Origins and Functional Significance of Eukaryotic Protein Folds.

Folds are the architecture and topology of a protein domain. Categories of folds are very few compared to the astronomical number of sequences. Eukaryotes have more protein folds than Archaea and Bacteria. These folds are of two types: shared with Archaea and/or Bacteria on one hand and specific to eukaryotic clades on the other hand. The first kind of folds is inherited from the first endosymbiosis and confirms the mixed origin of eukaryotes. In a dataset of 1073 folds whose presence or absence has been evidenced among 210 species equally distributed in the three super-kingdoms, we have identified 28 eukaryotic folds unambiguously inherited from Bacteria and 40 eukaryotic folds unambiguously inherited from Archaea. Compared to previous studies, the repartition of informational function is higher than expected for folds originated from Bacteria and as high as expected for folds inherited from Archaea. The second type of folds is specifically eukaryotic and associated with an increase of new folds within eukaryotes distributed in particular clades. Reconstructed ancestral states coupled with dating of each node on the tree of life provided fold appearance rates. The rate is on average twice higher within Eukaryota than within Bacteria or Archaea. The highest rates are found in the origins of eukaryotes, holozoans, metazoans, metazoans stricto sensu, and vertebrates: the roots of these clades correspond to bursts of fold evolution. We could correlate the functions of some of the fold synapomorphies within eukaryotes with significant evolutionary events. Among them, we find evidence for the rise of multicellularity, adaptive immune system, or virus folds which could be linked to an ecological shift made by tetrapods.

Revisiting Nature's "Unifying Patterns": A Biological Appraisal.

Effective bioinspiration requires dialogue between designers and biologists, and this dialogue must be rooted in a shared scientific understanding of living systems. To support learning from "nature's overarching design lessons" the Biomimicry Institute has produced ten "Unifying Patterns of Nature". These patterns have been developed to engage with those interested in finding biologically inspired solutions to human challenges. Yet, although well-intentioned and appealing, they are likely to dishearten biologists. The aim of this paper is to identify why and propose alternative principles based on evolutionary theory.

Genome structures resolve the early diversification of teleost fishes.

Accurate species phylogenies are a prerequisite for all evolutionary research. Teleosts are the largest and most diversified group of extant vertebrates, but relationships among their three oldest extant lineages remain unresolved. On the basis of seven high-quality new genome assemblies in Elopomorpha (tarpons, eels), we revisited the topology of the deepest branches of the teleost phylogeny using independent gene sequence and chromosomal rearrangement phylogenomic approaches. These analyses converged to a single scenario that unambiguously places the Elopomorpha and Osteoglossomorpha (arapaima, elephantnose fish) in a monophyletic sister group to all other teleosts, i.e., the Clupeocephala lineage (zebrafish, medaka). This finding resolves more than 50 years of controversy on the evolutionary relationships of these lineages and highlights the power of combining different levels of genome-wide information to solve complex phylogenies.

Protein folds as synapomorphies of the tree of life.

Several studies showed that folds (topology of protein secondary structures) distribution in proteomes may be a global proxy to build phylogeny. Then, some folds should be synapomorphies (derived characters exclusively shared among taxa). However, previous studies used methods that did not allow synapomorphy identification, which requires congruence analysis of folds as individual characters. Here, we map SCOP folds onto a sample of 210 species across the tree of life (TOL). Congruence is assessed using retention index of each fold for the TOL, and principal component analysis for deeper branches. Using a bicluster mapping approach, we define synapomorphic blocks of folds (SBF) sharing similar presence/absence patterns. Among the 1232 folds, 20% are universally present in our TOL, whereas 54% are reliable synapomorphies. These results are similar with CATH and ECOD databases. Eukaryotes are characterized by a large number of them, and several SBFs clearly support nested eukaryotic clades (divergence times from 1100 to 380 mya). Although clearly separated, the three superkingdoms reveal a strong mosaic pattern. This pattern is consistent with the dual origin of eukaryotes and witness secondary endosymbiosis in their phothosynthetic clades. Our study unveils direct analysis of folds synapomorphies as key characters to unravel evolutionary history of species.

