The first hyaenodont from the late Oligocene Nsungwe Formation of Tanzania: Paleoecological insights into the Paleogene-Neogene carnivore transition

<div><p>Throughout the Paleogene, most terrestrial carnivore niches in Afro-Arabia were occupied by Hyaenodonta, an extinct lineage of placental mammals. By the end of the Miocene, terrestrial carnivore niches had shifted to members of Carnivora, a clade with Eurasian origins. The transition from a hyaenodont-carnivore fauna to a carnivoran-carnivore fauna coincides with other ecological changes in Afro-Arabia as tectonic conditions in the African Rift System altered climatic conditions and facilitated faunal exchange with Eurasia. Fossil bearing deposits in the Nsungwe Formation in southwestern Tanzania are precisely dated to ~25.2 Ma (late Oligocene), preserving a late Paleogene Afro-Arabian fauna on the brink of environmental transition, including the earliest fossil evidence of the split between Old World monkeys and apes. Here we describe a new hyaenodont from the Nsungwe Formation, <i>Pakakali rukwaensis</i> gen. et sp. nov., a bobcat-sized taxon known from a portion of the maxilla that preserves a deciduous third premolar and alveoli of dP⁴ and M¹. The crown of dP³ bears an elongate parastyle and metastyle and a small, blade-like metacone. Based on alveolar morphology, the two more distal teeth successively increased in size and had relatively large protocones. Using a hyaenodont character-taxon matrix that includes deciduous dental characters, Bayesian phylogenetic methods resolve <i>Pakakali</i> within the clade Hyainailouroidea. A Bayesian biogeographic analysis of phylogenetic results resolve the <i>Pakakali</i> clade as Afro-Arabian in origin, demonstrating that this small carnivorous mammal was part of an endemic Afro-Arabian lineage that persisted into the Miocene. Notably, <i>Pakakali</i> is in the size range of carnivoran forms that arrived and began to diversify in the region by the early Miocene. The description of <i>Pakakali</i> is important for exploring hyaenodont ontogeny and potential influences of Afro-Arabian tectonic events upon mammalian evolution, providing a deep time perspective on the stability of terrestrial carnivore niches through time.</p></div

Geological context of Nsungwe 2 locality.

<p>Nsungwe 2 (yellow star in all portions of the figure) is a fossiliferous locality in the Songwe Member of the Nsungwe Formation in the Rukwa Rift Basin of southwestern Tanzania. <b>A</b>, The context of the Rukwa Rift Basin in Africa and <b>B</b>, in Tanzania. <b>C</b>, Geological map of the Nsungwe Formation and surrounding outcrop. <b>D</b>, Stratigraphic column of the fossiliferous section of the Songwe Member of the Nsungwe Formation with magnetostratigraphic correlations mapped through the section. Radiometric date of 25.2 Ma inferred from U-Pb zircon dating (see [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.ref027" target="_blank">27</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.ref037" target="_blank">37</a>]). <b>Ms</b>, Mudstone; <b>Ss</b>, Sandstone; <b>Cs</b>, Conglomerate; <b>Striped</b>, Volcanic tuff; <b>VGP lat</b>, virtual geomagnetic pole latitude; <b>Black</b>, normal polarity; <b>White</b>; reverse polarity.</p

Statistics related to major Afro-Arabian hyaenodont clades.

<p>Statistics related to major Afro-Arabian hyaenodont clades.</p

Tooth size and carnassialization in Afro-Arabian carnivora and Hyaenodonta.

<p>Tooth size and carnassialization in Afro-Arabian carnivora and Hyaenodonta.</p

<i>Pakakali</i> dP³ compared with dP³ of other hyainailouroids.

<p>(<b>A</b>) Digital model of <i>Pakakali rukwaensis</i> right rostral fragment (RRBP 09088) with dP³ in (<b>subscript 1</b>) occlusal view (<b>subscript 2</b>) and buccal (lateral) view with measurements used to estimate the size of M₁ overlaid. Comparative specimens scaled to same size as <i>Pakakali</i> with individual scale bars between the occlusal and buccal view of each specimen: (<b>B</b>) <i>Paroxyaena pavlovi</i> (images of cast of GGM no. Ca-300 and (<b>C</b>) <i>Pterodon dasyuroides</i> (BSPG 1879 XV 642), a hyainailourines from the late Eocene of Europe; (<b>D</b>) <i>Masrasector nananubis</i> (DPC 20882), a teratodontine from the late Eocene of Afro-Arabia and (<b>E</b>) <i>Leakitherium hiwegi</i> (KNM-RU 2949), a hyainailourine from the early Miocene of Afro-Arabia. Note variation in the metacone, paracone, and parastyle in each specimen.</p

Phylogeny and biogeography of Afro-Arabian Hyaenodonta.

