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Early Miocene Hippopotamids (Cetartiodactyla) Constrain the Phylogenetic and Spatiotemporal Settings of Hippopotamid Origin

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Early Miocene Hippopotamids (Cetartiodactyla) Constrain the Phylogenetic and Spatiotemporal Settings of Hippopotamid Origin Early Miocene hippopotamids (Cetartiodactyla) constrain the phylogenetic and spatiotemporal settings of hippopotamid origin Maeva Orliaca,1, Jean-Renaud Boisserieb,c, Laura MacLatchyd, and Fabrice Lihoreaua aInstitut des Sciences de l’Evolution, Unité Mixte de Recherche 5554, Université Montpellier 2, 34000 Montpellier, France; bCentre Français des Etudes Ethiopiennes/French Centre for Ethiopian Studies, Centre National de la Recherche Scientifique Unité de Service et de Recherche 3137, Addis Ababa, Ethiopia; cInstitut International de Paléoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironnements, Unité Mixte de Recherche 6046, Université de Poitiers, F-86022 Poitiers, France; and dDepartment of Anthropology, University of Michigan, Ann Arbor, MI 48109 Edited* by David Pilbeam, Harvard University, Cambridge, MA, and approved May 5, 2010 (received for review February 3, 2010) The affinities of the Hippopotamidae are at the core of the phy- ctyl clades (Cetancodonta, Ruminantia, Suoidea, and Tylopoda) logeny of Cetartiodactyla (even-toed mammals: cetaceans, ru- remained unresolved in recent combined analyses of extinct and minants, camels, suoids, and hippos). Molecular phylogenies extant data (ref. 9, figure 2; refs. 15 and 16). However, these and support Cetacea as sister group of the Hippopotamidae, implying other recent large-scale analyses aiming at clarifying cetartio- a long ghost lineage between the earliest cetaceans (∼53 Ma) and dactyl basal relationships (10, 11, 17–20) included none or only the earliest hippopotamids (∼16 Ma). Morphological studies have a limited subset of fossil “suiforms” classically and more con- proposed two different sister taxa for hippopotamids: suoids (no- troversially interpreted as hippopotamid stem groups and, in all tably palaeochoerids) or anthracotheriids. Evaluating these phylo- cases, no fossil hippopotamids. Failure to resolve the evolution genetic hypotheses requires substantiating the poorly known that led to Hippopotamidae hinders our understanding of the early history of the Hippopotamidae. Here, we undertake an orig- common ancestry between extant hippopotamids and cetaceans. inal morphological phylogenetic analysis including several “sui- In turn, this creates difficulties in resolving the earlier branching form” families and previously unexamined early Miocene taxa to of Ruminantia, Suoidea, and Tylopoda. A better understanding EVOLUTION test previous conflicting hypotheses. According to our results, of the evolutionary history of Hippopotamidae is thus a critical Morotochoerus ugandensis and Kulutherium rusingensis, until step in clarifying the relationships within Cetartiodactyla and is now regarded as the sole African palaeochoerid and the sole Afri- addressed in this paper. can bunodont anthracotheriid, respectively, are unambiguously The origin of the Hippopotamidae has been a subject of inquiries included within the Hippopotamidae. They are the earliest known for more than a century (see reviews in refs. 21–23), and identifying hippopotamids and set the family fossil record back to the early the stem group of these mammals is still a challenging issue for Miocene (∼21 Ma). The analysis reveals that hippopotamids dis- biologists (22, 23). A significant hippopotamid fossil record is thus played an unsuspected taxonomic and body size diversity and re- far found only for the Hippopotaminae (large hippopotamids dis- mained restricted to Africa during most of their history, until the playing a very derived morphology), which seem to appear abruptly latest Miocene. Our results also confirm the deep nesting of Hippo- in the late Miocene deposits of Africa, ∼7.5 Ma (24, 25). The potamidae within the paraphyletic Anthracotheriidae; this finding identification of the Paleogene-early Neogene cetartiodactyl group allows us to reconstruct the sequence of dental innovations that links from which hippopotamines are derived is thus challenging. advanced selenodont anthracotheriids to hippopotamids, previously The only other members of Hippopotamidae are represented a source of major disagreements on hippopotamid origins. The anal- in subfamily Kenyapotaminae by the genus Kenyapotamus Pick- ysis demonstrates a close relationship between Eocene choeropo- ford, 1983, known on the basis of mostly isolated dental remains tamids and anthracotheriids, a relationship that potentially fills from the middle and late Miocene of Kenya. This subfamily has the evolutionary gap between earliest hippopotamids and ceta- a first appearance datum (FAD) at ∼16 Ma (26), which extends ceans implied by molecular analyses. the