Musculotendinous system of mesopelagic fishes: Stomiiformes (Teleostei).

Every night the greatest migration on Earth starts in the deep pelagic oceans where organisms move up to the meso- and epipelagic to find food and return to the deeper zones during the day. One of the dominant fish taxa undertaking vertical migrations are the dragonfishes (Stomiiformes). However, the functional aspects of locomotion and the architecture of the musculotendinous system (MTS) in these fishes have never been examined. In general, the MTS is organized in segmented blocks of specific three-dimensional 'W-shaped' foldings, the myomeres, separated by thin sheets of connective tissue, the myosepta. Within a myoseptum characteristic intermuscular bones or tendons may be developed. Together with the fins, the MTS forms the functional unit for locomotion in fishes. For this study, microdissections of cleared and double stained specimens of seven stomiiform species (Astronesthes sp., Chauliodus sloani, Malacosteus australis, Eustomias simplex, Polymetme sp., Sigmops elongatus, Argyropelecus affinis) were conducted to investigate their MTS. Soft tissue was investigated non-invasively in E. schmidti using a micro-CT scan of one specimen stained with iodine. Additionally, classical histological serial sections were consulted. The investigated stomiiforms are characterized by the absence of anterior cones in the anteriormost myosepta. These cones are developed in myosepta at the level of the dorsal fin and elongate gradually in more posterior myosepta. In all but one investigated stomiiform taxon the horizontal septum is reduced. The amount of connective tissue in the myosepta is very low anteriorly, but increases gradually with body length. Red musculature overlies laterally the white musculature and exhibits strong tendons in each myomere within the muscle bundles dorsal and ventral to the horizontal midline. The amount of red musculature increases immensely towards the caudal fin. The elongated lateral tendons of the posterior body segments attach in a highly complex pattern on the caudal-fin rays, which indicates that the posterior most myosepta are equipped for a multisegmental force transmission towards the caudal fin. This unique anatomical condition might be essential for steady swimming during diel vertical migrations, when prey is rarely available.

Hierarchical analysis of ontogenetic time to describe heterochrony and taxonomy of developmental stages.

Even though an accurate description of early life stages is available for some teleostean species in form of embryonic and post-embryonic developmental tables, there is poor overlap between species-specific staging vocabularies beyond the taxonomic family level. What is called "embryonic period", "larval period", "metamorphosis", or "juvenile" is anatomically different across teleostean families. This problem, already pointed out 50 years ago, challenges the consistency of developmental biology, embryology, systematics, and hampers an efficient aquaculture diversification. We propose a general solution by producing a proof-of-concept hierarchical analysis of ontogenetic time using a set of four freshwater species displaying strongly divergent reproductive traits. With a parsimony analysis of a matrix where "operational taxonomic units" are species at a given ontogenetic time segment and characters are organs or structures which are coded present or absent at this time, we show that the hierarchies obtained have both very high consistency and retention index, indicating that the ontogenetic time is correctly grasped through a hierarchical graph. This allows to formally detect developmental heterochronies and might provide a baseline to name early life stages for any set of species. The present method performs a phylogenetic segmentation of ontogenetic time, which can be correctly seen as depicting ontophylogenesis.

The treeness of the tree of historical trees of life.

This paper compares and categorizes historical ideas about trees showing relationships among biological entities. The hierarchical structure of a tree is used to test the global consistency of similarities among these ideas; in other words we assess the "treeness" of the tree of historical trees. The collected data are figures and ideas about trees showing relationships among biological entities published or drawn by naturalists from 1555 to 2012. They are coded into a matrix of 235 historical trees and 141 descriptive attributes. From the most parsimonious "tree" of historical trees, treeness is measured by consistency index, retention index and homoplasy excess ratio. This tree is used to create sets or categories of trees, or to study the circulation of ideas. From an unrooted network of historical trees, treeness is measured by the delta-score. This unrooted network is used to measure and visualize treeness. The two approaches show a rather good treeness of the data, with respectively a retention idex of 0.83 and homoplasy excess ratio of 0.74, on one hand, and a delta-score of 0.26 on the other hand. It is interpreted as due to vertical transmission, i.e. an inheritance of shared ideas about biological trees among authors. This tree of trees is then used to test categories previously made. For instance, cladists and gradists are « paraphyletic ¼. The branches of this tree of trees suggest new categories of tree-thinkers that could have been overlooked by historians or systematists.

