Trilobite evolutionary rates constrain the duration of the Cambrian explosion.

Trilobites are often considered exemplary for understanding the Cambrian explosion of animal life, due to their unsurpassed diversity and abundance. These biomineralized arthropods appear abruptly in the fossil record with an established diversity, phylogenetic disparity, and provincialism at the beginning of Cambrian Series 2 (∼521 Ma), suggesting a protracted but cryptic earlier history that possibly extends into the Precambrian. However, recent analyses indicate elevated rates of phenotypic and genomic evolution for arthropods during the early Cambrian, thereby shortening the phylogenetic fuse. Furthermore, comparatively little research has been devoted to understanding the duration of the Cambrian explosion, after which normal Phanerozoic evolutionary rates were established. We test these hypotheses by applying Bayesian tip-dating methods to a comprehensive dataset of Cambrian trilobites. We show that trilobites have a Cambrian origin, as supported by the trace fossil record and molecular clocks. Surprisingly, they exhibit constant evolutionary rates across the entire Cambrian, for all aspects of the preserved phenotype: discrete, meristic, and continuous morphological traits. Our data therefore provide robust, quantitative evidence that by the time the typical Cambrian fossil record begins (∼521 Ma), the Cambrian explosion had already largely concluded. This suggests that a modern-style marine biosphere had rapidly emerged during the latest Ediacaran and earliest Cambrian (∼20 million years), followed by broad-scale evolutionary stasis throughout the remainder of the Cambrian.

Bayesian Morphological Clock Methods Resurrect Placoderm Monophyly and Reveal Rapid Early Evolution in Jawed Vertebrates.

The phylogeny of early gnathostomes provides an important framework for understanding one of the most significant evolutionary events, the origin and diversification of jawed vertebrates. A series of recent cladistic analyses have suggested that the placoderms, an extinct group of armoured fish, form a paraphyletic group basal to all other jawed vertebrates. We revised and expanded this morphological data set, most notably by sampling autapomorphies in a similar way to parsimony-informative traits, thus ensuring this data (unlike most existing morphological data sets) satisfied an important assumption of Bayesian tip-dated morphological clock approaches. We also found problems with characters supporting placoderm paraphyly, including character correlation and incorrect codings. Analysis of this data set reveals that paraphyly and monophyly of core placoderms (excluding maxillate forms) are essentially equally parsimonious. The two alternative topologies have different root positions for the jawed vertebrates but are otherwise similar. However, analysis using tip-dated clock methods reveals strong support for placoderm monophyly, due to this analysis favoring trees with more balanced rates of evolution. Furthermore, enforcing placoderm paraphyly results in higher levels and unusual patterns of rate heterogeneity among branches, similar to that generated from simulated trees reconstructed with incorrect root positions. These simulations also show that Bayesian tip-dated clock methods outperform parsimony when the outgroup is largely uninformative (e.g., due to inapplicable characters), as might be the case here. The analysis also reveals that gnathostomes underwent a rapid burst of evolution during the Silurian period which declined during the Early Devonian. This rapid evolution during a period with few articulated fossils might partly explain the difficulty in ascertaining the root position of jawed vertebrates.

Pre- versus post-mass extinction divergence of Mesozoic marine reptiles dictated by time-scale dependence of evolutionary rates.

The fossil record of a major clade often starts after a mass extinction even though evolutionary rates, molecular or morphological, suggest its pre-extinction emergence (e.g. squamates, placentals and teleosts). The discrepancy is larger for older clades, and the presence of a time-scale-dependent methodological bias has been suggested, yet it has been difficult to avoid the bias using Bayesian phylogenetic methods. This paradox raises the question of whether ecological vacancies, such as those after mass extinctions, prompt the radiations. We addressed this problem by using a unique temporal characteristic of the morphological data and a high-resolution stratigraphic record, for the oldest clade of Mesozoic marine reptiles, Ichthyosauromorpha. The evolutionary rate was fastest during the first few million years of ichthyosauromorph evolution and became progressively slower over time, eventually becoming six times slower. Using the later slower rates, estimates of divergence time become excessively older. The fast, initial rate suggests the emergence of ichthyosauromorphs after the end-Permian mass extinction, matching an independent result from high-resolution stratigraphic confidence intervals. These reptiles probably invaded the sea as a new ecosystem was formed after the end-Permian mass extinction. Lack of information on early evolution biased Bayesian clock rates.

The evolutionary relationships and age of Homo naledi: An assessment using dated Bayesian phylogenetic methods.

