Bayesian modelling of the fossil record enlightens the evolutionary history of Hemiptera

Understanding the nature and timing of metazoan origins is one of the most important, yet elusive, questions in evolutionary biology. Fossil data provide the most tangible evidence for the origin of early animal lineages, although additional evidence from molecular phylogenetics, molecular clock studies, and development has contributed to our current understanding. We review several lines of evidence to explore the nature and timing of early metazoan evolution and discuss how these data, when considered together, provide a more cohesive picture of the origin of animal diversity. We discuss how trace fossils and biomarkers provide compelling evidence for the origins of Bilateria and siliceous sponges. Using a molecular phylogenetic framework for metazoans, we discuss how fossils can be used to date the origin of clades. We use these fossil dates to perform a relaxed molecular clock analysis for estimating dates of nodes when no fossils are available. We also discuss current data from developmental biology that suggest that early metazoans possessed a sophisticated molecular toolkit for building complex body plans. We conclude that the best evidence for the origin of major metazoan lineages lies in the careful interpretation of the fossil record and that these data, when considered with phylogenetic and developmental evidence, support the notion that the Cambrian radiation is a real phenomenon that marks a critically important time in the history of life.

Reinvestigation of the anatomically preserved stem Palaeosmunda plenasioides from the Lopingian (Late Permian) of China has led to the establishment of Zhongmingella gen. nov. within the extinct family Guaireaceae (Osmundales). Zhongmingella has a rhizomatous stem with heterogeneous pith and cortex comprising parenchyma and uniformly distributed secretory cells, and is dictyostelic. In order to evaluate the systematic and phylogenetic position of Zhongmingella within Guaireaceae, and Guaireaceae within Osmundales, we conducted a preliminary cladistic analysis of a broad range of Osmundales and related taxa based on 18 extinct and six extant genera and subgenera. Results do not support the traditionally defined family Thamnopteroideae (Bathypteris, Chasmatopteris, Iegosigopteris, Thamnopteris, Zalesskya) and demonstrate that Thamnopteroideae is not a subfamily of Osmundaceae as previously thought. Guaireaceae is monophyletic but in addition to its traditionally defined members (Guairea, Lunea, Donwellicaulis, Itopsidema, Shuichengella, Zhongmingella) includes the stratigraphically younger genus Osmundacaulis previously placed in Osmundaceae. Guaireaceae is sister to Osmundaceae, Millerocaulis, Ashicaulis, Palaeosmunda and Aurealcaulis in the strict consensus, but in the majority-rule consensus Palaeosmunda, Aurealcaulis, Ashicaulis and Millerocaulis form the Osmundaceae stem group, with (Aurealcaulis, (Ashicaulis + Palaeosmunda)) sister to the extant genera. Stratigraphical analysis of the selected most parsimonious tree demonstrates that Osmundales underwent primary radiation during the Pennsylvanian and Permian, terminating abruptly around the time of the end-Permian mass extinction. Radiation within Osmundaceae occurred in the Triassic–Cretaceous and stratigraphically overlaps staggered extinctions in Guaireaceae and Osmundaceae from the Late Jurassic to mid-Cretaceous alongside the earliest angiosperm radiation. Our results identify the Osmundaceae stem and sister groups for the first time, and represent an important step in unravelling the evolutionary history of Osmundales. However, reconstructed whole-plant species are imperative to improve understanding of the relationships within the clade in deep time.

The record of the coevolution of oxygenic phototrophs and the environment is preserved in three forms: genomes of modern organisms, diverse geochemical signals of surface oxidation and diagnostic Proterozoic microfossils. When calibrated by fossils, genomic data form the basis of molecular clock analyses. However, different interpretations of the geochemical record, fossil calibrations and evolutionary models produce a wide range of age estimates that are often conflicting. Here, we show that multiple interpretations of the cyanobacterial fossil record are consistent with an Archean origin of crown-group Cyanobacteria. We further show that incorporating relative dating information from horizontal gene transfers greatly improves the precision of these age estimates, by both providing a novel empirical criterion for selecting evolutionary models, and increasing the stringency of sampling of posterior age estimates. Independent of any geochemical evidence or hypotheses, these results support oxygenic photosynthesis evolving at least several hundred million years before the Great Oxygenation Event (GOE), a rapid diversification of major cyanobacterial lineages around the time of the GOE, and a post-Cryogenian origin of extant marine picocyanobacterial diversity.

