1–249. Lange-Badré B. 1981. Les créodontes (Mammalia) de Bouxwiller (Bas-Rhin). Annales de Paléontologie, Vertébrés 67: 21–35.

915

Lange-Badré B, Haubold H. 1990. Les créodontes (mammifères) du gisement de Geiseltal (Éocène moyen, RDA). Geobios 23: 607–637. Lange-Badré B, Mathis C. 1992. Données nouvelles sur les Créodontes proviverrinés des zones MP 16 et MP 17 des phosphorites du Quercy. Bulletin du Muséum national d’histoire naturelle Section C 14: 161–184. Laurain M, Barta L, Bolin C, Guernet C, Gruas C, Louis P, Perreau M, Riveline J, Thiry M. 1983. Le sondage et la coupe du Mont Bernon à Epernay (Marne). Étude sédimentologique et paléontologique du stratotype du Sparnacien et de la série éocène. Géologie de la France 3: 235–253. Laurent Y, Adnet S, Bourdon E, Corbalan D, Danilo L, Duffaud S, Fleury G, Garcia G, Godinot M, Le Roux G, Maisonnave C, Métais G, Mourer-Chauviré C, Presseq B, Sigé B, Solé F. 2010. La Borie (Saint- Papoul, Aude): un gisement exceptionnel dans l’Éocène basal du Sud de la France. Bulletin de la Société d’Histoire Naturelle de Toulouse 146: 89–103. Leidy J. 1869. On the extinct Mammalia of Dakota and Nebraska: including an account of some allied forms from other localities, together with a synopsis of the mammalian remains of North America. Journal of the Academy of Natural Sciences Philadelphia 7: 1–472. Leidy J. 1871. Remains of extinct mammals from Wyoming. Proceedings of the Academy of Natural Sciences Philadelphia 1871: 113–116. Lemoine V. 1880. Sur les ossements fossiles des terrains tertiaires inférieurs des environs de Reims. Comptes Rendus de l’Association Française pour l’Avancement des Sciences, Congrès de Montpellier 1879: 585–594. Lemoine V. 1891. Étude d’ensemble sur les dents des mammifères fossiles des environs de Reims. Bulletin de la Société Géologique de France Série 3: 263–290. Lemoine V, Aumonier X. 1881. Terrains tertiaires des environs de Reims. Comptes Rendus de l’Association Française pour l’Avancement des Sciences, Congrès de Reims 1880: 605– 619. Lewis ME, Morlo M. 2010. Creodonta. In: Werdelin L, Sanders W, eds. Cenozoic mammals of Africa. Berkeley, CA: University of California Press, 543–560. Lillegraven J. 1969. Latest Cretaceous mammals of upper part of Edmonton Formation of Alberta, Canada, and review of marsupial-placental dichotomy in mammalian Edmonton. University of Kansas Paleontological Contributions 50: 1–122. Linnaeus C. 1758. Systema Naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Editio decima, reformata. Holmiae: Laurentius Salvius. ii, 824 pp. Marandat B. 1997. La disparité des faunes mammaliennes du niveau MP7 (Éocène inférieur) des domaines péri-mésogéens et nordique. Investigation d’un provincialisme intra-européen. Newsletters on Stratigraphy 35: 63– 82. Marandat B, Adnet S, Marivaux L, Martinez A, VianeyLiaud M, Tabuce R. 2012. A new mammalian fauna from


