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.
The effect of the Cretaceous–Palaeogene (K–Pg) mass extinction on the evolution of many groups, including placental mammals, has been hotly debated. The fossil record suggests a sudden adaptive radiation of placentals immediately after the event, but several recent quantitative analyses have reconstructed no significant increase in either clade origination rates or rates of character evolution in the Palaeocene. Here we use stochastic methods to date a recent phylogenetic analysis of Cretaceous and Palaeocene mammals and show that Placentalia likely originated in the Late Cretaceous, but that most intraordinal diversification occurred during the earliest Palaeocene. This analysis reconstructs fewer than 10 placental mammal lineages crossing the K–Pg boundary. Moreover, we show that rates of morphological evolution in the 5 Myr interval immediately after the K–Pg mass extinction are three times higher than background rates during the Cretaceous. These results suggest that the K–Pg mass extinction had a marked impact on placental mammal diversification, supporting the view that an evolutionary radiation occurred as placental lineages invaded new ecological niches during the Early Palaeocene.
There is a well-established discrepancy between paleontological and molecular data regarding the timing of the origin and diversification of placental mammals. Molecular estimates place interordinal diversification dates in the Cretaceous, while no unambiguous crown placental fossils have been found prior to the end-Cretaceous mass extinction. Here, the completeness of the eutherian fossil record through geological time is evaluated to assess the suggestion that a poor fossil record is largely responsible for the difference in estimates of placental origins. The completeness of fossil specimens was measured using the character completeness metric, which quantifies the completeness of fossil taxa as the percentage of phylogenetic characters available to be scored for any given taxon. Our data set comprised 33 published cladistic matrices representing 445 genera, of which 333 were coded at the species level.There was no significant difference in eutherian completeness across the Cretaceous/Paleogene (K/Pg) boundary. This suggests that the lack of placental mammal fossils in the Cretaceous is not due to a poor fossil record but more likely represents a genuine absence of placental mammals in the Cretaceous. This result supports the “explosive model” of early placental evolution, whereby placental mammals originated around the time of the K/Pg boundary and diversified soon after.No correlation was found between the completeness pattern observed in this study and those of previous completeness studies on birds and sauropodomorph dinosaurs, suggesting that different factors affect the preservation of these groups. No correlations were found with various isotope proxy measures, but Akaike information criterion analysis found that eutherian character completeness metric scores were best explained by models involving the marine-carbonate strontium-isotope ratios (87Sr/86Sr), suggesting that tectonic activity might play a role in controlling the completeness of the eutherian fossil record.
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.
An invited contribution to the special feature 'Putting fossils in trees: combining morphology, time and molecules to estimate phylogenies and divergence times'.Electronic supplementary material is available at http://dx.doi.org/10.1098/rsbl.2016.0051 or via http://rsbl.royalsocietypublishing.org. Evolutionary biologyThe impact of phylogenetic dating method on interpreting trait evolution: a case study of Cretaceous -Palaeogene eutherian body-size evolution T. J. D. Halliday 1 and A. Goswami 1,2 1 Department of Genetics, Evolution, and Environment, and 2 Department of Earth Sciences, University College London, Gower Street, London WC1E 6BT, UK TJDH, 0000-0002-4077-732XThe fossil record of the earliest Cenozoic contains the first large-bodied placental mammals. Several evolutionary models have been invoked to explain the transition from small to large body sizes, but methods for determining evolutionary mode of trait change depend on input from tree topology and divergence dates. Different dating methods may therefore affect inference of evolutionary model. Here, we fit models of body mass evolution onto dated phylogenies of Cretaceous and Palaeogene mammals, comparing the effect of dating method on interpretation of evolutionary model. Among traditional palaeontological dating approaches, an Ornstein-Uhlenbeck model with high alpha parameters is recovered as best-fitting when minimum-age dating is used, while branch-sharing methods are highly sensitive to topology. Release or release-radiate models are preferred when Bayesian fossilized birth-death method is used, but when using stochastic cal3 dating of trees, a model of increased evolutionary rate without a release in constraint at the Cretaceous-Palaeogene boundary has highest support. These results demonstrate unambiguously that choice of dating method is critical for interpretation of continuous trait evolution, and that care must therefore be taken to consider these effects in macroevolutionary studies.
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