In Bayesian molecular-clock dating of species divergences, rate models are used to construct the prior on the molecular evolutionary rates for branches in the phylogeny, with independent and autocorrelated rate models being commonly used. The two classes of models, however, can result in markedly different divergence time estimates for the same data set, and thus selecting the best rate model appears important for obtaining reliable inferences of divergence times. However, the properties of Bayesian rate model selection are not well understood, in particular when the number of sequence partitions analyzed increases and when age calibrations (such as fossil calibrations) are misspecified. Furthermore, Bayesian rate model selection is computationally expensive as it requires the calculation of marginal likelihoods by Markov Chain Monte Carlo sampling, and therefore, methods that can speed up the model selection procedure without compromising its accuracy are desirable. In this study, we use a combination of computer simulations and real data analysis to investigate the statistical behavior of Bayesian rate model selection and we also explore approximations of the likelihood to improve computational efficiency in large phylogenomic data sets. Our simulations demonstrate that the posterior probability for the correct rate model converges to one as more molecular sequence partitions are analyzed and when no calibrations are used, as expected due to asymptotic Bayesian model selection theory. Furthermore, we also show the model selection procedure is robust to slight misspecification of calibrations, and reliable inference of the correct rate model is possible in this case. However, we show that when calibrations are seriously misspecified, calculated model probabilities are completely wrong and may converge to one for the wrong rate model. Finally, we demonstrate that approximating the phylogenetic likelihood under an arcsine branch-length transform can dramatically reduce the computational cost of rate model selection without compromising accuracy. We test the approximate procedure on two large phylogenies of primates (372 species) and flowering plants (644 species), replicating results obtained on smaller data sets using exact likelihood. Our findings and methodology can assist users in selecting the optimal rate model for estimating times and rates along the Tree of Life.

Molecular clock methods allow biologists to estimate divergence times, which in turn play an important role in comparative studies of many evolutionary processes. It is well known that molecular age estimates can be biased by heterogeneity in rates of molecular evolution, but less attention has been paid to the issue of potentially erroneous fossil calibrations. In this study we estimate the timing of diversification in Centrarchidae, an endemic major lineage of the diverse North American freshwater fish fauna, through a new approach to fossil calibration and molecular evolutionary model selection. Given a completely resolved multi-gene molecular phylogeny and a set of multiple fossil-inferred age estimates, we tested for potentially erroneous fossil calibrations using a recently developed fossil cross-validation. We also used fossil information to guide the selection of the optimal molecular evolutionary model with a new fossil jackknife method in a fossil-based model cross-validation. The centrarchid phylogeny resulted from a mixed-model Bayesian strategy that included 14 separate data partitions sampled from three mtDNA and four nuclear genes. Ten of the 31 interspecific nodes in the centrarchid phylogeny were assigned a minimal age estimate from the centrarchid fossil record. Our analyses identified four fossil dates that were inconsistent with the other fossils, and we removed them from the molecular dating analysis. Using fossil-based model cross-validation to determine the optimal smoothing value in penalized likelihood analysis, and six mutually consistent fossil calibrations, the age of the most recent common ancestor of Centrarchidae was 33.59 million years ago (mya). Penalized likelihood analyses of individual data partitions all converged on a very similar age estimate for this node, indicating that rate heterogeneity among data partitions is not confounding our analyses. These results place the origin of the centrarchid radiation at a time of major faunal turnover as the fossil record indicates that the most diverse lineages of the North American freshwater fish fauna originated at the Eocene-Oligocene boundary, approximately 34 mya. This time coincided with major global climate change from warm to cool temperatures and a signature of elevated lineage extinction and origination in the fossil record across the tree of life. Our analyses demonstrate the utility of fossil cross-validation to critically assess individual fossil calibration points, providing the ability to discriminate between consistent and inconsistent fossil age estimates that are used for calibrating molecular phylogenies.

