Developmental origin underlies evolutionary rate variation across the placental skull.

The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

Attenuated evolution of mammals through the Cenozoic.

The Cenozoic diversification of placental mammals is the archetypal adaptive radiation. Yet, discrepancies between molecular divergence estimates and the fossil record fuel ongoing debate around the timing, tempo, and drivers of this radiation. Analysis of a three-dimensional skull dataset for living and extinct placental mammals demonstrates that evolutionary rates peak early and attenuate quickly. This long-term decline in tempo is punctuated by bursts of innovation that decreased in amplitude over the past 66 million years. Social, precocial, aquatic, and herbivorous species evolve fastest, especially whales, elephants, sirenians, and extinct ungulates. Slow rates in rodents and bats indicate dissociation of taxonomic and morphological diversification. Frustratingly, highly similar ancestral shape estimates for placental mammal superorders suggest that their earliest representatives may continue to elude unequivocal identification.

Rapid morphological evolution in placental mammals post-dates the origin of the crown group.

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.

Resolving the relationships of Paleocene placental mammals.

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.

Testing the inhibitory cascade model in Mesozoic and Cenozoic mammaliaforms.

BACKGROUND: Much 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. RESULTS: Results 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. CONCLUSIONS: Overall, 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.