<p>The portion of the “allcompat” Bayesian consensus tree containing all Afro-Arabian hyaenodonts included in the Bayesian phylogenetic analysis with BBM biogeographic results summarized in circle graphs over each node. The number in the center of the circle is the posterior probability for each node. The rectangles to the left of the OTU name represent the estimated age of each OTU based on a literature review. Taxa that span a long geological interval reflect either substantial specimen sampling or imprecise dates for localities, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.s003" target="_blank">S3 Appendix</a> for details of each OTU. The black vertical line in each OTU rectangle is the median estimated age of the OTU based on the Bayesian analysis. The bar for <i>Pakakali</i> is narrow because the age of the Nsungwe 2 is known with great precision. The proportion of the circle filled by each color reflects the probability that the clade originated from the corresponding continental area (<b>green</b>, Afro-Arabia; <b>purple</b>, Asia; <b>yellow</b>, Europe; <b>red</b>, North America; <b>grey</b> (on map), continents without hyaenodonts). Branches are colored with the most likely origin for each clade and gradients indicate branches that are likely dispersal events. <i>Pakakali</i> is nested within Hyainailouroidea and Teratodontinae, both clades that most likely originated in Afro-Arabia. The light red vertical bar illustrates the likely interval when Carnivora dispersed to Afro-Arabia and it crosses the hyaenodont lineages that were likely extant on the continent when carnivorans arrived. <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.s009" target="_blank">S1 Fig</a>. and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.s010" target="_blank">S1 Table</a> contain information on the expanded phylogeny of Hyaenodonta.</p

Afro-Arabian Paleogene and early Miocene carnivore morphospace occupation.

<p>A comparison the trigonid ratio for the hyaenodont M₂ and carnivoran M₁ in Afro-Arabia from the late Eocene through early Miocene. The X-axis is average mesiodistal length (mm) of the molars for each taxon included in the analysis as a proxy for body size. Note the scale is not continuous along the X-axis. The Y-axis is geological time expressed as geological ages and absolute age in millions of years (Ma). The timescale is not proportional in the early Miocene to accommodate the dense taxon sample through this interval. Each hyaenodont taxon included in the phylogenetic analysis is placed at the median age estimated by the tip-dating Bayesian analysis. Carnivorans found in the same localities as hyaenodonts in the analysis are placed in the same temporal range. Some taxa are found at multiple localities and the full age range estimated for each taxon is listed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.t002" target="_blank">Table 2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.s002" target="_blank">S2 Appendix</a>. The proportion of the horizontal bar that is colored reflects the proportion of the tooth occupied by the slicing carnassial complex. The proportion of the horizontal bar that is black reflects the proportion of the tooth occupied by the talonid complex. The longer the carnassial complex, the more vertebrate prey was likely incorporated into the diet of the taxon. <b>Orange</b>, Hyaenodonta; <b>Red</b>, Carnivora. <b>Yellow</b>, Prionogalidae. <b>Hyaenodonta: 1</b>, <i>Masrasector nananubis</i>; <b>2</b>, <i>Brycotherium ephalmos</i>; <b>3</b>, <i>Akhnatenavus nefertiticyon</i>; <b>4</b>, <i>“Sinopa” ethiopica</i>; <b>5</b>, <i>Metapterodon markgrafi</i>; <b>6</b>, <i>Apterodon langebadreae</i>; <b>7</b>, <i>Apterodon macrognathus</i>; <b>8</b>, <i>"Pterodon" phiomensis</i>; <b>9</b>, <i>"Pterodon" africanus</i>; <b>10</b>, <i>Akhnatenavus leptognathus</i>; <b>11</b>, <i>Masrasector ligabuei</i>; <b>12</b>, <i>Metasinopa fraasi</i>; <b>13</b>, <i>Metapterodon schlosseri</i>; <b>14</b>, <i>Masrasector aegypticum</i>; <b>15</b>, <i>Quasiapterodon minutus</i>; <b>16</b>, <i>Pterodon syrtos</i>; <b>17</b>, <i>Teratodon</i> (Meswa Bridge); <b>18</b>, <i>Mlanyama sugu</i>; <b>19</b>, <i>Hyainailouros spp</i>.; <b>20</b>, <i>Isohyaenodon matthewi</i>; <b>21</b>, <i>Teratodon</i> (Rusinga); <b>22</b>, <i>Metapterodon kaiseri</i>; <b>23</b>, <i>Isohyaenodon andrewsi</i>; <b>24</b>, <i>Buhakia moghraensis</i>; <b>25</b>, <i>Megistotherium osteothlastes</i>; <b>26</b>, <i>Isohyaenodon pilgrimi</i>; <b>27</b>, <i>Anasinopa libyca</i>; <b>28</b>, <i>Leakitherium hiwegi</i>; <b>29</b>, <i>Anasinopa leakeyi</i>. <b>Carnivora: 30</b>, <i>Mioprionodon hodopeus</i>; <b>31</b>, <i>Mioprionodon pickfordi</i>; <b>32</b>, <i>Legetetia nandii</i>; <b>33</b>, <i>Leptoplesictis namibiensis</i>; <b>34</b>, <i>Kenyalutra songhorensis</i>; <b>35</b>, <i>Ginsburgsmilus napakensis</i>; <b>36</b>, <i>Cynelos euryodon</i>; <b>37</b>, <i>Africanictis schmidtkittleri</i>; <b>38</b>, <i>Stenoplesictis muhoronii</i>; <b>39</b>, <i>Afrosmilus turkanae</i>; <b>40</b>, <i>Kichechia zamanae</i>; <b>41</b>, <i>Leptoplesictis mbitensis</i>; <b>42</b>, <i>Leptoplesictis rangwai</i>; <b>43</b>, <i>Leptoplesictis senutae</i>; <b>44</b>, <i>Herpestides aegypticus</i>; <b>45</b>, <i>Luogale rusingensis</i>; <b>46</b>, <i>Namibictis senuti</i>; <b>47</b>, <i>Diamantofelis ferox</i>; <b>48</b>, <i>Herpestides aequatorialis</i>; <b>49</b>, <i>Ketketictis solida</i>; <b>50</b>, <i>Moghradictis nedjema</i>; <b>51</b>, <i>Afrocyon burolleti</i>; <b>52</b>, <i>Africanictis meini</i>; <b>53</b>, <i>Africanictis hyaenoides</i>; <b>54</b>, <i>Amphicyon giganteus</i>; <b>55</b>, <i>Ysengrinia ginsburgi</i>; <b>56</b>, <i>Orangictis gariepensis</i>; <b>57</b>, <i>Namafelis minor</i>; <b>58</b>, <i>Syrtosmilus syrtensis</i>. <b>Prionogalidae: 59</b>, <i>Namasector soriae</i>; <b>60</b>, <i>Prionogale breviceps</i>.</p

