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Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data.

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100042).\n\nReconstructing ancestral characters on a phylogeny is an arduous task because the observed states at the tips of the tree correspond to a single realization of the underlying evolutionary process. Recently, it was proposed that ancestral traits can be indirectly estimated with the help of molecular data, based on the fact that life history traits influence substitution rates. Here we challenge these new approaches in the Cetartiodactyla, a clade of large mammals which, according to paleontology, derive from small ancestors. Analysing transcriptome data in 41 species, of which 22 were newly sequenced, we provide a dated phylogeny of the Cetartiodactyla and report a significant effect of body mass on the overall substitution rate, the synonymous vs. non-synonymous substitution rate and the dynamics of GC-content. Our molecular comparative analysis points toward relatively small Cetartiodactyla ancestors, in agreement with the fossil record, even though our data set almost exclusively consists of large species. This analysis demonstrates the potential of phylogenomic methods for ancestral trait reconstruction and gives credit to recent suggestions that the ancestor to placental mammals was a relatively large and long-lived animal.

evolutionary biology↗

Evolutionary history of New World monkeys revealed by molecular and fossil data

New World monkeys (parvorder Platyrrhini) are one of the most diverse groups of primates, occupying today a wide range of ecosystems in the American tropics and exhibiting large variations in ecology, morphology, and behavior. Although the relationships among the almost 200 living species are relatively well understood, we lack robust estimates of the timing of origin, the ancestral morphology, and the evolution of the distribution of the clade. Here we integrate paleontological and molecular evidence to investigate the evolutionary dynamics of extinct and extant platyrrhines. We develop an analytical framework to infer ancestral states, the evolution of body mass, and changes in latitudinal ranges through time. Our results show that extant platyrrhines originated some 5-10 million years earlier than previously assumed, likely dating back to the Middle Eocene ([~] 43 million years ago, Ma). The estimated ancestral platyrrhine was strikingly small - weighing [~] 0.4 kg, as compared to the largest modern species over 10 kg - matching the size of their presumed Eocene North African ancestors. Small-sized callitrichines (marmosets and tamarins) retained a small body mass throughout their evolutionary history, thus challenging the hypothesis of phyletic dwarfism as an explanation to their adaptive traits. In contrast, a rapid change in body mass range took place as the three families diverged between the Late Oligocene and the Early Miocene. That period also marks a peak in diversity of fossil platyrrhines and is associated with their widest latitudinal range, expanding as far to the South as Patagonia. This geographic expansion is temporally coincident with a significant increase in platyrrhine population size inferred from genomic data, and with warm and humid climatic conditions linked to the Miocene Climatic Optimum and the lower elevation of the Andes. These results unveil the early evolution of an iconic group of monkeys and showcase the advantages of integrating fossil and molecular data for estimating evolutionary rates and trends.

evolutionary biology↗

The West African lungfish provides insights into the evolution of tetrapod tail regeneration

Salamanders, frog tadpoles, and diverse lizards have the remarkable ability to regenerate tails. Paleontological data suggests that this capacity is plesiomorphic, yet when the developmental and genetic architecture of tail regeneration arose is poorly understood. Here we show morphological and molecular hallmarks of tetrapod tail regeneration in the West African lungfish Protopterus annectens, a living representative of the sister group of tetrapods. As in salamanders, lungfish tail regeneration occurs via formation of a proliferative blastema and restores original structures, including muscle, skeleton and spinal cord. In contrast to lizards and similar to salamanders and frogs, lungfish regenerate spinal cord neurons and reconstitute dorsoventral patterning of the tail. Similar to salamander and frog tadpoles, Shh is required for lungfish tail regeneration. Through RNA-seq analysis of uninjured and regenerating tail blastema, we show that the genetic program deployed during lungfish tail regeneration maintains extensive overlap with that of tetrapods, with the upregulation of genes and signaling pathways previously implicated in amphibian and lizard tail regeneration. Furthermore, the lungfish tail blastema showed marked upregulation of genes encoding post-transcriptional RNA processing components and transposon-derived genes. Our results show that developmental processes and genetic program of tetrapod tail regeneration were present at least near the base of the sarcopterygian clade and establish the lungfish as a valuable research system for regenerative biology.

