Molecular phylogenetic analysis, calibrated with fossils, resolves the time frame of the mammalian radiation.

Molecular phylogenetic studies have resolved placental mammals into four major groups, but have not established the full hierarchy of interordinal relationships, including the position of the root. The latter is critical for understanding the early biogeographic history of placentals. We investigated placental phylogeny using Bayesian and maximum-likelihood methods and a 16.4-kilobase molecular data set. Interordinal relationships are almost entirely resolved. The basal split is between Afrotheria and other placentals, at about 103 million years, and may be accounted for by the separation of South America and Africa in the Cretaceous. Crown-group Eutheria may have their most recent common ancestry in the Southern Hemisphere (Gondwana).

Competing hypotheses for the timing of the placental mammal radiation focus on whether extant placental orders originated and diversified before or after the Cretaceous-Tertiary (K/T) boundary. Molecular studies that have addressed this issue suffer from single calibration points, unwarranted assumptions about the molecular clock, and/or taxon sampling that lacks representatives of all placental orders. We investigated this problem using the largest available molecular data set for placental mammals, which includes segments of 19 nuclear and three mitochondrial genes for representatives of all extant placental orders. We used the Thorne/Kishino method, which permits simultaneous constraints from the fossil record and allows rates of molecular evolution to vary on different branches of a phylogenetic tree. Analyses that used different sets of fossil constraints, different priors for the base of Placentalia, and different data partitions all support interordinal divergences in the Cretaceous followed by intraordinal diversification mostly after the K/T boundary. Four placental orders show intraordinal diversification that predates the K/T boundary, but only by an average of 10 million years. In contrast to some molecular studies that date the rat–mouse split as old as 46 million years, our results show improved agreement with the fossil record and place this split at 16–23 million years. To test the hypothesis that molecular estimates of Cretaceous divergence times are an artifact of increased body size subsequent to the K/T boundary, we also performed analyses with a “K/T body size” taxon set. In these analyses, interordinal splits remained in the Cretaceous.

Modern felid species descend from relatively recent (<11 million years ago) divergence and speciation events that produced successful predatory carnivores worldwide but that have confounded taxonomic classifications. A highly resolved molecular phylogeny with divergence dates for all living cat species, derived from autosomal, X-linked, Y-linked, and mitochondrial gene segments (22,789 base pairs) and 16 fossil calibrations define eight principal lineages produced through at least 10 intercontinental migrations facilitated by sea-level fluctuations. A ghost lineage analysis indicates that available felid fossils underestimate (i.e., unrepresented basal branch length) first occurrence by an average of 76%, revealing a low representation of felid lineages in paleontological remains. The phylogenetic performance of distinct gene classes showed that Y-chromosome segments are appreciably more informative than mitochondrial DNA, X-linked, or autosomal genes in resolving the rapid Felidae species radiation.

Inter-species hybridization has been recently recognized as potentially common in wild animals, but the extent to which it shapes modern genomes is still poorly understood. Distinguishing historical hybridization events from other processes leading to phylogenetic discordance among different markers requires a well-resolved species tree that considers all modes of inheritance and overcomes systematic problems due to rapid lineage diversification by sampling large genomic character sets. Here, we assessed genome-wide phylogenetic variation across a diverse mammalian family, Felidae (cats). We combined genotypes from a genome-wide SNP array with additional autosomal, X- and Y-linked variants to sample ∼150 kb of nuclear sequence, in addition to complete mitochondrial genomes generated using light-coverage Illumina sequencing. We present the first robust felid time tree that accounts for unique maternal, paternal, and biparental evolutionary histories. Signatures of phylogenetic discordance were abundant in the genomes of modern cats, in many cases indicating hybridization as the most likely cause. Comparison of big cat whole-genome sequences revealed a substantial reduction of X-linked divergence times across several large recombination cold spots, which were highly enriched for signatures of selection-driven post-divergence hybridization between the ancestors of the snow leopard and lion lineages. These results highlight the mosaic origin of modern felid genomes and the influence of sex chromosomes and sex-biased dispersal in post-speciation gene flow. A complete resolution of the tree of life will require comprehensive genomic sampling of biparental and sex-limited genetic variation to identify and control for phylogenetic conflict caused by ancient admixture and sex-biased differences in genomic transmission.