A new peculiar species of the subterranean rodent Ctenomys (Rodentia, Ctenomyidae) from the Holocene of central Argentina

Journal Pre-proof A new peculiar species of the subterranean rodent Ctenomys (Rodentia, Ctenomyidae) from the Holocene of central Argentina Nahuel A. De Santi, Diego H. Verzi, A. Itatí Olivares, Pedro Piñero, Cecilia C. Morgan, Matías E. Medina, Diego E. Rivero, Eduardo P. Tonni PII:

S0895-9811(20)30012-2

DOI:

https://doi.org/10.1016/j.jsames.2020.102499

Reference:

SAMES 102499

To appear in:

Journal of South American Earth Sciences

Received Date: 4 December 2019 Revised Date:

8 January 2020

Accepted Date: 11 January 2020

Please cite this article as: De Santi, N.A., Verzi, D.H., Olivares, A.I., Piñero, P., Morgan, C.C., Medina, M.E., Rivero, D.E., Tonni, E.P., A new peculiar species of the subterranean rodent Ctenomys (Rodentia, Ctenomyidae) from the Holocene of central Argentina, Journal of South American Earth Sciences, https://doi.org/10.1016/j.jsames.2020.102499. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Elsevier Ltd. All rights reserved.

CRedit Author Statement Nahuel A. De Santi: Conceptualizacion, Formal analysis, Writing – Original Draft, Writing – Review and Editing, Visualization. Diego H. Verzi: Conceptualizacion, Writing – Original Draft, Writing – Review and Editing, Project administration. A. Itatí Olivares: Conceptualizacion, Formal analysis, Writing – Review and Editing, Visualization. Pedro Piñero: Writing – Original Draft, Visualization. Cecilia C. Morgan: Writing – Original Draft, Writing – Review and Editing. Matías E. Medina: Resources, Writing – Original Draft, Data Curation. Diego E. Rivero: Resources, Data Curation. Eduardo P. Tonni: Resources.

A new peculiar species of the subterranean rodent Ctenomys (Rodentia, Ctenomyidae) from the Holocene of central Argentina Nahuel A. De Santia, *, Diego H. Verzia, A. Itatí Olivaresa, Pedro Piñeroa, Cecilia C. Morgana, Matías E. Medinab, Diego E. Riveroc, Eduardo P. Tonnid a

Sección Mastozoología, Museo de La Plata, Facultad de Ciencias Naturales y Museo,

Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires,

Argentina,

CONICET,

e-mail:

[email protected];

[email protected]; [email protected]; [email protected] b

División Arqueología, Museo de La Plata, Facultad de Ciencias Naturales y Museo,

Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina, CONICET, e-mail: [email protected] c

Instituto de Estudios Histórico/Centro de Estudios Históricos “Prof. Carlos S. A. Segreti” y

Facultad de Filosofía y Humanidades, Universidad Nacional de Córdoba, Corro 308, 5000 Córdoba, Argentina, CONICET, e-mail: [email protected] d

División Paleontología Vertebrados, Museo de La Plata, Facultad de Ciencias Naturales y

Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina, e-mail: [email protected] *

Corresponding author. Sección Mastozoología, Museo de La Plata, Facultad de Ciencias

Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina. E-mail address: [email protected]

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Abstract The subterranean rodent Ctenomys is the single living representative of the family Ctenomyidae, and the most diverse genus within Hystricomorpha. Its fossil record begins in the late Pliocene and shows an increase in diversity since the Pleistocene. Here we describe a new middle-sized Ctenomys species from a large cranial sample collected at the archaeological site Quebrada del Real 1 in the high plains of the Pampa de Achala (Córdoba, Argentina). For this goal, we analyzed the cranial and mandibular shape variation through a geometric morphometric approach, and performed a comparative morphological analysis in the context of the living Ctenomys. The new species is characterized by having a wide rostrum with a deep rostral fossa, strong temporal fossa in the frontal, upper incisors strongly procumbent and with grooved enamel, and mandible with low corpus, long procumbent diastema and descending masseteric crest. A phylogenetic analysis demonstrated its close affinity with Ctenomys osvaldoreigi, an extant species from a nearby area. The new species represents the first notice of an extinct Ctenomys species from the Holocene. Given its peculiar morphology, the extinction of this species would have resulted in significant loss of morphological diversity, thus constraining the current boundaries of variation of the genus. The last record of the new species occurs in a period characterized by marked extinction of small mammals in southern South America mainly due to anthropic causes. Keywords: Ctenomys, Phylogeny, Geometric morphometrics, Holocene, Pampa de Achala

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1. Introduction Ctenomyidae is a family of hystricomorph rodents endemic to southern South America, represented in the living fauna only by the highly polytypic subterranean genus Ctenomys (Bidau, 2015; Freitas, 2016). The oldest fossils of the family are recorded in the late Oligocene-early Miocene of southern Peru, eastern Bolivia and southern Argentina (Lavocat, 1976; Shockey et al., 2009; Verzi et al., 2014, 2016). Nevertheless, the differentiation of the clade did not take place until the late Miocene, when several extinct genera with dental morphology similar to that of extant species (i.e. rootless molars with simplified, crescent-shaped occlusal morphology) are recorded in central and western Argentina (Reig et al., 1990; Verzi et al., 2014). This stage of differentiation of the clade Ctenomyidae involves the rise of lineages with disparate specializations for digging and subterranean life (Verzi, 2008). The only survivor of these modern lineages, Ctenomys, is recognized in the fossil record since the late Pliocene, although its origin, by split from its sister group, might be previous (Verzi, 2008; Verzi et al., 2010a). Ctenomys underwent strong cladogenesis that gave rise to over 70 extant species (Azurduy, 2005; Gardner et al., 2014; Patton et al., 2015) and an undetermined number of extinct ones (Mones, 1986 and literature therein; Verzi et al., 2004, 2010a; Azurduy, 2005; Lucero et al., 2008). This high rate of speciation is unique among family-level caviomorph clades (Álvarez et al., 2017). Accordingly, the genus is not only highly diverse in the living fauna, but also rich in the fossil record, especially since the Pleistocene. Whereas the Pliocene-middle Pleistocene fossils represent extinct species (Rusconi, 1931; Verzi et al., 2004 and literature therein; Verzi et al., 2010a), those described from latest Pleistocene-Holocene paleontological and archaeological sites correspond to extant species (e.g. Bárcena et al., 1985; Pardiñas, 2001; Quintana, 2004; Chan et al., 2005; Hadler et al., 2008; De Santi et al., 2018). Although this 3

could reflect the existence of a temporal pattern underlying the origin of living species, there could also be a bias due to poor knowledge of the paleontological and archaeological record of the genus. Indeed, at least part of the numerous materials recovered from the latest Pleistocene-Holocene, and not yet studied at the species level, could represent undescribed extinct species (e.g. Salemme and Tonni, 1983; Bonomo and Massigoge, 2004; Martín and San Román, 2010; Fernández et al., 2011, 2016; Medina et al., 2011; Salemme et al., 2012; Luna and Cruz, 2014; López et al., 2016; Tammone et al., 2017). During the Holocene, mammals experienced severe extinction due to climatic and/or anthropic causes (Turvey and Fritz, 2011; Teta et al., 2014); thus, it would be expected that Ctenomys populations, which are vulnerable due to some of their distinctive ecological features linked to the subterranean niche, may also have undergone extinction during this epoch. In this work we present an extensive sample of Ctenomys from the archaeological site Quebrada del Real 1 (QR1), located in the hilly region of central Argentina (Rivero et al., 2008; Rivero, 2009). The materials were recovered from middle-late Holocene levels and correspond to a recently extinct population. The new materials are described and compared to an exhaustive sample of extant species in order to test whether they correspond to any of the latter or, on the contrary, they represent a new extinct species. We also discuss the evolutionary information provided by these new materials.