evolutionary biology↗

A Total-Evidence Dated Phylogeny of Echinoids and the Evolution of Body Size across Adaptive Landscape

Several unique properties of echinoids (sea urchins) make them useful for exploring macroevolutionary dynamics, including their remarkable fossil record that can be incorporated into explicit phylogenetic hypotheses. However, this potential cannot be exploited without a robust resolution of the echinoid tree of life. We revisit the phylogeny of crown group Echinoidea using both the largest phylogenomic dataset compiled for the clade, as well as a large-scale morphological matrix with a dense fossil sampling. We also gather a new compendium of both tip and node age constraints, allowing us to combine phylogenomic, morphological and stratigraphic data using a total-evidence dating approach. For this, we develop a novel method for subsampling phylogenomic datasets that selects loci with high phylogenetic signal, low systematic biases and enhanced clock-like behavior. Our approach restructure much of the higher-level phylogeny of echinoids, and demonstrates that combining different data sources increases topological accuracy. We are able to resolve multiple alleged conflicts between molecular and morphological datasets, such as the position of Echinothurioida and Echinoneoida, as well as unravelling the relationships between sand dollars and their closest relatives. We then use this topology to trace the evolutionary history of echinoid body size through more than 270 million years, revealing a complex pattern of convergent evolution to stable peaks in macroevolutionary adaptive landscape. Our efforts show how combining phylogenomic and paleontological evidence offers new ways of exploring evolutionary forces operating across deep timescales.

evolutionary biology↗

Rewinding the molecular clock in the genus Carabus (Coleoptera: Carabidae): Revisiting Andujar et al. in light of new fossil evidence and the Gondwana split

1BackgroundMolecular clocks have become powerful tools given increasing sequencing and fossil resources. However, outcome of calibration analyses depend on choosing priors. Here we revisit a seminal dating study of the genus Carabus by Andujar et al. proposing that their prior choices need re-evaluation with the hypothesis that reflecting fossil evidence and the Gondwanan split properly rewinds the molecular clock significantly. We used the same dataset including five mitochondrial and four nuclear DNA fragments with 7888 nt total length. We set the root age based on the fossil evidence of Harpalinae ground beetles in the Upper Cretaceous and introduce the Paleogene divergence of the outgroup taxa Ceroglossus (endemic to South-America) and Pamborus + Maoripamborus (Australia, New Zealand) as a new prior based on current paleontological and geological literature. ResultsThe ultrametric time-calibrated tree of the extended nd5 dataset resulted in a median TMRCA Carabus age of 58.48 Ma (HPD95% 46.61-72.04), roughly 35 Ma older than in the Andujar study. The splits between C. rugosus and C. morbillosus (A), between C. riffensis from the European Mesocarabus (B), and between Eurycarabus and Nesaeocarabus (C) were dated to 19.19 (13.54-25.87), 25.95 (18.8-34.62), and 23.98 (17.28-31.47) Ma and were thus decidedly older than previously reported (7.48, 10.93, and 9.51 Ma). These changes were driven solely by constraining the Carabidae time tree root with Harpalinae amber fossils at [~]99 Ma. Utilizing the nd5 dating results of three well supported Carabus clades as secondary calibration points for the complete MIT-NUC data set lead to a TMRCA of Carabus of 53.56 (41.25-67.05) Ma compared to 25.16 (18.41-33.04) in Andujars study. ConclusionTaking into account the Gondwanan split as a new prior, together with the fossil evidence of the outgroup taxon Harpalini in the Late Cretaceous, our new approach supports an origin of the genus Carabus in the Paleocene-Early Eocene. Our results are preliminary due to the heavy reliance on the nd5 gene and thus will have to be tested with sufficient set of nuclear markers. In addition, uncertainties arise from dating the root age of the tree based on a single fossil and outgroup taxon which has a major effect on the results. Improvement of the fossil data base particularly in the supertribe Carabitae is thus strongly needed to reduce the currently large uncertainties in dating Carabus phylogeny.

