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.

In the aftermaths of mass extinction events, during radiations of clades, and in several other evolutionary scenarios, there is often a decoupling of taxonomic diversity and morphological disparity. The placental mammal radiation after the end‐Cretaceous mass extinction is one of the archetypal adaptive radiations, but the change in morphological disparity of the entire skeleton has never been quantified across this important boundary. We reconstruct ancestral morphologies of 680 discrete morphological characters onto dated phylogenies of 177 mostly Cretaceous and Palaeogene eutherians (placental mammals and their stem relatives). Using a new approach to incorporate morphologies representing ghost lineages, we assess three measures of morphological disparity (sum of ranges, sum of variances and mean pairwise dissimilarity) across stage‐level time bins within the Cretaceous and Palaeogene. We find that the range‐based metric suggests that eutherian disparity increased immediately after the end‐Cretaceous mass extinction, while both variance‐based metrics declined from the Campanian to the Maastrichtian, but showed no change in disparity from the Maastrichtian to the Puercan – the first North American Land Mammal Age of the Paleocene. Increases in variance‐based metrics lag behind the range‐based metric and per‐lineage accumulation rate, suggesting that the response of mammals to the Cretaceous–Palaeogene event was characterized by an early radiation that increased overall morphospace occupation, followed later by specialization that resulted in increased dissimilarity.

BackgroundMuch of the current research in the growing field of evolutionary development concerns relating developmental pathways to large-scale patterns of morphological evolution, with developmental constraints on variation, and hence diversity, a field of particular interest. Tooth morphology offers an excellent model system for such ‘evo-devo’ studies, because teeth are well preserved in the fossil record, and are commonly used in phylogenetic analyses and as ecological proxies. Moreover, tooth development is relatively well studied, and has provided several testable hypotheses of developmental influences on macroevolutionary patterns. The recently-described Inhibitory Cascade (IC) Model provides just such a hypothesis for mammalian lower molar evolution. Derived from experimental data, the IC Model suggests that a balance between mesenchymal activators and molar-derived inhibitors determines the size of the immediately posterior molar, predicting firstly that molars either decrease in size along the tooth row, or increase in size, or are all of equal size, and secondly that the second lower molar should occupy one third of lower molar area. Here, we tested the IC Model in a large selection of taxa from diverse extant and fossil mammalian groups, ranging from the Middle Jurassic (~176 to 161 Ma) to the Recent.ResultsResults show that most taxa (~65%) fell within the predicted areas of the Inhibitory Cascade Model. However, members of several extinct groups fell into the regions where m2 was largest, or rarely, smallest, including the majority of the polyphyletic “condylarths”. Most Mesozoic mammals fell near the centre of the space with equality of size in all three molars. The distribution of taxa was significantly clustered by diet and by phylogenetic group.ConclusionsOverall, the IC Model was supported as a plesiomorphic developmental system for Mammalia, suggesting that mammal tooth size has been subjected to this developmental constraint at least since the divergence of australosphenidans and boreosphenidans approximately 180 Ma. Although exceptions exist, including many ‘condylarths’, these are most likely to be secondarily derived states, rather than alternative ancestral developmental models for Mammalia.

Resolving the timing and pattern of early placental mammal evolution has been confounded by conflict among divergence date estimates from interpretation of the fossil record and from molecular-clock dating studies. Despite both fossil occurrences and molecular sequences favouring a Cretaceous origin for Placentalia, no unambiguous Cretaceous placental mammal has been discovered. Investigating the differing patterns of evolution in morphological and molecular data reveals a possible explanation for this conflict. Here, we quantified the relationship between morphological and molecular rates of evolution. We show that, independent of divergence dates, morphological rates of evolution were slow relative to molecular evolution during the initial divergence of Placentalia, but substantially increased during the origination of the extant orders. The rapid radiation of placentals into a highly morphologically disparate Cenozoic fauna is thus not associated with the origin of Placentalia, but post-dates superordinal origins. These findings predict that early members of major placental groups may not be easily distinguishable from one another or from stem eutherians on the basis of skeleto-dental morphology. This result supports a Late Cretaceous origin of crown placentals with an ordinal-level adaptive radiation in the early Paleocene, with the high relative rate permitting rapid anatomical change without requiring unreasonably fast molecular evolutionary rates. The lack of definitive Cretaceous placental mammals may be a result of morphological similarity among stem and early crown eutherians, providing an avenue for reconciling the fossil record with molecular divergence estimates for Placentalia.