LIMES: a tool for comparing species partition.

MOTIVATION: Species delimitation (SD) is on the verge of becoming a fully fledged research field in systematics, but the variety of available approaches tends to result in significant-sometimes striking-incongruences, when tested comparatively with a given taxonomic sampling. RESULTS: We present LIMES, an automatic calculation tool which qualitatively compares species partitions obtained by distinct SD approaches, regardless of their respective theoretical backgrounds, and even in absence of reference topology. The program implements four different previously published indexes, and allows their automated calculation. AVAILABILITY AND IMPLEMENTATION: LIMES is freely downloadable at www.limes.cnrs.fr. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Empathy and compassion toward other species decrease with evolutionary divergence time.

Currently the planet is inhabited by several millions of extremely diversified species. Not all of them arouse emotions of the same nature or intensity in humans. Little is known about the extent of our affective responses toward them and the factors that may explain these differences. Our online survey involved 3500 raters who had to make choices depending on specific questions designed to either assess their empathic perceptions or their compassionate reactions toward an extended photographic sampling of organisms. Results show a strong negative correlation between empathy scores and the divergence time separating them from us. However, beyond a certain time of divergence, our empathic perceptions stabilize at a minimum level. Compassion scores, although based on less spontaneous choices, remain strongly correlated to empathy scores and time of divergence. The mosaic of features characterizing humans has been acquired gradually over the course of the evolution, and the phylogenetically closer a species is to us, the more it shares common traits with us. Our results could be explained by the fact that many of these traits may arouse sensory biases. These anthropomorphic signals could be able to mobilize cognitive circuitry and to trigger prosocial behaviors usually at work in human relationships.

Understanding processes at the origin of species flocks with a focus on the marine Antarctic fauna.

Species flocks (SFs) fascinate evolutionary biologists who wonder whether such striking diversification can be driven by normal evolutionary processes. Multiple definitions of SFs have hindered the study of their origins. Previous studies identified a monophyletic taxon as a SF if it displays high speciosity in an area in which it is endemic (criterion 1), high ecological diversity among species (criterion 2), and if it dominates the habitat in terms of biomass (criterion 3); we used these criteria in our analyses. Our starting hypothesis is that normal evolutionary processes may provide a sufficient explanation for most SFs. We thus clearly separate each criterion and identify which biological (intrinsic) and environmental (extrinsic) traits are most favourable to their realization. The first part focuses on evolutionary processes. We highlight that some popular putative causes of SFs, such as key innovations or ecological speciation, are neither necessary nor sufficient to fulfill some or all of the three criteria. Initial differentiation mechanisms are diverse and difficult to identify a posteriori because a primary differentiation of one type (genetic, ecological or geographical) often promotes other types of differentiation. Furthermore, the criteria are not independent: positive feedbacks between speciosity and ecological diversity among species are expected whatever the initial cause of differentiation, and ecological diversity should enhance habitat dominance at the clade level. We then identify intrinsic and extrinsic factors that favour each criterion. Low dispersal emerges as a convincing driver of speciosity. Except for a genomic architecture favouring ecological speciation, for which assessment is difficult, high effective population sizes are the single intrinsic factor that directly enhances speciosity, ecological diversity and habitat dominance. No extrinsic factor appeared to enhance all criteria simultaneously but a combination of factors (insularity, fragmentation and environmental stability) may favour the three criteria, although the effect is indirect for habitat dominance. We then apply this analytical framework to Antarctic marine environments by analysing data from 18 speciose clades belonging to echinoderms (five unrelated clades), notothenioid fishes (five clades) and peracarid crustaceans (eight clades). Antarctic shelf environments and history appear favourable to endemicity and speciosity, but not to ecological specialization. Two main patterns are distinguished among taxa. (i) In echinoderms, many brooding, species-rich and endemic clades are reported, but without remarkable ecological diversity or habitat dominance. In these taxa, loss of the larval stage is probably a consequence of past Antarctic environmental factors, and brooding is suggested to be responsible for enhanced allopatric speciation (via dispersal limitation). (ii) In notothenioids and peracarids, many clades fulfill all three SF criteria. This could result from unusual features in fish and crustaceans: chromosome instability and key innovations (antifreeze proteins) in notothenioids, ecological opportunity in peracarids, and a genomic architecture favouring ecological speciation in both groups. Therefore, the data do not support our starting point that normal evolutionary factors or processes drive SFs because in these two groups uncommon intrinsic features or ecological opportunity provide the best explanation. The utility of the three-criterion SF concept is therefore questioned and guidelines are given for future studies.

