It has been hypothesized that a condensed nervous system with a medial ventral nerve cord is an ancestral character of Bilateria. The presence of similar dorsoventral molecular patterns along the nerve cords of vertebrates, flies, and an annelid has been interpreted as support for this scenario. Whether these similarities are generally found across the diversity of bilaterian neuroanatomies is unclear, and thus the evolutionary history of the nervous system is still contentious. To assess the conservation of the dorsoventral nerve cord patterning, we studied representatives of Xenacoelomorpha, Rotifera, Nemertea, Brachiopoda, and Annelida. None of the studied species show a conserved dorsoventral molecular regionalization of their nerve cords, not even the annelid Owenia fusiformis, whose trunk neuroanatomy parallels that of vertebrates and flies. Our findings restrict the use of molecular patterns to explain nervous system evolution, and suggest that the similarities in dorsoventral patterning and trunk neuroanatomies evolved independently in Bilateria.
The mouth opening of bilaterian animals develops either separate from (deuterostomy) or connected to (protostomy) the embryonic blastopore, the site of endomesoderm internalization. Although this distinction preluded the classification of bilaterian animals in Deuterostomia and Protostomia, and has influenced major scenarios of bilaterian evolution, the developmental basis for the appearance of these different embryonic patterns remains unclear. To identify the underlying mechanisms, we compared the development of two brachiopod species that show deuterostomy (Novocrania anomala) and protostomy (Terebratalia transversa), respectively. We show that the differential activity of Wnt signalling, together with the timing and location of mesoderm formation, correlate with the differential behaviour and fate of the blastopore. We further assess these principles in the spiral-cleaving group Annelida, and propose that the developmental relationships of mouth and blastoporal openings are secondary by-products of variations in axial and mesoderm development. This challenges the previous evolutionary emphasis on extant blastoporal behaviours to explain the origin and diversification of bilaterian animals.
Flatworms (Platyhelminthes) are a basally branching phylum that harbours a wealth of fascinating biology, including planarians with their astonishing regenerative abilities and the parasitic tape worms and blood flukes that exert a massive impact on human health. PlanMine (http://planmine.mpi-cbg.de/) has the mission objective of providing both a mineable sequence repository for planarians and also a resource for the comparative analysis of flatworm biology. While the original PlanMine release was entirely based on transcriptomes, the current release transitions to a more genomic perspective. Building on the recent availability of a high quality genome assembly of the planarian model species Schmidtea mediterranea, we provide a gene prediction set that now assign existing transcripts to defined genomic coordinates. The addition of recent single cell and bulk RNA-seq datasets greatly expands the available gene expression information. Further, we add transcriptomes from a broad range of other flatworms and provide a phylogeny-aware interface that makes evolutionary species comparisons accessible to non-experts. At its core, PlanMine continues to utilize the powerful InterMine framework and consistent data annotations to enable meaningful inter-species comparisons. Overall, PlanMine 3.0 thus provides a host of new features that makes the fascinating biology of flatworms accessible to the wider research community.
The fate of the blastopore during development in the bilaterian ancestor is currently not well understood. In deuterostomes, the blastopore forms the anus, but its fate in protostome groups is variable. This variability, combined with an absence of information from key taxa, hampers the reconstruction of the ancestral developmental mode of the Protostomia and the Bilateria. The blastopore fate of the bilaterian ancestor plays a crucial role in understanding the transition from radial to bilateral symmetric organisms. Priapulids have a conservative morphology, an abundant Cambrian fossil record, and a phylogenetic position that make them a key group in understanding protostome evolution. Here, we characterize gastrulation and the embryonic expression of genes involved in bilaterian foregut and hindgut patterning in Priapulus caudatus. We show that the blastopore gives rise to the anus at the vegetal pole and that the hindgut markers brachyury and caudal are expressed in the blastopore and anus, whereas the foregut markers foxA and goosecoid are expressed in the mouth in the animal hemisphere. Thereby, gastrulation in the conservatively evolving protostome P. caudatus follows strictly a deuterostomic pattern. These results are more compatible with a deuterostomic rather than protostomic (blastopore forms the mouth) or amphistomic (mouth and anus are formed simultaneously) mode of development in the last common bilaterian ancestor.
Flatworm embryology has attracted attention since the early beginnings of comparative evolutionary biology. Considered for a long time the most basal bilaterians, the Platyhelminthes (excluding Acoelomorpha) are now robustly placed within the Spiralia. Despite having lost their relevance to explain the transition from radially to bilaterally symmetrical animals, the study of flatworm embryology is still of great importance to understand the diversification of bilaterians and of developmental mechanisms. Flatworms are acoelomate organisms generally with a simple centralized nervous system, a blind gut, and lacking a circulatory organ, a skeleton and a respiratory system other than the epidermis. Regeneration and asexual reproduction, based on a totipotent neoblast stem cell system, are broadly present among different groups of flatworms. While some more basally branching groups - such as polyclad flatworms - retain the ancestral quartet spiral cleavage pattern, most flatworms have significantly diverged from this pattern and exhibit unique strategies to specify the common adult body plan. Most free-living flatworms (i.e. Platyhelminthes excluding the parasitic Neodermata) are directly developing, whereas in polyclads, also indirect developers with an intermediate free-living larval stage and subsequent metamorphosis are found. A comparative study of developmental diversity may help understanding major questions in evolutionary biology, such as the evolution of cleavage patterns, gastrulation and axial specification, the evolution of larval types, and the diversification and specialization of organ systems. In this review, we present a thorough overview of the embryonic development of the different groups of free-living (turbellarian) platyhelminths, including the Catenulida, Macrostomorpha, Polycladida, Lecithoepitheliata, Proseriata, Bothrioplanida, Rhabdocoela, Fecampiida, Prolecithophora and Tricladida, and discuss their main features under a consensus phylogeny of the phylum.
