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Fossils and Monophyly of Afrotheria: a Review of the Current Data A.O 146 A.O. Averianov, A.V. Lopatin Сборник трудов Зоологического музея МГУ им. М.В. Ломоносова Archives of Zoological Museum of Lomonosov Moscow State University Том / Vol. 54 Cтр. / Pр. 146–160 FOSSILS AND MONOPHYLY OF AFROTHERIA: A REVIEW OF THE CURRENT DATA A.O. Averianov1, A.V. Lopatin 1Zoological Institute, Russian Academy of Sciences; [email protected] Two groups of “afrotherians”, Macroscelidea and Paenungulata (Hy- racoidea, Proboscidea, Sirenia) are related to archaic ungulates (“con- dylarthrs”) Apheliscidae and Phenacodontidae, respectively. In such a case, however, the clade including Apheliscidae, Macroscelidea, Phe- nacodontidae, and Paenungulata should also include Perissodactyla, which makes Afrotheria paraphyletic. Tenrecoidea are likely related to an insectivorous grade Adapisoriculidae, which may belong to a pre-zhelestid radiation of the stem placental mammals. This hypothesis, if correct, im- plies an enormous phylogenetic gap between Tenrecoidea and the clade in cluding Macroscelidea and Paenungulata having originated from a more advanced group of archaic ungulates. The latter treatment invalidates the concept of Afrotheria as a group of closely related mammals originated in Africa. The origin of Tubulidentata is still obscure. ПАЛЕОНТОЛОГИЧЕСКАЯ ЛЕТОПИСЬ И МОНОФИЛИЯ AFROTHERIA: ОБЗОР СОВРЕМЕННЫХ ДАННЫХ А.О. Аверьянов1, А.В. Лопатин 1Зоологический институт РАН; [email protected] Две группы «афротериев», Macroscelidea и Paenungulata (Hyracoidea, Proboscidea, Sirenia), связаны происхождением с архаичными копыт- ными («кондиляртрами») Apheliscidae и Phenacodontidae, соответст- венно. В таком случае, однако, клада, включающая Apheliscidae, Mac- roscelidea, Phenacodontidae и Paenungulata, должна также включать Perissodactyla, что делает Afrotheria парафилетической группой. Ten- recoidea наиболее вероятно происходят от млекопитающих насеко- моядного уровня организации, Adapisoriculidae, которые могут при- надлежать к преджелестидной радиации стволовых плацентарных. Если эта гипотеза верна, то между Tenrecoidea и кладой, содержащей Macroscelidea и Paenungulata и происходящей от более продвинутых архаичных копытных, существует огромный филогенетический раз- © A.O. Averianov, A.V. Lopatin, 2016. Fossils and monophyly of Afrotheria 147 рыв. Эта трактовка делает концепцию Afrotheria, как группы возник- ших в Африке близкородственных млекопитающих, невалидной. Про- исхождение Tubulidentata пока не ясно. 1. Introduction Seiffert (2007) provided another com- The mammal phylogenetic tree has been bined analysis based on genomic data (nu- reshaped signifi cantly during past decades cleotide data, chromosomal associations, and by the molecular data (for review, see Ave- retroposons) and 400 morphological charac- rianov, Lopatin, 2014). The biggest surprise ters scored across 16 extant and 35 extinct came from the clade of endemic African afrotherians. A NONA analysis of his mor- mammals that included Recent groups Ten- phological data matrix with 10,000 ratchet recoidea (tenrecs and golden moles), Macro- replications (Goloboff, 1999) produced 38 scelidea (elephant shrews, or sengis), Tubu- most parsimonious trees with their consist- lidentata (aardvarks), Hyracoidea (hyraxes), ency index of 0.28 and retention index of Sirenia (sea cows), and Proboscidea (probos- 0.62. On the strict consensus tree, there were cideans) (Springer et al., 1997, 1999, 2004; no monophyletic Afrotheria, with Tenreco- Stanhope et al., 1998a,b; Madsen et al., 2001; idea (= Afrosoricida) being nested within Murphy et al., 2001; van Dijk et al., 2001; the Lipotyphla. Malia et al., 2002). Tabuce et al. (2007) described new Ter- Several morphological characters has tiary mammals from North Africa they tho- been proposed as the afrotherian synapo- ught to “reinforce the molecular Afrotheria morphies, including high count of dorsal clade”. However, no any tenrecoid taxon was vertebrae (Sánchez-Villagra et al., 2007), included in their data matrix and the clade characters of placenta (Mess, Carter, 2006), being “reinforced” was actually just Macro- shape of ankle bones (Seiffert, 2007; Tabuce scelidea + Paeningulata (Tabuce et al., 2007, et al., 2007), and late eruption of permanent fi g. 4). There and in a previous analysis (Zack teeth (Asher, Lehmann, 2008). However, all et al., 2005), macroscelideans and/or hyraxes these characters are either retention of plesio- are linked to the North American and Euro- morphic eutherian condition or parallelisms. pean apheliscid condylarths which disrupt However, “afrotherians” appeared to be the concept of Afrotheria as a monophyletic non-monophyletic on a morphology-based clade of the endemic African mammals. tree of Asher et al. (2003, fi g. 3), in which In the most