Phylogenetic classification of bony fishes.

BACKGROUND: Fish classifications, as those of most other taxonomic groups, are being transformed drastically as new molecular phylogenies provide support for natural groups that were unanticipated by previous studies. A brief review of the main criteria used by ichthyologists to define their classifications during the last 50 years, however, reveals slow progress towards using an explicit phylogenetic framework. Instead, the trend has been to rely, in varying degrees, on deep-rooted anatomical concepts and authority, often mixing taxa with explicit phylogenetic support with arbitrary groupings. Two leading sources in ichthyology frequently used for fish classifications (JS Nelson's volumes of Fishes of the World and W. Eschmeyer's Catalog of Fishes) fail to adopt a global phylogenetic framework despite much recent progress made towards the resolution of the fish Tree of Life. The first explicit phylogenetic classification of bony fishes was published in 2013, based on a comprehensive molecular phylogeny ( www.deepfin.org ). We here update the first version of that classification by incorporating the most recent phylogenetic results. RESULTS: The updated classification presented here is based on phylogenies inferred using molecular and genomic data for nearly 2000 fishes. A total of 72 orders (and 79 suborders) are recognized in this version, compared with 66 orders in version 1. The phylogeny resolves placement of 410 families, or ~80% of the total of 514 families of bony fishes currently recognized. The ordinal status of 30 percomorph families included in this study, however, remains uncertain (incertae sedis in the series Carangaria, Ovalentaria, or Eupercaria). Comments to support taxonomic decisions and comparisons with conflicting taxonomic groups proposed by others are presented. We also highlight cases were morphological support exist for the groups being classified. CONCLUSIONS: This version of the phylogenetic classification of bony fishes is substantially improved, providing resolution for more taxa than previous versions, based on more densely sampled phylogenetic trees. The classification presented in this study represents, unlike any other, the most up-to-date hypothesis of the Tree of Life of fishes.

Origin of an ancient hormone/receptor couple revealed by resurrection of an ancestral estrogen.

The origin of ancient ligand/receptor couples is often analyzed via reconstruction of ancient receptors and, when ligands are products of metabolic pathways, they are not supposed to evolve. However, because metabolic pathways are inherited by descent with modification, their structure can be compared using cladistic analysis. Using this approach, we studied the evolution of steroid hormones. We show that side-chain cleavage is common to most vertebrate steroids, whereas aromatization was co-opted for estrogen synthesis from a more ancient pathway. The ancestral products of aromatic activity were aromatized steroids with a side chain, which we named "paraestrols." We synthesized paraestrol A and show that it effectively binds and activates the ancestral steroid receptor. Our study opens the way to comparative studies of biologically active small molecules.

The Evolution of Musical Diversity: The Key Role of Vertical Transmission.