Molecular clock methods allow biologists to estimate divergence times, which in turn play an important role in comparative studies of many evolutionary processes. It is well known that molecular age estimates can be biased by heterogeneity in rates of molecular evolution, but less attention has been paid to the issue of potentially erroneous fossil calibrations. In this study we estimate the timing of diversification in Centrarchidae, an endemic major lineage of the diverse North American freshwater fish fauna, through a new approach to fossil calibration and molecular evolutionary model selection. Given a completely resolved multi-gene molecular phylogeny and a set of multiple fossil-inferred age estimates, we tested for potentially erroneous fossil calibrations using a recently developed fossil cross-validation. We also used fossil information to guide the selection of the optimal molecular evolutionary model with a new fossil jackknife method in a fossil-based model cross-validation. The centrarchid phylogeny resulted from a mixed-model Bayesian strategy that included 14 separate data partitions sampled from three mtDNA and four nuclear genes. Ten of the 31 interspecific nodes in the centrarchid phylogeny were assigned a minimal age estimate from the centrarchid fossil record. Our analyses identified four fossil dates that were inconsistent with the other fossils, and we removed them from the molecular dating analysis. Using fossil-based model cross-validation to determine the optimal smoothing value in penalized likelihood analysis, and six mutually consistent fossil calibrations, the age of the most recent common ancestor of Centrarchidae was 33.59 million years ago (mya). Penalized likelihood analyses of individual data partitions all converged on a very similar age estimate for this node, indicating that rate heterogeneity among data partitions is not confounding our analyses. These results place the origin of the centrarchid radiation at a time of major faunal turnover as the fossil record indicates that the most diverse lineages of the North American freshwater fish fauna originated at the Eocene-Oligocene boundary, approximately 34 mya. This time coincided with major global climate change from warm to cool temperatures and a signature of elevated lineage extinction and origination in the fossil record across the tree of life. Our analyses demonstrate the utility of fossil cross-validation to critically assess individual fossil calibration points, providing the ability to discriminate between consistent and inconsistent fossil age estimates that are used for calibrating molecular phylogenies.

End-Permian stratigraphic timeline applied to the timing of marine and non-marine extinctions

Weihong He, G.R. Shi, Yang Zhang, Tinglu Yang, Fei Teng.& Shunbao Wu, December 2012. Systematics and palaeoecology of Changhsingian (Late Permian) Ambocoeliidae brachiopods from South China and implications for the end-Permian mass extinction. Alcheringa 36, 515–530. ISSN 0311-5518. Four Ambocoeliidae brachiopod species including one new species (Crurithyris tazawai sp. nov., Crurithyris sp., Paracrurithyris pygmaea and Attenuatella mengi) are described from the Changhsingian (Late Permian) deep-water facies of South China. Analysis of the morphology, palaeoecology and palaeogeographical and temporal distributions of these species revealed that the presence of a delthyrium and/or the micro-ornaments among three of the four species (Crurithyris tazawai sp. nov., Paracrurithyris pygmaea and Attenuatella mengi) favoured an epifaunal (epiphytic) lifestyle. Morphological differences suggest that Paracrurithyris pygmaea may have been more effective metabolically in forming the shell compared with Attenuatella mengi and Crurithyris tazawai. The temporal and palaeogeographical distribution of Attenuatella suggests that A. mengi inhabited cool or cold deep waters. Both Crurithyris tazawai and Attenuatella mengi disappeared earlier in the stratigraphic record than Paracrurithyis pygmaea during the Permian–Triassic mass extinction. These differences in timing of extinction, morphology and palaeogeographical distributions suggest that oxygen deficiency and trophic resource limitation (a consequence of the changing composition of marine phytoplankton in the seas) may have contributed to the end-Permian mass extinction.