2. Geographic and stratigraphic setting The archeological site Quebrada del Real 1 is a rock cave located in the high plains of the Pampa de Achala (31° 40.330′ S, 64° 53.538′ W; Córdoba Province, Argentina) at an altitude of 1914 m.a.s.l. (Rivero et al., 2008; Rivero, 2009) (Fig. 1). The locality is surrounded by rocky outcrops, deep ravines and extensive meadows belonging to the upper 4

Sierras Grandes mountain range (Luti et al., 1979; Giorgis et al., 2011). From a zoogeographical viewpoint, the site is included in the Subandean District of the AndeanPatagonian Subregion and presents a faunal discontinuity with the rest of the province (Ringuelet, 1961). Three overlapping cultural components (C1 to C3) were detected during the archaeological excavation of the site, showing long-term human occupation from ca. 7400 BP to the late Holocene. The Lower Component (C1) assemblage is associated to lanceolate-shaped projectile points and charcoal dated at 5980 ± 50 years BP (LP-2133) and 7360 ± 120 BP (LP-2339). The Middle Component (C2) is dated at 2950 ± 90 BP (LP2042; charcoal). Finally, the Upper Component (C3) contains small-stemmed triangular arrow-points and pottery fragments that were temporally assigned to the Late Prehispanic Period (1500-360 BP), even before having radiocarbon dates (Rivero, 2009). In general, the evidence suggests that QR1 was used throughout the Holocene as a short-term camp to process and consume prey such as the Ctenomys analyzed here, but also guanaco (Lama guanicoe), pampas deer (Ozotoceros bezoarticus) and other small rodents including Holochilus vulpinus, Galea leucoblephara and Microcavia sp. (Rivero et al., 2008; Rivero, 2009; Medina et al., 2011, 2012; Buc et al., 2016). A high proportion of the Ctenomys specimens recovered from the site showed signs of cutting, scratching and burning (Medina et al., 2011). The environment at the site has not remained static over the entire time span it was occupied. Palaeoclimatic information indicates that the mountain environment that existed during the Pleistocene-Holocene transition (11000-9000 years BP) was different from the present one. Grasslands were more extensive due to the cold and dry climate conditions, connecting the high-plain to the lowland grasslands, precordilleran and cordilleran zones of central and northwestern Argentina (Adams and Faure, 1997; Carignano, 1999; Sanabria 5

and Argüello, 2003; Piovano et al., 2009; Andreazzini et al., 2013; Krapovickas and Tauber, 2016). This allowed the distributional drift of several species over these neighboring regions. The progressive onset of subtropical conditions since 8000-6000 BP redefined the landscape with the formation of the modern Sierra Chaco vegetation belt ca. 3000 BP and the biogeographical isolation of plant and animal biota above 1,500 m, with little fluctuation during the last 1000 years (Carignano, 1999; Cioccale, 1999; Sanabria and Argüello, 2003; Teta et al., 2005; Silva et al., 2011; Andreazzini et al., 2013; Yanes et al., 2014; Krapovickas and Tauber, 2016). Thus, the upper mountain grassland range where QR1 is located is defined as a "faunistic island" surrounded by Chacoan environments, providing geographical isolation to endemic species (Ringuelet, 1961; Cei, 1972; Bucher and Abalos, 1979; Polop, 1989; Cabido et al., 1998).

Fig. 1. Location map of Quebrada del Real 1 site (black triangle) and Ctenomys osvaldoreigi type locality (white triangle), both in Córdoba Province, Argentina. [planned for 1.5 column]

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3. Material and methods The Ctenomys sample from QR1 includes 1173 specimens (see Appendix A1). Only one of the skull fragments corresponds to a posterior region with part of the basicranium, occiput and auditory bullae; the remaining skull materials are fragments of the rostrum or palate, and a few isolated auditory bullae; only a few remains of skull and mandible have preserved incisors and molariforms. Nomenclature of craniomandibular traits follows Hill (1935), Woods (1972), Wahlert (1974, 1985), Wible et al. (2005), Verzi (2008), and Verzi et al. (2014, 2016). The following cranial and mandibular measurements were taken for the new materials (Appendix A2): BL, basioccipital length; BW, maximum bizygomatic width; CIL, condyle incisive length; CL, condylar length; DL, diastema length; IB, depth of i1 implantation (Verzi and Olivares, 2006); IW, incisor width; LAL, lower dp4-m3 alveolar length; LZA, length of the zygomatic arch; MMW, maximum mandibular width; MWm3, maximum width m3; PROC, upper incisor procumbency as expressed by Thomas’ angle (Reig et al., 1965); RW, width of the rostrum at level of premaxilla-maxilla suture; UAL, upper DP4M3 alveolar length. All measurements are expressed in millimeters and were taken using a digital caliper (0.01 mm). Upper teeth are indicated as I1, DP4, M1, M2, and M3, and lower teeth as i1, dp4, m1, m2, and m3. The new sample was compared with 676 specimens of 65 living species (Appendix A1). These materials are housed in the following collections: CBF, Colección Boliviana de Fauna, La Paz, Bolivia; CFA, Fundación de Historia Natural Félix de Azara, Buenos Aires, Argentina; CML, Colección Mamíferos Lillo, Tucumán, Argentina; FMNH, Field Museum of Natural History, Chicago, USA; MN/UFRJ, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil; IADIZA, Instituto Argentino de Investigaciones de 7

Zonas Áridas, Mendoza, Argentina; IEEUACH, Instituto de Ecología y Evolución de la Universidad Austral de Chile, Valdivia, Chile; IMCN CM, Instituto y Museo de Ciencias Naturales, San Juan, Argentina; MACN, Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina; MLP, Museo de La Plata, La Plata, Argentina; MMP Museo Municipal de Ciencias Naturales ‘Lorenzo Scaglia’, Mar del Plata, Argentina (Ma, Mastozoological colection). In addition, 7 species were compared through available photographs: C. andersoni (Gardner et al., 2014), C. bicolor (Stolz et al., 2013), C. erikacuellarae (Gardner et al., 2014), C. ibicuensis (Freitas et al., 2012), C. lami (Freitas, 2001), C. lessai (Gardner et al., 2014), and C. yatesi (Gardner et al., 2014). To assess the affinities of the QR1 sample, a combined phylogenetic analysis was performed on a dataset of 51 morphological characters and cytochrome b (cyt-b) sequences (1110 bp) obtained from GenBank. Morphological information included 23 new characters (characters 1 to 23 in Appendix A3) and 28 characters from Verzi (2008), Verzi et al. (2010a) and Olivares et al. (2012) (characters 24 to 51 in Appendix A3). Cyt-b sequences were aligned using BioEdit 7.2.0 (Hall, 1999) with the default values of gap opening and gap extension. The dataset of morphological traits was concatenated with the gene sequences, and extinct taxa were coded as missing for all molecular characters. This matrix contained a total of 51 characters and 34 taxa; the genera Thrichomys (Echimyidae), Octodontomys, Octomys (Octodontidae), †Actenomys, †Eucelophorus, and the early Pleistocene †Ctenomys chapalmalensis (Ctenomyidae) were included as outgroups (Verzi et al., 2010a). The ingroup included species of all major informally recognized Ctenomys clades, i.e. boliviensis group, Corrientes group, frater group, magellanicus group, mendocinus group, opimus group, talarum group, torquatus group, and tucumanus group (Parada et al., 2011). A parsimony analysis of the combined morphological and DNA 8

matrix was carried out treating gaps as missing data in TNT 1.1 (Goloboff et al., 2008a, 2008b). The heuristic search consisted of 1000 replicates of a Wagner tree with random addition sequence of taxa followed by TBR branch swapping. In addition, we performed an extra round of TBR on the optimal trees to increase the chance of finding all minimumlength topologies (Bertelli and Giannini, 2005). Variation in the cranial and mandibular shape of living and extinct Ctenomys was analyzed using 2D geometric morphometric techniques. For this analysis, we selected 275 skull (122) and mandible (153) fragments that were sufficiently complete, as well as 593 skulls and 517 mandibles belonging to subadult and adult individuals of 65 living Ctenomys species (see Appendix A1 for details). Two-dimensional coordinates were captured from digital images of the ventral view of the anterior portion of the cranium, i.e. palate, and the lateral view of the mandible. These views were selected as the most informative in terms of the state of preservation of the extinct sample. Eleven landmarks and four semilandmarks were used to capture palate shape (Appendix A4), and thirteen landmarks and twenty-three semilandmarks were selected in the lateral view of the mandible (Appendix A5). Landmark coordinates were digitized using tpsDig version 2.26 (Rohlf, 2016). The resulting Procrustes shape coordinates were analyzed using MorphoJ (Klingenberg, 2011) through principal component analyses (PCA). Principal components summarize and describe the major trends in shape variation among species and facilitate the visualization of shape ordination in a low-dimensional morphospace.

4. Results 4.1. Phylogeny

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The parsimony analysis based on the combined matrix resulted in a single most parsimonious tree, 1279 steps long (CI = 0.50; RI = 0.52; Fig. 2). In the recovered topology, Ctenomys QR1 clustered with the living C. osvaldoreigi, C. leucodon and C. tuconax, based on having the tip of the mastoid apophysis level with or ventral to the ventral margin of the external auditory meatus (character-state 18.1). Within this clade, Ctenomys QR1 was sister to C. osvaldoreigi, a relationship supported by having divergent anteromedial tips of the nasal bones, delimiting a space continuous with the dorsal opening of the interpremaxillary foramen (character-state 1.1), and the major palatine foramina opening in the maxilla, well rostrad to the maxilla-palatine suture (character-state 14.1).

