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Bilateria encompass the vast majority of the animal phyla. As the name states, they are bilaterally symmetric, that is with a morphologically clear main body axis connecting their anterior and posterior ends, a second axis running between their dorsal and ventral surfaces, and with a left side being roughly a mirror image of their right side. Bone morphogenetic protein (BMP) signalling has widely conserved functions in the formation and patterning of the second, dorso-ventral (DV) body axis, albeit to different extents in different bilaterian species. Whilst initial findings in the fruit fly Drosophila and the frog Xenopus highlighted similarities amongst these evolutionarily very distant species, more recent analyses featuring other models revealed considerable diversity in the mechanisms underlying dorsoventral patterning. In fact, as phylogenetic sampling becomes broader, we find that this axis patterning system is so evolvable that even its core components can be deployed differently or lost in different model organisms. In this review, we will try to highlight the diversity of ways by which BMP signalling controls bilaterality in different animals, some of which do not belong to Bilateria. Future research combining functional analyses and modelling is bound to give us some understanding as to where the limits to the extent of the evolvability of BMP-dependent axial patterning may lie. [ABSTRACT FROM AUTHOR]

The end‐Neoproterozoic transition marked a gradual but permanent shift between distinct configurations of Earth's biosphere. This interval witnessed the demise of the enigmatic Ediacaran Biota, ushering in the structured trophic webs and disparate animal body plans of Phanerozoic ecosystems. However, little consensus exists on the reality, drivers, and macroevolutionary implications of end‐Neoproterozoic extinctions. Here we evaluate potential drivers of late‐Neoproterozoic turnover by addressing recent findings on Ediacaran geochronology, the persistence of classical Ediacaran macrobionts into the Cambrian, and the existence of Ediacaran crown‐group eumetazoans. Despite renewed interest in the possibility of Phanerozoic‐style 'mass extinctions' in the latest Neoproterozoic, our synthesis of the available evidence does not support extinction models based on episodic geochemical triggers, nor does it validate simple ecological interpretations centred on direct competitive displacement. Instead, we argue that the protracted and indirect effects of early bilaterian innovations, including escalations in sediment engineering, predation, and the largely understudied impacts of reef‐building, may best account for the temporal structure and possible selectivity of late‐Neoproterozoic extinctions. We integrate these processes into a generalised model of early eumetazoan‐dominated ecologies, charting the disruption of spatial and temporal isotropy on the Ediacaran benthos as a consequence of diversifying macrofaunal interactions. Given the nature of resource distribution in Ediacaran ecologies, the continuities among Ediacaran and Cambrian faunas, and the convergent origins of ecologically disruptive innovations among bilaterians we suggest that the rise of Phanerozoic‐type biotas may have been unstoppable. [ABSTRACT FROM AUTHOR]

A branching body pattern with one head and many "tails", unique for recent Bilateria, was found in three species of endosymbiotic polychaetes of the family Syllidae (McIntosh, 1879; Glasby et al., 2012; Aguado et al., 2015, 2022). Among recent echinoderms, many species of crinoids, brittle stars, and holothurians have dendriform branching bodies with many distal, posterior ends of their arms, rays, and tentacles, which include the typical axial ambulacral complex. Multiple bifurcations of the posterior (distal) parts create fractal branching of the body pattern, representing a macroevolutionary transformation of the ancestral body plan in Bilateria. [ABSTRACT FROM AUTHOR]

Neurons underpin cognition in animals. However, the roots of animal cognition are elusive from both mechanistic and evolutionary standpoints. Two conceptual frameworks both highlight and promise to address these challenges. First, we discuss evidence that animal neural and other integrative systems evolved more than once (convergent evolution) within basal metazoan lineages, giving us unique experiments by Nature for future studies. The most remarkable examples are neural systems in ctenophores and neuroid-like systems in placozoans and sponges. Second, in addition to classical synaptic wiring, a chemical connectome mediated by hundreds of signal molecules operates in tandem with neurons and is the most information-rich source of emerging properties and adaptability. The major gap—dynamic, multifunctional chemical micro-environments in nervous systems—is not understood well. Thus, novel tools and information are needed to establish mechanistic links between orchestrated, yet cell-specific, volume transmission and behaviors. Uniting what we call chemoconnectomics and analyses of the cellular bases of behavior in basal metazoan lineages arguably would form the foundation for deciphering the origins and early evolution of elementary cognition and intelligence. [ABSTRACT FROM AUTHOR]

Bilateria exhibit whole-body handedness in internal structure. This left–right polarity is evolutionarily conserved with virtually no reversed extant lineage, except in molluscan Gastropoda. Phylogenetically independent snail groups contain both clockwise-coiled (dextral) and counterclockwise-coiled (sinistral) taxa that are reversed from each other in bilateral handedness as well as in coiling direction. Within freshwater Hygrophila, Lymnaea with derived dextrality have diaphanous related formin (diaph) gene duplicates, while basal sinistral groups possess one diaph gene. In terrestrial Stylommatophora, dextral Bradybaena also have diaph duplicates. Defective maternal expression of one of those duplicates gives rise to sinistral hatchlings in Lymnaea and handedness-mixed broods in Bradybaena, through polarity change in spiral cleavage of embryos. These findings led to the hypothesis that diaph duplication was crucial for the evolution of dextrality by reversal. The present study discovered that diaph duplication independently occurred four times and its duplicate became lost twice in gastropods. The dextrality of Bradybaena represents the ancestral handedness conserved across gastropods, unlike the derived dextrality of Lymnaea. Sinistral lineages recurrently evolved by reversal regardless of whether diaph had been duplicated. Amongst the seven formin gene subfamilies, diaph has most thoroughly been conserved across eukaryotes of the 14 metazoan phyla and choanoflagellate. Severe embryonic mortalities resulting from insufficient expression of the duplicate in both of Bradybaena and Lymnaea also support that diaph duplicates bare general roles for cytoskeletal dynamics other than controlling spiralian handedness. Our study rules out the possibility that diaph duplication or loss played a primary role for reversal evolution. [ABSTRACT FROM AUTHOR]