evolutionary biology↗

Climate change alters plant-herbivore interactions

Plant-herbivore interactions have evolved in response to co-evolutionary dynamics, along with selection driven by abiotic conditions. We examine how abiotic factors influence trait expression in both plants and herbivores to evaluate how climate change will alter this long-standing interaction. The paleontological record documents increased herbivory during periods of global warming in the deep past. In phylogenetically-corrected meta-analyses, we find that elevated temperatures, CO2 concentration, drought stress and nutrient conditions directly and indirectly induce greater herbivore consumption, primarily in agricultural systems. Additionally, elevated CO2 delays herbivore development, but increased temperatures accelerate development. For annual plants, higher temperatures, CO2, and drought stress increase foliar herbivory, and our meta-analysis suggests that greater temperatures and drought may heighten florivory in perennials. Human actions are causing concurrent shifts in CO2, temperature, precipitation regimes and nitrogen deposition, yet few studies evaluate interactions among these changing conditions. We call for additional multifactorial studies that simultaneously manipulate multiple climatic factors, which will enable us to generate more robust predictions of how climate change could disrupt plant-herbivore interactions. Finally, we consider how shifts in insect and plant phenology and distribution patterns could lead to ecological mismatches, and how these changes may drive future adaptation and coevolution between interacting species.

plant biology↗

From scales to armour: scale losses and trunk bony plate gains in ray-finned fishes

Actinopterygians (ray-finned fishes) are the most diversified group of vertebrates and are characterized by a variety of protective structures covering their tegument, the evolution of which has intrigued biologists for decades. Paleontological records showed that the first mineralized vertebrate skeleton was composed of dermal bony plates covering the body, including odontogenic and skeletogenic components. Later in evolution, the exoskeleton of actinopterygians trunk was composed of scale structures. Although scales are nowadays a widespread tegument cover, some contemporary lineages do not have scales but bony plates covering their trunk, whereas other lineages are devoid of any such structures. To understand the evolution of the tegument coverage and particularly the transition between different structures, we investigated the pattern of scale loss events along actinopterygian evolution and addressed the functional relationship between the scaleless phenotype and the ecology of fishes. Furthermore, we examined whether the emergence of trunk bony plates was dependent over the presence or absence of scales. To this aim, we used two recently published actinopterygian phylogenies, one including > 11,000 species, and by using stochastic mapping and Bayesian methods, we inferred scale loss events and trunk bony plate acquisitions. Our results reveal that a scaled tegument is the most frequent state in actinopterygians, but multiple independent scale loss events occurred along their phylogeny with essentially no scale re-acquisition. Based on linear mixed models, we found evidence supporting that after a scale loss event, fishes tend to change their ecology and adopt a benthic lifestyle. Furthermore, we show that trunk bony plates appeared independently multiple times along the phylogeny. By using fitted likelihood models for character evolution, we show that trunk bony plate acquisitions were dependent over a previous scale loss event. Overall, our findings support the hypothesis that tegument cover is a key evolutionary trait underlying actinopterygian radiation. Impact SummaryRay-finned fishes (actinopterygians) are the most diverse vertebrate group in the world. The majority of these fishes possess scales as a protective shield covering their trunk. However, several lineages display a body armour composed of trunk bony plates or are devoid of any protective structures. The diversity and the transitions between different tegument coverage types have not been previously studied in an evolutionary framework. Here, we investigate which structure was present at the origin of ray-finned fishes and how the different phenotypes emerged through time. We show that a scaled tegument was the most widespread sate along ray-finned fish evolution, yet scale losses occurred multiple independent times, while acquiring scales again almost never happened. Moreover, we reveal that scaleless teguments most probably led species to change their ecology and colonise the floors of oceans and water bodies. The functional advantages of a scaleless tegument in a benthic environment are yet to be demonstrated, but the increased cutaneous respiration could be an explanation. We show that trunk bony plates also emerged independently multiple times along the evolution of ray-finned fishes but these armours protecting the trunk can only appear after a scale loss event. Therefore, while the acquisitions of trunk bony plates are phylogenetically independent, they need a "common ground" to emerge. All together, our findings provide evidence that the various tegument covers have contributed to the outstanding diversification of ray-finned fishes.