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Fig. 2. Phylogenetic analysis. A single most parsimonious tree of combined morphological and molecular data (1279 steps in length), with bootstrap CG frequency/jackknife CG frequency values shown for each node. On the right, ventral view of cranium of Ctenomys MLP 2635 from Quebrada del Real 1 Site (QR1). [planned for 1.5 column]

4.2. Morphometric analysis 4.2.1. Palatal variation

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The morphospace delimited by the first two principal components of the aligned Procrustes Coordinates, PC1 and PC2, explained more than 40% of the total palatal shape variation in the Ctenomys sample (PC1 24.96%, PC2 17.71%; Fig. 3A). The influence of size was stronger on PC1 (25.06%, P<0.0001) than on PC2 (2.66%, P<0.0001). Ctenomys QR1 was distributed on negative scores along PC1, together with C. osvaldoreigi and C. leucodon with which it shared a relatively longer rostrum, shorter molar rows, and more posterior incisive foramina (Fig. 3A). A combination of the opposite characteristics for these morphological traits was present in the taxa located towards the positive values of this axis. The Ctenomys specimens with wider and shorter rostra, and narrower incisive foramina, were located on positive values of PC2, whereas those with the opposite traits presented negative values along this axis (Fig. 3A). These morphological differences did not separate species but rather reflected the existence of intraspecific variation, as attested by the fact that a given species was distributed along both positive and negative values on this axis. 4.2.2. Mandibular variation PC1 and PC2 explained nearly 50% of the total shape variation (PC1 34.84%, PC2 15.0%, Fig. 3B). Size explained 4.28% of mandibular shape variation along PC1 (P<0.0001) and 0.45% on PC2 (P> 0.05). Ctenomys QR1 occupied negative values along PC1 and was clearly separated from the remaining species by its longer and more procumbent diastema, shallower step anterior to the alveolus of dp4, lower coronoid process, shallower inferior sigmoid notch (i.e., the posterior border of the mandible between the condyloid process and the angular process), mandibular corpus shallow at level of dp4, and more descending masseteric crest. With the exception of C. osvaldoreigi, the living species were distributed 12

along positive PC1 values, with morphological features opposite to the ones described above. As in the morphospace of palatal shape variation, PC2 summarized intraspecific rather than interspecific variation. The main shape change observed along this axis concerned the morphology of the ramus, which was deeper toward positive values and shallower toward negative ones (Fig. 3B).

Fig. 3. Ordination of the extinct Ctenomys from Quebrada del Real 1 Site (QR 1) and 65 living Ctenomys species in the morphospace defined by the first two principal components of the aligned Procrustes coordinates (APC) of (A) cranial and (B) mandible shape variation. At top left of each scatterplot, illustrations of ventral view of anterior part of skull and lateral view of mandible showing placement of landmarks (solid dots) and semilandmarks (empty circles). Shape changes associated with positive (+) and negative (-)

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values of both axes are shown as wireframes: black dots and lines indicate shape changes with respect to the mean configuration (indicated with grey lines). [planned for 2 columns]

5. Systematic paleontology According to the results of the phylogenetic and comparative morphometric analyses, we recognize the sample from QR1 as a new species. Below we provide the formal description of this new taxon. Order Rodentia Bowdich, 1821 Suborder Hystricomorpha Brandt, 1855 Superfamily Octodontoidea Waterhouse, 1839 Family Ctenomyidae Lesson, 1842 Genus Ctenomys Blainville, 1826 Ctenomys viarapaensis sp. nov. (Figs. 4 and 5)

Holotype. MLP 2935, anterior portion of the cranium with the nasal bones, the right zygomatic arch and the occlusal portion of the right incisor (Fig. 4). Referred specimens. The holotype and 256 cranial fragments, 600 mandibular remains, and 316 incisor fragments (see Appendix A1 for details) Type locality. Quebrada del Real 1, Pampa de Achala. Age. Holocene (7360 – 360 years BP). Measurements of the holotype (in mm): LZA: 25.05; UAL: 11.42; RW: 15.09; DL: 20.16 (measurements of the sample in Table 1).

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Etymology. The specific name refers to Viarapa, the name given to the type locality, Pampa de Achala (Córdoba), during the XVI century. Diagnosis. Middle-sized species; rostrum wide, long and strongly procumbent; anterior ends of nasal bones markedly posterior to anterior end of diastema; medial margins of these anterior ends of the nasals divergent, delimiting a space consistent with the dorsal opening of the interpremaxillary foramen; rostral fossa for origin of M. masseter medialis pars anterior very deep, almost perforated in some of the larger specimens; zygomatic arch deep; anterior end of jugal markedly extended anteriorly, beyond the antorbital bar; suborbital fossa of the jugal present; strong fossa for origin of M. temporalis orbitalis in the frontal; major palatine foramina opening at level of anterior margin of M1 alveolus, well anteriad to maxillo-palatine suture; auditory bullae small, little inflated; tip of mastoid apophysis ventral to the ventral margin of external auditory meatus; mandible with low corpus and long procumbent diastema; chin process little developed; shallow step anterior to the alveolus of dp4; shallow inferior sigmoid notch; mandibular foramen near the condyle; masseteric crest descending; upper incisors strongly procumbent and with grooved enamel; bottom of upper incisor alveolar sheaths visible ventrally at level of DP4-M1; molars with cement surrounding DP4-M2 lingually and dp4-m2 labially (Figs. 4 and 5). Description. Ctenomys viarapaensis sp. nov. is a middle-sized species. The sample comprises considerable size variation; unfortunately, the characters more suitable to estimate age in Ctenomys (Verzi et al., 2010b and literature therein), in particular the condition of the basisphenoid–presphenoid suture, are not preserved. Nevertheless, the diagnostic features of the species occur throughout the sample irrespective of individual size, leading us to assume that smaller specimens correspond to juveniles. In addition, the

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sample does not show morphological differences between materials from different provenance levels. The rostrum is broad, long and markedly proclive. The interpremaxillary foramen is large and opens close to the anterior part of the incisive foramina as in C. osvaldoreigi (Figs. 4A and 6). The incisive foramina are narrow and the roots of the premaxillary septum are located dorsomedially as in C. osvaldoreigi, whereas they are horizontal in C. leucodon and C. tuconax. The bottom of the alveolar sheaths of the upper incisors are visible ventrally and located at the level of DP4-M1 (Fig. 4A). The major palatine foramina open on the maxillary at the level of the anterior margin of the M1 alveolus, well anteriad to the maxillary-palatine suture as in C. osvaldoreigi (Fig. 5B); in the other species analyzed these foramina are located more posteriorly and closer to the suture. The mesopterygoid fossa reaches the level of the M2-M3 boundary. The rostral fossa for origin of the M. masseter medialis anterior, pars infraorbitalis, is remarkably deep and almost perforated in some of the larger specimens, a feature unique within the genus (Fig. 5A). The facial portion of the lacrimal bone is subtriangular, not expanded over the frontal bone, whereas in C. osvaldoreigi, C. leucodon and C. tuconax, the lacrimal is expanded over the frontal. The first part of the nasolacrimal canal is long in C. viarapaensis because the opening of the lacrimal canal is markedly ventral with respect to the facial portion; a similar morphology is present in C. osvaldoreigi, C. leucodon and C. tuconax. A relatively small foramen for the nasolacrimal canal opens close to the alveolar sheath of the incisor, toward the sphenopalatine fissure, as in C. osvaldoreigi; in C. leucodon and C. tuconax, this foramen opens onto an unossified area between the maxillary lamina, posterior to the incisor alveolar sheath, and the margin of the sphenopalatine fissure (Fig. 5E). This maxillary lamina does not cover the antero-dorsal tip of the M1 alveolar sheath in C. 16

viarapaensis. There is a very marked fossa for the M. temporalis pars orbitalis in the posterior part of the orbit, which is unusually deep in the holotype and other large specimens of the new species (Fig. 5A). The zygomatic arch is strong and bowed; it is high, with a suborbital fossa on the dorsal margin of the jugal bone; the anterior end of the jugal is narrower and extends anterior to the level of the antorbital bar as in C. osvaldoreigi. The nasal bones are flat, not vaulted. Their anterior tips are markedly posterior to the level of the anterior end of the diastema. The medial margins of these anterior tips diverge so as to delimit a space consistent with the dorsal opening of the interpremaxillary foramen, as in C. osvaldoreigi. The auditory bullae are small, little inflated, and the jugular foramina are large (Fig. 5C); the auditory bullae are markedly narrower on the antero-external side as in C. osvaldoreigi and C. leucodon. The mastoid apophysis is long, its tip ventral to the ventral margin of the external auditory meatus (Fig. 5D). There is a large oval foramen in specimen MLP 2936. The buccinator and masticatory foramina are present in specimen MLP 2936. The upper incisors are strongly procumbent (Table 1) and bear grooves on the enameled surface (Fig. 5E and I) similar to those in C. conoveri; these grooves are more marked in larger specimens. The mandibular body is low and the diastema is long. The ‘step’ anterior to dp4 is slightly lower than in the other species analyzed. The chin process is poorly developed and little visible in lateral view, as in C. osvaldoreigi (Fig. 6). Unlike the condition in the latter species, the bottom of the alveolar sheath of dp4 does not protrude much. The dorsal portion of the masseteric fossa is larger than the ventral one. The masseteric crest is descending, unlike the remaining species analyzed that have a subhorizontal or even slightly ascending crest. The inferior sigmoid notch is shallow. The postcondyloid process 17

has a strong ventrolateral apophysis, similar to that of C. osvaldoreigi and more developed than in the remaining species analyzed. The lower incisor is deeply inserted; the bottom of its alveolar sheath and associated mandibular foramen are located near the condyle (Fig. 5F–H). As in C. osvaldoreigi, the molar crowns are partially covered by cement, on the lingual side of DP4-M2 and the labial side of dp4-m2 (Fig. 5J).

