Comprehensive total evidence phylogeny of chinchillids (Rodentia, Caviomorpha): Cheek teeth anatomy and evolution

Abstract

Rodents are the most diverse order of extant mammals, and caviomorph rodents, or New World hystricognaths, have a remarkable morphological disparity and a long fossil record that begins in the Eocene. Chinchilloidea is a poorly understood clade within Caviomorpha, from an evolutionary and phylogenetic perspective. It includes the extant families Chinchillidae and Dinomyidae, the extinct Neoepiblemidae and Cephalomyidae, and several extinct chinchilloids without a clear phylogenetic position, like Eoincamys, Borikenomys, Chambiramys, Ucayalimys, Incamys, Saremmys, Garridomys and Scotamys. The family Chinchillidae includes the extant Chinchilla and Lagidium, grouped in Chinchillinae, and the only living Lagostominae, Lagostomus maximus. Among extinct chinchillids, Eoviscaccia (early Oligocene-early Miocene of Argentina, Bolivia and Chile), Prolagostomus (early-middle Miocene of Argentina, Bolivia and Chile) and Pliolagostomus (early-middle Miocene of Argentina) are the only genera originally described as members of the family. Based on the study of specimens with unworn or little-worn cheek teeth, belonging to extinct and extant taxa, we propose homologies of the cheek teeth structures and perform a combined molecular and morphological phylogenetic analysis including extinct and extant taxa of all families of Chinchilloidea and all genera of Chinchillidae. Our phylogenetic analysis recovered three major lineages in the evolutionary history of Chinchilloidea. The first major lineage is composed of the extant taxa Chinchilla, Lagidium and Lagostomus, and the extinct genera Eoviscaccia, Prolagostomus, Pliolagostomus, Garridomys, Incamys, Loncolicu and Saremmys. Cephalomyid (Banderomys, Cephalomys, Litodontomys, Soriamys) and neoepiblemid (Neoepiblema, Perimys, Phoberomys, Scotamys) genera are part of the second major lineage, while dinomyids such as Dinomys, Drytomomys, Scleromys, 'Scleromys' and Tetrastylus constitute the third major lineage within Chinchilloidea. The phylogenetic position of some taxa previously considered as incertae sedis chinchilloids or without a clear suprageneric group (i.e. Incamys, Saremmys, Garridomys and Loncolicu) show that they belong to pan-Chinchillidae and conform the stem Chinchillidae along with Eoviscaccia. The euhypsodont crown Chinchillidae includes the living subfamilies Chinchillinae and Lagostominae. Dinomyidae and Eoincamys pascuali are recovered as the sisters of a major clade composed by 'Cephalomyidae'+Neopiblemidae and pan-Chinchillidae, and Chambiramys sylvaticus occupies a basal position to the same clade. Four major radiation events are identified in the evolutionary history of Chinchilloidea. The analysis of new morphological characters linked with molecular evidence as well as the addition of taxa of uncertain or unstable phylogenetic position or not considered in previous studies allowed us resolve part of the relationships within Chinchilloidea, particularly that of Chinchillidae, supporting preceding morphological hypotheses.

Keywords: Cenozoic; Chinchilloidea; South America; dental homologies; ontogeny.

FIGURE 1

Nomenclature of chinchilloid cheek teeth occlusal morphology, illustrated in Incamys bolivianus. (a) upper right deciduous premolar (DP4); (b) upper right premolar (P4); (c) upper right molar (M1‐M3); (d) lower right deciduous premolar (dp4); (e) lower right premolar (p4); (f) lower right molar (m1‐m3). Abbreviations: anl, anteroloph; ecd, ectolophid; Ed, entoconid; Hd, hypoconid; Hy, hypocone; hyd, hypolophid; Me, metacone; met I, metalophulid I; met II; metalophulid II; Md, metaconid; md, mesostylid; ms, mesostyle; msd, mesolophid; msl/msule, mesoloph/mesolophule; mtl, metaloph; mu, mure; Pa, paracone; Pd, protoconid; pod, posterlophid; pol, posteroloph; Pr, protocone; prl, protoloph

