Ancient gene linkages support ctenophores as sister to other animals

A central question in evolutionary biology is whether sponges or ctenophores (comb jellies) are the sister group to all other animals. These alternative phylogenetic hypotheses imply different scenarios for the evolution of complex neural systems and other animal-specific traits1,2,3,4,5,6. Conventional phylogenetic approaches based on morphological characters and increasingly extensive gene sequence collections have not been able to definitively answer this question7,8,9,10,11. Here we develop chromosome-scale gene linkage, also known as synteny, as a phylogenetic character for resolving this question12. We report new chromosome-scale genomes for a ctenophore and two marine sponges, and for three unicellular relatives of animals (a choanoflagellate, a filasterean amoeba and an ichthyosporean) that serve as outgroups for phylogenetic analysis. We find ancient syntenies that are conserved between animals and their close unicellular relatives. Ctenophores and unicellular eukaryotes share ancestral metazoan patterns, whereas sponges, bilaterians, and cnidarians share derived chromosomal rearrangements. Conserved syntenic characters unite sponges with bilaterians, cnidarians, and placozoans in a monophyletic clade to the exclusion of ctenophores, placing ctenophores as the sister group to all other animals. The patterns of synteny shared by sponges, bilaterians, and cnidarians are the result of rare and irreversible chromosome fusion-and-mixing events that provide robust and unambiguous phylogenetic support for the ctenophore-sister hypothesis. These findings provide a new framework for resolving deep, recalcitrant phylogenetic problems and have implications for our understanding of animal evolution.journal articl

Conserved novel ORFs in the mitochondrial genome of the ctenophore Beroe forskalii

To date, five ctenophore species’ mitochondrial genomes have been sequenced, and each contains open reading frames (ORFs) that if translated have no identifiable orthologs. ORFs with no identifiable orthologs are called unidentified reading frames (URFs). If truly protein-coding, ctenophore mitochondrial URFs represent a little understood path in early-diverging metazoan mitochondrial evolution and metabolism. We sequenced and annotated the mitochondrial genomes of three individuals of the beroid ctenophore Beroe forskalii and found that in addition to sharing the same canonical mitochondrial genes as other ctenophores, the B. forskalii mitochondrial genome contains two URFs. These URFs are conserved among the three individuals but not found in other sequenced species. We developed computational tools called pauvre and cuttlery to determine the likelihood that URFs are protein coding. There is evidence that the two URFs are under negative selection, and a novel Bayesian hypothesis test of trinucleotide frequency shows that the URFs are more similar to known coding genes than noncoding intergenic sequence. Protein structure and function prediction of all ctenophore URFs suggests that they all code for transmembrane transport proteins. These findings, along with the presence of URFs in other sequenced ctenophore mitochondrial genomes, suggest that ctenophores may have uncharacterized transmembrane proteins present in their mitochondria

Chromosome-Scale Genomes, Resolving the Sister Phylum to Other Animals, and Novel Bioluminescent Systems.

Understanding how animals evolved from unicellular life requires comprehensive analyses that sample all animal phyla. However, some major outstanding questions in evolutionary biology, such as the evolutionary provenance of neurons, developmental pathways, and animal-specific genes, remain unanswered for one reason: it is unclear whether sponges (phylum Porifera) or ctenophores (phylum Ctenophora) as the sister phylum to all other animals. Here, we resolved this question using a chromosome-scale, whole-genome comparative approach. First, we generated chromosome-scale genomes of ctenophore species, and of three species that are unicellular, and outgroups to the Metazoa. By comparing these genomes to other chromosome-scale animal genomes, we identified groupings of genes that have persisted together on the same chromosomes since the common ancestor of the Filozoa, more than one billion years ago. We track the fate of these linked genes in the genomes of extant species, and find irreversible chromosomal fusions-with-mixing that preclude sponges from being the sister phylum to other animals. Thus, ctenophores must be the sister phylum to other animals.As a parallel effort, we sought to use transcriptomics and genomics to study a trait that is common to many of the marine species that we studied above: bioluminescence. Light-emitting luciferase proteins are a useful tool for visualizing sub-cellular processes in microscopy, and are an interesting case of convergent evolution in over fifty clades. We used transcriptomics, full-length cDNA sequencing, and protein purification techniques to identify a novel luciferase in the polychaete worm Odontosylllis undecimdonta. This luciferase appears to be specific to the genus Odontosyllis, and there is no evidence for homologs in the transcriptomes of other polychaetes. In addition to the polychate luminescence, we also identified luminescence in a species of deep-sea sponge. This finding is significant, as reports of sponge luminescence in the past have been dubious. We used a biochemical approach to identify the luminous small molecule, coelenterazine, that is used in the bioluminescence reaction. A metagenomics sequencing approach revealed that the sponge sample contained little to no bacteria, and therefore the luminescence produced by the sponge was likely endogenous. Future efforts will focus on genome sequencing, and identifying the luciferase, to determine if the luciferase is truly encoded in the sponge genome

conchoecia/beroe_forskalii_mitogenome: 20171226 release

20171226 release of Beroe forskalii mitogenome annotation documents

The complete mitochondrial genome of Dascyllus trimaculatus (Rüppell, 1829)