Cranium

Mandible

Measurements BW BL LZA UAL RW DL IW PROC LAL CIL MMW MWm3 CL IB

Holotype 25.05 11.42 15.09 20.16 -

Mean 30.64 9.35 22.26 10.60 11.89 17.15 8.13 115º 10.82 32.74 40.96 32.22 3.82 4.21

SD 2.91 2.02 0.61 1.28 1.78 1.31 3.22 0.64 2.33 0.47 0.50

Range 28.95 - 30.64 9.35 19.74 - 25.05 9.16 - 12.25 9.82 - 15.09 12.42 - 20.69 6.82 - 10.33 119º - 113º 9.38 - 13.28 28.97 - 38.79 40.96 32.22 2.70 - 5.04 3.10 - 5.57

N 3 1 13 138 137 139 9 3 167 167 1 1 167 158

Table 1. Cranial and mandible measurements of Ctenomys viarapaensis sp. nov. from QR1. Abbreviations shown in Material and methods.

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Fig. 4. Ctenomys viarapaensis sp. nov. MLP 2935, holotype. (A) Ventral, (B) dorsal, and (C) lateral views of cranium. Scale bar equals 10 mm. [planned for a single column]

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Fig. 5. Ctenomys viarapaensis sp. nov. (A) Lateral view of cranium MLP 2936. (B) Ventral view of cranium and detail of maxillary portion MLP 2935, holotype. (C) Ventral view, and (D) right lateral view (left inverted) of basioccipital region MLP 2948. (E) Right lateral view of cranium MLP 2942 (left inverted). (F) Right lateral view of mandible MLP 2966. (G) Medial view of left mandible MLP 2967; (H) Dorsal view of mandible MLP 2966. (I) Anterior view of incisors MLP 2949. (J) Occlusal view of right Dp4-M1 and detail of M1 MLP 2939. Abbreviations: ab, auditory bullae; am, auditory meatus; ce, cement; co, condylar process; cp, coronoid process; if, incisive foramina; ig, incisor grooves; ip, interpremaxillary foramen; i1, incisive alveolus; jf, jugular foramen; lf, lacrimal foramen; ma, mastoid apophysis; mc, masseteric crest; mf, mandibular foramen; mpf, major palatine

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foramen; M1, alveolus of M1; M2, alveolus of M2; ps, premaxillary septum; proc, upper incisor procumbency; rf, rostral fossa; sf, sphenopalatine fissure; tf, temporal fossa; va, ventrolateral apophysis of the postcondyloid process. Scale bar 10 mm except J, 1 mm. [planned for 2 columns]

Fig. 6. Ctenomys osvaldoreigi CFA 12170, holotype. (A) Ventral, (B) dorsal, and (C) lateral views of cranium. (D) Anterior view of upper incisors, (E) lateral, and (F) dorsal views of mandible. Scale bar equals 10 mm except D, 5 mm. [planned for 2 columns]

6. Discussion and conclusions The morphological and morphometric analyses suggest strong similarity between C. viarapaensis and the extant C. osvaldoreigi. Noticeably, the latter species, which is known with certainty only for its type locality, is distributed over the same geographical area as C. viarapaensis, in the Sierras Grandes of Córdoba, about 30 km northeast of the site QR1 (Fig. 1; Bidau, 2015; Freitas, 2016). Moreover, a population presumably belonging to C. osvaldoreigi has been detected in Pampa de Achala, approximately 5 km east of the site QR1 (Torres, 2018). This context suggests the possibility that C. viarapaensis may be part of the variation of C. osvaldoreigi, representing a local population whose morphological 21

distinctiveness could be a result of its adjustment to palaeoenvironmental changes during the Holocene. Variation within lineages generated by geography and time has long been recognized in the Quaternary record of rodents (Chaline, 1987; Barnosky, 1993; Martin, 1993; Barnosky and Bell, 2003; Teta and Campo, 2017). In this case, beyond the morphological similarities shared with its neighboring species, C. viarapaensis has features that clearly differentiate it from the rest of the species analyzed. In addition to its unique mandibular shape (with low corpus and long procumbent diastema, small chin process, shallow step anterior to the alveolus of dp4, and descending masseteric crest), the fossae for M. temporalis pars orbitalis and for the M. masseter medialis pars anterior of C. viarapaensis are unusually deep, and the latter includes a canal that is nearly perforated in some specimens, which would have housed some of the fibers of this muscle. This morphology is unique among the species analyzed. In addition, the enameled surface of the incisors of C. viarapaensis bears strong grooves, especially on the upper incisors; among extant species, this feature is only shared with C. conoveri (Osgood, 1946; Bidau, 2015; Teta and Ríos, 2017). Given that these traits are clearly derived with respect to the condition present in C. osvaldoreigi, the possibility that C. viarapaensis represents a chronomorph ancestral to the lineage that led to the living C. osvaldoreigi may be dismissed. Rather, we propose that C. viarapaensis resulted from cladogenetic events that would have split it from the lineage of C. osvaldoreigi during or prior to the Holocene. Although a comparative morphofunctional analysis that includes C. viarapaensis in the context of the variation of the genus is necessary, it is clear that this species presents craniomandibular and dental specializations associated to tooth-digging ability (Verzi and Olivares, 2006): (a) long cranial and mandibular diastemas; (b) strong and flaring zygomatic arches; (c) very deep fossae for the M. masseter medialis pars anterior and 22

temporalis pars orbitalis; (d) very narrow auditory bullae, especially anteriorly; (e) postcondyloid process with a strong ventrolateral apophysis; (f) strongly procumbent upper incisors (high Thomas’ angle); (g) deeply inserted upper and lower incisors (low IB values). The strong zygomatic arches and deep fossae able to accommodate large adductor muscles, and the deeply inserted and procumbent incisors suitable for the development of high outforces at their tips and for the frontal attack to the soil, are universal specializations among subterranean rodents (Hildebrand, 1985; Lessa, 1990; Nevo, 1999; Stein, 2000; Verzi and Olivares, 2006). In addition, a strong ventrolateral apophysis of the postcondyloid process, as part of a peculiar postglenoid articular region in ctenomyids, prevents dislocation of the condyle when strong forces are exerted at the tip of the incisors during excavation; the narrower anteroexternal portion of the bulla complements the function of this postglenoid articulation (Verzi and Olivares, 2006). All these specializations are shared by living species of the genus assumed to be essentially toothdiggers (Verzi and Olivares, 2006; Verzi, 2008; Morgan et al., 2017). Moreover, although epigenetic muscle-bone interactions throughout ontogeny may influence the depth of the fossae for muscle insertion (Herring, 1993; Hallgrimsson et al., 2004, 2007; Zelditch et al., 2006), the morphology of these fossae in C. viarapaensis is unique among both living and extinct Ctenomys irrespective of their size. Thus, at least from a qualitative viewpoint, this species is clearly one of the most specialized for tooth-digging in the genus. As previously mentioned, Ctenomys is recorded since the late Pliocene (Verzi et al., 2010). The fossils from the late Pliocene-middle Pleistocene represent extinct species (Gervais and Ameghino, 1880; Ameghino, 1902; Rusconi, 1930, 1931; Mones and Castiglioni, 1979; Frailey et al., 1980; Verzi et al., 2004; Azurduy, 2005) whereas those described from latest Pleistocene-Holocene paleontological and archaeological deposits 23

correspond to species of the living fauna (e.g. Pardiñas, 2001; Quintana, 2004; Chan et al., 2005; Hadler et al., 2008; De Santi et al., 2018). This pattern could be reflecting the existence of a minimum age for the first appearances of the extant representatives of the genus. Nevertheless, even accepting this hypothesis, extinction would also be expected to occur during this lapse, and this should be reflected in the paleontological and archaeological record of that time. Ctenomys populations are vulnerable to extinction on account of some of their distinctive ecological features, such as patchy distribution, limited vagility, and small effective numbers (Reig et al., 1990). In support of the latter, a Holocene decrease of effective population size through local extinction has been detected for the extant species C. sociabilis due to environmental, non-anthropogenic factors (Chan et al., 2005, 2006, Tammone et al., 2016, 2018). In the last 500 years BP, the extinction of small mammals in southern South America would have accelerated due to anthropic causes (Teta et al., 2014). The extinction of C. viarapaensis could be part of this scenario, as supported by the extensive evidence of processing and consumption recorded in the sample (Medina et al., 2011). C. viarapaensis represents the first record of an extinct Ctenomys species in the Holocene. Given its peculiar morphology, the extinction of this species would have resulted in a significant loss of morphological diversity constraining the boundaries of the current variation of the genus. The scarcity of studies on Ctenomys materials recovered from Holocene sites suggests that this information provided by C. viarapaensis may not be the exception, but rather an example of the bias in the knowledge of the morphological variation represented in the record of this lapse. New studies of the abundant material recovered from Holocene paleontological and archaeological sites are necessary to

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understand the role played by late extinction in the configuration of the current morphological diversity of Ctenomys.

