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1. NEW PHYLOGENY OF LITOPTERNA AND “ARCHAIC” PALEOGENE UNGULATES ENLIGHTENS THE INTERFAMILIARY AFFINITIES WITHIN THE ORDER

   Puschel, Hans P. ; Shelley, Sarah L. ; Williamson, Thomas E. ; Perini, Fernando ; Wible, John R. ; Brusatte, Stephen L. ( November 2022 , Journal of vertebrate paleontology)

   South American Ungulates (SANUs) exhibit astonishing morphological and ecological diversity due to their almost complete isolation during their early evolution. This unique diversity coupled with the limited fossil record of their earliest evolution makes it difficult to establish their phylogenetic position within the placental mammal tree. Litopterna is the second most diverse order of SANUs after only Notoungulata, with species ranging from the middle Paleocene (~63 Ma) to the late Pleistocene. Among SANUs, litopterns are characterized by having cursorial limbs similar to Holarctic groups like Perissodactyla. Currently there are 67 genera of litopterns grouped into nine families, and the affinities of the Paleogene families remain unclear. Furthermore, it is unclear how litopterns are related to older groups of “archaic” Paleogene ungulates of South America (Kollpaninae and Didolodontidae) and North America (e.g., Mioclaenidae), and other SANUs. To test the phylogenetic relationships of Litopterna, we assembled a new morphological matrix with ~1000 craniodental and postcranial characters for 79 taxa. The data were subjected to Bayesian and maximum parsimony analyses. We conducted tip-dated and undated Bayesian analyses using a Mk + G model of morphological evolution. Fifty percent majority rule consensus trees were obtained from the sampled trees from each analysis. The parsimony analysis resulted in ten most parsimonious trees and a strict consensus was computed. The consensus trees derived from the different analyses were largely congruent. A traditional monophyletic Litopterna failed to be recovered as Protolipternidae was closely related to Didolodontidae. Litopterna was found more closely related to Kollpaninae than to North American Mioclaenidae, and Kollpaninae did not form a monophyletic group with the latter. Adianthidae and Indaleciidae were found in a relatively basal position within Litopterna. Macraucheniidae was found as a sister group to Proterotheriidae, whereas Anisolambdidae was the sister group of Sparnotheriodontidae, these four families forming a monophyletic group. By utilizing a more comprehensive approach, these results alter previous conceptions of the intrafamilial affinities within Litopterna and their position among other Paleogene ungulates, shedding new light on how litopterns evolved and diversified during the Paleogene of South America. Funding Sources ANID-PFCHA-Doctorado en el extranjero Becas Chile-2018-72190003, ERC starting grant PalM 756226, NSF DEB 1654949 and 1654952 

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2. THE PHYLOGENY OF PALEOCENE MAMMALS AND THE EVOLUTION OF PLACENTALIA

   Shelley, Sarah L. ; PALM Working Group ( November 2022 , Journal of vertebrate paleontology)

   Resolving the phylogenetic relationships among Paleocene mammals has been a longstanding goal in paleontology. Constructing an accurate and comprehensive phylogeny for Paleocene mammals is a worthwhile objective in itself, but it also provides a framework on which we can better understand the origin of placental mammals and the evolutionary processes underlying the diversification of mammals before, during, and after the end-Cretaceous mass extinction. More recently, a robust Palaeocene mammal phylogeny has become a much-coveted tool for reconciling discrepancies between morphological and molecular evidence for the phylogeny and diversification of Placentalia. Here, we present a novel phylogenetic dataset to test hypotheses regarding Paleocene mammal phylogeny and the origin and diversification of Placentalia. To date, our matrix combines phenomic data for 36 extant mammal species and 107 fossil species scored for 2540 morphological characters alongside 26 genes sequenced for 47 species. We utilized a reductive morphological scoring strategy in order to minimize assumptions and test hypotheses on homology. Multiple sequence alignments were performed in MEGA-X for each gene. We then analysed the data using Bayesian methods and explored the effects of different approaches. Relaxed clock analyses using a molecular constraint and an FBD prior are congruent with the diversification of many extant orders prior to the K-Pg boundary. Relaxed clocked total-evidence analyses (morphology and molecules) using an FBD prior resulted in older ages of diversification than those estimated by our relaxed clock molecular constraint model and previous molecular studies. Within Placentalia, our phylogenies provide support for the divergence of Atlantogenata (Afrotheria and Xenarthra) from Boreoeutheria (Euarchontoglires and Laurasiatheria). Among the Paleocene taxa, ‘condylarths’ are distributed along the base of Laurasiatheria with members of ‘Arctocyonidae’ recovered as sister taxa to Artiodactyla; enigmatic groups such as Pantodonta and Taeniodonta are recovered as crown placentals whereas Leptictida is not. Our Paleocene mammal phylogeny is a critical step toward better understanding placental mammal evolution. Ultimately, this work will facilitate the investigation of fundamental questions previously encumbered by the lack of a well-resolved phylogeny. 

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3. Virtual endocranial and inner ear endocasts of the Paleocene ‘condylarth’ Chriacus : new insight into the neurosensory system and evolution of early placental mammals

   https://doi.org/10.1111/joa.13084  

   Bertrand, Ornella C. ; Shelley, Sarah L. ; Wible, John R. ; Williamson, Thomas E. ; Holbrook, Luke T. ; Chester, Stephen G. B. ; Butler, Ian B. ; Brusatte, Stephen L. ( October 2019 , Journal of Anatomy)

   The end‐Cretaceous mass extinction allowed placental mammals to diversify ecologically and taxonomically as they filled ecological niches once occupied by non‐avian dinosaurs and more basal mammals. Little is known, however, about how the neurosensory systems of mammals changed after the extinction, and what role these systems played in mammalian diversification. We here use high‐resolution computed tomography (CT) scanning to describe the endocranial and inner ear endocasts of two species,Chriacus pelvidensandChriacus baldwini, which belong to a cluster of ‘archaic’ placental mammals called ‘arctocyonid condylarths’ that thrived during theca. 10 million years after the extinction (the Paleocene Epoch), but whose relationships to extant placentals are poorly understood. The endocasts provide new insight into the paleobiology of the long‐mysterious ‘arctocyonids’, and suggest thatChriacuswas an animal with anencephalization quotient (EQ)range of 0.12–0.41, which probably relied more on its sense of smell than vision, because the olfactory bulbs are proportionally large but the neocortex and petrosal lobules are less developed. Agility scores, estimated from the dimensions of the semicircular canals of the inner ear, indicate thatChriacuswas slow to moderately agile, and its hearing capabilities, estimated from cochlear dimensions, suggest similarities with the extant aardvark.Chriacusshares many brain features with other Paleocene mammals, such as a small lissencephalic brain, large olfactory bulbs and small petrosal lobules, which are likely plesiomorphic for Placentalia. The inner ear ofChriacusalso shares derived characteristics of the elliptical and spherical recesses with extinct species that belong to Euungulata, the extant placental group that includes artiodactyls and perissodactyls. This lends key evidence to the hypothesized close relationship betweenChriacusand the extant ungulate groups, and demonstrates that neurosensory features can provide important insight into both the paleobiology and relationships of early placental mammals.

    

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4. Journal of Vertebrate Paleontology, Program and Abstracts

   Bertrand, O.C. ; Brusatte, S. L. ; Shelley, S. L. ; Wible, J. R. ; Williamson, T. E. ; Chester, S. G. ; Holbrook, L. T. ; Lyson, T. R. ; Smith, T. ; Meng, J. ( October 2020 , Society of Vertebrate paleontology)

   The end-Cretaceous mass extinction, 66 million years ago, profoundly reshaped the biodiversity of our planet. After likely originating in the Cretaceous, placental mammals (species giving live birth to well-developed young) survived the extinction and quickly diversified in the ensuing Paleocene. Compared to Mesozoic species, extant placentals have advanced neurosensory abilities, enabled by a proportionally large brain with an expanded neocortex. This brain construction was acquired by the Eocene, but its origins, and how its evolution relates to extinction survivorship and recovery, are unclear, because little is known about the neurosensory systems of Paleocene species. We used high-resolution computed tomography (CT) scanning to build digital brain models in 29 extinct placentals (including 23 from the Paleocene). We added these to data from the literature to construct a database of 98 taxa, from the Jurassic to the Eocene, which we assessed in a phylogenetic context. We find that the Phylogenetic Encephalization Quotient (PEQ), a measure of relative brain size, increased in the Cretaceous along branches leading to Placentalia, but then decreased in Paleocene clades (taeniodonts,phenacodontids, pantodonts, periptychids, and arctocyonids). Later, during the Eocene, the PEQ increased independently in all crown groups (e.g., euarchontoglirans and laurasiatherians). The Paleocene decline in PEQ was driven by body mass increasing much more rapidly after the extinction than brain volume. The neocortex remained small, relative to the rest of the brain, in Paleocene taxa and expanded independently in Eocene crown groups. The relative size of the olfactory bulbs, however, remained relatively stable over time, except for a major decrease in Euarchontoglires and some Eocene artiodactyls, while the petrosal lobules (associated with eye movement coordination) decreased in size in Laurasiatheria but increased in Euarchontoglires. Our results indicate that an enlarged, modern-style brain was not instrumental to the survival of placental mammal ancestors at the end-Cretaceous, nor to their radiation in the Paleocene. Instead, opening of new ecological niches post-extinction promoted the diversification of larger body sizes, while brain and neocortex sizes lagged behind. The independent increase in PEQ in Eocene crown groups is related to the expansion of the neocortex, possibly a response to ecological specialization as environments changed, long after the extinction. 

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5. A genomic timescale for placental mammal evolution

   https://doi.org/10.1126/science.abl8189  

   Foley, Nicole M. ; Mason, Victor C. ; Harris, Andrew J. ; Bredemeyer, Kevin R. ; Damas, Joana ; Lewin, Harris A. ; Eizirik, Eduardo ; Gatesy, John ; Karlsson, Elinor K. ; Lindblad-Toh, Kerstin ; et al ( April 2023 , Science)

   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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