Biology subjects

Andreas Hejnol

Publications and source records attributed to Andreas Hejnol.

4 recordsLinked to original sources

bioRxiv2016

Conserved traits of spiralian development in the bryozoan Membranipora membranacea

BackgroundSpiral cleavage is a remarkably conserved pattern of embryogenesis present in animals of the clade Spiralia, such as annelids, molluscs, flatworms and nemerteans. However, not all spiralians display spiral cleavage. Recent phylogenies suggest that the spiral arrangement of embryonic blastomeres is an ancestral trait for the Spiralia and that it was secondarily modified in several spiralian lineages, such as gastrotrichs, brachiopods and bryozoans. To better understand the evolution of cleavage patterns in relation to blastomere fate maps and embryonic gene expression, we describe the cell lineage and molecular patterning in the embryogenesis of the bryozoan Membranipora membranacea.\n\nResultsM. membranacea develops through a unique stereotypic cleavage pattern with biradial symmetry and an embryo organized in identical quadrants with synchronous cell divisions. The quadrant identities are established as early as the 28-cell stage, when one vegetal blastomere (3D) activates the MAPK pathway, marking the future posterior region of the larva. Cells from this posterior quadrant divide asynchronously in subsequent stages leading to the morphological differentiation between quadrants. The first quartet of M. membranacea gives rise to the apical organ and ciliated band, the second and third quartet forms the oral/anal ectoderm, the fourth quartet the mesoderm and the vegetal blastomeres form the endoderm. We found that the early embryonic organization and the fate map of these early blastomeres in the bryozoan embryo are similar to a typical spiral-cleaving embryo. Furthermore we observe that correspondent blastomeres between the bryozoan and spiral-cleaving embryos share similar molecular identities, as revealed by the activity of MAPK and the expression of otx and foxa. The development of M. membranacea mainly differs from spiral-cleaving embryos in the downstream portions of the cell lineage, and in the origin of the mesoderm, which is formed by multiple fourth quartet blastomeres.\n\nConclusionsThe similarity between the fate map of M. membranacea and spiral-cleaving embryos indicates that the cleavage geometry of the bryozoan evolved decoupled from other spiralian developmental traits. In this case, the blastomere fates remained evolutionarily conserved despite the drastic modification in the cleavage pattern from spiral to biradial. These findings suggest that blastomere fates of spiral-cleaving embryos might not be linked to the stereotypic spiral cleavage pattern, but depend on other factors, such as the underlying molecular patterning. Our comparative analysis on the bryozoan reveals yet another facet of how early development evolves and helps to shed some light into the developmental diversity of spiralians.

Developmental Biology↗

bioRxiv2016

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

Temporal collinearity is often regarded as the force preserving Hox clusters in vertebrate genomes. Studies that combine genomic and gene expression data in invertebrates would allow generalizing this observation across all animals, but are scarce, particularly within Lophotrochozoa (e.g., snails and segmented worms). Here, we use two brachiopod species -Terebratalia transversa, Novocrania anomala- to characterize the complement, cluster and expression of their Hox genes. T. transversa has an ordered, split cluster with ten genes (lab, pb, Hox3, dfd, scr, lox5, antp, lox4, post2, post1), while N. anomala has nine (missing post1). Our in situ hybridization, qPCR and stage specific transcriptomic analyses show that brachiopod Hox genes are neither strictly temporally nor spatially collinear; only pb (in T. transversa), Hox3 and dfd (in both brachiopods) show staggered mesodermal expression. The spatial expression of the Hox genes in both brachiopod species correlates with their morphology and demonstrates cooption of Hox genes in the chaetae and shell fields, two major lophotrochozoan morphological novelties. The shared and specific expression of a subset of Hox genes, Arx and Zic orthologs in chaetae and shell-fields between brachiopods, mollusks, and annelids supports the deep conservation of the molecular basis forming these lophotrochozoan hallmarks. Our findings challenge that collinearity alone preserves lophotrochozoan Hox clusters, indicating that additional genomic traits need to be considered in understanding Hox evolution.

Evolutionary Biology↗

bioRxiv2016

Increased taxon sampling reveals thousands of hidden orthologs in flatworms

Gene gains and losses shape the gene complement of animal lineages and are a fundamental aspect of genomic evolution. Acquiring a comprehensive view of the evolution of gene repertoires is however limited by the intrinsic limitations of common sequence similarity searches and available databases. Thus, a subset of the complement of an organism consists of hidden orthologs, those with no apparent homology with common sequenced animal lineages --mistakenly considered new genes-- but actually representing fast evolving orthologs of presumably lost proteins. Here, we describe 'Leapfrog', an automated pipeline that uses increased taxon sampling to overcome long evolutionary distances and identify hidden orthologs in large transcriptomic databases. As a case study, we used 35 transcriptomes of 29 flatworm lineages to recover 3,597 hidden orthologs. Unexpectedly, we do not observe a correlation between the number of hidden orthologs in a lineage and its 'average' evolutionary rate. Hidden orthologs do not show unusual sequence composition biases (e.g. GC content, average length, domain composition), but do appear to be more common in genes with binding or catalytic activity. By using 'Leapfrog', we identify key centrosome-related genes and homeodomain classes previously reported as absent in free-living flatworms, e.g. planarians. Altogether, our findings demonstrate that hidden orthologs comprise a significant proportion of the gene repertoire, qualifying the impact of gene losses and gains in gene complement evolution.

Bioinformatics↗

bioRxiv2016

Expression of segment polarity genes in brachiopods supports a non-segmental ancestral role of engrailed for bilaterians

The diverse and complex developmental mechanisms of segmentation have been more thoroughly studied in arthropods, vertebrates and annelids--distantly related animals considered to be segmented. Far less is known about the role of \"segmentation genes\" in organisms that lack a segmented body. Here we investigate the expression of the arthropod segment polarity genes engrailed, wnt1 and hedgehog in the development of brachiopods--marine invertebrates without a subdivided trunk but closely related to the segmented annelids. We found that a stripe of engrailed expression demarcates the ectodermal boundary that delimits the anterior region of Terebratalia transversa and Novocrania anomala embryos. In T. transversa, this engrailed domain is abutted by a stripe of wnt1 expression in a pattern similar to the parasegment boundaries of insects--except for the expression of hedgehog, which is restricted to endodermal tissues of the brachiopod embryos. We found that pax6 and pax2/5/8, putative regulators of engrailed, also demarcate the anterior boundary in the two species, indicating these genes might be involved in the anterior patterning of brachiopod larvae. In a comparative phylogenetic context, these findings suggest that bilaterians might share an ancestral, non-segmental domain of engrailed expression during early embryogenesis.

Evolutionary Biology↗