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Convergence of Afrotherian and Laurasiatherian Ungulate-Like Mammals: First Morphological Evidence from the Paleocene of Morocco.

ABSTRACT: Molecular-based analyses showed that extant "ungulate" mammals are polyphyletic and belong to the two main clades Afrotheria (Paenungulata) and Laurasiatheria (Euungulata: Cetartiodactyla-Perissodactyla). However, paleontological and neontological studies hitherto failed to demonstrate the morphological convergence of African and Laurasian "ungulate" orders. They support an "Altungulata" group including the Laurasian order Perissodactyla and the African superorder Paenungulata and characterized especially by quadritubercular and bilophodont molars adapted for a folivorous diet. We report new critical fossils of one of the few known African condylarth-like mammal, the enigmatic Abdounodus from the middle Paleocene of Morocco. They show that Abdounodus and Ocepeia display key intermediate morphologies refuting the homology of the fourth main cusp of upper molars in Paenungulata and Perissodactyla: Paenungulates unexpectedly have a metaconule-derived pseudohypocone, instead of a cingular hypocone. Comparative and functional dental anatomy of Abdounodus demonstrates indeed the convergence of the quadritubercular and bilophodont pattern in "ungulates". Consistently with our reconstruction of the structural evolution of paenungulate bilophodonty, the phylogenetic analysis relates Abdounodus and Ocepeia to Paenungulata as stem taxa of the more inclusive new clade Paenungulatomorpha which is distinct from the Perissodactyla and Anthracobunidae. Abdounodus and Ocepeia help to identify the first convincing synapomorphy within the Afrotheria-i.e., the pseudohypocone-that demonstrates the morphological convergence of African and Laurasian ungulate-like placentals, in agreement with molecular phylogeny. Abdounodus and Ocepeia are the only known representatives of the early African ungulate radiation predating the divergence of extant paenungulate orders. Paenungulatomorpha evolved in Africa since the early Tertiary independently from laurasiatherian euungulates and "condylarths" such as apheliscids. The rapid early Tertiary radiation of the Afrotheria and Paenungulatomorpha, as illustrated by the Paleocene Moroccan mammals, is concurrent with that of the Laurasiatheria in a general, explosive mammal evolution in both the South and North Tethyan continents following the K/Pg event.

SUBMITTER: Gheerbrant E

PROVIDER: S-EPMC4934866 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:While key early(iest) fossils were recently discovered for several crown afrotherian mammal orders, basal afrotherians, e.g., early Cenozoic species that comprise sister taxa to Paenungulata, Afroinsectiphilia or Afrotheria, are nearly unknown, especially in Africa. Possible stem condylarth-like relatives of the Paenungulata (hyraxes, sea-cows, elephants) include only Abdounodus hamdii and Ocepeia daouiensis from the Selandian of Ouled Abdoun Basin, Morocco, both previously only documented by lower teeth. Here, we describe new fossils of Ocepeia, including O.grandis n. sp., and a sub-complete skull of O. daouiensis, the first known before the Eocene for African placentals. O.daouiensis skull displays a remarkable mosaic of autapomophic, ungulate-like and generalized eutherian-like characters. Autapomorphies include striking anthropoid-like characters of the rostrum and dentition. Besides having a basically eutherian-like skull construction, Ocepeia daouiensis is characterized by ungulate-like, and especially paenungulate-like characters of skull and dentition (e.g., selenodonty). However, some plesiomorphies such as absence of hypocone exclude Ocepeia from crown Paenungulata. Such a combination of plesiomorphic and derived characters best fits with a stem position of Ocepeia relative to Paenungulata. In our cladistic analyses Ocepeia is included in Afrotheria, but its shared derived characters with paenungulates are not optimized as exclusive synapomorphies. Rather, within Afrotheria Ocepeia is reconstructed as more closely related to insectivore-like afroinsectiphilians (i.e., aardvarks, sengis, tenrecs, and golden moles) than to paenungulates. This results from conflict with undetected convergences of Paenungulata and Perissodactyla in our cladistic analysis, such as the shared bilophodonty. The selenodont pattern best supports the stem paenungulate position of Ocepeia; that, however, needs further support. The remarkable character mosaic of Ocepeia makes it the first known "transitional fossil" between insectivore-like and ungulate-like afrotherians. In addition, the autapomorphic family Ocepeiidae supports the old--earliest Tertiary or Cretaceous--endemic evolution of placentals in Africa, in contrast to hypotheses rooting afrotherians in Paleogene Laurasian "condylarths".

