Chaetognaths (arrow worms) are an enigmatic group of marine animals whose phylogenetic position remains elusive, in part because they display a mix of developmental and morphological characters ...associated with other groups 1, 2. In particular, it remains unclear whether they are a sister group to protostomes 1, 2, one of the principal animal superclades, or whether they bear a closer relationship with some spiralian phyla 3, 4. Addressing the phylogenetic position of chaetognaths and refining our understanding of relationships among spiralians are essential to fully comprehend character changes during bilaterian evolution 5. To tackle these questions, we generated new transcriptomes for ten chaetognath species, compiling an extensive phylogenomic dataset that maximizes data occupancy and taxonomic representation. We employed inference methods that consider rate and compositional heterogeneity across taxa to avoid limitations of earlier analyses 6. In this way, we greatly improved the resolution of the protostome tree of life. We find that chaetognaths cluster together with rotifers, gnathostomulids, and micrognathozoans within an expanded Gnathifera clade and that this clade is the sister group to other spiralians 7, 8. Our analysis shows that several previously proposed groupings are likely due to systematic error, and we propose a revised organization of Lophotrochozoa with three main clades: Tetraneuralia (mollusks and entoprocts), Lophophorata (brachiopods, phoronids, and ectoprocts), and a third unnamed clade gathering annelids, nemerteans, and platyhelminthes. Consideration of classical morphological, developmental, and genomic characters in light of this topology indicates secondary loss as a fundamental trend in spiralian evolution.
•Chaetognaths are gnathiferans, the sister group to other spiralians•Lophotrochozoans are divided in three main clades, including Tetraneuralia•A new clade is made of annelids, nemerteans, and platyhelminths•Compositional heterogeneity affects the reconstruction of the protostome tree
Marlétaz et al. used new data and refined methods to improve the phylogenetic placement of chaetognaths, an enigmatic group of marine animals. They relate to gnathiferans, a sister group of other spiralians, and include rotifers and gnathostomulids. Spiralians are subdivided in three main clades (including Tetraneuralia and Lophotrochozoa).
Although it is widely believed that early vertebrate evolution was shaped by ancient whole-genome duplications, the number, timing and mechanism of these events remain elusive. Here, we infer the ...history of vertebrates through genomic comparisons with a new chromosome-scale sequence of the invertebrate chordate amphioxus. We show how the karyotypes of amphioxus and diverse vertebrates are derived from 17 ancestral chordate linkage groups (and 19 ancestral bilaterian groups) by fusion, rearrangement and duplication. We resolve two distinct ancient duplications based on patterns of chromosomal conserved synteny. All extant vertebrates share the first duplication, which occurred in the mid/late Cambrian by autotetraploidization (that is, direct genome doubling). In contrast, the second duplication is found only in jawed vertebrates and occurred in the mid-late Ordovician by allotetraploidization (that is, genome duplication following interspecific hybridization) from two now-extinct progenitors. This complex genomic history parallels the diversification of vertebrate lineages in the fossil record.
Abstract
Hox and ParaHox genes encode transcription factors with similar expression patterns in divergent animals. The
Pdx
(
Xlox
) homeobox gene, for example, is expressed in a sharp spatial domain ...in the endodermal cell layer of the gut in chordates, echinoderms, annelids and molluscs. The significance of comparable gene expression patterns is unclear because it is not known if downstream transcriptional targets are also conserved. Here, we report evidence indicating that a classic transcriptional target of Pdx1 in vertebrates, the
insulin
gene, is a likely direct target of Pdx in Pacific oyster adults. We show that one
insulin
-related gene,
cgILP
, is co-expressed with
cgPdx
in oyster digestive tissue. Transcriptomic comparison suggests that this tissue plays a similar role to the vertebrate pancreas. Using ATAC-seq and ChIP, we identify an upstream regulatory element of the c
gILP
gene which shows binding interaction with cgPdx protein in oyster hepatopancreas and demonstrate, using a cell culture assay, that the oyster Pdx can act as a transcriptional activator through this site, possibly in synergy with NeuroD. These data argue that a classic homeodomain-target gene interaction dates back to the origin of Bilateria.
The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that ...underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects.
Pteropods are planktonic gastropods that are considered as bio-indicators to monitor impacts of ocean acidification on marine ecosystems. In order to gain insight into their adaptive potential to ...future environmental changes, it is critical to use adequate molecular tools to delimit species and population boundaries and to assess their genetic connectivity. We developed a set of target capture probes to investigate genetic variation across their large-sized genome using a population genomics approach. Target capture is less limited by DNA amount and quality than other genome-reduced representation protocols, and has the potential for application on closely related species based on probes designed from one species.
We generated the first draft genome of a pteropod, Limacina bulimoides, resulting in a fragmented assembly of 2.9 Gbp. Using this assembly and a transcriptome as a reference, we designed a set of 2899 genome-wide target capture probes for L. bulimoides. The set of probes includes 2812 single copy nuclear targets, the 28S rDNA sequence, ten mitochondrial genes, 35 candidate biomineralisation genes, and 41 non-coding regions. The capture reaction performed with these probes was highly efficient with 97% of the targets recovered on the focal species. A total of 137,938 single nucleotide polymorphism markers were obtained from the captured sequences across a test panel of nine individuals. The probes set was also tested on four related species: L. trochiformis, L. lesueurii, L. helicina, and Heliconoides inflatus, showing an exponential decrease in capture efficiency with increased genetic distance from the focal species. Sixty-two targets were sufficiently conserved to be recovered consistently across all five species.
