Our ability to correlate biological evolution with climate change, geological evolution, and other historical patterns is essential to understanding the processes that shape biodiversity. Combining data from the fossil record with molecular phylogenetics represents an exciting synthetic approach to this challenge. The first molecular divergence dating analysis (Zuckerkandl and Pauling 1962) was based on a measure of the amino acid differences in the hemoglobin molecule, with replacement rates established (calibrated) using paleontological age estimates from textbooks (e.g., Dodson 1960). Since that time, the amount of molecular sequence data has increased dramatically, affording ever-greater opportunities to apply molecular divergence approaches to fundamental problems in evolutionary biology. To capitalize on these opportunities, increasingly sophisticated divergence dating methods have been, and continue to be, developed. In contrast, comparatively, little attention has been devoted to critically assessing the paleontological and associated geological data used in divergence dating analyses. The lack of rigorous protocols for assigning calibrations based on fossils raises serious questions about the credibility of divergence dating results (e.g., Shaul and Graur 2002; Brochu et al. 2004; Graur and Martin 2004; Hedges and Kumar 2004; Reisz and Müller 2004a, 2004b; Theodor 2004; van Tuinen and Hadly 2004a, 2004b; van Tuinen et al. 2004; Benton and Donoghue 2007; Donoghue and Benton 2007; Parham and Irmis 2008; Ksepka 2009; Benton et al. 2009; Heads 2011).

The fossil record suggests a rapid radiation of placental mammals following the Cretaceous–Paleogene (K–Pg) mass extinction 65 million years ago (Ma); nevertheless, molecular time estimates, while highly variable, are generally much older. Early molecular studies suffer from inadequate dating methods, reliance on the molecular clock, and simplistic and over-confident interpretations of the fossil record. More recent studies have used Bayesian dating methods that circumvent those issues, but the use of limited data has led to large estimation uncertainties, precluding a decisive conclusion on the timing of mammalian diversifications. Here we use a powerful Bayesian method to analyse 36 nuclear genomes and 274 mitochondrial genomes (20.6 million base pairs), combined with robust but flexible fossil calibrations. Our posterior time estimates suggest that marsupials diverged from eutherians 168–178 Ma, and crown Marsupialia diverged 64–84 Ma. Placentalia diverged 88–90 Ma, and present-day placental orders (except Primates and Xenarthra) originated in a ∼20 Myr window (45–65 Ma) after the K–Pg extinction. Therefore we reject a pre K–Pg model of placental ordinal diversification. We suggest other infamous instances of mismatch between molecular and palaeontological divergence time estimates will be resolved with this same approach.

With our increasing ability for generating whole-genome sequences, comparative analysis of whole genomes has become a powerful tool for understanding the structure, function, and evolutionary history of human and other vertebrate genomes. By virtue of their position basal to bony vertebrates, cartilaginous fishes (class Chondrichthyes) are a valuable outgroup in comparative studies of vertebrates. Recently, a holocephalan cartilaginous fish, the elephant shark, Callorhinchus milii (Subclass Holocephali: Order Chimaeriformes), has been proposed as a model genome, and low-coverage sequence of its genome has been generated. Despite such an increasing interest, the evolutionary history of the modern holocephalans-a previously successful and diverse group but represented by only 39 extant species-and their relationship with elasmobranchs and other jawed vertebrates has been poorly documented largely owing to a lack of well-preserved fossil materials after the end-Permian about 250 Ma. In this study, we assembled the whole mitogenome sequences for eight representatives from all the three families of the modern holocephalans and investigated their phylogenetic relationships and evolutionary history. Unambiguously aligned sequences from these holocephalans together with 17 other vertebrates (9,409 nt positions excluding entire third codon positions) were subjected to partitioned maximum likelihood analysis. The resulting tree strongly supported a single origin of the modern holocephalans and their sister-group relationship with elasmobranchs. The mitogenomic tree recovered the most basal callorhinchids within the chimaeriforms, which is sister to a clade comprising the remaining two families (rhinochimaerids and chimaerids). The timetree derived from a relaxed molecular clock Bayesian method suggests that the holocephalans originated in the Silurian about 420 Ma, having survived from the end-Permian (250 Ma) mass extinction and undergoing familial diversifications during the late Jurassic to early Cretaceous (170-120 Ma). This postulated evolutionary scenario agrees well with that based on the paleontological observations.

Significance: All genes are duplicated by whole-genome duplication (WGD), reverting in number over time, but the actual timing of genome reshaping through gene loss remains poorly understood. We estimated the spatiotemporal loss/persistence pattern of 6,892 gene lineage pairs after the teleost-specific WGD, using careful orthology assignment and a reliable time-calibrated tree. We found that massive gene loss did occur in the first 60 My, mainly due to events involving the simultaneous loss of multiple redundant genes, and the rate of loss then slowed to an approximately constant level for the subsequent 250 My. Similar genomic gene arrangements within teleosts imply that rapid gene loss led to the reshaping of the teleost genomes before their major divergence.