BMP signaling has a conserved function in patterning the dorsal-ventral body axis in Bilateria and the directive axis in anthozoan cnidarians. So far, cnidarian studies have focused on the role of different BMP signaling network components in regulating pSMAD1/5 gradient formation. Much less is known about the target genes downstream of BMP signaling. To address this, we generated a genome-wide list of direct pSMAD1/5 target genes in the anthozoan Nematostella vectensis, several of which were conserved in Drosophila and Xenopus. Our ChIP-seq analysis revealed that many of the regulatory molecules with documented bilaterally symmetric expression in Nematostella are directly controlled by BMP signaling. We identified several so far uncharacterized BMP-dependent transcription factors and signaling molecules, whose bilaterally symmetric expression may be indicative of their involvement in secondary axis patterning. One of these molecules is zswim4-6, which encodes a novel nuclear protein that can modulate the pSMAD1/5 gradient and potentially promote BMP-dependent gene repression.

Materials collected on the territory of the southeastern White Sea area, including diversely preserved body imprints, combined body-trace fossils, specimens with signs of intravital damage and regeneration, and extended ontogenetic series, make it possible to significantly widen the data on the body plan and biology of Dickinsonia , the oldest known mobile animal, included in the Late Precambrian taxon of high rank, Proarticulata. A number of reconstructed anatomical features were added to the obvious directly observed features of Dickinsonia , such as a consistent body shape lacking lateral appendages and temporary outgrowths, transverse differentiation, and anterior–posterior polarity. These reconstructed features include dorsoventral polarity, ciliated mucus-secreting epithelium underlain by a basal lamina, two rows of blind food-gathering pockets, absence of a through-gut, nervous system of diffusive type, axial support band and muscle fibres. Such a set of features indicates the affinity of Dickinsonia and Proarticulata as a whole (the only known Ediacaran Metazoa) to Urbilateria, a hypothetical ancestor of bilaterally symmetrical animals. [ABSTRACT FROM AUTHOR]

Paleontological data on the appearance and development of metazoan axial symmetry are compared with molecular genetic evidence to determine the axial body plan and growth vectors of bilaterian organisms by the coordinated functioning cascades of signaling pathways Wnt, BMP, Nodal, Hedgehog, and regulatory Hox and ParaHox gene clusters. The axial body symmetry in most bilaterians is associated with the uniaxial growth vector. Posterior body growth ensured by the progenitor stem cell pool of the growth zone localized at the preterminal end of the body became a cardinal evolutionary innovation in Bilateria. The conservatism of ancestral molecular mechanisms of bilaterian body plan specification is combined with their flexibility, which provided the possibility of evolutionary transformations of the axial pattern of the organism. Radical evolutionary changes with the formation of additional growth zones are reported in the representatives of Deuterostomia (Vertebrata and Echinodermata). In modern vertebrates, while the main ancestral axis of body growth is preserved, two pairs of additional growth zones (limb buds) emerged. They are considered paramorphic homologs (replicates) of the posterior part of the main body axis. The pentamerous pattern of the body plan and growth of recent echinoderms can be explained as a result of the multiplication of the ancestral organizing center of axial architectonics and its radialization during larval metamorphosis (or in early embryogenesis during lecithotrophic development) with a corresponding multiplication of growth zones localized at the ends of rays (ambulacra). It is consistent with paleontological data and the concept of echinoderm rays as paramorphic homologs of the main body axis of the bilaterian ancestors of echinoderms. [ABSTRACT FROM AUTHOR]

The Hox gene cluster, responsible for patterning of the head–tail axis, is an ancestral feature of all bilaterally symmetrical animals (the Bilateria) that remains intact in a wide range of species. We can say that the Hox cluster evolved successfully only once since it is commonly the same in all groups, with labial-like genes at one end of the cluster expressed in the anterior embryo, and Abd-B-like genes at the other end of the cluster expressed posteriorly. This review attempts to make sense of the Hox gene cluster and to address the following questions. How did the Hox cluster form in the protostome-deuterostome last common ancestor, and why was this with a particular head–tail polarity? Why is gene clustering usually maintained? Why is there collinearity between the order of genes along the cluster and the positions of their expressions along the embryo? Why do the Hox gene expression domains overlap along the embryo? Why have vertebrates duplicated the Hox cluster? Why do Hox gene knockouts typically result in anterior homeotic transformations? How do animals adapt their Hox clusters to evolve new structural patterns along the head–tail axis? [ABSTRACT FROM AUTHOR]

Animal species present relatively high levels of gene conservation, and yet they display a great variety of cell type and tissue phenotypes. These diverse phenotypes are mainly specified through differential gene usage, which relies on several mechanisms. Two of the most relevant mechanisms are regulated gene transcription, usually referred to as gene expression (rGE), and regulated alternative splicing (rAS). Several works have addressed how either rGE or rAS contributes to phenotypic diversity throughout evolution, but a back-to-back comparison between the two molecular mechanisms, specifically highlighting both their common regulatory principles and unique properties, is still missing. In this review, we propose an innovative framework for the unified comparison between rGE and rAS from different perspectives: the three-dimensional (3D)-evo space. We use the 3D-evo space to comprehensively (a) review the molecular basis of rGE and rAS (i.e., the molecular axis), (b) depict the tissue-specific phenotypes they contribute to (i.e., the tissue axis), and (c) describe the determinants that drive the evolution of rGE and rAS programs (i.e., the evolution axis). Finally, we unify the perspectives emerging from the three axes by discussing general trends and specific examples of rGE and rAS tissue program evolution. [ABSTRACT FROM AUTHOR]