Acknowledgements We thank MA Reguero, P Teta, A Martinelli, M Ezcurra, L Chornogubsky, G D’Elía, M Díaz, S Bogan, MI Rosi, J Oliveira, S Giannoni and J Vargas Mattos; A Álvarez for kindly providing photographs of specimens from FMNH. We acknowledge the critical comments and suggestions of FJ Fernández and two anonymous reviewers which improved the manuscript. This research was supported by Agencia Nacional de Promoción Científica y Tecnológica PICT 2016-2881.

Appendix A. Supplementary data Supplementary data related to this article can be found at

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APPENDIX A

A new peculiar species of the subterranean rodent Ctenomys (Rodentia, Ctenomyidae) from the Holocene of central Argentina Nahuel A. De Santi a, b, *, Diego H. Verzia, b, A. Itatí Olivares a, b, Pedro Piñero a, b, Cecilia C. Morgan a, b, Matías E. Medina b, c, Diego E. Rivero b, d, Eduardo P. Tonnib, e a

Sección Mastozoología, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina b

CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina

c

División Arqueología, Museo de La Plata, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina d

Instituto de Estudios Históricos/Centro de Estudios Históricos “Prof. Carlos S. A. Segreti” y Facultad de Filosofía y Humanidades, Universidad Nacional de Córdoba

e

División Paleontología Vertebrados, Museo de La Plata Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina *

Corresponding author: [email protected]

Contents: APPENDIX A1. Taxa and specimens examined. APPENDIX A2. Measurements taken for morphological analyses of the skull in Ctenomys. APPENDIX A3. Matrix of characters for Ctenomys viarapaensis nov. sp. APPENDIX A4. Definition of cranial landmarks and semilandmarks. APPENDIX A5. Definition of mandibular landmarks and semilandmarks.

APPENDIX A1. Taxa and specimens examined. Taxon Echimyidae Thrichomys apereoides Octodontidae Octodontomys gliroides

Octomys mimax

Acronym MN 42403. CML 2872, 7137, 7138, 7139, 7143; MACN 2792, 2794, 2795, 2796, 3052, 17832, 17834, 17835, 17837, 25197; MLP 25.XI.98.1; MMPMa 2532, 3557. IADIZA CM 03067, 06852, 06855; IMCN_CM 024; MACN 13674, 13770, 13773, 13675.

Ctenomyidae †Eucelophorus chapalmalensis †Actenomys priscus †Ctenomys chapalmalensis Ctenomys andersoni Ctenomys argentinus

Ctenomys australis

Ctenomys azarae Ctenomys bergi Ctenomys bicolor Ctenomys boliviensis Ctenomys bonettoi Ctenomys budini (C. frater) Ctenomys chasiquensis Ctenomys coludo Ctenomys conoveri Ctenomys colburni Ctenomys coyhaiquensis

Ctenomys dorbignyi Ctenomys dorsalis Ctenomys emilianus Ctenomys erikacuellarae Ctenomys flamarioni

MLP 91.IV.25.146, 96.III.11.1. MMP 2012-M; MMP 4225-M MACN 12681 (holotype), 19243, 19247, 19248, 19249, 19250, 19255, 19256; MMP 298-S, 356-S, 357-S, 358-S, 377-S, 444-S, 481-S, 483-S, 575-S, 601-S, 606-S, 613-S, 642-S, 646-M, 845-M, 889-M, 890-M, 891-M, 1061-M, 1214-M, 1223-M, 1225-M, 1226M, 1227-M, 1229-M, 1230-M, 1319-M, 1449-M, 1526-M, 1620-M, 1622-M, 1730-M. MSB 63387. CFA 12023; MACN 17403, 17405, 23675; MMPMa 2450, 2451, 2452, 2453, 4074. CFA 11925; MACN 19669, 19670, 19746, 20129, 20135, 20136, 20146, 20147, 20148, 20157; MLP 3.V.48.4, 3.XI.95.5, 7.XI.95.2, 7.XI.95.4, 7.XI.95.5, 7.XI.95.6, 7.XI.95.7, 10.XI.95.2, 26.IX.08.32; MMPMa 2425, I1047, I1048, I1051, I1052, I1053, I1061, I1062, I1072, I1075, I1081, I1088, I1089, I1803. CFA 11700, 11738, 11766, 11822, 11826; MLP 1.I.03.7, 5.VI.00.14, 20.V.02.7, 20.V.02.9, 30.V.01.6. CFA 11130, 11131, 11159, 11165, 11166, 11169, 11170, 11187, 11288; MACN 19650. FMNH 28357, 28358; TR 1462. MACN 50.282. CFA 11456, 11457, 11458, 11460, 11461, 11462, 11463, 11464, 11466, 11467, 11468, 11476, 11486, 11488, 12456, 12457, 12470, 12471, 12664, 12665; MMPMa C-0673. MACN 30272, 19541, 27.87, 30.274, 32.61, 30.269 [C. budini sylvanus (C. frater)]. CFA 11429, 11430; MLP 2540, 2545, 27.XII.01.62. FMNH 46137, 46138. CFA 11839. IEEUACH 4232, 4233; FMNH 124270. IEEUACH 5624, 5627, 5628, 5631, 5635, 5636, 5644, 5645, 5650; FMNH 134279. CFA 11217, 11219, 11223, 11224, 11225, 11227, 11230, 11236, 11238, 11245, 11246, 11493, 11494, 11500, 11522, 12148; MACN 23277; MMPMa 3425, 3426, 3428, 3429, 3452, 3456. FMNH 54392, 63868. MMPMa 1506, 1510. MSB63391. MLP 28.V.01.5, 28.V.01.6; MMPMa 4998, DZRS-011.

Ctenomys fodax

Ctenomys frater

Ctenomys fulvus

Ctenomys haigi

Ctenomys ibicuiensis Ctenomys johanis Ctenomys juris Ctenomys knighti Ctenomys lami

Ctenomys latro

Ctenomys lessai Ctenomys leucodon Ctenomys lewisi Ctenomys luteolus (C. opimus)