recent morphological analysis Tubulidentata were shown to link to Xenar- utilizing an enormous number of phenotypic thra, Paenungulata to Ungulata, Afrosoricida characters (4541), a morphological consen- to Lipotyphla, and Macroscelidea to Glires. sus tree implies no monophyletic Afrotheria Few morphological phylogenetic analy- (O’Leary et al., 2013, supplementary fi g. ses that include all afrotherian groups do not S2). Golden moles are linked to the true support monophyletic status of the Afroth- moles, tenrecs to the hedgehogs, and ele- eria. According to a combined analysis of phant shrews to the extinct North American morphological and molecular data by Asher leptictids adapted to ricocheted locomotion. et al. (2003), the crown group Afrotheria in- Evidently, both molecular sequence and cludes embrithopods, Plesiorycteropus, des- parsimony morphological analyses have their mostylians, the “condylarths” Hyopsodus, own limitations. The lack of the intermediate Meniscotherium, and possibly Phenacodus. taxa which would fi ll the gaps between the 148 A.O. Averianov, A.V. Lopatin Recent clades is critical for the both analyses. and fully developed lower molar talonids, In such a situation, the only possible way to while Qatranilestes, known from the lower solve the afrotherian problem seems to be the dentition only, has reduced molar talonids. tracing the possible ancestors of the modern Widanelfarasia is similar with Protenrec and clades in the fossil record. In this article, we some modern tenrecids in such derived char- review the known fossil record of the groups acters as ectocrista and ectofossa on P4, distal included in Afrotheria by the molecular data. root of P3 placed mesial to the P4 protocone, and “stepped” transition between P4 and an- 2. Review of the taxa terior premolars (Seiffert et al., 2007). Thus phylogenetic position of Widanelfarasia as 2.1. Tenrecoidea a stem tenrecid is a more preferable hypoth- The suprafamiliar nomenclature of this esis (Seiffert et al., 2007; Seiffert, 2010). clade is confusing. We follow Asher (2005), Dilambdogale was found to be a sister taxon Asher (2010), and Asher and Helgen (2010) to Widanelfarasia and it also shows incipient in using Tenrecoidea (=Afrosoricida, = Ten- ectorista and ectofossa on P4 (Seiffert, 2010). recomorpha) for the clade including Tenreci- dae + Chrysochloridae. The adapisoriculids 2.1.2. Chrysochloridae Todralestes variabilis and Afrodon chleuhi There are 21 modern species of golden- from the late Paleocene of Morocco (Gheer- moles (Chrysochloridae) distributed in sub- brant, 1994, 1995) have been placed as stem Saharan Africa (Asher et al., 2010). The tenrecoids in the phylogenetic analysis by modern species, or distinct species very close Seiffert (2010). to the modern ones, are known from the Plio- Pleistocene of South Africa (Broom, 1941, 2.1.1. Tenrecidae 1948; de Graaff, 1957; Asher, 2010; Asher, There are 30 modern species of this clade Avery, 2010). The generically distinct extinct distributed in Africa (Potamogalinae) and golden mole Prochrysochloris miocaenicus Madagascar (Tenrecinae) (Asher, Hofreiter, is known from the early Miocene of Kenya 2006; Asher, 2010). Three extinct taxa from and possibly Namibia (Butler, Hopwood, the early Miocene of Kenya and Uganda, 1957; Butler, 1984; Mein, Pickford, 2003; Protenrec tricuspis, Erythrozootes chamer- Asher, 2010). It differs from the modern pes, and Parageogale aletris, are members chrysochlorids by unreduced posterior mo- of the crown-group Tenrecidae (Butler, 1984; lars (a normal M3 is present, M2 is widest Poduschka, Poduschka, 1985; Asher, 2010). upper molar), smaller and less molariform Another species, Protenrec butleri, is known anterior upper premolars, and less reduced from the early Miocene of Namibia (Mein, talonids on lower molars. Pickford, 2003). Jawharia tenrecoides and All these traits are plesiomorphic rela- Qatranilestes oligocaenus from the early tive to the modern taxa, which have M3 lost Oligocene of Egypt and Widanelfarasia or very reduced, M2 reduced, and lower bowni, W. rasmusseni, and Dilambdogale molar talonids small single cusped or lack- gheerbranti from the late Eocene of Egypt ing altogether. Modern chrysochlorids and are either stem tenrecids or stem tenrecoids Prochrysochloris have zalambdodont den- (Seiffert, Simons, 2000; Seiffert et al., 2007; tition with reduced metaconid and talonid Seiffert, 2010). Widanelfarasia and Dilamb- basin (McDowell, 1958; Asher, Sánchez-Vil- dogale both have dilambdodont upper molars lagra, 2005). The phylogenetic position of Fossils and monophyly of Afrotheria 149 Prochrysochloris is likely outside the crown Herodotius pattersoni from the late Eocene group Chrysochloridae (Asher, 2010). of Egypt, Nementchatherium senarhense The oldest named stem taxon of
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