The organization of genomes into chromosomes is critical for processes such as genetic recombination, environmental adaptation, and speciation. All animals with bilateral symmetry inherited a genome structure from their last common ancestor that has been highly conserved in some taxa but seemingly unconstrained in others. However, the evolutionary forces driving these differences and the processes by which they emerge have remained largely uncharacterized. Here, we analyze genome organization across the phylum Annelida using 23 chromosome-level annelid genomes. We find that while many annelid lineages have maintained the conserved bilaterian genome structure, the Clitellata, a group containing leeches and earthworms, possesses completely scrambled genomes. We develop a rearrangement index to quantify the extent of genome structure evolution and show that, compared to the last common ancestor of bilaterians, leeches and earthworms have among the most highly rearranged genomes of any currently sampled species. We further show that bilaterian genomes can be classified into two distinct categories-high and low rearrangement-largely influenced by the presence or absence, respectively, of chromosome fission events. Our findings demonstrate that animal genome structure can be highly variable within a phylum and reveal that genome rearrangement can occur both in a gradual, stepwise fashion, or rapid, all-encompassing changes over short evolutionary timescales., (© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)

Sequencing of genomes of unicellular eukaryotes Holozoa (Monosiga brevicollis, Capsaspora owczarzaki), basal multicellular Porifera and Cnidaria, and Bilateria showed that the gene repertoire and gene regulatory networks that play a key role in the evolution of multicellular animals, in particular, in the formation of the mesoderm, have an earlier origin than was expected. The appearance of Cnidaria and Bilateria occurred before the Cambrian explosion when an unprecedented number of new forms of organisms evolved. It is assumed that the molecular genetic basis of the Cambrian explosion was preceded by Hox genes, which provided a fundamental complication of the genetic developmental programs of Bilateria (Erwin and Davidson, 2002; Davidson, 2006; Carroll, 2008; Holland, 2015). [ABSTRACT FROM AUTHOR]

During the Late Neoproterozoic and Early Cambrian, a series of paleogeographic and paleoecological events occurred associated with deglaciations and the evolution of life. The appearance of fossils representing diverse phyla, novel body plans and complex ecologies in Ediacaran and Cambrian sedimentary successions has sparked diverse hypotheses about potential drivers for the radiation of early animals during this interval. Recently, new macroscopic fossils of carbonaceous compressions with unique features have been found in Anning, Yunnan, China. The fossils’ bodies are ribbon-shaped and bilaterally symmetric, with dense longitudinal features and transversal features. The fossils occur 0.68 m below a bentonite interlayer which has been dated 535.2 ± 1.7 Ma by Ri-xiang Zhu and his team in 2009. The relatively simply morphology of these fossils, coupled with a lack of preserved internal structures challenge efforts taxonomically identify the precursor organism and definitively ally it to a living group. However, the symmetry and unusual features of the body are analogous to members of Platyzoa. The presence of ribbon-shaped fossils in the Zhongyicun Member in Anning indicates that these organisms were at least a locally significant component of Cambrian seafloor ecosystems, and may hold important implications for our understanding of the early evolution of Bilateria.

Peptides and protein hormones form the largest group of secreted signals that mediate intercellular communication and are central regulators of physiology and behavior in all animals. Phylogenetic analyses and biochemical identifications of peptide-receptor systems reveal a broad evolutionary conservation of these signaling systems at the molecular level. Substantial progress has been made in recent years on characterizing the physiological and putative ancestral roles of many peptide systems through comparative studies in invertebrate models. Several peptides and protein hormones are not only molecularly conserved but also have conserved roles across animal phyla. Here, we focus on functional insights gained in the nematode Caenorhabditis elegans that, with its compact and well-described nervous system, provides a powerful model to dissect neuroendocrine signaling networks involved in the control of physiology and behavior. We summarize recent discoveries on the evolutionary conservation and knowledge on the functions of peptide and protein hormone systems in C. elegans. [ABSTRACT FROM AUTHOR]

Most organisms possess time-keeping devices called circadian clocks. At the molecular level, circadian clocks consist of transcription–translation feedback loops (TTFLs). Although some components of the negative TTFL are conserved across the animals, important differences exist between typical models, such as mouse and the fruit fly. In Drosophila , the key components are PERIOD (PER) and TIMELESS (TIM-d) proteins, whereas the mammalian clock relies on PER and CRYPTOCHROME (CRY-m). Importantly, how the clock has maintained functionality during evolutionary transitions between different states remains elusive. Therefore, we systematically described the circadian clock gene setup in major bilaterian lineages and identified marked lineage-specific differences in their clock constitution. Then we performed a thorough functional analysis of the linden bug Pyrrhocoris apterus , an insect species comprising features characteristic of both the Drosophila and the mammalian clocks. Unexpectedly, the knockout of timeless-d , a gene essential for the clock ticking in Drosophila , did not compromise rhythmicity in P. apterus , it only accelerated its pace. Furthermore, silencing timeless-m , the ancestral timeless type ubiquitously present across animals, resulted in a mild gradual loss of rhythmicity, supporting its possible participation in the linden bug clock, which is consistent with timeless-m role suggested by research on mammalian models. The dispensability of timeless-d in P. apterus allows drawing a scenario in which the clock has remained functional at each step of transition from an ancestral state to the TIM-d-independent PER + CRY-m system operating in extant vertebrates, including humans. [ABSTRACT FROM AUTHOR]

