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Dunn, C. W.

Publications and source records attributed to Dunn, C. W..

11 recordsLinked to original sources

Organisms associated with siphonophores revealed by short-read whole-genome sequencing

Siphonophores are associated with prey, parasites, microbes, and other organisms in the open ocean, but little is known about these siphonophore cobionts. To learn more about them, we investigated molecular bycatch: their DNA captured during siphonophore genome sequencing. We reanalysed 213 specimens of Physalia, Nanomia, Bargmannia and other siphonophores sequenced in four previously published studies. We recovered 104 bacterial genomes forming 32 genome clusters, including recurrent Metamycoplasmataceae and diverse proteobacteria, groups also found with other cnidarians. Bacterial communities differed among Physalia species sampled in the southwestern Pacific. We identified non-siphonophore eukaryotes from ribosomal markers in 38 specimens, including fish and copepods consistent with prey, parasitic flatworms, and Perkinsela-like relatives of amoeba endosymbionts. Alfonsino (Beryx) sequences in one Hawaiian P. utriculus specimen are consistent with capture of pelagic young of deepwater fishes. Molecular bycatch reveals the diversity of siphonophore associates from specimens already collected for genome research.

genomics↗

Argonaute-2 slicing of Rtl1 promotes skeletal muscle development and postnatal survival

Argonaute (AGO) proteins associate with small guide RNAs to bind and repress mRNA targets. AGO2 is the primary AGO slicer in mammals, cleaving RNAs that base-pair extensively to its guide RNA. Disrupting the slicing activity of AGO2 in mice causes neonatal lethality, however, the specific cell types and substrates that contribute to this lethality are not known. Through a combination of genetic, histologic, and molecular approaches, we identify retrotransposon-like-1 (Rtl1) as a key AGO2 slicing substrate in placental endothelium and skeletal muscle, and show that AGO2 slicing in skeletal muscle, but not endothelium, is required for postnatal viability. Loss of AGO2 slicing causes cell-autonomous, pathologic changes in skeletal muscle, characterized by larger fibers, increased central nuclei, prominent central clearings, and induction of transcripts associated with heat shock proteins. Induced expression of RTL1, a domesticated retrotransposon-derived protein that can self-assemble into viral-like capsids, activates a similar heat shock protein response in cultured myoblasts, underscoring the importance of limiting excess RTL1 during muscle development. Taken together, our findings demonstrate a critical role for AGO2 slicing in skeletal muscle development that is, at least in part, due to its repression of a domesticated retrotransposon.

molecular biology↗

From surfacing to stranding: The origins and dispersal dynamics of a neustonic siphonophore

The siphonophore Physalia physalis regularly strands along the US East Coast, yet the dynamics driving its seasonal and geographic distribution in this region remain poorly understood. Building on a new understanding of Physalia population structure from genomic analyses, we integrate iNaturalist observational data with a biologically-informed particle-tracking model to investigate the origins, dispersal, and stranding dynamics of P. physalis in the northwest Atlantic. We identify adult and juvenile observations of stranded P. physalis and initialize particles based on juvenile distributions. Our particle-tracking model incorporates recent research on Physalia drift hydrodynamics and high-resolution environmental data to simulate dispersal over twelve months. Results show a winter juvenile peak within a constrained nursery region encompassing the Straits of Florida and Gulf of Mexico. Simulated P. physalis undergo rapid Gulf Stream transport, with limited nursery region recirculation, indicating a source-sink population dynamic. Large-scale distribution of P. physalis is primarily governed by current-driven advection, while wind and wave processes drive nearshore transport and stranding. Using this framework, we characterize the role of the Gulf Stream and seasonal wind patterns in shaping P. physalis strandings in distinct US East Coast regions. We find that mesoscale eddies influence P. physalis transport in offshore regions and theorize that seasonal Gulf Stream dynamics, including eddy activity and shifts in current position and intensity, modulate strandings north of Cape Hatteras. Our study highlights the Gulf Streams critical role in shaping neustonic distributions in the North Atlantic and the broader transport dynamics that drive dispersal in global Physalia populations.

ecology↗

A Chromosome-Scale Genome of Nanomia septata Reveals Extensive Rearrangement But No Clear Driver of the Unique Colony-Level Organization of Siphonophores

