Flatworms number among the most diverse invertebrate phyla and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships ...within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. In this study, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked 'microturbellarian' groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates.
Animal Phylogeny and Its Evolutionary Implications Dunn, Casey W; Giribet, Gonzalo; Edgecombe, Gregory D ...
Annual review of ecology, evolution, and systematics,
11/2014, Letnik:
45, Številka:
1
Journal Article
Recenzirano
In recent years, scientists have made remarkable progress reconstructing the animal phylogeny. There is broad agreement regarding many deep animal relationships, including the monophyly of animals, ...Bilateria, Protostomia, Ecdysozoa, and Spiralia. This stability now allows researchers to articulate the diminishing number of remaining questions in terms of well-defined alternative hypotheses. These remaining questions include relationships at the base of the animal tree, the position of Xenacoelomorpha, and the internal relationships of Spiralia. Recent progress in the field of animal phylogeny has important implications for our understanding of the evolution of development, morphology, genomes, and other characters. A remarkable pattern emerges-there is far more homoplasy for all these characters than had previously been anticipated, even among many complex characters such as segmentation and nervous systems. The fossil record dates most deep branches of the animal tree to an evolutionary radiation in the early Cambrian with roots in the Late Neoproterozoic.
Molecular biology has provided a rich dataset to develop hypotheses of nervous system evolution. The startling patterning similarities between distantly related animals during the development of ...their central nervous system (CNS) have resulted in the hypothesis that a CNS with a single centralized medullary cord and a partitioned brain is homologous across bilaterians. However, the ability to precisely reconstruct ancestral neural architectures from molecular genetic information requires that these gene networks specifically map with particular neural anatomies. A growing body of literature representing the development of a wider range of metazoan neural architectures demonstrates that patterning gene network complexity is maintained in animals with more modest levels of neural complexity. Furthermore, a robust phylogenetic framework that provides the basis for testing the congruence of these homology hypotheses has been lacking since the advent of the field of ‘evo-devo’. Recent progress in molecular phylogenetics is refining the necessary framework to test previous homology statements that span large evolutionary distances. In this review, we describe recent advances in animal phylogeny and exemplify for two neural characters—the partitioned brain of arthropods and the ventral centralized nerve cords of annelids—a test for congruence using this framework. The sequential sister taxa at the base of Ecdysozoa and Spiralia comprise small, interstitial groups. This topology is not consistent with the hypothesis of homology of tripartitioned brain of arthropods and vertebrates as well as the ventral arthropod and rope-like ladder nervous system of annelids. There can be exquisite conservation of gene regulatory networks between distantly related groups with contrasting levels of nervous system centralization and complexity. Consequently, the utility of molecular characters to reconstruct ancestral neural organization in deep time is limited.
Evolutionary developmental biology, the interdisciplinary effort of illuminating the conserved similarities and differences during animal development across all phylogenetic clades, has gained ...renewed interest in the past decades. As technology (immunohistochemistry, next‐generation sequencing, advanced imaging, and computational resources) has advanced, so has our ability of resolving fundamental hypotheses and overcoming the genotype–phenotype gap. This rapid progress, however, has also exposed gaps in the collective knowledge around the choice and representation of model organisms. It has become clear that evo‐devo requires a comparative, large‐scale approach including marine invertebrates to resolve some of the most urgent questions about the phylogenetic positioning and character traits of the last common ancestors. Many invertebrates at the base of the tree of life inhabit marine environments and have been used for some years due to their accessibility, husbandry, and morphology. Here, we briefly review the major concepts of evolutionary developmental biology and discuss the suitability of established model organisms to address current research questions, before focussing on the importance, application, and state‐of‐the‐art of marine evo‐devo. We highlight novel technical advances that progress evo‐devo as a whole.