Homo naledi is a recently discovered species of fossil hominin from South Africa. A considerable amount is already known about H. naledi but some important questions remain unanswered. Here we report a study that addressed two of them: "Where does H. naledi fit in the hominin evolutionary tree?" and "How old is it?" We used a large supermatrix of craniodental characters for both early and late hominin species and Bayesian phylogenetic techniques to carry out three analyses. First, we performed a dated Bayesian analysis to generate estimates of the evolutionary relationships of fossil hominins including H. naledi. Then we employed Bayes factor tests to compare the strength of support for hypotheses about the relationships of H. naledi suggested by the best-estimate trees. Lastly, we carried out a resampling analysis to assess the accuracy of the age estimate for H. naledi yielded by the dated Bayesian analysis. The analyses strongly supported the hypothesis that H. naledi forms a clade with the other Homo species and Australopithecus sediba. The analyses were more ambiguous regarding the position of H. naledi within the (Homo, Au. sediba) clade. A number of hypotheses were rejected, but several others were not. Based on the available craniodental data, Homo antecessor, Asian Homo erectus, Homo habilis, Homo floresiensis, Homo sapiens, and Au. sediba could all be the sister taxon of H. naledi. According to the dated Bayesian analysis, the most likely age for H. naledi is 912 ka. This age estimate was supported by the resampling analysis. Our findings have a number of implications. Most notably, they support the assignment of the new specimens to Homo, cast doubt on the claim that H. naledi is simply a variant of H. erectus, and suggest H. naledi is younger than has been previously proposed.

Integrative Phylogenetics: Tools for Palaeontologists to Explore the Tree of Life.

The modern era of analytical and quantitative palaeobiology has only just begun, integrating methods such as morphological and molecular phylogenetics and divergence time estimation, as well as phenotypic and molecular rates of evolution. Calibrating the tree of life to geological time is at the nexus of many disparate disciplines, from palaeontology to molecular systematics and from geochronology to comparative genomics. Creating an evolutionary time scale of the major events that shaped biodiversity is key to all of these fields and draws from each of them. Different methodological approaches and data employed in various disciplines have traditionally made collaborative research efforts difficult among these disciplines. However, the development of new methods is bridging the historical gap between fields, providing a holistic perspective on organismal evolutionary history, integrating all of the available evidence from living and fossil species. Because phylogenies with only extant taxa do not contain enough information to either calibrate the tree of life or fully infer macroevolutionary dynamics, phylogenies should preferably include both extant and extinct taxa, which can only be achieved through the inclusion of phenotypic data. This integrative phylogenetic approach provides ample and novel opportunities for evolutionary biologists to benefit from palaeontological data to help establish an evolutionary time scale and to test core macroevolutionary hypotheses about the drivers of biological diversification across various dimensions of organisms.

Molecular and morphological clocks for estimating evolutionary divergence times.

BACKGROUND: Matrices of morphological characters are frequently used for dating species divergence times in systematics. In some studies, morphological and molecular character data from living taxa are combined, whereas others use morphological characters from extinct taxa as well. We investigated whether morphological data produce time estimates that are concordant with molecular data. If true, it will justify the use of morphological characters alongside molecular data in divergence time inference. RESULTS: We systematically analyzed three empirical datasets from different species groups to test the concordance of species divergence dates inferred using molecular and discrete morphological data from extant taxa as test cases. We found a high correlation between their divergence time estimates, despite a poor linear relationship between branch lengths for morphological and molecular data mapped onto the same phylogeny. This was because node-to-tip distances showed a much higher correlation than branch lengths due to an averaging effect over multiple branches. We found that nodes with a large number of taxa often benefit from such averaging. However, considerable discordance between time estimates from molecules and morphology may still occur as  some intermediate nodes may show large time differences between these two types of data. CONCLUSIONS: Our findings suggest that node- and tip-calibration approaches may be better suited for nodes with many taxa. Nevertheless, we highlight the importance of evaluating the concordance of intrinsic time structure in morphological and molecular data before any dating analysis using combined datasets.

Data partitioning and correction for ascertainment bias reduce the uncertainty of placental mammal divergence times inferred from the morphological clock.

Bayesian estimates of divergence times based on the molecular clock yield uncertainty of parameter estimates measured by the width of posterior distributions of node ages. For the relaxed molecular clock, previous works have reported that some of the uncertainty inherent to the variation of rates among lineages may be reduced by partitioning data. Here we test this effect for the purely morphological clock, using placental mammals as a case study. We applied the uncorrelated lognormal relaxed clock to morphological data of 40 extant mammalian taxa and 4,533 characters, taken from the largest published matrix of discrete phenotypic characters. The morphologically derived timescale was compared to divergence times inferred from molecular and combined data. We show that partitioning data into anatomical units significantly reduced the uncertainty of divergence time estimates for morphological data. For the first time, we demonstrate that ascertainment bias has an impact on the precision of morphological clock estimates. While analyses including molecular data suggested most divergences between placental orders occurred near the K-Pg boundary, the partitioned morphological clock recovered older interordinal splits and some younger intraordinal ones, including significantly later dates for the radiation of bats and rodents, which accord to the short-fuse hypothesis.