Siphonophores (Cnidaria:Hydrozoa) are pelagic colonial marine invertebrates with many highly specialized bodies (zooids) within a single colony. Their unique biology and ecological importance have made them of particular interest. Recent work revealed siphonophore genomes to be larger than in most other cnidarians. To investigate siphonophores genome biology and develop resources for future studies, we sequenced the genome of a single Nanomia septata to chromosome scale. The haploid genome is 1.5GB across 8 chromosomes, a reduction relative to the 15 chromosomes seen in closely related hydrozoan genomes, and is highly rearranged, consistent with multiple mixing events. Genome expansion occurred through intergenic repeat expansion, with protein-coding genes shorter than in most cnidarians. We found no genomic features clearly associated with siphonophores exceptional colony-level complexity. Gene families that play critical roles in cnidarian development have not expanded, and gene proximity was not generally correlated to their expression across zooids, except in male gonophores. To contextualize these observations, we genome sequenced 20 additional Nanomia specimens across the globe and mapped them to our chromosome-scale reference. Population genomic analyses support three previously recognized species of Nanomia, and at least one additional undescribed species. Overlapping geographic distribution of some Nanomia species suggest reproductive isolation in sympatry. Phylogenetic analyses of genome size indicate Nanomia septata and Nanomia cara have similarly large genomes between 1.5-1.7GB, while Nanomia bijuga and an undescribed species show a secondary reduction to 0.7GB. These results highlight how genomic factors have shaped colony organization and genome diversity within Nanomia.

genomics↗

Giants among Cnidaria: large nuclear genomes and rearranged mitochondrial genomes in siphonophores

Siphonophores (Cnidaria:Hydrozoa) are abundant predators found throughout the ocean and are important components in worldwide zooplankton. They range in length from a few centimeters to tens of meters. They are gelatinous, fragile, and difficult to collect, so many aspects of the biology of these 190 species remain poorly understood. To survey siphonophore genome diversity, we performed Illumina sequencing of 32 species sampled broadly across the phylogeny. Sequencing depth was sufficient to estimate nuclear genome size from k-mer spectra in 8 specimens, ranging from 0.7-4.8Gb. In 6 specimens we got heterozygosity estimates between 0.7-5.3%. Rarefaction analyses indicate k-mer peaks can be absent with as much as 30x read coverage, suggesting minimum genome sizes range from 1.0-3.8Gb in the remaining 27 samples without k-mer peaks. This work confirms most siphonophore nuclear genomes are large, but also identifies several with reduced size that are tractable targets for future siphonophore nuclear genome assembly projects. We also assembled mitochondrial genomes for 32 specimens from these new data, indicating a conserved gene order among Hydrozoa, Cystonectae and some Physonectae, also revealing the ancestral gene organization of siphonophores. There then was extensive rearrangement of mitochondrial genomes within other physonects and in Calycophorae, including the repeated loss of atp8. Though siphonophores comprise a small fraction of cnidarian species, this survey greatly expands our understanding of cnidarian genome diversity. This study further illustrates both the importance of deep phylogenetic sampling and the utility of Illumina genome skimming in understanding genomic diversity of a clade. SignificanceDescriptions of basic genome features, such as nuclear genome size and mitochondrial genome sequences, remain sparse across many clades in the tree of life, leading to over generalizations from very small sample sizes and often limiting selection of optimal species for genome assembly efforts. Here we use Illumina genome skimming to assess a variety of genome features across 35 siphonophores (Cnidaria). This deep dive within a single clade identifies six species that are optimal candidates of future genomic work, and reveals greater range in nuclear genome size and diversity of mitochondrial genome orders within siphonophores than had been described across all Cnidaria.

evolutionary biology↗

Evolution of gene expression across species and specialized zooids in Siphonophora

BackgroundSiphonophores are complex colonial animals, consisting of asexually-produced bodies (called zooids) that are functionally specialized for specific tasks, including feeding, swimming, and sexual reproduction. Though this extreme functional specialization has captivated biologists for generations, its genomic underpinnings remain unknown. We use RNA-seq to investigate gene expression patterns in five zooids and one specialized tissue (pneumatophore) across seven siphonophore species. Analyses of gene expression across species present several challenges, including identification of comparable expression changes on gene trees with complex histories of speciation, duplication, and loss. Here, we conduct three analyses of expression. First, we examine gene expression within species. Then, we conduct classical analyses examining expression patterns between species. Lastly, we introduce Speciation Branch Filtering, which allows us to examine the evolution of expression in a phylogenetic framework. ResultsWithin and across species, we identified hundreds of zooid-specific and species-specific genes, as well as a number of putative transcription factors showing differential expression in particular zooids and developmental stages. We found that gene expression patterns tended to be largely consistent in zooids with the same function across species, but also some large lineage-specific shifts in gene expression. ConclusionsOur findings show that patterns of gene expression have the potential to define zooids in colonial organisms. We also show that traditional analyses of the evolution of gene expression focus on the tips of gene phylogenies, identifying large-scale expression patterns that are zooid or species variable. The new explicit phylogenetic approach we propose here focuses on branches (not tips) offering a deeper evolutionary perspective into specific changes in gene expression within zooids along all branches of the gene (and species) trees.