FIGURE 2

Little‐worn lower cheek teeth of living chinchilloids. (a) Lagidium sp., MACN‐Ma 50.280, right lower jaw with p4‐m2; (b) Lagostomus maximus, MACN‐Ma 49.238, right lower jaw with p4‐m3; (c) Dinomys branickii, MACN‐Ma 12962, right lower jaw with dp4‐m1. Abbreviations: al m2‐m3, alveolus of m2 and m3; al m3, alveolus of m3; dp4, fourth lower deciduous premolar; m1, first lower molar; m2, second lower molar; m3, third lower molar; p4, fourth lower premolar; other abbreviations as in Figure 1. Scale bar 10 mm

FIGURE 3

Lower cheek teeth of selected Chinchilloidea. (a) Incamys bolivianus, MNHN‐SAL not numbered, left p4‐m3 (reversed); (b) Saremmys ligcura, MPEF‐PV 11341, right p4‐m3; (c) Garridomys curunuquem, MOZ‐PV 920 (holotype), left p4‐m3 (reversed); (d‐e) Eoviscaccia australis, (d) MACN‐CH 1875, left p4 (reversed); (e) MACN‐Pv‐CH 179, right m1 or m2; (f) Eoviscaccia boliviana, MNHN‐LAC 5, left p4‐m2 (reversed); (g) Scleromys quadrangulatus, MLP‐Pv 82‐VI‐3‐2 (holotype), right p4‐m3; H‐I. Banderomys leanzai, (h) PVPH 369, right p4; (i) PVPH 366, right m1 or m2; (j) Perimys intermedius, MACN‐Pv‐SC 2037, right p4; (k) Perimys sp., MLP‐Pv 15‐80, left dp4‐m1 (reversed); (l) Neoepiblema horridula, MACN‐Pv 4580, right p4‐m2; (m‐o) Phoberomys burmeisteri; (m) MACN‐Pv 2446, left p4 (reversed); (n) MACN‐Pv 2645, right lower molar; (o) MACN‐Pv 3475, right m1 or m2. Abbreviations as in Figure 1. Scale bars equals 2 mm, except in (m‐o) where it equals 5 mm. Modified from Busker et al., 2019 (b); Kramarz et al., (c); Kramarz, (d‐e); Kramarz, (g); Kramarz, (h‐i); and Kramarz, (j)

FIGURE 4

Upper premolars of selected Chinchilloidea. (a) Incamys bolivianus, MNHN‐SAL 117, left P4 (reversed); (b) ‘Scleromys’ colombianus, UCMP 40549, right P4; (c) Eoviscaccia australis, MACN‐Pv‐CH 1862, right P4; (d) Scleromys quadrangulatus, MACN‐Pv‐SC 3840, right P4; (e) Perimys sp., MLP‐Pv 68‐I‐17‐12, left P4 (reversed). Abbreviations as in Figure 1. Scale bars equals 2 mm. B, not to scale. Modified from Fields, (b); Kramarz, (c); Kramarz, (d); and Kramarz, (e)

FIGURE 5

Strict consensus of 260 MPT of 311 steps, given by the morphological analysis showing phylogenetic relationships of major clades of Chinchilloidea. White dots indicate families Dinomyidae, Neoepiblemidae and pan‐Chinchillidae. CI, consistency index; RI, retention index.

FIGURE 6

Phylogenetic relationships of major clades of Chinchilloidea. (a) Strict consensus of the most parsimonious trees and (b) majority‐rule consensus (Bayesian Inference) resulting from the analysis with morphological dataset. Numbers associated to the nodes indicates in (a) bootstrap support values and absolute Bremer support index and (b) posterior probability values

FIGURE 7

Phylogenetic relationships of major clades of Chinchilloidea. (a) Strict consensus of the most parsimonious trees and (b) majority‐rule consensus (Bayesian Inference) resulting from the analysis with combined dataset (morphological and molecular). Numbers associated to the nodes indicates in (a) bootstrap support values and absolute Bremer support index and (b) posterior probability values

FIGURE 8

Strict consensus tree of combined dataset showing phylogenetic relationships of major clades of Chinchilloidea, calibrated with geological time. Light orange horizontal bars represent radiation events discussed in the text. Bonae, Bonaerian; Casam, Casamayoran; Chap, Chapadmalalan; Chasi, Chasicoan; Colhue, Colhuehuapian; Collon, Colloncuran; Desead, Deseadan; Ense, Ensenadan; Huay, Huayquerian; Laven, Laventan; Marpla, Marplatan; Monte, Montehermosan; Muster, Mustersan; ‘Pintu’, ‘Pinturan’; Santac, Santacrucian; Tingui, Tinguirirican