Here we present a detailed accounting of organic microfossils from late Ediacaran sediments of Finland, from the island of Hailuoto (northwest Finnish coast), and the Saarijärvi meteorite impact structure (~170 km northeast of Hailuoto, mainland Finland). Fossils were recovered from fine-grained thermally immature mudstones and siltstones and are preserved in exquisite detail. The majority of recovered forms are sourced from filamentous prokaryotic and protistan-grade organisms forming interwoven microbial mats. Flattened Nostoc-ball-like masses of bundled Siphonophycus filaments are abundant, alongside Rugosoopsis and Palaeolyngbya of probable cyanobacterial origin. Acritarchs include Chuaria, Leiosphaeridia, Symplassosphaeridium and Synsphaeridium. Significantly, rare spine-shaped sclerites of bilaterian origin were recovered, providing new evidence for a nascent bilaterian fauna in the terminal Ediacaran. These findings offer a direct body-fossil insight into Ediacaran mat-forming microbial communities, and demonstrate that alongside trace fossils, detection of a bilaterian fauna prior to the Cambrian might also be sought among the emerging record of small carbonaceous fossils (SCFs). [ABSTRACT FROM AUTHOR]

The Cambrian Explosion by nature is a three-phased explosion of animal body plans alongside episodic biomineralization, pulsed change of generic diversity, body size variation, and progressive increase of ecosystem complexity. The Cambrian was a time of crown groups nested by numbers of stem groups with a high-rank taxonomy of Linnaean system (classes and above). Some stem groups temporarily succeeded while others were ephemeral and underrepresented by few taxa. The high number of stem groups in the early history of animals is a major reason for morphological gaps across phyla that we see today. Most phylum-level clades achieved their maximal disparity (or morphological breadth) during the time interval close to their first appearance in the fossil record during the early Cambrian, whereas others, principally arthropods and chordates, exhibit a progressive exploration of morphospace in subsequent Phanerozoic. The overall envelope of metazoan morphospace occupation was already broad in the early Cambrian though it did not reach maximal disparity nor has diminished significantly as a consequence of extinction since the Cambrian. Intrinsic and extrinsic causes were extensively discussed but they are merely prerequisites for the Cambrian Explosion. Without the molecular evolution, there could be no Cambrian Explosion. However, the developmental system is alone insufficient to explain Cambrian Explosion. Time-equivalent environmental changes were often considered as extrinsic causes, but the time coincidence is also insufficient to establish causality. Like any other evolutionary event, it is the ecology that make the Cambrian Explosion possible though ecological processes failed to cause a burst of new body plans in the subsequent evolutionary radiations. The Cambrian Explosion is a polythetic event in natural history and manifested in many aspects. No simple, single cause can explain the entire phenomenon. [ABSTRACT FROM AUTHOR]

The subfamily GH13_1 of alpha-amylases is typical of Fungi, but it is also found in some unicellular eukaryotes (e.g., Amoebozoa, choanoflagellates) and non-bilaterian Metazoa. Since a previous study in 2007, GH13_1 amylases were considered ancestral to the Unikonts, including animals, except Bilateria, such that it was thought to have been lost in the ancestor of this clade. The only alpha-amylases known to be present in Bilateria so far belong to the GH13_15 and 24 subfamilies (commonly called bilaterian alpha-amylases) and were likely acquired by horizontal transfer from a proteobacterium. The taxonomic scope of Eukaryota genomes in databases has been greatly increased ever since 2007. We have surveyed GH13_1 sequences in recent data from ca. 1600 bilaterian species, 60 non-bilaterian animals and also in unicellular eukaryotes. As expected, we found a number of those sequences in non-bilaterians: Anthozoa (Cnidaria) and in sponges, confirming the previous observations, but none in jellyfishes and in Ctenophora. Our main and unexpected finding is that such fungal (also called Dictyo-type) amylases were also consistently retrieved in several bilaterian phyla: hemichordates (deuterostomes), brachiopods and related phyla, some molluscs and some annelids (protostomes). We discuss evolutionary hypotheses possibly explaining the scattered distribution of GH13_1 across bilaterians, namely, the retention of the ancestral gene in those phyla only and/or horizontal transfers from non-bilaterian donors.

The Hox gene cluster, responsible for patterning of the head–tail axis, is an ancestral feature of all bilaterally symmetrical animals (the Bilateria) that remains intact in a wide range of species. We can say that the Hox cluster evolved successfully only once since it is commonly the same in all groups, with labial-like genes at one end of the cluster expressed in the anterior embryo, and Abd-B-like genes at the other end of the cluster expressed posteriorly. This review attempts to make sense of the Hox gene cluster and to address the following questions. How did the Hox cluster form in the protostome-deuterostome last common ancestor, and why was this with a particular head–tail polarity? Why is gene clustering usually maintained? Why is there collinearity between the order of genes along the cluster and the positions of their expressions along the embryo? Why do the Hox gene expression domains overlap along the embryo? Why have vertebrates duplicated the Hox cluster? Why do Hox gene knockouts typically result in anterior homeotic transformations? How do animals adapt their Hox clusters to evolve new structural patterns along the head–tail axis?

The Sox family of transcription factors regulates many processes during metazoan development, including stem cell maintenance and nervous system specification. Characterizing the repertoires and roles of these genes can therefore provide important insights into animal evolution and development. We further characterized the Sox repertoires of several arachnid species with and without an ancestral whole-genome duplication and compared their expression between the spider Parasteatoda tepidariorum and the harvestman Phalangium opilio. We found that most Sox families have been retained as ohnologs after whole-genome duplication and evidence for potential subfunctionalization and/or neofunctionalization events. Our results also suggest that Sox21b-1 likely regulated segmentation ancestrally in arachnids, playing a similar role to the closely related SoxB gene, Dichaete , in insects. We previously showed that Sox21b-1 is required for the simultaneous formation of prosomal segments and sequential addition of opisthosomal segments in P. tepidariorum. We studied the expression and function of Sox21b-1 further in this spider and found that although this gene regulates the generation of both prosomal and opisthosomal segments, it plays different roles in the formation of these tagmata reflecting their contrasting modes of segmentation and deployment of gene regulatory networks with different architectures. [ABSTRACT FROM AUTHOR]