evolutionary biology↗

Machine learning (decision tree analysis) identifies ecological selectivity patterns across the end-Permian mass extinction

Decision tree algorithms are rarely utilized in paleontological research, and here we show that machine learning algorithms can be used to identify determinants of extinction as well as predict extinction risk. This application of decision tree algorithms is important because the ecological selectivity of mass extinctions can reveal critical information on organismic traits as key determinants of extinction and hence the causes of extinction. To understand which factors led to the mass extinction of life during an extreme global warming event, we quantified the ecological selectivity of marine extinctions in the well-studied South China region during the end-Permian mass extinction using the categorized gradient boosting algorithm. We find that extinction selectivity varies between different groups of organisms and that a synergy of multiple environmental stressors best explains the overall end-Permian extinction selectivity pattern. Extinction risk was greater for genera that were limited to deep-water habitats, had a stationary mode of life, possessed a siliceous skeleton or, less critically, had calcitic skeletons. These selective losses directly link the extinction to the environmental effects of rapid injections of carbon dioxide into the ocean-atmosphere system, specifically the combined effects of expanded oxygen minimum zones, rapid warming, and ocean acidification.

evolutionary biology↗

A skyline birth-death process for inferring the population size from a reconstructed tree with occurrences

Phylodynamic models generally aim at jointly inferring phylogenetic relationships, model parameters, and more recently, population size through time for clades of interest, based on molecular sequence data. In the fields of epidemiology and macroevolution these models can be used to estimate, respectively, the past number of infected individuals (prevalence) or the past number of species (paleodiversity) through time. Recent years have seen the development of "total-evidence" analyses, which combine molecular and morphological data from extant and past sampled individuals in a unified Bayesian inference framework. Even sampled individuals characterized only by their sampling time, i.e. lacking morphological and molecular data, which we call occurrences, provide invaluable information to reconstruct past population sizes. Here, we present new methodological developments around the Fossilized Birth-Death Process enabling us to (i) efficiently incorporate occurrence data while remaining computationally tractable and scalable; (ii) consider piecewise-constant birth, death and sampling rates; and (iii) reconstruct past population sizes, with or without knowledge of the underlying tree. We implement our method in the RevBayes software environment, enabling its use along with a large set of models of molecular and morphological evolution, and validate the inference workflow using simulations under a wide range of conditions. We finally illustrate our new implementation using two empirical datasets stemming from the fields of epidemiology and macroevolution. In epidemiology, we apply our model to the Covid-19 outbreak on the Diamond Princess ship. We infer the total prevalence throughout the outbreak, by taking into account jointly the case count record (occurrences) along with viral sequences for a fraction of infected individuals. In macroevolution, we present an empirical case study of cetaceans. We infer the diversity trajectory using molecular and morphological data from extant taxa, morphological data from fossils, as well as numerous fossil occurrences. Our case studies highlight that the advances we present allow us to further bridge the gap between between epidemiology and pathogen genomics, as well as paleontology and molecular phylogenetics.