Music, like languages, is one of the key components of our culture, yet musical evolution is still poorly known. Numerous studies using computational methods derived from evolutionary biology have been successfully applied to varied subset of linguistic data. One of the major drawback regarding musical studies is the lack of suitable coded musical data that can be analysed using such evolutionary tools. Here we present for the first time an original set of musical data coded in a way that enables construction of trees classically used in evolutionary approaches. Using phylogenetic methods, we test two competing theories on musical evolution: vertical versus horizontal transmission. We show that, contrary to what is currently believed, vertical transmission plays a key role in shaping musical diversity. The signal of vertical transmission is particularly strong for intrinsic musical characters such as metrics, rhythm, and melody. Our findings reveal some of the evolutionary mechanisms at play for explaining musical diversity and open a new field of investigation in musical evolution.

Finding our way through phenotypes.

Despite a large and multifaceted effort to understand the vast landscape of phenotypic data, their current form inhibits productive data analysis. The lack of a community-wide, consensus-based, human- and machine-interpretable language for describing phenotypes and their genomic and environmental contexts is perhaps the most pressing scientific bottleneck to integration across many key fields in biology, including genomics, systems biology, development, medicine, evolution, ecology, and systematics. Here we survey the current phenomics landscape, including data resources and handling, and the progress that has been made to accurately capture relevant data descriptions for phenotypes. We present an example of the kind of integration across domains that computable phenotypes would enable, and we call upon the broader biology community, publishers, and relevant funding agencies to support efforts to surmount today's data barriers and facilitate analytical reproducibility.

The gas bladder of puffers and porcupinefishes (Acanthomorpha: Tetraodontiformes): phylogenetic interpretations.

The anatomy of the gas bladder of Diodontidae (porcupinefishes) and Tetraodontidae (pufferfishes) was studied on the basis of dissections and magnetic resonance imaging. Among the examined taxa of Tetraodontiformes, only puffers and porcupinefishes possess a thick walled and dorsally U-shaped or crescent-moon-shaped gas bladder. In the tetraodontid genus Lagocephalus the gas bladder is reduced to a rudiment. The species belonging to the genera Canthigaster, Arothron, and some species of Tetraodon differ in the positioning of their crescent-moon-shaped gas bladder. These observations confirm the close relationship of: (i) Diodontidae and Tetraodontidae and (ii) Canthigaster, Arothron, and some species of Tetraodon. The heterogeneity of the genus Tetraodon is supported by the gas bladder morphology, as previously suggested by molecular studies.

Is the species flock concept operational? The Antarctic shelf case.

There has been a significant body of literature on species flock definition but not so much about practical means to appraise them. We here apply the five criteria of Eastman and McCune for detecting species flocks in four taxonomic components of the benthic fauna of the Antarctic shelf: teleost fishes, crinoids (feather stars), echinoids (sea urchins) and crustacean arthropods. Practical limitations led us to prioritize the three historical criteria (endemicity, monophyly, species richness) over the two ecological ones (ecological diversity and habitat dominance). We propose a new protocol which includes an iterative fine-tuning of the monophyly and endemicity criteria in order to discover unsuspected flocks. As a result nine « full ¼ species flocks (fulfilling the five criteria) are briefly described. Eight other flocks fit the three historical criteria but need to be further investigated from the ecological point of view (here called "core flocks"). The approach also shows that some candidate taxonomic components are no species flocks at all. The present study contradicts the paradigm that marine species flocks are rare. The hypothesis according to which the Antarctic shelf acts as a species flocks generator is supported, and the approach indicates paths for further ecological studies and may serve as a starting point to investigate the processes leading to flock-like patterning of biodiversity.

Categorizing ideas about trees: a tree of trees.