• Mitochondrial genomes exhibit a large variability in architecture and content. • HERMES quantifies the amount of molecular change among mitochondrial genomes. • We present the improved version of HERMES, as well as an updated software. • Ten case studies are evaluated with the HERMES approach in the present paper. • HERMES provides original insights and uncovers patterns of molecular evolution. Mitochondrial chromosomes have diversified among eukaryotes and many different architectures and features are now acknowledged for this genome. Here we present the improved HERMES index, which can measure and quantify the amount of molecular change experienced by mitochondrial genomes. We test the improved approach with ten molecular phylogenetic studies based on complete mitochondrial genomes, representing six bilaterian Phyla. In most cases, HERMES analysis spotted out clades or single species with peculiar molecular synapomorphies, allowing to identify phylogenetic and ecological patterns. The software presented herein handles linear, circular, and multi-chromosome genomes, thus widening the HERMES scope to the complete eukaryotic domain. [ABSTRACT FROM AUTHOR]

BMP signaling has a conserved function in patterning the dorsal-ventral body axis in Bilateria and the directive axis in anthozoan cnidarians. So far, cnidarian studies have focused on the role of different BMP signaling network components in regulating pSMAD1/5 gradient formation. Much less is known about the target genes downstream of BMP signaling. To address this, we generated a genome-wide list of direct pSMAD1/5 target genes in the anthozoan Nematostella vectensis , several of which were conserved in Drosophila and Xenopus . Our ChIP-seq analysis revealed that many of the regulatory molecules with documented bilaterally symmetric expression in Nematostella are directly controlled by BMP signaling. We identified several so far uncharacterized BMP-dependent transcription factors and signaling molecules, whose bilaterally symmetric expression may be indicative of their involvement in secondary axis patterning. One of these molecules is zswim4-6 , which encodes a novel nuclear protein that can modulate the pSMAD1/5 gradient and potentially promote BMP-dependent gene repression., Competing Interests: PK, AS, AP, BZ, KR, DČ, PM, GG No competing interests declared, (© 2024, Knabl, Schauer et al.)

The subfamily GH13_1 of alpha-amylases is typical of Fungi, but it is also found in some unicellular eukaryotes (e.g., Amoebozoa, choanoflagellates) and non-bilaterian Metazoa. Since a previous study in 2007, GH13_1 amylases were considered ancestral to the Unikonts, including animals, except Bilateria, such that it was thought to have been lost in the ancestor of this clade. The only alpha-amylases known to be present in Bilateria so far belong to the GH13_15 and 24 subfamilies (commonly called bilaterian alpha-amylases) and were likely acquired by horizontal transfer from a proteobacterium. The taxonomic scope of Eukaryota genomes in databases has been greatly increased ever since 2007. We have surveyed GH13_1 sequences in recent data from ca. 1600 bilaterian species, 60 non-bilaterian animals and also in unicellular eukaryotes. As expected, we found a number of those sequences in non-bilaterians: Anthozoa (Cnidaria) and in sponges, confirming the previous observations, but none in jellyfishes and in Ctenophora. Our main and unexpected finding is that such fungal (also called Dictyo-type) amylases were also consistently retrieved in several bilaterian phyla: hemichordates (deuterostomes), brachiopods and related phyla, some molluscs and some annelids (protostomes). We discuss evolutionary hypotheses possibly explaining the scattered distribution of GH13_1 across bilaterians, namely, the retention of the ancestral gene in those phyla only and/or horizontal transfers from non-bilaterian donors. [ABSTRACT FROM AUTHOR]

Humans belong to the vast clade of species known as the bilateria, with a bilaterally symmetrical body plan. Over the course of evolution, exceptions to symmetry have arisen. Among chordates, the internal organs have been arranged asymmetrically in order to create more efficient functioning and packaging. The brain has also assumed asymmetries, although these generally trade off against the pressure toward symmetry, itself a reflection of the symmetry of limbs and sense organs. In humans, at least, brain asymmetries occur in independent networks, including those involved in language and manual manipulation biased to the left hemisphere, and emotion and face perception biased to the right. Similar asymmetries occur in other species, notably the great apes. A number of asymmetries are correlated with conditions such as dyslexia, autism, and schizophrenia, and have largely independent genetic associations. The origin of asymmetry itself, though, appears to be unitary, and in the case of the internal organs, at least, may depend ultimately on asymmetry at the molecular level.

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria as seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that support for the Cnidaria + Bilateria clade can be assigned to this source of systematic error. In interpreting these results, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution.

Sperm structure of the Xenacoelomorpha (Acoelomorpha plus Xenoturbellida) is updated in the light of new discoveries or new interpretations of existing data. Nemertodermatida and Acoela (Acoelomorpha) have introsperm with certain basic features in common, but all acoels lack acrosomes and usually have two flagella with unusual combinations of microtubules, whereas all nemertodermatids have small, simple acrosomes and a typical 9 + 2 flagellum. Xenoturbellida is currently considered as the sister taxon to Acoelomorpha. Xenoturbella bocki has an aquasperm that has almost nothing in common with the sperm of Acoelomorpha. We argue that the aquasperm ultrastructure of X. bocki has much in common with sperm of hemichordates and to some extent echinoderms, which was previously disputed. Molecular analyses have on the one hand supported a connection with deuterostomes but on the other hand have negated it, suggesting that the closest common ancestor of Xenacoelomorpha is either the Nephrozoa, Deuterostomia or Protostomia. Sperm structure is highly diverse among Xenacoelomorpha, with protostome-like traits in Acoelomorpha and deuterostome-like traits in Xenoturbella. Assuming Xenacoelomorph monophyly and ancestral introsperm in this taxon, however, suggests that the re-expression of the aquasperm form of Xenoturbella, involving some key changes in sperm morphology, is a secondarily derived state that could have occurred through "progenetic spermiogenesis" with the precocious development of round spermatids to maturity. [ABSTRACT FROM AUTHOR]

