With the dawn of the Paleogene, the mammalian survivors of the Cretaceous–Paleogene mass extinction, 66 million years ago, found themselves in an emptied landscape. Within a million years of the bolide impact, placental mammals reached a diversity and abundance never seen during the Age of Dinosaurs. The North American ‘condylarths’ were amongst the first mammals to diversify during the early Paleogene and are often considered the ancestral ‘stock’ from which other euungulate groups evolved. Amongst these, Phenacodontidae are often regarded to lie at the base of the perissodactyl family tree, but their phylogenetic position, and that of other ‘condylarths’, remain contentious. Tetraclaenodon, a medium-sized herbivorous phenacodontid from the Torrejonian (~64 to ~62 Ma) of North America is generally recognized as the oldest member of Phenacodontidae, and thus is instrumental for untangling the evolutionary relationships of ‘condylarths’ and perissodactyls. Here we present new information on Tetraclaenodon based on a description of new and previously known fossil material from the San Juan Basin of New Mexico, U.S.A., which we studied using high-resolution computed tomography (CT) scanning. From CT scans of the cranium, we segmented the brain endocast, which is relatively small and smooth (lissencephalic), similar to that of other Paleocene mammals. The petrosal lobules, which are involved in eye movement coordination, are small. The semi-circular canals associated with balance, provide an agility score of 3 indicating that Tetraclaenodon was probably moderately agile, similar to the extant raccoon dog or the aardwolf. A multivariate analysis of tarsal measurements for a sample of Paleocene and extant mammals, which informs locomotor style, indicates that Tetraclaenodon was most suited to terrestrial locomotion. This is in line with anatomical and myological features of the limbs of Tetraclaenodon and other phenacodontids, early perissodactyls and extant mammals. These findings contradict previous studies that designated Tetraclaenodon as a scansorial mammal, capable of habitually climbing trees. Our results shed light on the locomotory adaptations of Tetraclaenodon in comparison to more cursorial phenacodontids and perissodactyls, such as Phenacodus and Hyrachyus. The earliest member of the perissodactyl stem lineage apparently lacked the more cursorial adaptations of their relatives in the late Paleocene and onwards.
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This content will become publicly available on April 28, 2024
A genomic timescale for placental mammal evolution
INTRODUCTION Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. RATIONALE Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. RESULTS Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. CONCLUSION Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting.
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- NSF-PAR ID:
- 10421105
- Author(s) / Creator(s):
- ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; more »
- Date Published:
- Journal Name:
- Science
- Volume:
- 380
- Issue:
- 6643
- ISSN:
- 0036-8075
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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With the dawn of the Paleogene, the mammalian survivors of the Cretaceous–Paleogene mass extinction, 66 million years ago, found themselves in an emptied landscape. Within a million years of the bolide impact, placental mammals reached a diversity and abundance never seen during the Age of Dinosaurs. The North American ‘condylarths’ were amongst the first mammals to diversify during the early Paleogene and are often considered the ancestral ‘stock’ from which other euungulate groups evolved. Amongst these, Phenacodontidae are often regarded to lie at the base of the perissodactyl family tree, but their phylogenetic position, and that of other ‘condylarths’, remain contentious. Tetraclaenodon, a medium-sized herbivorous phenacodontid from the Torrejonian (~64 to ~62 Ma) of North America is generally recognized as the oldest member of Phenacodontidae, and thus is instrumental for untangling the evolutionary relationships of ‘condylarths’ and perissodactyls. Here we present new information on Tetraclaenodon based on a description of new and previously known fossil material from the San Juan Basin of New Mexico, U.S.A., which we studied using high-resolution computed tomography (CT) scanning. From CT scans of the cranium, we segmented the brain endocast, which is relatively small and smooth (lissencephalic), similar to that of other Paleocene mammals. The petrosal lobules, which are involved in eye movement coordination, are small. The semi-circular canals associated with balance, provide an agility score of 3 indicating that Tetraclaenodon was probably moderately agile, similar to the extant raccoon dog or the aardwolf. A multivariate analysis of tarsal measurements for a sample of Paleocene and extant mammals, which informs locomotor style, indicates that Tetraclaenodon was most suited to terrestrial locomotion. This is in line with anatomical and myological features of the limbs of Tetraclaenodon and other phenacodontids, early perissodactyls and extant mammals. These findings contradict previous studies that designated Tetraclaenodon as a scansorial mammal, capable of habitually climbing trees. Our results shed light on the locomotory adaptations of Tetraclaenodon in comparison to more cursorial phenacodontids and perissodactyls, such as Phenacodus and Hyrachyus. The earliest member of the perissodactyl stem lineage apparently lacked the more cursorial adaptations of their relatives in the late Paleocene and onwards.more » « less
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