A hallmark of metazoan evolution is the emergence of genomic mechanisms that implement cell-type-specific functions. However, the evolution of metazoan cell types and their underlying gene regulatory ...programmes remains largely uncharacterized. Here, we use whole-organism single-cell RNA sequencing to map cell-type-specific transcription in Porifera (sponges), Ctenophora (comb jellies) and Placozoa species. We describe the repertoires of cell types in these non-bilaterian animals, uncovering diverse instances of previously unknown molecular signatures, such as multiple types of peptidergic cells in Placozoa. Analysis of the regulatory programmes of these cell types reveals variable levels of complexity. In placozoans and poriferans, sequence motifs in the promoters are predictive of cell-type-specific programmes. By contrast, the generation of a higher diversity of cell types in ctenophores is associated with lower specificity of promoter sequences and the existence of distal regulatory elements. Our findings demonstrate that metazoan cell types can be defined by networks of transcription factors and proximal promoters, and indicate that further genome regulatory complexity may be required for more diverse cell type repertoires.
There is considerable interest in comparing functional genomic data across species. One goal of such work is to provide an integrated understanding of genome and phenotype evolution. Most comparative ...functional genomic studies have relied on multiple pairwise comparisons between species, an approach that does not incorporate information about the evolutionary relationships among species. The statistical problems that arise from not considering these relationships can lead pairwise approaches to the wrong conclusions and are a missed opportunity to learn about biology that can only be understood in an explicit phylogenetic context. Here, we examine two recently published studies that compare gene expression across species with pairwise methods, and find reason to question the original conclusions of both. One study interpreted pairwise comparisons of gene expression as support for the ortholog conjecture, the hypothesis that orthologs tend to have more similar attributes (expression in this case) than paralogs. The other study interpreted pairwise comparisons of embryonic gene expression across distantly related animals as evidence for a distinct evolutionary process that gave rise to phyla. In each study, distinct patterns of pairwise similarity among species were originally interpreted as evidence of particular evolutionary processes, but instead, we find that they reflect species relationships. These reanalyses concretely show the inadequacy of pairwise comparisons for analyzing functional genomic data across species. It will be critical to adopt phylogenetic comparative methods in future functional genomic work. Fortunately, phylogenetic comparative biology is also a rapidly advancing field with many methods that can be directly applied to functional genomic data.
Despite rapid advances in the study of metazoan evolutionary history 1, phylogenomic analyses have so far neglected a number of microscopic lineages that possess a unique combination of characters ...and are thus informative for our understanding of morphological evolution. Chief among these lineages are the recently described animal groups Micrognathozoa and Loricifera, as well as the two interstitial “Problematica” Diurodrilus and Lobatocerebrum 2. These genera show a certain resemblance to Annelida in their cuticle and gut 3, 4; however, both lack primary annelid characters such as segmentation and chaetae 5. Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa 6, 7—lineages that are grouped by some analyses into “Platyzoa,” a clade whose status remains uncertain 1, 8–11. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa. Lobatocerebrum and Diurodrilus are found to be deeply nested members of Annelida, and unequivocal support is found for Micrognathozoa as the sister group of Rotifera. Analyses using site-heterogeneous substitution models further recover a lophophorate clade and position Loricifera + Priapulida as sister group to the remaining Ecdysozoa. Finally, with several meiofaunal lineages branching off early in the diversification of Spiralia, the emerging concept of a microscopic, acoelomate, direct-developing ancestor of Spiralia is reviewed.
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•Diurodrilus and Lobatocerebrum, two problematic meiofauna, are miniaturized annelids•Micrognathozoa, the newest-described animal phylum, is the sister group of Rotifera•Bayesian mixture models recover strong support for deep spiralian relationships•Two clades comprising Platyzoa form separate early branches in Spiralia
Laumer et al. reconstruct the phylogeny of Spiralia, the animal group including molluscs, annelids, flatworms, and many microscopic worms. The new tree suggests that some previously unsampled, interstitial Problematica originated through miniaturization from large-bodied ancestors but also implies a primarily interstitial origin for many lineages.