Abstract The Ecdysozoa is a major animal clade whose main uniting feature is a distinctive growth strategy that requires the periodical moulting of the external cuticle. The staggering diversity within Ecdysozoa has prompted substantial efforts to reconstruct their origin and early evolution. Based on palaentological and developmental data, we proposed a scenario for the early evolution of the ecdysozoan clade Panarthropoda (Onychophora, Tardigrada, Euarthropoda), and postulated that a terminal mouth is ancestral for this lineage. In light of the accompanying comment by Claus Nielsen, we take this opportunity to clarify the significance of our argumentation for Panarthropoda in the phylogenetic context of Ecdysozoa, and Bilateria more broadly. We conclude that the ancestral ecdysozoan most likely had an adult terminal mouth, and that the last common ancestors of all the phyla that constitute Ecdysozoa almost certainly also had an adult terminal mouth. The occurrence of a ventral-facing mouth in various adult ecdysozoans – particularly panarthropods – is the result of convergence. Despite the paucity of embryological data on fossil taxa, we contemplate the likelihood that a developmentally early ventral mouth opening could be ancestral for Ecdysozoa, and if so, then this would represent a symplesiomorphy of Bilateria as a whole. Highlights • We reply to Nielsen's proposal that the ancestral Panarthropod had a ventral mouth. • Fossils demonstrate the presence of a terminal anterior facing mouth in adult stem-group scalidophorans and panarthropods. • Palaeontological data suggest that the last common ancestor of Ecdysozoa had an adult terminal mouth. • Extant panarthropod development suggests that palaeoscolecids and lobopodians may have had an embryonic ventral mouth. [ABSTRACT FROM AUTHOR]

Molluscs are extremely diverse invertebrate animals with a rich fossil record, highly divergent life cycles, and considerable economical and ecological importance. Key representatives include worm‐like aplacophorans, armoured groups (e.g. polyplacophorans, gastropods, bivalves) and the highly complex cephalopods. Molluscan origins and evolution of their different phenotypes have largely remained unresolved, but significant progress has been made over recent years. Phylogenomic studies revealed a dichotomy of the phylum, resulting in Aculifera (shell‐less aplacophorans and multi‐shelled polyplacophorans) and Conchifera (all other, primarily uni‐shelled groups). This challenged traditional hypotheses that proposed that molluscs gradually evolved complex phenotypes from simple, worm‐like animals, a view that is corroborated by developmental studies that showed that aplacophorans are secondarily simplified. Gene expression data indicate that key regulators involved in anterior–posterior patterning (the homeobox‐containing Hox genes) lost this function and were co‐opted into the evolution of taxon‐specific novelties in conchiferans. While the bone morphogenetic protein (BMP)/decapentaplegic (Dpp) signalling pathway, that mediates dorso‐ventral axis formation, and molecular components that establish chirality appear to be more conserved between molluscs and other metazoans, variations from the common scheme occur within molluscan sublineages. The deviation of various molluscs from developmental pathways that otherwise appear widely conserved among metazoans provides novel hypotheses on molluscan evolution that can be tested with genome editing tools such as the CRISPR/Cas9 (clustered regularly interspaced short palindromic repeats/clustered regularly interspaced short palindromic repeats‐associated protein9) system. [ABSTRACT FROM AUTHOR]

The nervous systems in most bilaterians are centralized, composed of central nervous systems (CNS) and peripheral nervous systems (PNS). Common molecular and cellular patterns of medial nerve cords have been observed in various distantly related bilaterians, suggesting deep homology of CNS. The development patterns of PNS, however, are more diverse than CNS across different phylogenetic lineages and the evolution of PNS so far has been thought to be polygenic. The molecular and cellular programs during the development of PNS among different bilaterian branches are drastically different. For example, vertebrate PNS is essentially derived from neural crest cells and placodes, which are largely vertebrate innovations and do not exist in invertebrates. On the other hand, the lack of common precursor cell types does not necessarily lead to the conclusion of different evolutionary origins. Homology needs to be examined with a deeper and broader scope. In this review, we examined the molecular, cellular and developmental characteristics of PNS in a broad range of bilaterians to summarize our current understanding of variation and potentially conserved themes. These comparisons demonstrate that there exist both migratory and non‐migratory neuroblasts in the lateral border of CNS precursors in most model bilaterian animals. These lateral border neuroblasts are specified by conserved gene regulatory network and give rise to sensory neurons, suggesting that lateral border neuroblasts represent the progenitor of PNS and share deep homology among different branches of Bilateria. Future studies are needed to elucidate the evo‐devo mechanisms of the lateral neural borders as PNS progenitors. Investigating the molecular mechanisms underlying the activation of these differentiation gene batteries in different animals will illustrate conserved developmental roles of lateral neural borders. [ABSTRACT FROM AUTHOR]