Ctenomys magellanicus

Ctenomys mendocinus

Ctenomys maulinus

Ctenomys minutus

MMPMa 3136. CBF 940, 2307; CFA 12105, 12127; CML 7235, 7241, 8472; FMNH 23241, 23242, 29051; MACN 23280. CML 430, 772, 845, 886, 964, 1163, 1395, 1916; FMNH 23218, 34916; MLP 7.X.92.1, 7.X.92.2, 7.X.92.3, 7.XI.95.10, 9.XI.95.2. CFA 11377, 12289, 12430; CML 00248, 00249, 00254, 00363; MACN 13.565, 19.053, 19.771, 23.592; MMPMa 1925; IEEUACH 1526, 1527, 1529, 1531, 1532, 1534, 1535, 1536, 1537, 1540, 1542, 1543, 1545, 1546, 1549, 343. TR 1065. CFA 12452. CFA 12115, 12116, 12124; CML 367. CML 683; MACN 27.66. TR 76. CFA 11307, 11388, 11624, 11626, 11627, 11628, 11629; CML 263, 1541, 01585; MACN 19826, 23.285, 26.143, 30.358; MLP 3.XI.95.6; MMPMa 1-87, 2426, 2428, 2999, 3187, 3188, 3189, 3190. MSB 67111. CBF 3658, 3659, 4999, 5793; FMNH 52468, 52469. CBF 02281, 2282; FMNH 29056. FMNH 29050, 41278; MACN 3049, 36360. CML 1764, 1822, 1953; FMNH 50735, 50742, 50744; CFA 11835, 11864, 12231 (C. magellanicus fueguinus), 12315 (C. magellanicus fueguinus); MLP 9.XI.09.49, 9.XI.09.50, 9.XI.09.51, 9.XI.09.52, 9.XI.09.53, 9.XI.09.54, 9.XI.09.55, 9.XI.09.57, 9.XI.09.58, 9.XI.09.59, 9.XI.09.61, 9.XI.09.62, 9.XI.09.63, 9.XI.09.64, 9.XI.69.56; MMPMa 2500, 2501, 2502, 7; IEEUACH 326 (C. magellanicus fueguinus), 344, 348, 349, 350, 351, 352, 1503 (C. magellanicus fueguinus), 1513 (C. magellanicus fueguinus), 1518 (C. magellanicus fueguinus), 1522 (C. magellanicus fueguinus), 1524 (C. magellanicus fueguinus), 1536 (C. magellanicus fueguinus), 1547 (C. magellanicus fueguinus), 3313 (C. magellanicus fueguinus). CFA 12021, 12045, 12095, 12104, 12133, 12184; CML 2408; IADIZA CM 02830, 0232, 02836, 02838, 02981, 02982, 02983, 02984, 02987, 02989, 03407, 06419, 06431, 06441, 06475, 06612, 06615, 06621, 06622, 06626, 06627, 06630, 06631, 06632, 06633, 06681, 06699, 06705, 06709, 06743, 06744; MACN 28.92, 28.95, 28.103, 28.104, 33.224; MLP 3.XI.95.7; MMPMa 2276, 2655, 2711. FMNH 50731, 50733; MACN 20.654; MLP 7.X.92.10; IEEUACH 1584 (C. maulinus bruneus), 1586 (C. maulinus bruneus), 1592 (C. maulinus bruneus), 1619 (C. maulinus bruneus), 1672, 1677, 1678, 1684. CFA 11393, 11394, 11397, 11403, 11407, 11408, 11412, 11416, 11418, 11420, 11774,

Ctenomys nigriceps (C. opimus) Ctenomys occultus

Ctenomys opimus

Ctenomys osvaldoreigi Ctenomys pearsoni

Ctenomys perrensi

Ctenomys peruanus Ctenomys pilarensis Ctenomys pontifex Ctenomys porteousi

Ctenomys pundit Ctenomys rionegrensis Ctenomys robustus (C. fulvus) Ctenomys roigi Ctenomys rosendopascuali Ctenomys saltarius Ctenomys scagliai Ctenomys sericeus Ctenomys sociabilis Ctenomys steinbachi Ctenomys sylvanus (C. frater)

Ctenomys talarum

Ctenomys torquatus

11779, 11782; CML 1414; FMNH 98291. FMNH 23231. CFA 11133, 11186, 11620; CML 971, 972; MMPMa 3183, 3184, 3185. CFA 12113; CBF 00929; CML 7130, 7131, 7244, 8438; FMNH 53639, 53643, 53644; MACN 36358, 36361, 36364, 36368, 36372, 36373, 36376, 36377; MLP 12.XI.02.16, 12.XI.02.17, 12.XI.02.18; MMPMa 2202, 3101, 3102, 3103, 3104, 3105. CFA 11098, 11099, 11100, 11101, 11102, 11104, 11108, 11109, 11110, 11111, 11112, 11115, 12170, 12696, 12700. FMNH 29302; MLP 30.XI.93.3, 30.XI.93.4. CFA 11428, 11929, 11940, 11947, 11954, 12060, 12079, 12233, 12234, 12237, 12301, 12305, 12374; MACN 23273, 23618; MLP 7.X.92.6; MMPMa 2437, 2438, 2440, 8-VI. FMNH 52464, 52465. CFA 11869. CFA 11819, 12007, 12012, 12017, 12398, 12401. FMNH 23238, 23239; MLP 2541; MMPMa 1340, 1347, 2996, 2997, 3198, 3213, 3215, 3216, 3219, 3220, 3221, 3223, 3309, I1047, I1413, I1542, I1548. CFA 11267, 11269, 11289, 11301, 11365, 11367, 11614, 11615, 11617, 12139, 12181, 12182, 12455; CML 2410. MLP provisional numbers CA 412, CA 393, EV 1137 FMNH 29066. FMNH 23226, 23227, 23228. CFA 11296, 11616, 11635, 11646, 12172, 12183, 12461, 12463, 12464; MMPMa 2410, 2411, 2412, 3461. CFA 11249, 11255, 11270, 11273, 11275, 11283, 11293. CFA 12100, 12101; CML 854, 856, 858, 8469. MACN 23283. FMNH 35340, 35341. MACN 20655; MMPMa 3708, 3709, 3710; IEEUACH 1728, 1729, 1730. CBF 00942, 00943, 00944; FMNH 51894, 51895. CML 255, 7235, 7242, 8472; FMNH 29048, 41275, 41276. CML 1821, 1856, 1943, 2134; MACN 19545, 19874, 23197, 23205, 23207, 23235, 23236, 23257, 23258, 23259, 23263; MLP 1.VIII.00.9, 1.VIII.00.10, 1.VIII.00.12, 1.VIII.00.13, 1.XI.95.8, 2.V.00.1, 2.V.00.3, 3.VIII.99.1, 3.XI.95, 3.XI.95.1, 3.XI.95.2, 3.XI.95.4, 3.XII.02.15, 10.V.87.2, 10.V.87.6, 10.V.87.8, 10.XI.95.7, 23.VIII.01.4, 23.VIII.01.9, 23.VIII.01.10, 23.VIII.01.11, 23.VIII.01.12, 26.VIII.01.8, 4.XI.02.3, 27.VI.97.1, 27.VI.97.2, 27.XII.01.31, 27.XII.01.52, 27.XII.01.53, 27.XII.97.1, 2547; MMPMa 4000, 4001, 4002, 4003, 4006, 4030, 4031, 4032, 4034, 4035, 4036, 4037, 4039, 4040, 4041, 4042, 4043, 4044. CFA 12033, 12851;

Ctenomys tuconax

Ctenomys tucumanus

Ctenomys validus Ctenomys yatesi Ctenomys yolandae

†Ctenomys viarapaensis nov. sp.

CML 1938; FMNH 27702, 27703; MACN 19562, 19563, 19708, 19709, 19711, 20211, 24536. MACN 23286; MLP 12.VI.70.4, 12.VI.70.6, 27.III.78.2, 28.V.01.1; MMPMa 2429, 2430, 2960, 2962, 2963, 2969, 3182, 3309, 3311, 3342, 3346, 3695. CFA 11259, 11260, 11261; CML 247, 684, 685, 1686, 7245; MACN 19618, 19930, 19931, 19933, 19934, 19936, 19937, 19939, 19941, 19943, 19947, 19948, 19949, 19951, 19952, 19954, 19955, 19957, 19958, 19959, 19960, 19961, 20220, 20235, 23284; MLP 12.VI.70.2, 1838; MMPMa 2298, 3181, 3181A. CFA 12044, 12176; CML 2409. AM 260835. CFA 11152, 11162, 11191, 11248. MLP 2943, MLP 2945 (fragment of the anterior portion of the cranium with the nasal bones and left zygomatic arch), MLP 2941 (fragment of anterior portion of the cranium with left zygomatic arch), MLP 2942, MLP 2949 (fragment of anterior portion of the cranium with both incisors damaged), MLP 2938, MLP 2946 (fragment of anterior portion of the cranium with right zygomatic arch), MLP 2937 (fragment of anterior portion of the cranium with both zygomatic arches and right incisor damaged), MLP 2936 (fragment of anterior portion of the cranium with both zygomatic arches and portion of basicranium), MLP 2947 (fragment of anterior portion of the cranium with both zygomatic arches and left DP4), MLP 2939 (fragment of anterior portion of the cranium with both incisors damaged, right DP4-M1 and left M1), MLP 2940 (fragment of anterior portion of the cranium with the nasal bones, left incisor damaged and left DP4), MLP 2944 (fragment of the anterior portion of the cranium with nasal bones), MLP 2948 (occipital portion of the cranium with both auditory bullae), MLP 2950, MLP 2952, MLP 2953, MLP 2955 (left hemimandible with a fragment of the incisor), MLP 2957 (left hemimandible with dp4-m2), MLP 2954, MLP 2951, MLP 2956, MLP 2961, MLP 2962, MLP 2963, MLP 2964, MLP 2965 (right hemimandible with a fragment of the incisor), MLP 2960 (right hemimandible with dp4), MLP 2959 (right hemimandible with dp4-m3), MLP 2958, MLP 2967, MLP 2968 (right hemimandible with the complete incisor), MLP 2966 (complete mandible without incisors), IEH 100 (62 incisors, 65 right hemimandibles, 70 left hemimandibles, 33 fragments of the cranium), IEH 101 (78 incisors, 89 right hemimandibles, 83 left hemimandibles, 76 fragments of the cranium), IEH 102 (37 incisors, 46 right hemimandibles, 37 left hemimandibles, 24 fragments of the cranium), IEH 103 (95 incisors, 77 right hemimandibles, 57 left hemimandibles, 76 fragments of the cranium), IEH 104 (38 incisors, 27 right hemimandibles, 19 left hemimandibles, 19 fragments of the cranium), IEH 105 (1 incisor, 1 fragment of the cranium), IEH 106 (7 incisors, 8 right hemimandibles, 8 left hemimandibles, 7 fragments of the cranium).

