Middle Eocene rodents from Peruvian Amazonia reveal the pattern and timing of caviomorph origins and biogeography

Abstract

The long-term isolation of South America during most of the Cenozoic produced a highly peculiar terrestrial vertebrate biota, with a wide array of mammal groups, among which caviomorph rodents and platyrrhine primates are Mid-Cenozoic immigrants. In the absence of indisputable pre-Oligocene South American rodents or primates, the mode, timing and biogeography of these extraordinary dispersals remained debated. Here, we describe South America's oldest known rodents, based on a new diverse caviomorph assemblage from the late Middle Eocene (approx. 41 Ma) of Peru, including five small rodents with three stem caviomorphs. Instead of being tied to the Eocene/Oligocene global cooling and drying episode (approx. 34 Ma), as previously considered, the arrival of caviomorphs and their initial radiation in South America probably occurred under much warmer and wetter conditions, around the Mid-Eocene Climatic Optimum. Our phylogenetic results reaffirm the African origin of South American rodents and support a trans-Atlantic dispersal of these mammals during Middle Eocene times. This discovery further extends the gap (approx. 15 Myr) between first appearances of rodents and primates in South America.

Figure 1.

Stratigraphical range of CTA-27 locality (inferred by radioisotopy, vertebrate biochronology and palynostratigraphy) and Mid-Cenozoic global climate. The age of CTA-27 is bracketed between 41.6 Ma (base of the Gran Barranca Member [23,24]) and 40.94 Ma (youngest age provided by ⁴⁰Ar/³⁹Ar datings at CTA-29; electronic supplementary material, figure S6). Age of both key Palaeogene vertebrate localities and biotic events of South America are based on data from Flynn et al. [19], Goin et al. [25,26], Goin & Candela [27], Shockey et al. [28], López [29] and Vucetich et al. [13]. Global climate is inferred by the δ¹⁸O temperature scale of Zachos et al. [30] (red curve to the right), showing the Mid-Eocene Climatic Optimum by the time of deposition of CTA-27. Barran., Barrancan; Barton., Bartonian; FAD, first appearance datum; Mus., Mustersan; Priabon., Priabonian; SALMA, South American Land Mammal Age; Tingui., Tinguirirican.

Figure 2.

Scanning electron microscope images (in occlusal view) and dimensions (length × width, in millimetres) of fossil caviomorph teeth from CTA-27. (a–k) Cachiyacuy contamanensis new gen. and sp.: (a) MUSM 1870, right (r) M³ (2.34 × 2.44); (b) MUSM 1871, r M² (holotype; 2.22 × 2.69); (c) MUSM 1872, left (l) M¹ (reversed; 2.07 × 2.22); (d) MUSM 1873, r P⁴ (1.82 × 2.38); (e) MUSM 1874, l DP⁴ (reversed; 2.03 × 1.98); (f) MUSM 1875, DP³ (0.77 × 0.82); (g) MUSM 1876, r M₃ (2.46 × 2.24); (h) MUSM 1877, r M₂ (2.44 × 2.36); (i) MUSM 1878, r M₁ (2.15 × 1.99); (j) MUSM 1879, r P₄ (1.99 × 2.0); (k) MUSM 1880, r DP₄ (2.31 × 1.53). (l–s) Cachiyacuy kummeli new gen. and sp.: (l) MUSM 1881, broken r P⁴ (reversed; 1.16 × –); (m) MUSM 1882, l M¹ (holotype; 1.45 × 1.63); (n) MUSM 1883, l M² (1.69 × 1.87); (o) MUSM 1884, l M³ (1.67 × 1.71); (p) MUSM 1885, r M₃ (1.6 × 1.47); (q) MUSM 1886, r M₂ (1.83 × 1.67); (r) MUSM 1887, r M₁ (1.59 × 1.54); (s) MUSM 1888, l DP₄ (reversed; 1.53 × 1.2). (t–z) Canaanimys maquiensis new gen. and sp.: (t) MUSM 1889, r M³ (1.5 × 1.87); (u) MUSM 1890, r M² (holotype; 1.63 × 1.95); (v) MUSM 1891, l M¹ (reversed; 1.46 × 1.82); (w) MUSM 1892, l M₃ (1.71 × 1.36); (x) MUSM 1893, l M₂ (reversed; 1.8 × 1.79); (y) MUSM 1894, l M₁ (reversed; 1.54 × 1.57); (z) MUSM 1895, broken r DP₄ (−×1.07). (a′–d′) Eobranisamys sp.: (a′) MUSM 1896, l P⁴ (1.86 × 2.33); (b′) MUSM 1897, l M¹ (2.39 × 2.49); (c′) MUSM 1898, broken r M₂ (−×2.23); (d′) MUSM 1899, l M₃ (2.47 × 2.06). (e′,f′) cf. Eoespina sp.: (e′) MUSM 1912, r M² (1.48 × 1.85); (f′) MUSM 1913, l M² (1.51 × 1.77).

Figure 3.

Phylogeny and dispersal scenario of Palaeogene caviomorph rodents and related taxa. (a) Phylogeny of Contamana rodents among Palaeogene ctenohystricans (Ctenohystrica), hystricognaths (Hystricognathi) and caviomorphs (Caviomorpha). Strict consensus cladogram obtained with a maximum-parsimony PAUP (phylogenetic analysis using parsimony) heuristic search (see the electronic supplementary material). The consistency (CI), retention (RI) and homoplasy (HI) indices of the 13 shortest trees (859 steps) are 0.33, 0.63 and 0.68, respectively. Branch support of the concerned nodes (Bremer indices) appears in the electronic supplementary material, figure S2a. Contamana rodents included in this analysis (bold type) are stem caviomorphs (i.e. not referable to Octodontoidea, Erethizontidae or Cavioidea). cf. Eoespina sp. (not included, two teeth) is interpreted as a stem octodontoid. Eobranisamys sp. (four teeth) might be connected to the Eobranisamys romeropittmanae branch (Cavioidea), which suggests a late Middle Eocene age for the common ancestor of cavioids. Sister-group relationships between Gaudeamus (advanced phiomorph; Old World Hystricognath, OWH) and Eoincamys (caviomorph) probably document a striking convergent dental evolution [11,14], rather than independent dispersal from South America to Africa. Light-grey shaded bar illustrates molecular estimate ranges for the caviomorph–phiomorph split (CPS; 45.4 ± 4.1 Ma [9]), thus located behind the morphologically supported CPS node (grey triangle). On top, dark-grey tree sketches phylogenetic relationships among living ctenohystricans as supported by molecular data [9]. Barran., Barrancan; Barton., Bartonian; Itab., Itaboraian; Mus., Mustersan; Pel., Peligran; Priabon., Priabonian; Rioch., Riochican; SALMA, South American Land Mammal Age; Seland., Selandian; Thanet., Thanetian; Tingui., Tinguirirican; Species name abbreviations: bo., bolivianus; br., brachyodon; l., luribayensis; m., medianus; pa., pascuali; pr., paraphiomyoides; ro., romeropittmanae; s., schaubi. Rodent drawings by M. J. Orliac. See the electronic supplementary material for further details. (b) Palaeogeographic world map at 40 Ma and privileged phylogeographic sketch of Palaeogene hystricognath rodents, as inferred by both the consensus tree shown in (a) and the geographical range of concerned taxa (coloured circles; same colour codes as in (a)).