Investigations into the evolutionary history of the common chimpanzee, Pan troglodytes, have produced inconsistent results due to differences in the types of molecular data considered, the model assumptions employed, and the quantity and geographical range of samples used. We amplified and sequenced 24 complete P. troglodytes mitochondrial genomes from fecal samples collected at multiple study sites throughout sub-Saharan Africa. Using a "relaxed molecular clock," fossil calibrations, and 12 additional complete primate mitochondrial genomes, we analyzed the pattern and timing of primate diversification in a Bayesian framework. Our results support the recognition of four chimpanzee subspecies. Within P. troglodytes, we report a mean (95% highest posterior density [HPD]) time since most recent common ancestor (tMRCA) of 1.026 (0.811-1.263) Ma for the four proposed subspecies, with two major lineages. One of these lineages (tMRCA = 0.510 [0.387-0.650] Ma) contains P. t. verus (tMRCA = 0.155 [0.101-0.213] Ma) and P. t. ellioti (formerly P. t. vellerosus; tMRCA = 0.157 [0.102-0.215] Ma), both of which are monophyletic. The other major lineage contains P. t. schweinfurthii (tMRCA = 0.111 [0.077-0.146] Ma), a monophyletic clade nested within the P. t. troglodytes lineage (tMRCA = 0.380 [0.296-0.476] Ma). We utilized two analysis techniques that may be of widespread interest. First, we implemented a Yule speciation prior across the entire primate tree with separate coalescent priors on each of the chimpanzee subspecies. The validity of this approach was confirmed by estimates based on more traditional techniques. We also suggest that accurate tMRCA estimates from large computationally difficult sequence alignments may be obtained by implementing our novel method of bootstrapping smaller randomly subsampled alignments.

The genus Iksookimia contains six species of primary freshwater fishes that are endemic to South Korea. Previous phylogenetic studies, based on DNA sequence data from three or fewer loci, have suggested non-monophyly of the genus, providing inconsistent resolutions of the relationships of Iksookimia. Our coalescent and concatenation-based phylogenetic analyses, utilizing seven unlinked nuclear-encoded genes, strongly supported Iksookimia as a monophyletic group, emphasizing the importance of multi-locus data in investigating complicated phylogenetic relationships. A relaxed molecular clock analysis using fossil calibrations, indicated that the origin of the major lineages of Iksookimia occurred between ∼12 to 5 Ma, which is consistent with the Miocene uplift of the Taebaek and Sobaek Mountains and the Miocene activation of the major south-eastern faults. These palaeogeographic events may have served as vicariant events in the diversification of Iksookimia.

The genome sequence is an icon of early twenty-first century biology. Genomes of nearly 2000 cellular organisms, and from many thousands of organelles and viruses, are now in the public domain. For biological research in individual species, the genome sequence increasingly provides the common

The Sternorrhyncha, which comprise about 18,700 described recent species, is a suborder of the Hemiptera, one of big five most diverse insect orders. In the modern fauna, these tiny phytophages comprise insects of great ecological and economic importance, like aphids (Aphidomorpha), scale insects (Coccidomorpha), whiteflies (Aleyrodomorpha) and psyllids (Psylloidea). Their evolutionary history can be traced back to the Late Carboniferous, but the early stages of their evolution and diversification is poorly understood, with two known extinct groups—Pincombeomorpha and Naibiomorpha variously placed in classifications and relationships hypotheses. Most of the recent Sternorrhyncha groups radiated rapidly during the Cretaceous. Here we report the new finding of very specialised sternorrhynchans found as inclusions in mid-Cretaceous amber from Kachin state (northern Myanmar), which represent another extinct lineage within this hemipteran suborder. These fossils, proposed to be placed in a new infraorder, are revealed to be related to whiteflies and psyllids. We present, also for the first time, the results of phylogenetic analyses covering extinct and extant lineages of the Sternorrhyncha.