Abstract Inheritance (sequestration of a localized determinant: germplasm) and zygotic induction are two modes of metazoan primordial germ cell (PGC) specification. vasa and nanos homologs are evolutionarily conserved germline marker genes that have been used to examine the ontogeny of germ cells in various animals. In the lepidopteran insect Bombyx mori, although the lack of vasa homolog (BmVLG) protein localization as well as microscopic observation suggested the lack of germplasm, classical embryo manipulation studies and the localization pattern of Bm-nosO (one of the four nanos genes in Bombyx) maternal mRNA in the egg raised the possibility that an inheritance mode is operating in Bombyx. Here, we generated Bm-nosO knockouts to examine whether the localized mRNA acts as a localized germ cell determinant. Contrary to our expectations, Bm-nosO knockout lines could be established. However, these lines frequently produced abnormal eggs, which failed to hatch, to various extent depending on the individuals. We also found that Bm-nosO positively regulated BmVLG expression at least during embryonic stage, directly or indirectly, indicating that these genes were on the same developmental pathway for germ cell formation in Bombyx. These results suggest that these conserved genes are concerned with stable germ cell production. On the other hand, from the aspect of BmVLG as a PGC marker, we showed that maternal Bm-nosO product(s) as well as early zygotic Bm-nosO activity were redundantly involved in PGC specification; elimination of both maternal and zygotic gene activities (as in knockout lines) resulted in the apparent lack of PGCs, indicating that an inheritance mechanism indeed operates in Bombyx. This, however, together with the fact that germ cells are produced at all in Bm-nosO knockout lines, also suggests the possibility that, in Bombyx, not only this inheritance mechanism but also an inductive mechanism acts in concert to form germ cells or that loss of early PGCs are compensated for by germline regeneration: mechanisms that could enable the evolution of preformation. Thus, Bombyx could serve as an important organism in understanding the evolution of germ cell formation mechanisms; transition between preformation and inductive modes. Highlights • Bombyx nanosO knockout lines were generated by genome editing. • PGCs were undetected by molecular marker vasa in knockout lines. • Knockout lines could accomplish gametogenesis with frequent anomalies in oogenesis. • Bombyx PGC formation may involve both inheritance and inductive modes. • Alternatively, Bombyx may have germline regeneration mechanisms. [ABSTRACT FROM AUTHOR]

Abstract: Architectonics is the study of the division of the animal body into modular structures that are to some extent autonomous in their ontogeny and phylogeny. Thereby it allows key points in the ontogeny of many fossil taxa to be identified. Studying the symmetry of the mutual arrangement of the modular structures of the organism and its evolution, together with the analysis of architectonics, promorphology helps to clarify the evolution of ontogeny in real geological time and thereby brings together paleontology and developmental biology. The application of this approach to echinoderms enables the presence of a torsion process in the ontogeny of all Pelmatozoa and Soluta (among Carpozoa), and the absence of this process in Stylophora, to be demonstrated. The analysis of architectonics and promorphology of Paleozoic tetracorals (Rugosa) revealed the correlation of the oral-aboral and dorsal-ventral axes of their larvae with the oral-aboral and directive axes of the polyp developing from them. This shows that the bilateral symmetry of Anthozoa and possibly of all Cnidaria preceded their radial symmetry. [ABSTRACT FROM AUTHOR]

Abstract: The idea of Hox genes and their work was developed in the studies of classical model animals belonging to the lineages of Ecdysozoa (Drosophila, Tribolium, Caenorhabditis) and Deuterostomia (mouse, chicken, Xenopus, and zebrafish). Subsequently the list of objects was continued by Spiralia (mollusks, polychaetes, brachiopods, rotiferans) and expanded every year by animals with complicated phylogenetic positions or interesting developmental programs. To date, a sufficient set of data has been accumulated to search for ancestral, i.e., constant, features in representatives of different taxa, based on similarities and dissimilarities in the usage of Hox genes to try to reconstruct UrBilateria—a common ancestor of bilateral animals. [ABSTRACT FROM AUTHOR]

Abstract Bilaterian embryos are triploblastic organisms which develop three complete germ layers (ectoderm, mesoderm, and endoderm). While the ectoderm develops mainly from the animal hemisphere, there is diversity in the location from where the endoderm and the mesoderm arise in relation to the animal-vegetal axis, ranging from endoderm being specified between the ectoderm and mesoderm in echinoderms, and the mesoderm being specified between the ectoderm and the endoderm in vertebrates. A common feature is that part of the mesoderm segregates from an ancient bipotential endomesodermal domain. The process of segregation is noisy during the initial steps but it is gradually refined. In this review, we discuss the role of the Notch pathway in the establishment and refinement of boundaries between germ layers in bilaterians, with special focus on its interaction with the Wnt/β-catenin pathway. Highlights • We review the role of Notch in the division of germ layers in bilaterians. • Canonical and non-canonical roles for Notch are considered. • Interactions of Notch and β-catenin signaling are discussed. • We focus in common and different outcomes of these pathways in bilaterians. [ABSTRACT FROM AUTHOR]

Most studies that utilize ancient DNA have focused on specific groups of organisms or even single species. Instead, the whole biodiversity of eukaryotes can be described using universal phylogenetic marker genes found within well‐preserved sediment cores that cover the post‐glacial period. Sedimentary ancient DNA samples from Lake Lielais Svētiņu, eastern Latvia, at a core depth of 1,050 cm in ~150 year intervals were used to determine phylotaxonomy in domain Eukaryota. Phylotaxonomic affiliation of >1,200 eukaryotic phylotypes revealed high richness in all major eukaryotic groups—Alveolata, Stramenopiles, Cercozoa, Chlorophyta, Charophyta, Nucletmycea, and Holozoa. The share of organisms that originate from terrestrial ecosystems was about one third, of which the most abundant molecular operational taxonomic units were Fungi and tracheal/vascular plants, which demonstrates the usefulness of using lake sediments to reconstruct the terrestrial paleoecosystems that surround them. Phylotypes that originate from the lake ecosystem belonged to various planktonic organisms; phyto‐, proto,‐ and macrozooplankton, and vascular aquatic plants. We observed greater richness of several planktonic organisms that can be associated with higher trophic status during the warm climate period between 4,000 and 8,000 years ago and an increase in eukaryotic richness possibly associated with moderate human impact over the last 2,000 years. [ABSTRACT FROM AUTHOR]