evolutionary biology↗

How to align arthropod legs

Arthropods (insects, "crustaceans", myriapods, and chelicerates) display a fascinating diversity of ectodermal structures like plates, horns, helmets, knobs, carapaces, mimicry outgrowths, and wings. The origins and relationships of these structures has tantalized researchers for over a century: did these structures arise de novo in each lineage, or do they emerge from shared, ancestral primordia present in some or even all arthropods? One way to begin answering this is to assess the position and context of these structures on arthropod bodies: do these structures emerge from proximal embryonic leg segments that were converted into the body wall, or do they represent dorsal, non-leg-derived structures? Here, the expression of pannier, araucan, and drumstick - genes previously shown to distinguish proximal leg segments in crustaceans and insects - are examined in a chelicerate representative, the tarantula Acanthoscurria. This gene expression comparison, together with over a century of gene functional, morphological, embryological, and paleontological data, suggests that all arthropod leg segments correspond to each other in a one-to-one fashion, but that in many arthropod lineages, the base of the ancestral leg in the embryo flattens and expands to form the body wall of the adult. This would mean that many arthropod outgrowths which appear to stand on the lateral body wall, such as wings, tergal plates, and gin traps, are derived from the ancestral/embryonic leg base, and likely arose from shared, ancestral primordia present on this leg base in all arthropods. The analysis detailed here means that a simple three- or four-gene in situ expression experiment with pannier, araucan, and drumstick can elucidate the homologies of any arthropod ectodermal structure of interest, including beetle horns, treehopper helmets, and more.

developmental biology↗

Mitochondrial genome phylogeny of voles and lemmings (Rodentia: Arvicolinae): evolutionary and taxonomic implications

Arvicolinae is one of the most impressive placental radiations with over 150 extant and numerous extinct species that emerged since the Miocene in the Northern Hemisphere. The phylogeny of Arvicolinae has been studied intensively for several decades using morphological and genetic methods. Here, we sequenced 30 new mitochondrial genomes to better understand the evolutionary relationships among the major tribes and genera within the subfamily. The phylogenetic and molecular dating analyses based on 11,391 bp concatenated alignment of protein-coding mitochondrial genes confirmed the monophyly of the subfamily. While Bayesian analysis provided a high resolution across the entire tree, Maximum Likelihood tree reconstruction showed weak support for the ordering of divergence and interrelationships of tribal level taxa within the most ancient radiation. Both the interrelationships among tribes Lagurini, Ellobiusini and Arvicolini, comprising the largest radiation and the position of the genus Dinaromys within it also remained unresolved. For the first time complex relationships between genus level taxa within the species-rich tribe Arvicolini received full resolution. Particularly Lemmiscus was robustly placed as sister to the snow voles Chionomys in the tribe Arvicolini in contrast with a long-held belief of its affinity with Lagurini. Molecular dating of the origin of Arvicolinae and early divergences obtained from the mitogenome data were consistent with fossil records. The mtDNA estimates for putative ancestors of the most genera within Arvicolini appeared to be much older than it was previously proposed in paleontological studies.

zoology↗

Dental caries in wild primates: interproximal cavities on anterior teeth

Dental caries has been reported in a variety of primates, although is still considered rare in wild populations. In this study, 11 catarrhine primates were studied for the presence of caries. A differential diagnosis of lesions found in interproximal regions of anterior teeth was undertaken, since they had been previously described as both carious and non-carious in origin. Each permanent tooth was examined macroscopically, with severity and position of lesions recorded. Two specimens were micro-CT scanned to assess demineralization. The differential diagnosis confirmed the cariogenic nature of interproximal cavities on anterior teeth (ICATs). Overall results show 3.3% of teeth are carious, with prevalence varying among species from 0% to over 7% of teeth affected. ICATs occurred in Pan troglodytes (9.8%), Gorilla gorilla gorilla (2.6%), Cercopithecus denti (22.4%), Presbytis femoralis (19.5%) and Cercopithecus mitis (18.3%). They make up 87.9% of carious lesions on anterior teeth. These results likely reflect dietary and food processing differences among species, but also between the sexes (e.g., 9.3% of teeth of female chimpanzees were carious vs. 1.8% in males). Processing cariogenic fruits and seeds with the anterior dentition (e.g., wadging) likely contributes to ICAT formation. Further research is needed on living populations to ascertain behavioral/dietary influences on caries occurrence in primates. Given the constancy of ICATs in frugivorous primates, their presence in archaeological and paleontological specimens may shed light on diet and food processing behaviors in fossil primates.