In situ hybridization is a widely employed technique allowing spatial visualization of gene expression in fixed specimens. It has greatly advanced our understanding of biological processes, including ...developmental regulation. In situ protocols are today routinely followed in numerous laboratories, and although details might change, they all include a hybridization step, where specific antisense RNA or DNA probes anneal to the target nucleic acid sequence. This step is generally carried out at high temperatures and in a denaturing solution, called hybridization buffer, commonly containing 50% (v/v) formamide – a hazardous chemical. When applied to the soft-bodied hydrozoan medusa Clytia hemisphaerica, we found that this traditional hybridization approach was not fully satisfactory, causing extensive deterioration of morphology and tissue texture which compromised our observation and interpretation of results. We thus tested alternative solutions for in situ detection of gene expression and, inspired by optimized protocols for Northern and Southern blot analysis, we substituted the 50% formamide with an equal volume of 8M urea solution in the hybridization buffer. Our new protocol not only yielded better morphologies and tissue consistency, but also notably improved the resolution of the signal, allowing more precise localization of gene expression and reducing aspecific staining associated with problematic areas. Given the improved results and reduced manipulation risks, we tested the urea protocol on other metazoans, two brachiopod species (Novocrania anomala and Terebratalia transversa) and the priapulid worm Priapulus caudatus, obtaining a similar reduction of aspecific probe binding. Overall, substitution of formamide by urea during in situ hybridization offers a safer alternative, potentially of widespread use in research, medical and teaching contexts. We encourage other workers to test this approach on their study organisms, and hope that they will also obtain better sample preservation, more precise expression patterns and fewer problems due to aspecific staining, as we report here for Clytia medusae and Novocrania and Terebratalia developing larvae.
•An alternative ISH protocol is proposed, substituting formamide with urea.•Specimen morphology appears to be better preserved.•Signal detection significantly improves, reducing non-specific staining.•The method, developed for C. hemisphaerica, was successful with additional species.•Less toxic and simple, it constitutes a useful addition to existing techniques.
A sea star is only a head Hejnol, Andreas
Trends in genetics,
March 2024, 2024-03-00, 20240301, Letnik:
40, Številka:
3
Journal Article
Recenzirano
Odprti dostop
Where are the front and back ends in a sea star? Formery et al. recently tackled this long-standing mystery using state-of-the-art molecular tools, leading them to suggest that a sea star may be ...constructed from components that, in other animals, would constitute only the head.
Where are the front and back ends in a sea star? Formery et al. recently tackled this long-standing mystery using state-of-the-art molecular tools, leading them to suggest that a sea star may be constructed from components that, in other animals, would constitute only the head.
Brachiopods and molluscs are lophotrochozoans with hard external shells which are often believed to have evolved convergently. While palaeontological data indicate that both groups are descended from ...biomineralising Cambrian ancestors, the closest relatives of brachiopods, phoronids and bryozoans, are mineralised to a much lower extent and are comparatively poorly represented in the Palaeozoic fossil record. Although brachiopod and mollusc shells are structurally analogous, genomic and proteomic evidence indicates that their formation involves a complement of conserved, orthologous genes. Here, we study a set of genes comprised of 3 homeodomain transcription factors, one signalling molecule and 6 structural proteins which are implicated in mollusc and brachiopod shell formation, search for their orthologs in transcriptomes or genomes of brachiopods, phoronids and bryozoans, and present expression patterns of 8 of the genes in postmetamorphic juveniles of the rhynchonelliform brachiopod T. transversa. Transcriptome and genome searches for the 10 target genes in the brachiopods Terebratalia transversa, Lingula anatina, Novocrania anomala, the bryozoans Bugula neritina and Membranipora membranacea, and the phoronids Phoronis australis and Phoronopsis harmeri resulted in the recovery of orthologs of the majority of the genes in all taxa. While the full complement of genes was present in all brachiopods with a single exception in L. anatina, a bloc of four genes could consistently not be retrieved from bryozoans and phoronids. The genes engrailed, distal-less, ferritin, perlucin, sp1 and sp2 were shown to be expressed in the biomineralising mantle margin of T. transversa juveniles. The gene expression patterns we recovered indicate that while mineralised shells in brachiopods and molluscs are structurally analogous, their formation builds on a homologous process that involves a conserved complement of orthologous genes. Losses of some of the genes related to biomineralisation in bryozoans and phoronids indicate that loss of the capacity to form mineralised structures occurred already in the phoronid-bryozoan stem group and supports the idea that mineralised skeletons evolved secondarily in some of the bryozoan subclades.
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