Including autapomorphies is important for paleontological tip-dating with clocklike data, but not with non-clock data.

Tip-dating, where fossils are included as dated terminal taxa in Bayesian dating inference, is an increasingly popular method. Data for these studies often come from morphological character matrices originally developed for non-dated, and usually parsimony, analyses. In parsimony, only shared derived characters (synapomorphies) provide grouping information, so many character matrices have an ascertainment bias: they omit autapomorphies (unique derived character states), which are considered uninformative. There has been no study of the effect of this ascertainment bias in tip-dating, but autapomorphies can be informative in model-based inference. We expected that excluding autapomorphies would shorten the morphological branchlengths of terminal branches, and thus bias downwards the time branchlengths inferred in tip-dating. We tested for this effect using a matrix for Carboniferous-Permian eureptiles where all autapomorphies had been deliberately coded. Surprisingly, date estimates are virtually unchanged when autapomorphies are excluded, although we find large changes in morphological rate estimates and small effects on topological and dating confidence. We hypothesized that the puzzling lack of effect on dating was caused by the non-clock nature of the eureptile data. We confirm this explanation by simulating strict clock and non-clock datasets, showing that autapomorphy exclusion biases dating only for the clocklike case. A theoretical solution to ascertainment bias is computing the ascertainment bias correction (Mkparsinf), but we explore this correction in detail, and show that it is computationally impractical for typical datasets with many character states and taxa. Therefore we recommend that palaeontologists collect autapomorphies whenever possible when assembling character matrices.

Dating placentalia: Morphological clocks fail to close the molecular fossil gap.

Dating the origin of Placentalia has been a contentious issue for biologists and paleontologists. Although it is likely that crown-group placentals originated in the Late Cretaceous, nearly all molecular clock estimates point to a deeper Cretaceous origin. An approach with the potential to reconcile this discrepancy could be the application of a morphological clock. This would permit the direct incorporation of fossil data in node dating, and would break long internal branches of the tree, so leading to improved estimates of node ages. Here, we use a large morphological dataset and the tip-calibration approach of MrBayes. We find that the estimated date for the origin of crown mammals is much older, ∼130-145 million years ago (Ma), than fossil and molecular clock data (∼80-90 Ma). Our results suggest that tip calibration may result in estimated dates that are more ancient than those obtained from other sources of data. This can be partially overcome by constraining the ages of internal nodes on the tree; however, when this was applied to our dataset, the estimated dates were still substantially more ancient than expected. We recommend that results obtained using tip calibration, and possibly morphological dating more generally, should be treated with caution.

Bayesian phylogenetic estimation of fossil ages.

Recent advances have allowed for both morphological fossil evidence and molecular sequences to be integrated into a single combined inference of divergence dates under the rule of Bayesian probability. In particular, the fossilized birth-death tree prior and the Lewis-Mk model of discrete morphological evolution allow for the estimation of both divergence times and phylogenetic relationships between fossil and extant taxa. We exploit this statistical framework to investigate the internal consistency of these models by producing phylogenetic estimates of the age of each fossil in turn, within two rich and well-characterized datasets of fossil and extant species (penguins and canids). We find that the estimation accuracy of fossil ages is generally high with credible intervals seldom excluding the true age and median relative error in the two datasets of 5.7% and 13.2%, respectively. The median relative standard error (RSD) was 9.2% and 7.2%, respectively, suggesting good precision, although with some outliers. In fact, in the two datasets we analyse, the phylogenetic estimate of fossil age is on average less than 2 Myr from the mid-point age of the geological strata from which it was excavated. The high level of internal consistency found in our analyses suggests that the Bayesian statistical model employed is an adequate fit for both the geological and morphological data, and provides evidence from real data that the framework used can accurately model the evolution of discrete morphological traits coded from fossil and extant taxa. We anticipate that this approach will have diverse applications beyond divergence time dating, including dating fossils that are temporally unconstrained, testing of the 'morphological clock', and for uncovering potential model misspecification and/or data errors when controversial phylogenetic hypotheses are obtained based on combined divergence dating analyses.This article is part of the themed issue 'Dating species divergences using rocks and clocks'.