time range of Hippopotamidae into the middle Miocene. To date, kenyapotamines have been recorded only in Africa, in va- Africa | dental pattern | Hippopotamoidea | paleobiogeography rious Kenyan localities (26–31) and elsewhere in Africa (Tunisia, ref. 32; Ethiopia, refs. 33 and 34). Their morphology and di- he question of the immediate affinities of the Hippopotamidae versity are now better understood (22). Recent phylogenetic Tis central to a major unresolved issue of mammalian evolution: analyses suggested that the Kenyapotaminae are the sister taxon the phylogeny of the Cetartiodactyla and the terrestrial origins of of the Hippopotaminae and that the Hippopotamidae are mono- the Cetacea. For many years there had been two separate prob- phyletic as well as deeply nested within the extinct, paraphyletic lems: the ancestry of whales and whether hippopotamuses were Anthracotheriidae (22, 35). However, a morphological gap re- related to pigs or anthracotheres. The arrival of cladistics, molec- mains between these earliest known hippopotamids and their hypothesized antracotheriid stem group (22). ular studies, and large-scale computer analyses led to the surprising Despite this step forward, there is still no consensus on the assertion that whales were either the sister group of artiodactyls or earliest history of the hippopotamids. Phylogenies are divided nested within them. This brought together both the old problems between two mutually exclusive candidates for a hippopotamid and overshadowed the second. Nowadays molecular analyses of extant species suggest that Cetacea are the sister group of Hip- popotamidae (e.g., refs. 1–8) whereas a close Hippopotamidae/ Author contributions: M.O., J.-R.B., L.M., and F.L. designed research; M.O., J.-R.B., and F.L. Suoidea relationship is suggested by morphological data from fossil performed research; M.O., J.-R.B., and F.L. analyzed data; and M.O., J.-R.B., L.M., and F.L. and extant species (e.g., ref. 9, figure 5; refs. 10 and 11). Use of wrote the paper. enlarged data sets mainly drawn from molecular sources support The authors declare no conflict of interest. a Cetacea + Hippopotamidae clade (Cetancodonta), but produce *This Direct Submission article had a prearranged editor. conflicting results for the placement of Suoidea (5, 12–14). 1To whom correspondence should be addressed. E-mail: [email protected]. The consideration of fossil data has seemed to introduce more This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. confusion, because the relationships between major cetartioda- 1073/pnas.1001373107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1001373107 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 stem group: Anthracotheriidae (e.g., ref. 16) and Suoidea (e.g., cladistic analysis unambiguously rejected a suoid origin for the ref. 9, figure 5; and ref. 11). Among the latter, palaeochoerids also Hippopotamidae. Two major clades are supported: a robust clade known as “Old World peccaries” (36), have been favored in some Suina (i.e., entelodonts + suoids; clade S, Fig. 2A) and a clade contributions (23, 29). The morphological gap between the ear- gathering Choeropotamus, the paraphyletic anthracotheriids and liest known hippopotamids and their potential sister taxon exists the Hippopotamidae, in agreement with Hippopotamoidea sensu either because relevant remains are not yet documented in the (43) (clade H, Figs. 2A and 3). The latter clade is defined by known fossil record or because earlier hippopotamid remains presence of a mesostyle on upper molars (311; RI = 1.00), con- have been collected, but not recognized as such. nection between pre- and postcristae of upper molar labial cusps In this study we addressed the challenging question of the im- with cingular structure (321; RI = 1.00), paraconule of upper mediate affinities of hippopotamids by reexamining Morotochoerus molars independent with its own crest pattern (281; RI = 0.75), ugandensis Pickford, 1998 (36) (Fig. 1 A–D)andKulutherium ken- postparacrista and premetacrista do not form a straight line (331; yensis Pickford, 2007 (Fig. 1F), two bunodont early Miocene eastern RI = 0.70), p4 with flat lingual wall and convex buccal wall (511; Africa suiforms known through partial dentitions. M. ugandensis RI = 0.66), P4 labial orientation of the preparacrista (201;RI= (Moroto, Uganda, dated >20.6 Ma) (37) was initially referred to as 0.75), and protocone of the P4 crescentic (231; RI = 0.57). The a small anthracotheriid (38), later to the schizochoerine tayassuids tree basal relationships remain unresolved with a major polytomy (36), and finally assigned to the “Palaeochoeridae,” as their only involving the raoellid Khirtharia, Cebochoerus, the Suina, and the African representative (ref. 39 and ref. 40, table 2). This makes this (Choeropotamus, Hippopotamoidea) clade. Khirtharia branches material crucial in testing previous
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