The Diptera, or true flies (mosquitoes, gnats, and house flies) comprise 12-15% of animal species, and are the most ecologically diverse order of insects, spanning ecological roles from detritivory to vertebrate blood feeding and leaf mining. The earliest known fossil Diptera are from the early Triassic 240 mya, and the order probably arose in the late Permian. The earliest brachyceran fossils are found in the late Triassic and earliest Jurassic, but the diversification of the extremely diverse Calyptrata (ca. 30% of described species) began in the late Creataceous. The monophyly of the order is supported by numerous morphological and biological characters and molecular data sets. The major lineages within the order are well established, and we summarize major recent phylogenetic analyses in a supertree for the Diptera. Most studies concur that the traditional subordinal group Nematocera is paraphyletic, but relationships between the major lineages of these flies are not recovered consistently. There is particular instability around the placement of the tipulids and their relatives and the families of the Psychodomorpha as traditionally defined. The other major suborder, Brachycera, is clearly monophyletic, and the relationships between major brachyceran lineages have become clearer in recent decades. The Eremoneura, Cyclorrhapha, Schizophora and Calyptrata are monophyletic, however the “Orthorrhapha” and “Aschiza” are paraphyletic, and it is likely that the “Acalyptrata” are also. Ongoing phylogenetic analyses that span the diversity of the order shall establish a robust phylogeny of the group with increased quantitative rigor. This will enable a more precise understanding of the evolution of the morphology, biogeography, biology, and physiology of flies.

ABSTRACTBayesian analysis of radiocarbon (14C) dates in North American archaeology is increasing, especially among archaeologists working in deeper time. However, historical archaeologists have been slow to embrace these new techniques, and there have been only a few examples of the incorporation of calendar dates as informative priors in Bayesian models in such work in the United States. To illustrate the value of Bayesian approaches to sites with both substantial earlier Native American occupations as well as a historic era European presence, we present the results of our Bayesian analysis of 14C dates from the earlier Guale village and the Mission period contexts from the Sapelo Shell Ring Complex (9MC23) in southern Georgia. Jefferies and Moore have explored the Spanish Mission period deposits at this site to better understand the Native American interactions with the Spanish during the 16th and 17th centuries along the Georgia Coast. Given the results of our Bayesian modeling, we can say with some degree of confidence that the deposits thus far excavated and sampled contain important information dating to the 17th-century mission on Sapelo Island. In addition, our modeling of new dates suggests the range of the pre-Mission era Guale village. Based on these new dates, we can now say with some degree of certainty which of the deposits sampled likely contain information that dates to one of the critical periods of Mission period research, the AD 1660–1684 period that ushered in the close of mission efforts on the Georgia Coast.

The number and complexity of molecular dating studies has increased over the past decade. Along with a broadening acceptance of their utility has come significant controversy over the methods and models that are appropriate, as well as the accuracy of the estimates yielded by molecular clock analyses. Radically different age estimates have been published for the same divergences from analyses of different datasets with different fossil constraints obtained with different methods, and the underlying explanation for these differences is often unclear. Here we utilize two previously published datasets to examine the effect of fossil calibrations and taxon sampling on the age estimates for two deep eukaryote divergences in an attempt to discern the relative impact of these factors. Penalized likelihood, non-parametric rate smoothing, and Bayesian methods were utilized to generate age estimates for the origin of the Metazoa from a 7-gene dataset and for the divergence of Eukaryotes from a 129-gene dataset. From these analyses, it is clear that the fossil calibrations chosen and the method for applying constraints to these nodes have a large impact on age estimates, while the degree of taxon sampling within a dataset is less important in terms of the resulting age estimates. Concerns and recommendations for addressing these two factors when initiating a dating analysis are discussed.