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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 The affinities of the Hippopotamidae are at the core of the phy- remained unresolved in recent combined analyses of extinct and logeny of Cetartiodactyla (even-toed mammals: cetaceans, ru- extant data (ref. 9, figure 2; refs. 15 and 16). However, these and minants, camels, suoids, and hippos). Molecular phylogenies other recent large-scale analyses aiming at clarifying cetartio- support Cetacea as sister group of the Hippopotamidae, implying dactyl basal relationships (10, 11, 17–20) included none or only a long ghost lineage between the earliest cetaceans (∼53 Ma) and a limited subset of fossil “suiforms” classically and more con- the earliest hippopotamids (∼16 Ma). Morphological studies have troversially interpreted as hippopotamid stem groups and, in all proposed two different sister taxa for hippopotamids: suoids (no- cases, no fossil hippopotamids. Failure to resolve the evolution tably palaeochoerids) or anthracotheriids. Evaluating these phylo- that led to Hippopotamidae hinders our understanding of the genetic hypotheses requires substantiating the poorly known common ancestry between extant hippopotamids and cetaceans. early history of the Hippopotamidae. Here, we undertake an orig- In turn, this creates difficulties in resolving the earlier branching inal morphological phylogenetic analysis including several “sui- of Ruminantia, Suoidea, and Tylopoda. A better understanding form” families and previously unexamined early Miocene taxa to of the evolutionary history of Hippopotamidae is thus a critical test previous conflicting hypotheses. According to our results, step in clarifying the relationships within Cetartiodactyla and is Morotochoerus ugandensis and Kulutherium rusingensis, until addressed in this paper. EVOLUTION now regarded as the sole African palaeochoerid and the sole Afri- The origin of the Hippopotamidae has been a subject of inquiries can bunodont anthracotheriid, respectively, are unambiguously for more than a century (see reviews in refs. 21–23), and identifying included within the Hippopotamidae. They are the earliest known the stem group of these mammals is still a challenging issue for hippopotamids and set the family fossil record back to the early biologists (22, 23). A significant hippopotamid fossil record is thus Miocene (∼21 Ma). The analysis reveals that hippopotamids dis- far found only for the Hippopotaminae (large hippopotamids dis- played an unsuspected taxonomic and body size diversity and re- playing a very derived morphology), which seem to appear abruptly mained restricted to Africa during most of their history, until the in the late Miocene deposits of Africa, ∼7.5 Ma (24, 25). The fi latest Miocene. Our results also con rm the deep nesting of Hippo- identification of the Paleogene-early Neogene cetartiodactyl group fi potamidae within the paraphyletic Anthracotheriidae; this nding from which hippopotamines are derived is thus challenging. allows us to reconstruct the sequence of dental innovations that links The only other members of Hippopotamidae are represented advanced selenodont anthracotheriids to hippopotamids, previously in subfamily Kenyapotaminae by the genus Kenyapotamus Pick- a source of major disagreements on hippopotamid origins. The anal- ford, 1983, known on the basis of mostly isolated dental remains ysis demonstrates a close relationship between Eocene choeropo- fi from the middle and late Miocene of Kenya. This subfamily has tamids and anthracotheriids, a relationship that potentially lls a first appearance datum (FAD) at ∼16 Ma (26), which extends the evolutionary gap between earliest hippopotamids and ceta- the time range of Hippopotamidae into the middle Miocene. To ceans implied by molecular analyses. date, kenyapotamines have been recorded only in Africa, in va- rious Kenyan localities (26–31) and elsewhere in Africa (Tunisia, Africa | dental pattern | Hippopotamoidea | paleobiogeography ref. 32; Ethiopia, refs. 33 and 34). Their morphology and di- versity are now better understood (22). Recent phylogenetic he question of the immediate affinities of the Hippopot- analyses suggested that the Kenyapotaminae are the sister taxon Tamidae is central to a major unresolved issue of mammalian of the Hippopotaminae and that the Hippopotamidae are mono- evolution: the phylogeny of the Cetartiodactyla and the terrestrial phyletic as well as deeply nested within the extinct, paraphyletic origins of the Cetacea. For many years there had been two sep- Anthracotheriidae (22, 35). However, a morphological gap re- arate problems: the ancestry of whales and whether hippopota- mains between these earliest known hippopotamids and their muses were related to pigs or anthracotheres. The arrival of hypothesized antracotheriid stem group (22). cladistics, molecular studies, and large-scale computer analyses Despite this step forward, there is still no consensus on the led to the surprising assertion that whales were either the sister earliest history of the hippopotamids. Phylogenies are divided group of artiodactyls or nested within them. This brought together between two mutually exclusive candidates for a hippopotamid both the old problems and overshadowed the second. Nowadays stem group: Anthracotheriidae (e.g., ref. 16) and Suoidea (e.g., molecular analyses of extant species suggest that Cetacea are the ref. 9, figure 5; and ref. 11). Among the latter, palaeochoerids also sister group of Hippopotamidae (e.g., refs. 1–8) whereas a close Hippopotamidae/Suoidea relationship is suggested by morpho- fi logical data from fossil and extant species (e.g., ref. 9, gure 5; Author contributions: M.O., J.-R.B., L.M., and F.L. designed research; M.O., J.-R.B., and F.L. refs. 10 and 11). Use of enlarged data sets mainly drawn from performed research; M.O., J.-R.B., and F.L. analyzed data; and M.O., J.-R.B., L.M., and F.L. molecular sources support a Cetacea + Hippopotamidae clade wrote the paper. (Cetancodonta), but produce conflicting results for the placement The authors declare no conflict of interest. of Suoidea (5, 12–14). *This Direct Submission article had a prearranged editor. The consideration of fossil data has seemed to introduce more 1To whom correspondence should be addressed. E-mail: [email protected]. confusion, because the relationships between major cetartioda- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ctyl clades (Cetancodonta, Ruminantia, Suoidea, and Tylopoda) 1073/pnas.1001373107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1001373107 PNAS Early Edition | 1of6 Downloaded by guest on September 26, 2021 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 hypotheses linking the Hippo- with (Choeropotamus, Hippopotamoidea) or at the base of potamidae to palaeochoerids. Surprisingly, it has never been dis- a (Suina, (Choeropotamus, Hippopotamoidea)) clade. Cebo- cussed as such by proponents of
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