zoology↗

Problems using ordinal traits with continuous measures of functional diversity

Continuous indices of functional diversity are popular in studies examining community structure and ecosystem function across a wide range of subfields from paleontology to range management. These indices were designed to replace the use of more arbitrary, discrete functional groups or guilds; however, the effect of typical methodological decisions on these new continuous measures has not been fully investigated. To test the effect of using ordinal traits in functional diversity analysis, I first calculated relative functional diversity index values in real plant communities with real continuous trait data and Euclidean distances. I then compared these original values to "treatment" functional diversity index values obtained by discretizing the trait data and using Gowers distance. Agreement between original and treatment values was highly unpredictable and often abysmal. Small methodological choices, such as whether to treat a functional trait as continuous (mm) or ordinal ("small", "medium", "large"), could completely change a perceived functional diversity relationship along an environmental gradient. Some parameter combinations returned results that were no better than random noise. Because simple methodological choices can have such a large impact on continuous functional diversity indices, it is ambiguous whether analyses using ordinal traits are actually measuring an underlying functional diversity relationship between communities or just reflecting the arbitrary parameter choices of researchers.

ecology↗

New Insights on the Evolutionary Relationships Between the Major Lineages of Amoebozoa

The supergroup Amoebozoa unites a wide diversity of amoeboid organisms and encompasses enigmatic lineages recalcitrant to modern phylogenetics. Deep divergences, taxonomic placement of some key taxa and character evolution in the group largely remain poorly elucidated or controversial. We surveyed available Amoebozoa genomes and transcriptomes to mine conserved putative single copy genes, which were used to enrich gene sampling and generate the largest supermatrix (824 genes) in the group to date. We recovered a well-resolved and supported tree of Amoebozoa, revealing novel deep level relationships and resolving placement of enigmatic lineages congruent with morphological data. In our analysis the deepest branching group is Tubulinea. A recent proposed major clade Tevosa, uniting Evosea and Tubulinea, is not supported. Based on the new phylogenetic tree, paleoecological and paleontological data as well as data on the biology of presently living amoebozoans, we hypothesize that the evolution of Amoebozoa probably was driven with the need to disrupt and graze on microbial mats - a dominant ecosystem of the mid-Proterozoic period of the Earth history.

evolutionary biology↗

Sampling bias and the robustness of ecological metrics for plant-damage-type association networks

Plants and their insect herbivores have been a dominant component of the terrestrial ecological landscape for the past 410 million years and feature intricate evolutionary patterns and co-dependencies. A complex systems perspective allows for both detailed resolution of these evolutionary relationships as well as comparison and synthesis across systems. Using proxy data of insect herbivore damage (denoted by the damage type or DT) preserved on fossil leaves, functional bipartite network representations provide insights into how plant-insect associations depend on geological time, paleogeographical space, and environmental variables such as temperature and precipitation. However, the metrics measured from such networks are prone to sampling bias. Such sensitivity is of special concern for plant-DT association networks in paleontological settings where sampling effort is often severely limited. Here, we explore the sensitivity of functional bipartite network metrics to sampling intensity and identify sampling thresholds above which metrics appear robust to sampling effort. Across a broad range of sampling efforts, we find network metrics to be less affected by sampling bias and/or sample size than richness metrics, which are routinely used in studies of fossil plant-DT interactions. These results provide reassurance that cross-comparisons of plant-DT networks offer insights into network structure and function and support their widespread use in paleoecology. Moreover, these findings suggest novel opportunities for using plant-DT networks in neontological terrestrial ecology to understand functional aspects of insect herbivory across geological time, environmental perturbations, and geographic space.