Damselfishes (family Pomacentridae) comprise approximately 400 species that play an important ecological role in temperate and coral reefs. Here, for the first time, we assemble and annotate the mitochondrial genome of Dascyllus trimaculatus, the three-spot dascyllus, a planktivorous damselfish that primarily recruits in anemones. The circular genome of D. trimaculatus is 16,967 bp in length and contains 13 protein-coding genes, 22 transfer RNA genes, two ribosomal RNA genes, and a control region. Gene arrangement and codon usage is similar to reported mitochondrial genomes of other damselfish genera, and a phylogenetic analysis of a set of damselfish representatives is consistent with known evolutionary analyses

Chromosome-level genome of the three-spot damselfish, Dascyllus trimaculatus

Damselfishes (Family: Pomacentridae) are a group of ecologically important, primarily coral reef fishes that include over 400 species. Damselfishes have been used as model organisms to study recruitment (anemonefishes), the effects of ocean acidification (spiny damselfish), population structure, and speciation (Dascyllus). The genus Dascyllus includes a group of small-bodied species, and a complex of relatively larger bodied species, the Dascyllus trimaculatus species complex that is comprised of several species including D. trimaculatus itself. The three-spot damselfish, D. trimaculatus, is a widespread and common coral reef fish species found across the tropical Indo-Pacific. Here, we present the first-genome assembly of this species. This assembly contains 910 Mb, 90% of the bases are in 24 chromosome-scale scaffolds, and the Benchmarking Universal Single-Copy Orthologs score of the assembly is 97.9%. Our findings confirm previous reports of a karyotype of 2n = 47 in D. trimaculatus in which one parent contributes 24 chromosomes and the other 23. We find evidence that this karyotype is the result of a heterozygous Robertsonian fusion. We also find that the D. trimaculatus chromosomes are each homologous with single chromosomes of the closely related clownfish species, Amphiprion percula. This assembly will be a valuable resource in the population genomics and conservation of Damselfishes, and continued studies of the karyotypic diversity in this clade

Laboratory culture of the California Sea Firefly Vargula tsujii (Ostracoda: Cypridinidae): Developing a model system for the evolution of marine bioluminescence

© 2020, The Author(s). Bioluminescence, or the production of light by living organisms via chemical reaction, is widespread across Metazoa. Laboratory culture of bioluminescent organisms from diverse taxonomic groups is important for determining the biosynthetic pathways of bioluminescent substrates, which may lead to new tools for biotechnology and biomedicine. Some bioluminescent groups may be cultured, including some cnidarians, ctenophores, and brittle stars, but those use luminescent substrates (luciferins) obtained from their diets, and therefore are not informative for determination of the biosynthetic pathways of the luciferins. Other groups, including terrestrial fireflies, do synthesize their own luciferin, but culturing them is difficult and the biosynthetic pathway for firefly luciferin remains unclear. An additional independent origin of endogenous bioluminescence is found within ostracods from the family Cypridinidae, which use their luminescence for defense and, in Caribbean species, for courtship displays. Here, we report the first complete life cycle of a luminous ostracod (Vargula tsujii Kornicker & Baker, 1977, the California Sea Firefly) in the laboratory. We also describe the late-stage embryogenesis of Vargula tsujii and discuss the size classes of instar development. We find embryogenesis in V. tsujii ranges from 25–38 days, and this species appears to have five instar stages, consistent with ontogeny in other cypridinid lineages. We estimate a complete life cycle at 3–4 months. We also present the first complete mitochondrial genome for Vargula tsujii. Bringing a luminous ostracod into laboratory culture sets the stage for many potential avenues of study, including learning the biosynthetic pathway of cypridinid luciferin and genomic manipulation of an autogenic bioluminescent system

Image5_Speciation of pelagic zooplankton: Invisible boundaries can drive isolation of oceanic ctenophores.pdf

The study of evolution and speciation in non-model systems provides us with an opportunity to expand our understanding of biodiversity in nature. Connectivity studies generally focus on species with obvious boundaries to gene flow, but in open-ocean environments, such boundaries are difficult to identify. Due to the lack of obvious boundaries, speciation and population subdivision in the pelagic environment remain largely unexplained. Comb jellies (Phylum Ctenophora) are mostly planktonic gelatinous invertebrates, many of which are considered to have freely interbreeding distributions worldwide. It is thought that the lobate ctenophore Bolinopsis infundibulum is distributed throughout cooler northern latitudes and B. vitrea warmer. Here, we examined the global population structure for species of Bolinopsis with genetic and morphological data. We found distinct evolutionary patterns within the genus, where B. infundibulum had a broad distribution from northern Pacific to Atlantic waters despite many physical barriers, while other species were geographically segregated despite few barriers. Divergent patterns of speciation within the genus suggest that oceanic currents, sea-level, and geological changes over time can act as either barriers or aids to dispersal in the pelagic environment. Further, we used population genomic data to examine evolution in the open ocean of a distinct lineage of Bolinopsis ctenophores from the North Eastern Pacific. Genetic information and morphological observations validated this as a separate species, Bolinopsis microptera, which was previously described but has recently been called B. infundibulum. We found that populations of B. microptera from California were in cytonuclear discordance, which indicates a secondary contact zone for previously isolated populations. Discordance at this scale is rare, especially in a continuous setting.</p