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, 92 (1), 521-550

Resolving the Relationships of Paleocene Placental Mammals

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Resolving the Relationships of Paleocene Placental Mammals

Thomas J D Halliday et al. Biol Rev Camb Philos Soc.

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.

Keywords: Condylarthra; Palaeogene; Placentalia; evolution; palaeontology; phylogeny; radiation.

Figures

Figure 1
Figure 1
A depiction, in broad terms, of changes in understanding of the relationships of placental mammals over the last 20 years. (A) Broad understanding of placental mammal relationships prior to the advent of molecular data. ‘Condylarth’ families were considered basal to Ungulata, a number of plesiomorphic taxa were grouped together as Insectivora, whales were considered a separate order, and pangolins were joined with xenarthrans in Edentata. (B) The current consensus on placental mammal phylogeny. While the relationships of extant groups are clear – Cetacea is a subgroup of Artiodactyla, Carnivora and Pholidota are sister taxa, Ungulata and Insectivora are polyphyletic – the relationships of Paleocene taxa have become far more uncertain. In both, dotted lines represent uncertainty.
Figure 2
Figure 2
The constraint applied to all analyses, derived from the molecular understanding of the relationships of extant placental mammal groups. In CM and DM analyses, Xenarthra was composed of Chaetophractus, Bradypus and Tamandua; Paenungulata: Eritherium and Procavia; Tenrecidae: Potamogale; Macroscelidea: Chambius and Rhynchocyon. Glires was composed of Tribosphenomys, Paramys and Gomphos; Scandentia: Tupaia and Ptilocercus; Dermoptera: Cynocephalus; Primates: Saxonella , Cantius, and Adapis. Pholidota was composed of Eomanis and Eurotamandua, Carnivoramorpha by Miacis and Viverravus. Eulipotyphla was represented by Domnina, Oreotalpa, Blarina, Solenodon and Echinosorex. Chiroptera was represented by Pteropus, Perissodactyla by Eohippus and Hyracotherium, Cetacea by Rodhocetus, and other artiodactyls by Gobiohyus, Poebrotherium, Leptomeryx and Elomeryx. In the CF and DF analyses, additional taxa were, for Xenarthra, Utaetus; Dilambdogale was added in a polytomy with Macroscelidea and Tenrecidae within Afroinsectiphilia; for Glires, Rhombomylus; for Dermoptera Elpidophorus, Worlandia and Plagiomene; for Primates, Elphidotarsius, Plesiadapis and Notharctus; for Carnivoramorpha, Didymictis, Vulpavus, Protictis and Uintacyon; for Eulipotyphla, Litocherus, Uropsilus and Centetodon; for Chiroptera, Onychonycteris and Icaronycteris; for Perissodactyla, Heptodon, Homogalax, Litolophus and Lambdotherium; and for Cetacea, Pakicetus. In the CP and DP analyses, Purgatorius was further constrained within Primates.
Figure 3
Figure 3
Strict consensus of all discrete, unconstrained (DU) trees within one step of the most parsimonious trees. Colours represent members of extant orders as follows: pink, Xenarthra; purple, Afrotheria; sky blue, Glires; light blue, Scandentia; mid‐blue, Dermoptera; royal blue, primates; brown, Eulipotyphla; dark green, Artiodactyla; light green, Perissodactyla; yellow, Chiroptera; orange, Pholidota; red, Carnivora.
Figure 4
Figure 4
Strict consensus of trees derived from the discrete data set with the full constraints applied (DF analysis). Colours are as in Fig. 3.

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