Taxonomic affinities of the enigmatic <i>Prionogale breviceps</i>, early Miocene, Kenya

<p><i>Prionogale breviceps</i> is a tiny carnivorous mammal from the early Miocene of eastern Africa. Originally, specimens were interpreted as the adult morphology of the taxon. The dentition did not obviously align <i>Prionogale</i> with the carnivorous lineages present in Afro-Arabia during the early Miocene: Hyaenodonta and Carnivora. When <i>Namasector</i> was discovered in Namibia, the small taxa were placed together in Prionogalidae and aligned with Hyaenodonta. In this study, based on comparisons to hyaenodont specimens preserving deciduous dentition, the holotype of <i>Prionogale</i> is reinterpreted as preserving dP3 and dP4. Some of the lower dental specimens attributed to the taxon preserve dp4. The holotype of <i>Namasector</i> also preserves deciduous dental material. A phylogenetic analysis that includes deciduous dental characters for a broader sample of hyaenodonts resolved Prionogalidae as a clade. Understanding of the deciduous dentition of <i>Prionogale</i> allows future analyses to compare homologous morphology, and to explore the environmental factors that shaped carnivorous mammal evolution through the Miocene.</p

<i>Pakakali rukwaensis</i> holotype (RRBP 09088).

<p>Rostrum fragment from the right maxilla of <i>Pakakali rukwaensis</i> discovered at Nsungwe 2 locality, Nsungwe Formation, late Oligocene (~25.2 Ma) with dP³, alveoli of dP⁴ (or P⁴) and M¹ in (<b>A</b>) occlusal view, (<b>B</b>) occlusal-lingual view, (<b>C</b>) buccal (lateral) view, (<b>D</b>) lingual (medial) view, (<b>E</b>) dorsal view, (<b>F</b>) mesial (rostral) view, (<b>G</b>) distal (caudal) view. Digital model of the specimen is available as <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0185301#pone.0185301.s004" target="_blank">S4 Appendix</a> and as Project 303 at Morphosource.</p

Caudal vertebrae of Colubroid Morphotype C (RRBP 07674) from the late Oligocene of Tanzania with comparison to extant <i>Duberria lutrix</i>.

<p>A, RRBP 07674, caudal vertebra; B, <i>Duberria lutrix</i> (CM 145121), caudal series.</p