APPENDIX A2. Measurements taken for morphological analyses of the skull in Ctenomys. (A) Ventral, and (B) lateral views of cranium. (C) lingual, and (D) dorsal views of mandible.

APPENDIX A3. Matrix of characters of Ctenomys viarapensis nov. sp. Character 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

25

26 27 28

Description Medial margins of the nasal bones: non-divergent (0); divergent, delimiting a space consistent with the dorsal opening of the interpremaxillary foramen (1). Medial margins of premaxillae in front of the incisive foramina: fused in the midline (0); lateroventral to the roots of the premaxillary septum (1). Frontal participating in the dorsal root of the antorbital zygomatic bar: no (0); yes (1). Facial process of the lacrimal and frontal on the antorbital zygomatic bar: facial process protruding respect to the frontal (0); not protruding (1). Maxilo-jugal suture in the zygomatic arch: not reaching the level of the anterior margin of the antorbital zygomatic bar (0); anteriorly extended beyond the level of the antorbital zygomatic bar (1). Dorsal part (‘‘first part’’ sensu Hill 1935: 123) of the nasolacrimal canal: long (0); very short because the lacrimal foramen is closer to the facial portion of the lacrimal bone (1). Dorsal part of the nasolacrimal canal: anteroventrally oriented (0); more anteriorly oriented (1). Lateromedial wall of the nasolacrimal canal: not in contact with the alveolar sheath of the M1 (0); in contact the alveolar sheath of the M1 (1). Posteromedial wall of the nasolacrimal canal: not hiding the laterodorsal portion of the alveolar sheath of the M1 (0); hiding on to laterodorsal portion of the alveolar sheath of the M1 (1). Suture on the maxilla: posterior to the nasolacrimal canal (0); on the nasolacrimal canal (1). Maxillary suture on the nasolacrimal canal: medial in its proximal part, and then posterolateral; not in contact with the alveolar sheath of the M1 (0); medial in contact with the alveolar sheath of the M1 (1); lateral, not in contact with the alveolar sheath of the M1 (2). Position of the major palatine foramina: at the level of the boundary DP4-M1 (0); at the level of the M1 (1). Anterior end of the mesopterygoid fossa: at the level of M1-M2 (0); at the level of the M2 or M2-M3 (1); at the level of the M3 (2). Maxilla-palatine suture: near or even in contact with the major palatine foramina (0); markedly posterior to the major palatine foramina (1). Posterior margin of the alisphenoid, posterolateral to the foramen ovale: transverse, sub-parallel to the anterior margin of the bulla (0); oblique, posterolaterally oriented (1). Contact between the posterolateral margin of the alisphenoid and the auditory bulla: wide (0); narrow or absent (1). Contact between pterygoid or palatine and the auditory bulla: only the pterygoid contacting the anterior end of the auditory bulla (0); both pterygoid and palatine contacting the anterior end of the auditory bulla (1). Ventral tip of the mastoid apophysis: dorsal to the ventral border of the external auditory meatus (0); at the level of, or more ventral than, the external auditory meatus (1). Extra-alveolar portion of the lower incisor: short (0); long (1). Morphology of the mandibular notch for the tendon of the M. masseter medialis pars anterior: shallow, with a slightly marked ventral margin (0); deep, with a marked ventral margin (1). Ventrolateral apophysis of the postcondyloid process: posterolaterally oriented (0); laterally oriented (1). Grooves on the enameled surface of the incisors: absent (0); present (1). Sperm morphology (Vitullo et al., 1988): symmetric (0); asymmetric (1). Sphenopalatine foramen: oblique and extended posteriorly over alveolar sheath of M1 or M1-2 (0); divided by M1 alveolar sheath into vertical portion anterior to M1 alveolar sheath, and posterior portion dorsal to M1 alveolar sheath expanded (1); vertical in front of M1 alveolar sheath, with or without independent relict posterior to M1 (2). Rostral masseteric fossa: dorsal to the alveolar sheath of I1, progressively narrow anterior, shallow, and ending with a pointed outline level with the anterior end of the incisive foramina (0); dorsal to the alveolar sheath of the I1, deep and ending in a curved crest slightly anterior to or level with the premaxillary-maxillary suture (1); with portions dorsal and ventral to the alveolar sheath of I1 present and shallow; the anterior end occupying almost the entire height of the rostrum and limited by a more straight crest located ventrally level with the anterior end of the incisive foramina or anterior to them (2); with portions dorsal and ventral to the alveolar sheath of I1 present and very deep; portion ventral to the I1 extending greatly anterior to the incisive foramina (3). Lateral flange of the canal for infraorbital nerve: present, and with free dorsal margin (0); present and with dorsal margin in contact with bottom of alveolar sheath of upper incisor (1); very wide and covering bottom of alveolar sheath of upper incisor laterally and posteriorly (2); very reduced or absent (3). Bottom of alveolar sheath of upper incisor: free in the diastema, or in the orbital region (0); lodged in a cavity of the maxillary, anterior to alveolar sheath of M1 (1); lodged in a cavity of the maxillary, lateral to alveolar sheath of M1 (2). Incisive foramina: with lateral walls concave and approximately symmetric anterior and posterior to the premaxillarymaxillary suture; suture located near middle of lateral wall of the foramen or more anteriorly (0); foramina extended and progressively narrow anterior to the premaxillary-maxillary suture; suture nearer to posterior part of the foramen (1).

