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Resolving the relationships of Paleocene placental mammals.

ABSTRACT: The 'Age of Mammals' began in the Paleocene epoch, the 10 million year interval immediately following the Cretaceous-Palaeogene mass extinction. The apparently rapid shift in mammalian ecomorphs from small, largely insectivorous forms to many small-to-large-bodied, diverse taxa has driven a hypothesis that the end-Cretaceous heralded an adaptive radiation in placental mammal evolution. However, the affinities of most Paleocene mammals have remained unresolved, despite significant advances in understanding the relationships of the extant orders, hindering efforts to reconstruct robustly the origin and early evolution of placental mammals. Here we present the largest cladistic analysis of Paleocene placentals to date, from a data matrix including 177 taxa (130 of which are Palaeogene) and 680 morphological characters. We improve the resolution of the relationships of several enigmatic Paleocene clades, including families of 'condylarths'. Protungulatum is resolved as a stem eutherian, meaning that no crown-placental mammal unambiguously pre-dates the Cretaceous-Palaeogene boundary. Our results support an Atlantogenata-Boreoeutheria split at the root of crown Placentalia, the presence of phenacodontids as closest relatives of Perissodactyla, the validity of Euungulata, and the placement of Arctocyonidae close to Carnivora. Periptychidae and Pantodonta are resolved as sister taxa, Leptictida and Cimolestidae are found to be stem eutherians, and Hyopsodontidae is highly polyphyletic. The inclusion of Paleocene taxa in a placental phylogeny alters interpretations of relationships and key events in mammalian evolutionary history. Paleocene mammals are an essential source of data for understanding fully the biotic dynamics associated with the end-Cretaceous mass extinction. The relationships presented here mark a critical first step towards accurate reconstruction of this important interval in the evolution of the modern fauna.

SUBMITTER: Halliday TJ

PROVIDER: S-EPMC6849585 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Resolving the relationships of Paleocene placental mammals.

Halliday Thomas J D TJ Upchurch Paul P Goswami Anjali A

Biological reviews of the Cambridge Philosophical Society 20151221 1

The 'Age of Mammals' began in the Paleocene epoch, the 10 million year interval immediately following the Cretaceous-Palaeogene mass extinction. The apparently rapid shift in mammalian ecomorphs from small, largely insectivorous forms to many small-to-large-bodied, diverse taxa has driven a hypothesis that the end-Cretaceous heralded an adaptive radiation in placental mammal evolution. However, the affinities of most Paleocene mammals have remained unresolved, despite significant advances in und ...[more]

PMID: 28075073

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Project description: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.

Project description:BackgroundGenome-wide studies of intron dynamics in mammalian orthologous genes have found convincing evidence for loss of introns but very little for intron turnover. Similarly, large-scale analysis of intron dynamics in a few vertebrate genomes has identified only intron losses and no gains, indicating that intron gain is an extremely rare event in vertebrate evolution. These studies suggest that the intron-rich genomes of vertebrates do not allow intron gain. The aim of this study was to search for evidence of de novo intron gain in domesticated genes from an analysis of their exon/intron structures.ResultsA phylogenomic approach has been used to analyse all domesticated genes in mammals and chordates that originated from the coding parts of transposable elements. Gain of introns in domesticated genes has been reconstructed on well established mammalian, vertebrate and chordate phylogenies, and examined as to where and when the gain events occurred. The locations, sizes and amounts of de novo introns gained in the domesticated genes during the evolution of mammals and chordates has been analyzed. A significant amount of intron gain was found only in domesticated genes of placental mammals, where more than 70 cases were identified. De novo gained introns show clear positional bias, since they are distributed mainly in 5' UTR and coding regions, while 3' UTR introns are very rare. In the coding regions of some domesticated genes up to 8 de novo gained introns have been found. Intron densities in Eutheria-specific domesticated genes and in older domesticated genes that originated early in vertebrates are lower than those for normal mammalian and vertebrate genes. Surprisingly, the majority of intron gains have occurred in the ancestor of placentals.ConclusionsThis study provides the first evidence for numerous intron gains in the ancestor of placental mammals and demonstrates that adequate taxon sampling is crucial for reconstructing intron evolution. The findings of this comprehensive study slightly challenge the current view on the evolutionary stasis in intron dynamics during the last 100 - 200 My. Domesticated genes could constitute an excellent system on which to analyse the mechanisms of intron gain in placental mammals.

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Resolving the relationships of Paleocene placental mammals.

Publications

Resolving the relationships of Paleocene placental mammals.

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