The target capture protocol used in this study was effective in capturing genome-wide variation in the focal species L. bulimoides, suitable for population genomic analyses, while providing insights into conserved genomic regions in related species. The present study provides new genomic resources for pteropods and supports the use of target capture-based protocols to efficiently characterise genomic variation in small non-model organisms with large genomes.
Abstract
Bobtail and bottletail squid are small cephalopods with striking anti-predatory defensive mechanisms, bioluminescence, and complex morphology; that inhabit nektobenthic and pelagic ...environments around the world’s oceans. Yet, the evolution and diversification of these animals remain unclear. Here, we used shallow genome sequencing of thirty-two bobtail and bottletail squids to estimate their evolutionary relationships and divergence time. Our phylogenetic analyses show that each of Sepiadariidae, Sepiolidae, and the three subfamilies of the Sepiolidae are monophyletic. We found that the ancestor of the Sepiolinae very likely possessed a bilobed light organ with bacteriogenic luminescence. Sepiolinae forms a sister group to Rossinae and Heteroteuthinae, and split into Indo-Pacific and Atlantic-Mediterranean lineages. The origin of these lineages coincides with the end of the Tethys Sea and the separation of these regions during the Eocene and the beginning of the Oligocene. We demonstrated that sepiolids radiated after the Late Cretaceous and that major biogeographic events might have shaped their distribution and speciation.
Xenacoelomorphs, a group of worms with simple body organization, have been proposed to represent the first offshoot of bilaterians. A new study shows that they might instead belong to the ...deuterostomes, just as echinoderms and vertebrates.
Xenacoelomorphs, a group of worms with simple body organization, have been proposed to represent the first offshoot of bilaterians. A new study shows that they might instead belong to the deuterostomes, just as echinoderms and vertebrates.
Summary
Mangroves are adapted to harsh environments, such as high ultraviolet (UV) light, low nutrition, and fluctuating salinity in coastal zones. However, little is known about the transcriptomic ...and epigenomic basis of the resilience of mangroves due to limited available genome resources.
We performed a de novo genome assembly and in natura epigenome analyses of the mangrove Bruguiera gymnorhiza, one of the dominant mangrove species. We also performed the first genome‐guided transcriptome assembly for mangrove species.
The 309 Mb of the genome is predicted to encode 34 403 genes and has a repeat content of 48%. Depending on its growing environment, the natural B. gymnorhiza population showed drastic morphological changes associated with expression changes in thousands of genes. Moreover, high‐salinity environments induced genome‐wide DNA hypermethylation of transposable elements (TEs) in the B. gymnorhiza. DNA hypermethylation was concurrent with the transcriptional regulation of chromatin modifier genes, suggesting robust epigenome regulation of TEs in the B. gymnorhiza genome under high‐salinity environments.
The genome and epigenome data in this study provide novel insights into the epigenome regulation of mangroves and a better understanding of the adaptation of plants to fluctuating, harsh natural environments.
See also the Commentary on this article by Johannes, 233: 1971–1973.
Bobtail squid are emerging models for host-microbe interactions, behavior, and development, yet their species diversity and distribution remain poorly characterized. Here, we combine mitochondrial ...and transcriptome sequences with morphological analysis to describe three species of bobtail squid (Sepiolidae: Sepiolinae) from the Ryukyu archipelago, and compare them with related taxa. One Ryukyuan type was previously unknown, and is described here as
sp. nov. Another Ryukyuan type is morphologically indistinguishable from
Sasaki, 1913. Molecular analyses, however, place this taxon within the genus
Steenstrup, 1887, and additional morphological investigation led to formal rediagnosis of
and reassignment of this species as
comb. nov. While no adults from the third Ryukyuan type were found, sequences from hatchlings suggest a close relationship with
Reid, 2011, known from Australia and East Timor. The broadly sampled transcriptomes reported here provide a foundation for future phylogenetic and comparative studies.
Abstract
Spiralians represent the least studied superclade of bilaterian animals, despite exhibiting the widest diversity of organisms. Although spiralians include iconic organisms, such as octopus, ...earthworms and clams, a lot remains to be discovered regarding their phylogeny and biology. Here, we review recent attempts to apply single-cell transcriptomics, a new pioneering technology enabling the classification of cell types and the characterisation of their gene expression profiles, to several spiralian taxa. We discuss the methodological challenges and requirements for applying this approach to marine organisms and explore the insights that can be brought by such studies, both from a biomedical and evolutionary perspective. For instance, we show that single-cell sequencing might help solve the riddle of the homology of larval forms across spiralians, but also to better characterise and compare the processes of regeneration across taxa. We highlight the capacity of single-cell to investigate the origin of evolutionary novelties, as the mollusc shell or the cephalopod visual system, but also to interrogate the conservation of the molecular fingerprint of cell types at long evolutionary distances. We hope that single-cell sequencing will open a new window in understanding the biology of spiralians, and help renew the interest for these overlooked but captivating organisms.
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