916

F. SOLÉ ET AL.

the earliest Eocene (Ilerdian) of the Corbières (Southern France): palaeobiogeographical implications. Swiss Journal of Geosciences 105: 417–434. Martin R. 1906. Revision der obereocaenen und unteroligocaenen Creodonten Europas. Revue Suisse de Zoologie 14: 405– 600. Mathis C. 1985. Contribution à la connaissance des Mammifères de Robiac (Éocène supérieur): Creodonta et Carnivora. Bulletin du Muséum National d’Histoire Naturelle 7: 305– 326. Matthes HW. 1952. Die Creodontier aus der mitteleozänen Braunkohle des Geiseltales. Hallesches Jahrbuch für Mitteldeutsche Erdgeschicht 1: 201–240. Matthes HW. 1967. Erstmaliger Nachweis eines Vertreters der Oxyaeninae Trouessart 1885 (Creodonta) in Europa. Geologie Jahrbuhr 16: 452–456. Matthew WD. 1909. The Carnivora and Insectivora of the Bridger Basin, middle Eocene. Memoirs of the American Museum of Natural History 9: 289–567. Matthew WD, Granger W. 1925. New Mammals from the Irdin Manha Eocene of Mongolia. American Museum Novitates 198: 1–10. Merriam CH. 1888. Description of a new fox from southern California. Proceedings of the Biological Society of Washington 4: 135–138. Morlo M. 1999. Niche structure and evolution in creodont (Mammalia) faunas of the European and North American Eocene. Geobios 32: 297–305. Morlo M, Bastl K, Wenhao W, Schaal SFK. 2014. The first species of Sinopa (Hyaenodontida, Mammalia) from outside of North America: implications for the history of the genus in the Eocene of Asia and North America. Palaeontology 57: 111–125. Morlo M, Gunnell G, Nagel D. 2010. Ecomorphological analysis of carnivore guilds in the Eocene through Miocene of Laurasia. In: Goswami A, Friscia A, eds. New contributions to the natural history of Carnivora. Cambridge, UK: Cambridge University Press, 269–310. Morlo M, Gunnell GF. 2003. Small limnocyonines (Hyaenodontidae, Mammalia) from the Bridgerian Middle Eocene of Wyoming: Thinocyon, Prolimnocyon, and Iridodon, new genus. Contributions from the Museum of Paleontology 31: 43–78. Morlo M, Habersetzer J. 1999. The Hyaenodontidae (Creodonta, Mammalia) from the lower Middle Eocene (MP 11) of Messel (Germany) with special remarks on new x-ray methods. Courier Forschungsinstitut Senckenberg 216: 31– 73. Neal JE. 1996. A summary of Paleogene sequence stratigraphy in northwest European and the North Sea. In: Knox RW, Dunay RE, eds. Correlation of the Early Paleogene in Northwest Europe. Osney Mead, Oxford, UK: Geological Society Publication, The Alden Press, 15–42. Nixon KC. 1999. Winclada (BETA) v. 0.9.9. Published by the author, Ithaca, NY. Ogg JG, Lugowski A. 2013. TS creator – visualization of enhanced Geologic Time Scale 2012 database. Available at: http:// www.tscreator.org

Owen R. 1837. Teeth. In: Todd RB, ed. The cyclopaedia of anatomy and physiology. Vol. 4. London, UK: Sherwood, Gilbert, and Piper, 864–935. Peigné S, Morlo M, Chaimanee Y, Ducrocq S, Tun ST, Jaeger J-J. 2007. New discoveries of hyaenodontids (Creodonta, Mammalia) from the Pondaung Formation, Middle Eocene, Myanmar – paleobiogeographic implications. Geodiversitas 29: 441–458. Pilgrim GE. 1932. The fossil Carnivora of India. Memoirs of the Geological Survey of India, Palaeontologia indica 18: 1–232. Plaziat JC. 1981. Late Cretaceous to late Eocene paleogeographic evolution of southwest Europe. Palaeogeography, Palaeoclimatology, Paleoecology 36: 263– 320. Polly PD. 1994. What if anything is a creodont? Journal of Vertebrate Paleontology 14 (Supplement): 42A. Polly PD. 1996. The skeleton of Gazinocyon vulpeculus gen. et comb. nov. and the cladistic relationships of Hyaenodontidae (Eutheria, Mammalia). Journal of Vertebrate Paleontology 16: 303–319. Polly PD, Lange-Badré B. 1993. A new genus Eurotherium (Mammalia, Creodonta) in reference to taxonomic problems with some hyaenodontids from Eurasia. Comptes Rendus de l’Académie des Sciences, Série II 317: 991–996. Rich THV. 1971. Deltatheridia, Carnivora, and Condylarthra (Mammalia) of the Early Eocene, Paris Basin, France. University of California Publications in Geological Sciences 88: 1–72. Russell DE. 1975. Paleoecology of the Paleocene-Eocene transition in Europe. Contributions to Primatology 5: 28–61. Rütimeyer L. 1862. Eocaene Säugetiere aus dem Gebiet des Schweizerischen Jura. Neue Denkschriften der allgemeinen Schweizerischen Gesellschaft für die gesammten Naturwissenschaften 19: 1–98. Rütimeyer L. 1891. Die eocäne Säugethier-Welt von Egerkingen. Abhandlungen der Schweizerischen Palaeontologischen Gesellschaft 18: 1–153. Savage RJG. 1965. Fossil mammals of Africa: 19. The Miocene Carnivora of East Africa. Bulletin of the British Museum of Natural History 10: 239–316. Schlosser M. 1886. Paläontologische Notizen. Über das Verhältnis der Cope’schen Creodonta zu den übrigen Fleischfressern. Morphologische Jahrbuch 12: 287–294. Smith T, Rana RS, Missiaen P, Rose KD, Sahni A, Singh H, Singh L. 2007. High bat (Chiroptera) diversity in the Early Eocene of India. Naturwissenchaften 94: 1003–1009. Smith T, Smith R. 2001. The creodonts (Mammalia, Ferae) from the Paleocene-Eocene transition in Belgium (Tienen Formation, MP7). Belgian Journal of Zoology 131: 117–135. Solé F. 2013. New proviverrine genus from the Early Eocene of Europe and the first phylogeny of Late Paleocene-Middle Eocene hyaenodontidans (Mammalia). Journal of Systematic Paleontology 11: 375–398. Solé F. 2014. New carnivoraforms from the early Eocene of Europe and their bearing on the evolution of the Carnivoraformes. Palaeontology. doi: 10.1111/pala.12097. Solé F, Gheerbrant E, Godinot M. 2011. New data on the Oxyaenidae from the Early Eocene of Europe; biostratigraphic,