Neuropeptides are neurosecretory signaling molecules in protostomes and deuterostomes (together Nephrozoa). Little, however, is known about the neuropeptide complement of the sister group of Nephrozoa, the Xenacoelomorpha, which together form the Bilateria. Because members of the xenacoelomorph clades Xenoturbella, Nemertodermatida, and Acoela differ extensively in their central nervous system anatomy, the reconstruction of the xenacoelomorph and bilaterian neuropeptide complements may provide insights into the relationship between nervous system evolution and peptidergic signaling. Here, we analyzed transcriptomes of seven acoels, four nemertodermatids, and two Xenoturbella species using motif searches, similarity searches, mass spectrometry and phylogenetic analyses to characterize neuropeptide precursors and neuropeptide receptors. Our comparison of these repertoires with previously reported nephrozoan and cnidarian sequences shows that the majority of annotated neuropeptide GPCRs in cnidarians are not orthologs of specific bilaterian neuropeptide receptors, which suggests that most of the bilaterian neuropeptide systems evolved after the cnidarian–bilaterian evolutionary split. This expansion of more than 20 peptidergic systems in the stem leading to the Bilateria predates the evolution of complex nephrozoan organs and nervous system architectures. From this ancient set of neuropeptides, acoels show frequent losses that correlate with their divergent central nervous system anatomy. We furthermore detected the emergence of novel neuropeptides in xenacoelomorphs and their expansion along the nemertodermatid and acoel lineages, the two clades that evolved nervous system condensations. Together, our study provides fundamental insights into the early evolution of the bilaterian peptidergic systems, which will guide future functional and comparative studies of bilaterian nervous systems. [ABSTRACT FROM AUTHOR]

Bilateria are the predominant clade of animals on Earth. Despite having evolved a wide variety of body plans and developmental modes, they are characterized by common morphological traits. By default, researchers have tried to link clade-specific genes to these traits, thus distinguishing bilaterians from non-bilaterians, by their gene content. Here we argue that it is rather biological processes that unite Bilateria and set them apart from their non-bilaterian sisters, with a less complex body morphology. To test this hypothesis, we compared proteomes of bilaterian and non-bilaterian species in an elaborate computational pipeline, aiming to search for a set of bilaterian-specific genes. Despite the limited confidence in their bilaterian specificity, we nevertheless detected Bilateria-specific functional and developmental patterns in the sub-set of genes conserved in distantly related Bilateria. Using a novel multi-species GO-enrichment method, we determined the functional repertoire of genes that are widely conserved among Bilateria. Analyzing expression profiles in three very distantly related model species—D. melanogaster, D. rerio and C. elegans—we find characteristic peaks at comparable stages of development and a delayed onset of expression in embryos. In particular, the expression of the conserved genes appears to peak at the phylotypic stage of different bilaterian phyla. In summary, our study illustrate how development connects distantly related Bilateria after millions of years of divergence, pointing to processes potentially separating them from non-bilaterians. We argue that evolutionary biologists should return from a purely gene-centric view of evolution and place more focus on analyzing and defining conserved developmental processes and periods.

We belong to a clade of species known as the bilateria, with a body plan that is essentially symmetrical with respect to left and right, an adaptation to the indifference of the natural world to mirror-reflection. Limbs and sense organs are in bilaterally symmetrical pairs, dictating a high degree of symmetry in the brain itself. Bilateral symmetry can be maladaptive, though, especially in the human world where it is important to distinguish between left and right sides, and between left-right mirror images, as in reading directional scripts. The brains of many animals have evolved asymmetries, often but not exclusively in functions not dependent on sensory input or immediate reaction to the environment. Brain asymmetries in humans have led to exaggerate notions of a duality between the sides of the brain. The tradeoff between symmetry and asymmetry results in individual differences in brain asymmetries and handedness, contributing to a diversity of aptitude and divisions of labor. Asymmetries may have their origin in fundamental molecular asymmetries going far back in biological evolution.

ABSTRACT Classical ecology provides principles for construction and function of biological communities, but to what extent these apply to the animal-associated microbiota is just beginning to be assessed. Here, we investigated the influence of several well-known ecological principles on animal-associated microbiota by characterizing gut microbial specimens from bilaterally symmetrical animals (Bilateria) ranging from flies to whales. A rigorously vetted sample set containing 265 specimens from 64 species was assembled. Bacterial lineages were characterized by 16S rRNA gene sequencing. Previously published samples were also compared, allowing analysis of over 1,098 samples in total. A restricted number of bacterial phyla was found to account for the great majority of gut colonists. Gut microbial composition was associated with host phylogeny and diet. We identified numerous gut bacterial 16S rRNA gene sequences that diverged deeply from previously studied taxa, identifying opportunities to discover new bacterial types. The number of bacterial lineages per gut sample was positively associated with animal mass, paralleling known species-area relationships from island biogeography and implicating body size as a determinant of community stability and niche complexity. Samples from larger animals harbored greater numbers of anaerobic communities, specifying a mechanism for generating more-complex microbial environments. Predictions for species/abundance relationships from models of neutral colonization did not match the data set, pointing to alternative mechanisms such as selection of specific colonists by environmental niche. Taken together, the data suggest that niche complexity increases with gut size and that niche selection forces dominate gut community construction. IMPORTANCE The intestinal microbiome of animals is essential for health, contributing to digestion of foods, proper immune development, inhibition of pathogen colonization, and catabolism of xenobiotic compounds. How these communities assemble and persist is just beginning to be investigated. Here we interrogated a set of gut samples from a wide range of animals to investigate the roles of selection and random processes in microbial community construction. We show that the numbers of bacterial species increased with the weight of host organisms, paralleling findings from studies of island biogeography. Communities in larger organisms tended to be more anaerobic, suggesting one mechanism for niche diversification. Nonselective processes enable specific predictions for community structure, but our samples did not match the predictions of the neutral model. Thus, these findings highlight the importance of niche selection in community construction and suggest mechanisms of niche diversification.