Project description:BackgroundAfrotheria comprises a newly recognized clade of mammals with strong molecular evidence for its monophyly. In contrast, morphological data uniting its diverse constituents, including elephants, sea cows, hyraxes, aardvarks, sengis, tenrecs and golden moles, have been difficult to identify. Here, we suggest relatively late eruption of the permanent dentition as a shared characteristic of afrotherian mammals. This characteristic and other features (such as vertebral anomalies and testicondy) recall the phenotype of a human genetic pathology (cleidocranial dysplasia), correlations with which have not been explored previously in the context of character evolution within the recently established phylogeny of living mammalian clades.ResultsAlthough data on the absolute timing of eruption in sengis, golden moles and tenrecs are still unknown, craniometric comparisons for ontogenetic series of these taxa show that considerable skull growth takes place prior to the complete eruption of the permanent cheek teeth. Specimens showing less than half (sengis, golden moles) or two-thirds (tenrecs, hyraxes) of their permanent cheek teeth reach or exceed the median jaw length of conspecifics with a complete dentition. With few exceptions, afrotherians are closer to median adult jaw length with fewer erupted, permanent cheek teeth than comparable stages of non-afrotherians. Manatees (but not dugongs), elephants and hyraxes with known age data show eruption of permanent teeth late in ontogeny relative to other mammals. While the occurrence of delayed eruption, vertebral anomalies and other potential afrotherian synapomorphies resemble some symptoms of a human genetic pathology, these characteristics do not appear to covary significantly among mammalian clades.ConclusionMorphological characteristics shared by such physically disparate animals such as elephants and golden moles are not easy to recognize, but are now known to include late eruption of permanent teeth, in addition to vertebral anomalies, testicondy and other features. Awareness of their possible genetic correlates promises insight into the developmental basis of shared morphological features of afrotherians and other vertebrates.

Project description:BackgroundThe placental mammalian clade Afrotheria is now supported by diverse forms of genomic data, but interordinal relationships within, and morphological support for, the group remains elusive. As a means for addressing these outstanding problems, competing hypotheses of afrotherian interordinal relationships were tested through simultaneous parsimony analysis of a large data set (> 4,590 parsimony informative characters) containing genomic data (> 17 kb of nucleotide data, chromosomal associations, and retroposons) and 400 morphological characters scored across 16 extant and 35 extinct afrotherians.ResultsParsimony analysis of extant taxa alone recovered the interordinal topology (Afrosoricida, ((Macroscelidea, Tubulidentata), (Hyracoidea, (Proboscidea, Sirenia)))). Analysis following addition of extinct taxa instead supported Afroinsectivora (Afrosoricida + Macroscelidea) and Pseudoungulata (Tubulidentata + Paenungulata), as well as Tethytheria (Proboscidea + Sirenia). This latter topology is, however, sensitive to taxon deletion and different placements of the placental root, and numerous alternative interordinal arrangements within Afrotheria could not be statistically rejected. Relationships among extinct stem members of each afrotherian clade were more stable, but one alleged stem macroscelidean (Herodotius) never grouped with that clade and instead consistently joined pseudoungulates or paenungulates. When character transformations were optimized onto a less resolved afrotherian tree that reflects uncertainty about the group's interordinal phylogeny, a total of 21 morphological features were identified as possible synapomorphies of crown Afrotheria, 9 of which optimized unambiguously across all character treatments and optimization methods.ConclusionInstability in afrotherian interordinal phylogeny presumably reflects rapid divergences during two pulses of cladogenesis - the first in the Late Cretaceous, at and just after the origin of crown Afrotheria, and the second in the early Cenozoic, with the origin of crown Paenungulata. Morphological evidence for divergences during these two pulses either never existed or has largely been "erased" by subsequent evolution along long ordinal branches. There may, nevertheless, be more morphological character support for crown Afrotheria than is currently assumed; the features identified here as possible afrotherian synapomorphies can be further scrutinized through future phylogenetic analyses with broader taxon sampling, as well as recovery of primitive fossil afrotherians from the Afro-Arabian landmass, where the group is likely to have first diversified.

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Convergence of Afrotherian and Laurasiatherian Ungulate-Like Mammals: First Morphological Evidence from the Paleocene of Morocco.

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