EVOLUTION OF THE PROVIVERRINAE paleobiogeographic and paleoecologic implications. Palaeontologia Electronica 14: 1–41. palaeo-electronica.org/ 2011_2/258/index.html. Solé F, Gheerbrant E, Godinot M. 2013a. The Sinopaninae and Arfianinae (Hyaenodontida, Mammalia) from the Early Eocene of Europe and Asia; evidence for dispersals in Laurasia around the P/E boundary and for an unnoticed faunal turnover in Europe. Geobios 46: 313–327. Solé F, Lhuillier J, Adaci M, Bensalah M, Mahboubi M, Tabuce R. 2013b. The hyaenodontids from the Gour Lazib area (?Early Eocene, Algeria): implications concerning the systematics and the origin of the Hyainailourinae. Journal of Systematic Paleontology. doi: 10.1080/ 14772019.2013.795196. Sudre J, Erfurt J. 1996. Les artiodactyles du gisement yprésien terminal de Prémontré (Aisne, France). Palaeovertebrata 25: 391–414. Szalay FS. 1967. The affinities of Apterodon (Mammalia, Deltatheridia, Hyaenodontidae). American Museum Novitates 2293: 1–17. Teilhard P. 1921. Les mammifères de l’Éocène inférieur français et leurs gisements. Annales de Paléontologie 11: 1–108. Van Valen L. 1965. Some European Proviverrini (Mammalia, Deltatheridia). Palaeontology 8: 638–665. Van Valen L. 1966. Deltatheridia, a new order of mammals. Bulletin of the American Museum of Natural History 132: 1–126. Van Valen L. 1969. Evolution of dental growth and adaptation in mammalian carnivores. Evolution 23: 96–117. Van Valkenburgh B. 1988. Trophic diversity in past and present guilds of large predatory mammals. Paleobiology 14: 155– 173. Van Valkenburgh B. 1990. Skeletal and dental predictors of body mass in carnivores. In: Damuth J, MacFadden BJ, eds. Body size in mammalian paleobiology: estimation and biological implication. Cambridge: Cambridge University Press, 181–205.

917

Van Valkenburgh B. 1999. Major patterns in the history of carnivorous mammals. Annual Review of Earth and Planetary Sciences 27: 463–493. Van Valkenburgh B. 2007. Déjà vu: the evolution of feeding morphologies in the Carnivora. Integrative and Comparative Biology 47: 147–161. Van Valkenburgh B, Wang XM, Damuth J. 2004. Cope’s rule, hypercarnivory and extinction in North American canids. Science 306: 101–104. Wang X, Tedford R, Taylor BE. 1999. Phylogenetic systematics of the Borophaginae (Carnivora: Canidae). Bulletin of the American Museum of Natural History 243: 1–391. Werdelin L. 1989. Constraint and adaptation in the bonecracking canid Osteoborus (Mammalia, Canidae). Paleobiology 15: 387–401. Wible JR, Rougier GW, Novacek MJ, Asher RJ. 2009. The eutherian mammal Maelestes gobiensis from the late Cretaceous of Mongolia and the phylogeny of Cretaceous Eutheria. Bulletin of the American Museum of Natural History 327: 1–123. Wing SL, Bao H, Koch PL. 1999. An early Eocene cool period? Evidence for continental cooling during the warmest part of the Cenozoic. In: Hibert BT, MacLeod KG, Wing SL, eds. Warm climates in earth history. Cambridge: Cambridge University Press, 197–237. Woodburne MO, Gunnell GF, Stucky RK. 2009. Climate directly influences Eocene mammal fauna dynamics in North America. Proceedings of the National Academy of Sciences, USA 106: 13399–13403. Wortman JL. 1902. Studies of Eocene Mammalia in the Marsh collection, Peabody Museum. Part I. Carnivora. Paper 7. American Journal of Science 13: 197–206. Zachos J, Dickens GR, Richard EZ. 2008. An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics. Nature 451: 279–283. Zachos J, Pagani M, Sloan L, Thomas E, Billups K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to Present. Science 292: 686–693.

SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Appendix Appendix Appendix Appendix

S1. S2. S3. S4.

Reference material and literature used for comparison. Characters. Data matrix. Data for the stratocladistic analysis.