ecology↗

Inaccurate fossil placement does not compromise tip-dated divergence times

Time-scaled phylogenies underpin the interrogation of evolutionary processes across deep timescales, as well as attempts to link these to Earths history. By inferring the placement of fossils and using their ages as temporal constraints, tip dating under the fossilised-birth death (FBD) process provides a coherent prior on divergence times. At the same time, it also links topological and temporal accuracy, as incorrectly placed fossil terminals should misinform divergence times. This could pose serious issues for obtaining accurate node ages, yet the interaction between topological and temporal error has not been thoroughly explored. We simulate phylogenies and associated morphological datasets using methodologies that incorporate evolution under selection, and are benchmarked against empirical datasets. We find that datasets of moderate sizes (300 characters) and realistic levels of missing data generally succeed in inferring the correct placement of fossils on a constrained extant backbone topology, and that true node ages are usually contained within Bayesian posterior distributions. While increased fossil sampling improves the accuracy of inferred ages, topological and temporal errors do not seem to be linked: analyses in which fossils resolve less accurately do not exhibit elevated errors in node age estimates. At the same time, divergence times are systematically biased, a pattern that stems from a mismatch between the FBD prior and the shape of our simulated trees. While these results are encouraging, suggesting even fossils with uncertain affinities can provide useful temporal information, they also emphasise that paleontological information cannot overturn discrepancies between model priors and the true diversification history.

evolutionary biology↗

Diversification of the Ruminant Skull Along an Evolutionary Line of Least Resistance

Morphological integration is relevant to evolutionary biology and paleontology because the structure of variation within populations determines the ways in which a population can respond to selective pressures. However, understanding the macroevolutionary consequences of morphological integration is elusive because the adaptive landscape is dynamic and population-level constraints themselves evolve. By analyzing a previously published dataset of 2859 ruminant crania with 3D geometric morphometrics and phylogenetic comparative methods, we find that variation within and between ruminant species is biased by a highly conserved mammalian-wide allometric pattern, CREA, where larger species have proportionally longer faces. More tightly integrated species and species more biased towards CREA have diverged farther from their ancestors, and Ruminantia as a clade diversified farther than expected in the direction anticipated by CREA. Our analyses indicate that CREA acts as an evolutionary line of least resistance and facilitates morphological diversification due to its alignment with the browser-grazer continuum. These results demonstrate that biological processes constraining variation at the microevolutionary level can produce highly directional phenotypic evolution over macroevolutionary timescales.

evolutionary biology↗

Novel Complete Methanogenic Pathways in Longitudinal Genomic Study of Monogastric Age-Associated Archaea

BackgroundArchaea perform critical roles in the microbiome system, including utilizing hydrogen to allow for enhanced microbiome member growth and influencing overall host health. With the majority of microbiome research focussing on bacteria, the functions of archaea are largely still under investigation. Understanding methanogenic functions during the host lifetime will add to the limited knowledge on archaeal influence on gut and host health. In our study, we determined lifelong archaea detection and methanogenic functions while assessing global and host distribution of our novel archaeal metagenome assembled genomes (MAGs). We followed 7 monogastric swine throughout their life, from birth to adult (1-156 days of age), and collected feces at 22 time points. The samples underwent gDNA extraction, Illumina sequencing, bioinformatic quality and assembly processes, and MAG taxonomic assignment and functional annotation. ResultsWe generated 1,130 non-redundant MAGs with 8 classified as methanogenic archaea. The taxonomic classifications were as follows: orders Methanomassiliicoccales (5) and Methanobacteriales (3); genera UBA71 (3), Methanomethylophilus (1), MX-02 (1), and Methanobrevibacter (3). We recovered the first US swine Methanobrevibacter UBA71 sp006954425 and Methanobrevibacter gottschalkii MAGs. The Methanobacteriales MAGs were identified primarily during the young, preweaned host whereas Methanomassiliicoccales primarily in the adult host. Moreover, we identified our methanogens in metagenomic sequences from Chinese swine, US adult humans, Mexican adult humans, Swedish adult humans, and paleontological humans, indicating that methanogens span different hosts, geography and time. We determined complete metabolic pathways for all three methanogenic pathways: hydrogenotrophic, methylotrophic, and acetoclastic. This study provided the first evidence of acetoclastic methanogenesis in monogastric archaea which indicated a previously unknown capability for acetate utilization in methanogenesis for monogastric methanogens. Overall, we hypothesized that the age-associated detection patterns were due to differential substrate availability via the host diet and microbial metabolism, and that these methanogenic functions are likely crucial to methanogens across hosts. This study provided a comprehensive, genome-centric investigation of monogastric-associated methanogens which will further our understanding of microbiome development and functions.

microbiology↗