29 30 31 32 33 34

35

36

37 38 39 40

41

42 43 44 45 46 47 48

49

50 51

Premaxillary-maxillary suture at medial margin of incisive foramen: level with its portion lateral to the foramen (0); displaced forward (1). Ventral margin of rostrum: not widened or only slightly widened but without protuberance at premaxillary-maxillary suture (0); widened forming a marked protuberance level with premaxillary-maxillary suture (1). Incisive foramina: wide, at least ¼ of rostrum width (both measured at the premaxillary-maxillary suture (0); narrow, less than ¼ of rostrum width (1). Anterior extension of the maxillary into posterior margin of incisive foramen: scarcely developed or absent (0); maxillary extended anteriad, on the same horizontal plane as premaxillary septum, constraining the incisive foramen posteriorly (1); maxillary extended anterodorsally with respect to premaxillary septum, constraining the incisive foramen posteriad (2). Premaxillary septum: with posterior ends of premaxillaries joined medially forming a pointed projection (0); with posterodorsal ends of premaxillaries divergent, each one forming a lateral apophysis (1). Dorsal part of the nasolacrimal canal: with a posterior margin (0); posterior margin scarcely differentiated or absent (1). External auditory meatus (EAM): short, moderately protruding with respect to auditory bulla and epitympanic recess (petrosal bulla) (ER) (0); protruding, with anterodorsal and anterior margin oriented anteriad, forming a smooth anterior concavity (1); forming a protruding tube with its anterior wall moderately to very concave; ER forming a horizontal flat surface (2); forming a protruding tube very narrow anteroposteriorly and kidney-shaped in cross section due to marked concavity of its anterior wall; ER dorsal to the EAM, very narrow (3). Zygomatic portion of squamosal: subhorizontal and forming at least the posterior half of paraorbitary process (0); never reaching the end of paraorbitary process; this process formed mostly or exclusively by the jugal (1). State 1 is associated with a reduced orbital region, which is defined on the zygoma by a more anterior placement of the paraorbitary process. Maxillary and alisphenoid in basitemporal region: contacting each other or separated by dorsal portion of the lateral palatine plate (0); separated by dorsal portion of the lateral palatine plate, which is expanded over both the alveolar sheath of M3 and the alisphenoid (1); strongly joined through a maxillary apophysis posterolateral to the M3 alveolar sheath (2). Auditory bulla: ovoid (0); pyriform, with anterior portion narrow and strongly oblique major axis (1); pyriform, very narrow, with a pit ventrolateral to the EAM (2). Alveolar margin of the mandibular molar series: descending ventromedially anterior to dp4 (0); not descending anterior to dp4 (1). Origin of masseteric crest of the mandible: incorporating the notch for the tendon of M. masseter medialis (0); posterior to the notch (1). Although this character is uninformative in the present analysis, state 1 is a synapomorphy of OctodontidaeCtenomyidae within the context of Caviomorpha (see Verzi, 1999). Masseteric area of the mandible: without protuberances corresponding to bottom portion of alveoli of molars (0); with a rounded protuberance near origin of masseteric crest, corresponding to the bottom of alveolus of m2 (1); with a protuberance that lacks distinct margins, corresponding to the bottom of alveolus of m2, placed between dorsal and ventral divisions of the masseteric fossa (2); with a marked ovoid protrusion corresponding to the bottom of alveolus of m3, between the dorsal and ventral divisions of the masseteric fossa (3); with a scarcely visible protrusion corresponding to the bottom of alveolus of m3 in the dorsal division of the masseteric fossa (4). The states present in Octodontidae and Ctenomyidae are associated to the occurrence of hypsodonty. Postcondyloid process: developed, with a weak protuberance on its ventral margin or without it (0); very reduced or absent (1); with a strong lateral apophysis on its ventral margin (2). The ventrolateral apophysis of Ctenomys adjusts to the EAM when the mandible is articulated in the postglenoid region (see Verzi and Olivares, 2006). Mandibular diastema: without a step anterior to dp4 (0); with a step anterior to dp4 (1). Chin process: level with dp4 in lateral view, or slightly anterior (0); behind the level of dp4 (1). Bottom of m1 alveolus: slightly protruding in the mandible, and anterior to origin of masseteric crest (0); forming a marked protrusion at origin of masseteric crest (1). Molars: with flexi and flexids persistent in adults (0); only with mesoflexus/id and hypoflexus/id persistent (1); with flexi vestigial or absent, and reduced flexids (2); with flexi/ids vestigial or absent (3). State 3 is a clear synapomorphy of Ctenomyidae (Verzi, 1999). DP4-M2: with transverse lophs (0); eight shaped, with two transverse lobes separated by the hypoflexus and mesoflexus (1); with posterior lobe not labially extended and without flexi (2). M3: not reduced to moderately reduced, with morphology similar to remaining molars (0); reduced, with occlusal outline subcircular and posterior lobe narrow (1); reduced, with posterior or posterolingual face flat and anterior lobe protruding (2). Occlusal design of Dp4-m2: transverse lophids (0); figure eight-shaped, with two transverse lobes separated by hypoflexid and mesoflexid (1); slightly oblique rounded lobes, with reduced hypoflexid and mesoflexid (2); subrhombic to crescentshaped and with a lingual concavity limited by an anterior protrusion (3); subrhombic with a weak labial fold (trace of hypoflexid?) (4); semilunar with a weak labial fold (5); subrhombic with weak labial and lingual folds (traces of flexids?) to semilunar and with only a wide lingual concavity (6). The occlusal subrhombic morphology is ancestral to a more curved “semilunar” shape in the Xenodontomys and Eucelophorus lineages (Verzi, 2002, 2008; Verzi et al., 2004). Posterolingual margin of anterior lobe of DP4: not protruding or with a slightly rounded edge (0); with a sharp edge (1). m3 implanted dorsolaterally to incisor (0); with posterolateral or posterior implantation, dorsal to i1 (1).

APPENDIX A4. Definition of cranial landmarks and semilandmarks: Anterior portion of the skull in ventral view.

Landmarks 1 Anterior tip of suture between premaxillae (Fornel et al., 2010). 2 Anterolateral extremity of incisor alveolus (Fornel et al., 2010). 3 Posterior-most point of the root of the premaxillary septum. 4 Lateral edge of incisive foramen in suture between premaxilla and maxilla (Fornel et al., 2010). 5 Lateral edge of the rostrum between premaxillary-maxillary suture. 6 Anterior point of root of zygomatic arch (Fornel et al., 2010). 7 Anteriormost point of premolar alveolus (Fornel et al., 2010). 8 Posterior palatine foramen. 9 Anterior-most point of the maxilla-palatine suture. 10 Posterior extremity of suture between palatines (Fornel et al., 2010). 11 Posterior extremity of III molar alveolus (Fornel et al., 2010). Semilandmarks 12 to 14 Between landmarks 2 and 5. 15 Between landmarks 3 and 4.

APPENDIX A5. Definition of mandibular landmarks and semilandmarks: Lateral view.

Landmarks 1 2 3 4 5 6 7 8 9 10

Antero-dorsal border of incisor alveolus (Álvarez et al., 2011). Extreme of diastema invagination (Álvarez et al., 2011). Anterior end of mandibular toothrow (Álvarez et al., 2011). Anterior end of base of coronoid process (Álvarez et al., 2011). Tip of coronoid process (Álvarez et al., 2011). Maximum curvature of incisura mandibulae (Álvarez et al., 2011). Anterior edge of condylar process (Álvarez et al., 2011). Posterior edge of condylar process. Posteriormost edge of postcondyloid process (Álvarez et al., 2011). Maximum curvature of curve between postcondyloid process and angular process (Álvarez et al., 2011). 11 Posteriormost point of masseteric crest. 12 Posteriormost point on ventral border of mandibular corpus (Álvarez et al., 2011). 13 Anterior end of masseteric crest. 14 Antero-ventral border of incisor alveolus (Álvarez et al., 2011). Semilandmarks 15 to 17 Between landmarks 1 and 2. 18 to 21 Between landmarks 4 and 5. 22 Between landmarks 5 and 6. 23 and 24 Between landmarks 6 and 7. 25 to 27 Between landmarks 9 and 10. 28 and 29 Between landmarks 10 and 11. 30 to 32 Between landmarks 11 and 12. 33 to 37 Between landmarks 12 and 14.

References Álvarez, A., Perez, I.S., Verzi D.H., 2011. Ecological and phylogenetic influence on mandible shape variation of South American caviomorph rodents (Rodentia: Hystricomorpha). Biological Journal of Linnean Society, 102, 828–837. Fornel, R., Cordeiro-Estrela, P., Freitas, T.R., 2010. Skull shape and size variation in Ctenomys minutus (Rodentia: Ctenomyidae) in geographical, chromosomal polymorphism, and environmental contexts. Biological Journal of the Linnean Society, 101, 705–720. Verzi, D.H., 1999. The dental evidence on the differentiation of the ctenomyine rodents (Caviomorpha, Octodontidae, Ctenomyinae). Acta Theriologica, 44, 263–282. Verzi, D.H., 2002. Patrones de evolución morfológica en Ctenomyinae (Rodentia, Octodontidae). Mastozoología Neotropical, 9, 309–328. Verzi, D.H., 2008. Phylogeny and adaptative diversity of rodents of the family Ctenomyidae (Caviomorpha): delimiting lineages and genera in the fossil record. Journal of Zoology, 274, 386–394. Verzi, D.H., Olivares A.I., 2006. Craniomandibular joint in South American burrowing rodents (Ctenomyidae): adaptations and constraints related to a specialized mandibular position in digging. Journal of Zoology, 270, 488–501. Verzi, D., Deschamps, C., Tonni, E.P., 2004. Biostratigraphic and palaeoclimatic meaning of the Middle Pleistocene South American rodent Ctenomys kraglievichi (Caviomorpha, Octodontidae). Palaeogeography, Palaeoclimatology, Palaeoecology, 212, 315–329. Vitullo, A.D, Roldan, E.R.S., Merani, M.S., 1988. On the morphology of spermatozoa of tuco-tucos, Ctenomys (Rodentia: Ctenomyidae): New data and its implications for the evolution of the genus. The Zoological Society of London, 215, 675–683.

Table 1. Cranial and mandible measurements of Ctenomys viarapaensis sp. nov. from QR1. Abbreviations shown in Material and methods.

Cranium

Mandible

Measurements BW BL LZA UAL RW DL IW PROC LAL CIL MMW MWm3 CL IB

Holotype 25.05 11.42 15.09 20.16 -

Mean 30.64 9.35 22.26 10.60 11.89 17.15 8.13 115º 10.82 32.74 40.96 32.22 3.82 4.21

SD 2.91 2.02 0.61 1.28 1.78 1.31 3.22 0.64 2.33 0.47 0.50

Range 28.95 - 30.64 9.35 19.74 - 25.05 9.16 - 12.25 9.82 - 15.09 12.42 - 20.69 6.82 - 10.33 119º - 113º 9.38 - 13.28 28.97 - 38.79 40.96 32.22 2.70 - 5.04 3.10 - 5.57

N 3 1 13 138 137 139 9 3 167 167 1 1 167 158

HIGHLIGHTS A new species of the rodent Ctenomys from the Holocene of Pampa de Achala, central Argentina, is described. Phylogenetic analysis shows close relationship between the new species and the living Ctenomys osvaldoreigi. This is the first report of extinction of a Ctenomys species in the Holocene.

Declaration of interests X The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: