A genomic exploration of the early evolution of extant cats and their sabre-toothed relatives.

Background: The evolutionary relationships of Felidae during their Early-Middle Miocene radiation is contentious. Although the early common ancestors have been subsumed under the grade-group Pseudaelurus, this group is thought to be paraphyletic, including the early ancestors of both modern cats and extinct sabretooths. Methods: Here, we sequenced a draft nuclear genome of Smilodon populator, dated to 13,182 ± 90 cal BP, making this the oldest palaeogenome from South America to date, a region known to be problematic for ancient DNA preservation. We analysed this genome, together with genomes from other extinct and extant cats to investigate their phylogenetic relationships. Results: We confirm a deep divergence (~20.65 Ma) within sabre-toothed cats. Through the analysis of both simulated and empirical data, we show a lack of gene flow between Smilodon and contemporary Felidae. Conclusions: Given that some species traditionally assigned to Pseudaelurus originated in the Early Miocene ~20 Ma, this indicates that some species of Pseudaelurus may be younger than the lineages they purportedly gave rise to, further supporting the hypothesis that Pseudaelurus was paraphyletic.

Genomic Adaptations and Evolutionary History of the Extinct Scimitar-Toothed Cat, Homotherium latidens.

Homotherium was a genus of large-bodied scimitar-toothed cats, morphologically distinct from any extant felid species, that went extinct at the end of the Pleistocene [1-4]. They possessed large, saber-form serrated canine teeth, powerful forelimbs, a sloping back, and an enlarged optic bulb, all of which were key characteristics for predation on Pleistocene megafauna [5]. Previous mitochondrial DNA phylogenies suggested that it was a highly divergent sister lineage to all extant cat species [6-8]. However, mitochondrial phylogenies can be misled by hybridization [9], incomplete lineage sorting (ILS), or sex-biased dispersal patterns [10], which might be especially relevant for Homotherium since widespread mito-nuclear discrepancies have been uncovered in modern cats [10]. To examine the evolutionary history of Homotherium, we generated a ∼7x nuclear genome and a ∼38x exome from H. latidens using shotgun and target-capture sequencing approaches. Phylogenetic analyses reveal Homotherium as highly divergent (∼22.5 Ma) from living cat species, with no detectable signs of gene flow. Comparative genomic analyses found signatures of positive selection in several genes, including those involved in vision, cognitive function, and energy consumption, putatively consistent with diurnal activity, well-developed social behavior, and cursorial hunting [5]. Finally, we uncover relatively high levels of genetic diversity, suggesting that Homotherium may have been more abundant than the limited fossil record suggests [3, 4, 11-14]. Our findings complement and extend previous inferences from both the fossil record and initial molecular studies, enhancing our understanding of the evolution and ecology of this remarkable lineage.