The aim of this study is to explore whether matrices and MP trees used to produce systematic categories of organisms could be useful to produce categories of ideas in history of science. We study the history of the use of trees in systematics to represent the diversity of life from 1766 to 1991. We apply to those ideas a method inspired from coding homologous parts of organisms. We discretize conceptual parts of ideas, writings and drawings about trees contained in 41 main writings; we detect shared parts among authors and code them into a 91-characters matrix and use a tree representation to show who shares what with whom. In other words, we propose a hierarchical representation of the shared ideas about trees among authors: this produces a "tree of trees." Then, we categorize schools of tree-representations. Classical schools like "cladists" and "pheneticists" are recovered but others are not: "gradists" are separated into two blocks, one of them being called here "grade theoreticians." We propose new interesting categories like the "buffonian school," the "metaphoricians," and those using "strictly genealogical classifications." We consider that networks are not useful to represent shared ideas at the present step of the study. A cladogram is made for showing who is sharing what with whom, but also heterobathmy and homoplasy of characters. The present cladogram is not modelling processes of transmission of ideas about trees, and here it is mostly used to test for proximity of ideas of the same age and for categorization.

Conveniently pre-tagged and pre-packaged: extended molecular identification and metagenomics using complete metazoan mitochondrial genomes.

BACKGROUND: Researchers sorely need markers and approaches for biodiversity exploration (both specimen linked and metagenomics) using the full potential of next generation sequencing technologies (NGST). Currently, most studies rely on expensive multiple tagging, PCR primer universality and/or the use of few markers, sometimes with insufficient variability. METHODOLOGY/PRINCIPAL FINDINGS: We propose a novel approach for the isolation and sequencing of a universal, useful and popular marker across distant, non-model metazoans: the complete mitochondrial genome. It relies on the properties of metazoan mitogenomes for enrichment, on careful choice of the organisms to multiplex, as well as on the wide collection of accumulated mitochondrial reference datasets for post-sequencing sorting and identification instead of individual tagging. Multiple divergent organisms can be sequenced simultaneously, and their complete mitogenome obtained at a very low cost. We provide in silico testing of dataset assembly for a selected set of example datasets. CONCLUSIONS/SIGNIFICANCE: This approach generates large mitogenome datasets. These sequences are useful for phylogenetics, molecular identification and molecular ecology studies, and are compatible with all existing projects or available datasets based on mitochondrial sequences, such as the Barcode of Life project. Our method can yield sequences both from identified samples and metagenomic samples. The use of the same datasets for both kinds of studies makes for a powerful approach, especially since the datasets have a high variability even at species level, and would be a useful complement to the less variable 18S rDNA currently prevailing in metagenomic studies.

Visceral anatomy of ocean sunfish (Mola mola (L., 1758), Molidae, Tetraodontiformes) and angler (Lophius piscatorius (L., 1758), Lophiidae, Lophiiformes) investigated by non-invasive imaging techniques.

The purpose of this work is to examine the gross visceral anatomy of ocean sunfish and angler using non-invasive imaging techniques: computed tomography imaging (CT) and magnetic resonance imaging (MRI). Similarities and differences in the internal organisation of these two species are verified. Both species lack a swimbladder and present a significant asymmetry in the hepatic lobes, an elongated bile duct terminating close to the stomach, a compact thyroid embedded in a blood lacuna, and very reduced brain and spinal cord. These observations are important in regard to the close relationships between Tetraodontiformes and Lophiiformes, established by several molecular works, but not yet confirmed by morpho-anatomical data. However the occurrence of these features has to be examined in other taxa before phylogenetic hypotheses are proposed.

Origins of specificity and promiscuity in metabolic networks.

How enzymes have evolved to their present form is linked to the question of how pathways emerged and evolved into extant metabolic networks. To investigate this mechanism, we have explored the chemical diversity present in a largely unbiased data set of catalytic reactions processed by modern enzymes across the tree of life. In order to get a quantitative estimate of enzyme chemical diversity, we measure enzyme multispecificity or promiscuity using the reaction molecular signatures. Our main finding is that reactions that are catalyzed by a highly specific enzyme are shared by poorly divergent species, suggesting a later emergence of this function during evolution. In contrast, reactions that are catalyzed by highly promiscuous enzymes are more likely to appear uniformly distributed across species in the tree of life. From a functional point of view, promiscuous enzymes are mainly involved in amino acid and lipid metabolisms, which might be associated with the earliest form of biochemical reactions. In this way, results presented in this paper might assist us with the identification of primeval promiscuous catalytic functions contributing to life's minimal metabolism.