Temporal collinearity is often considered the main force preserving Hox gene clusters in animal genomes. Studies that combine genomic and gene expression data are scarce, however, particularly in invertebrates like the Lophotrochozoa. As a result, the temporal collinearity hypothesis is currently built on poorly supported foundations. Here we characterize the complement, cluster, and expression of Hox genes in two brachiopod species, Terebratalia transversa and Novocrania anomala. T. transversa has a split cluster with 10 genes (lab, pb, Hox3, Dfd, Scr, Lox5, Antp, Lox4, Post2, and Post1), whereas N. anomala has 9 genes (apparently missing Post1). Our in situ hybridization, real-time quantitative PCR, and stage-specific transcriptomic analyses show that brachiopod Hox genes are neither strictly temporally nor spatially collinear; only pb (in T. transversa), Hox3 (in both brachiopods), and Dfd (in both brachiopods) show staggered mesodermal expression. Thus, our findings support the idea that temporal collinearity might contribute to keeping Hox genes clustered. Remarkably, expression of the Hox genes in both brachiopod species demonstrates cooption of Hox genes in the chaetae and shell fields, two major lophotrochozoan morphological novelties. The shared and specific expression of Hox genes, together with Arx, Zic, and Notch pathway components in chaetae and shell fields in brachiopods, mollusks, and annelids provide molecular evidence supporting the conservation of the molecular basis for these lophotrochozoan hallmarks.chaetae | shell fields | Lophotrochozoa | Wiwaxia | Hox cluster
Hox genes are often clustered in animal genomes and exhibit spatial and/or temporal collinearity. It is generally believed that temporal collinearity is the major force preserving Hox clusters. However, studies combining genomic and gene expression analyses of Hox genes are scarce, particularly within Spiralia and Lophotrochozoa (e.g. mollusks, segmented worms, and flatworms). Here, we use two brachiopod species -Terebratalia transversa and Novocrania anomala-that respectively belong to the two major brachiopod lineages to characterize their Hox complement, the presence of a Hox cluster, and the temporal and spatial expression of their Hox genes.We demonstrate that the Hox complement consists of ten Hox genes in T. transversa (lab, pb, Hox3, dfd, scr, lox5, antp, lox4, post2 and post1) and nine in N. anomala (missing post1). Additionally, T. transversa has an ordered, split Hox cluster. Expression analyses reveal that Hox genes are neither temporally nor spatially collinear, and only the genes pb (in T. transversa), Hox3 and dfd (in both brachiopods) show staggered expression in the mesoderm. Remarkably, lab, scr, antp and post1 are associated with the development of the chaetae and shell-forming epithelium, as also observed in annelid chaetae and mollusk shell fields. This, together with the expression of Arx homeobox, supports the deep conservation of the molecular basis for chaetae formation and shell patterning in Lophotrochozoa. Our findings challenge the current evolutionary scenario that (temporal) collinearity is the major mechanism preserving Hox clusters, and suggest that Hox genes were involved in the evolution of lophotrochozoan novelties.
BackgroundThe life cycle of many animals includes a larval stage, which has diversified into an astonishing variety of ecological strategies. The Nemertea is a group of spiralians that exhibits a broad diversity of larval forms, including the iconic pilidium. A pelagic planktotrophic pilidium is the ancestral form in the Pilidiophora, but several lineages exhibit deviations of this condition, mostly as a transition to pelagic lecithotrophy. The most extreme case occurs, however, in the Pilidiophoran Lineus ruber, which exhibits an adelphophagic intracapsular pilidium, the so-called Schmidt’s larva.ResultsWe combined confocal laser scanning microscopy and gene expression studies to characterize the development and metamorphosis of the Schmidt’s larva of L. ruber. The larva forms after gastrulation, and comprises a thin epidermis, a proboscis rudiment and two pairs of imaginal discs from which the juvenile will develop. The cells internalized during gastrulation form a blind gut and the blastopore gives rise to the mouth of the larva and juvenile. The Schmidt’s larva eats other siblings that occupy the same egg capsule, accumulating nutrients for the juvenile. A gradual metamorphosis involves the differentiation of the juvenile cell types from the imaginal discs and the shedding of the larval epidermis. The expression of evolutionarily conserved anterior (foxQ2, six3/6, gsc, otx), endomesodermal (foxA, GATA456-a, twi-a) and posterior (evx, cdx) markers demonstrate that the juvenile retains the molecular patterning of the Schmidt’s larva. After metamorphosis, the juveniles stay over 20 days within the egg masses, until they are fully mature and hatch.ConclusionsThe evolution of the intracapsular Schmidt’s larva involved the loss of the typical feeding structures of the planktotrophic pilidium and a precocious formation of the imaginal discs, as also observed in other pelagic lecithotrophic forms. However, no special adaptations are observed related to adelphophagy. As in planktotrophic pilidium, the molecular mechanism patterning the juvenile is only active in the imaginal discs and not during the early development of the larva, suggesting two separate molecular programs during nemertean embryogenesis. Our results illuminate the diversification of larval forms in the Pilidiophora and Nemertea, and thus on the developmental mechanisms underlying metazoan larval evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0023-5) contains supplementary material, which is available to authorized users.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
334 Leonard St
Brooklyn, NY 11211
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.