Early Miocene hippopotamids (Cetartiodactyla) constrain the phylogenetic and spatiotemporal settings of hippopotamid origin

Abstract

The affinities of the Hippopotamidae are at the core of the phylogeny of Cetartiodactyla (even-toed mammals: cetaceans, ruminants, camels, suoids, and hippos). Molecular phylogenies support Cetacea as sister group of the Hippopotamidae, implying a long ghost lineage between the earliest cetaceans (approximately 53 Ma) and the earliest hippopotamids (approximately 16 Ma). Morphological studies have proposed two different sister taxa for hippopotamids: suoids (notably palaeochoerids) or anthracotheriids. Evaluating these phylogenetic hypotheses requires substantiating the poorly known early history of the Hippopotamidae. Here, we undertake an original morphological phylogenetic analysis including several "suiform" families and previously unexamined early Miocene taxa to test previous conflicting hypotheses. According to our results, Morotochoerus ugandensis and Kulutherium rusingensis, until now regarded as the sole African palaeochoerid and the sole African bunodont anthracotheriid, respectively, are unambiguously included within the Hippopotamidae. They are the earliest known hippopotamids and set the family fossil record back to the early Miocene (approximately 21 Ma). The analysis reveals that hippopotamids displayed an unsuspected taxonomic and body size diversity and remained restricted to Africa during most of their history, until the latest Miocene. Our results also confirm the deep nesting of Hippopotamidae within the paraphyletic Anthracotheriidae; this finding allows us to reconstruct the sequence of dental innovations that links advanced selenodont anthracotheriids to hippopotamids, previously a source of major disagreements on hippopotamid origins. The analysis demonstrates a close relationship between Eocene choeropotamids and anthracotheriids, a relationship that potentially fills the evolutionary gap between earliest hippopotamids and cetaceans implied by molecular analyses.

Fig. 1.

Dentition of Morotochoerus ugandensis: lingual (A) and occlusal (B) views of the right dentary (holotype: MOR 177–178) and lingual (C) and occlusal (D) views of the left maxillary fragment (MOR II BUMP 350), compared with the occlusal view of the right M1 of Kenyapotamus ternani (E, holotype: KNM-FT 3934, reversed) and of the left M1 of Kulutherium rusingense (F, holotype: R 773′49, cast at Natural History Museum, London). The white outlines suggest the respective body masses of the figured hippopotamids, estimated from m1 measurements (47). (Scale bar: 10 mm.)

Fig. 2.

Phylogeny of hippopotamoids based on the consensus of 78 parsimonious trees (consensus tree length = 234; CI = 0.39; RI = 0.75). (A) whole data matrix; (B) relationships within Hippopotaminae when excluding Hippopotamus. H, Hippopotamoidea; h, Hippopotamidae; S, Suina. Shaded numbers indicate nonambiguous synapomorphies, and solid numbers indicate Bremer support. Abbreviations: Archaeopotamus h, A. harvardi; Archaeopotamus l., A. lothagamensis; Kenyapotamus c., K. coryndonae; Kenyapotamus t., K. ternani.

Fig. 3.

Sketches of p4, lower and upper molars (from top to bottom) of (A) Palaeochoerus, (B) Choeropotamus, (C) Bothriogenys, (D) Morotochoerus, (E) Kulutherium, (F) Kenyapotamus, and (G) Hexaprotodon. H, Hippopotamoidea; h, Hippopotamidae; s, Suoidea. Color correspondence: upper molars, red, postparacrista and premetacrista; pink, parastyle and mesiostyle; and orange, metastyles and distostyles; lower cheek teeth, dark green, postmetacristid and postprotocristid; light green, postectohypocristids; light blue, premetacristid; blue, preprotocristid; purple, postectoprotocristid and postectometacristid; violet, hypoconid; and brown, accessory conulids. The arrow indicates mesial (to top) and lingual (to left) directions.

Fig. 4.

Temporal distribution, divergence estimates, and suggested phylogenetic relationships within cetartiodactyls classically related to the question of hippopotamid origin. The putative position of Cetacea is based on work by Boisserie et al. (35); that of Raoellidae is based on work by Thewissen et al. (11). E.T.C.D., estimated time for cetancodont differentiation; H./Cet., molecular divergence estimates between extant hippopotamids and cetaceans (data from refs. , , and 77); Hip./Ch., molecular divergence estimates between extant Hippopotamus and Choeropsis (data from ref. 59); H. FAD, first appearance datum for the Hippopotamidae based on this work (on the right, previous FAD); A, scenario for an emergence of the Hippopotamidae from a stock of Asian advanced bothriodontines; B, scenario for an emergence of the Hippopotamidae from a stock of African archaic bothriodontines (see text for discussion). White diamond symbols indicate dispersals to Africa.