evolutionary biology↗

Rooting the animal tree of life

There has been considerable debate about the placement of the root in the animal tree of life, which has emerged as one of the most challenging problems in animal phylogenetics. This debate has major implications for our understanding of the earliest events in animal evolution, including the origin of the nervous system. Some phylogenetic analyses support a root that places the first split in the phylogeny of living animals between sponges and all other animals (the Porifera-sister hypothesis), and others find support for a split between comb jellies and all other animals (Ctenophora-sister). These analyses differ in many respects, including in the genes considered, species considered, molecular evolution models, and software. Here we systematically explore the rooting of the animal tree of life under consistent conditions by synthesizing data and results from 15 previous phylogenomic studies and performing a comprehensive set of new standardized analyses. It has previously been suggested that site-heterogeneous models favor Porifera-sister, but we find that this is not the case. Rather, Porifera-sister is only obtained under a narrow set of conditions when the number of site-heterogeneous categories is unconstrained and range into the hundreds. Site-heterogenous models with a fixed number of dozens of categories support Ctenophora-sister, and cross-validation indicates that such models fit the data just as well as the unconstrained models. Our analyses shed light on an important source of variation between phylogenomic studies of the animal root. The datasets and analyses consolidated here will also be a useful test-platform for the development of phylogenomic methods for this and other difficult problems.

evolutionary biology↗

The Evolution of Siphonophore Tentilla as Specialized Tools for Prey Capture

Predator specialization has often been considered an evolutionary dead-end due to the constraints associated with the evolution of morphological and functional optimizations throughout the organism. However, in some predators, these changes are localized in separate structures dedicated to prey capture. One of the most extreme cases of this modularity can be observed in siphonophores, a clade of pelagic colonial cnidarians that use tentilla (tentacle side branches armed with nematocysts) exclusively for prey capture. Here we study how siphonophore specialists and generalists evolve, and what morphological changes are associated with these transitions. To answer these questions, we: (1) measured 29 morphological characters of tentacles from 45 siphonophore species, (2) mapped these data to a phylogenetic tree, and (3) analyzed the evolutionary associations between morphological characters and prey type data from the literature. Instead of a dead-end, we found that siphonophore specialists can evolve into generalists, and that specialists on one prey type have directly evolved into specialists on other prey types. Our results show that siphonophore tentillum morphology has strong evolutionary associations with prey type, and suggest that shifts between prey types are linked to shifts in the morphology, mode of evolution, and genetic correlations of tentilla and their nematocysts. The evolutionary history of siphonophore specialization helps build a broader perspective on predatory niche diversification via morphological innovation and evolution. These findings contribute to understanding how specialization and morphological evolution have shaped present-day food webs. Significance StatementPredatory specialization is often associated with the evolution of modifications in the morphology of the prey capture apparatus. Specialization has been considered an evolutionary dead-end due to the constraints associated with these morphological changes. However, in predators like siphonophores, armed with modular structures used exclusively for prey capture, this assumption is challenged. Our results show that siphonophores can evolve generalism and new prey-type specializations by modifying the morphological states, modes of evolution, and genetic correlations between the parts of their prey capture apparatus. These findings demonstrate how studying open-ocean non-bilaterian predators can reveal novel patterns and mechanisms in the evolution of specialization. Understanding these evolutionary processes is fundamental to the study of food-web structure and complexity.

evolutionary biology↗

Morphology and development of the Portuguese man of war, Physalia physalis

The Portuguese man of war, Physalia physalis, is a siphonophore that uses a gas-filled float as a sail to catch the wind. It is one of the most conspicuous, but poorly understood members of the pleuston, a community of organisms that occupy a habitat at the sea-air interface. The development, morphology, and colony organization of P. physalis is very different from all other siphonophores. Here, we propose a framework for homologizing the axes with other siphonophores, and also suggest that the tentacle bearing zooids should be called tentacular palpons. We also look at live and fixed larval and non-reproductively mature juvenile specimens, and use optical projection tomography to build on existing knowledge about the morphology and development of this species. Previous descriptions of P. physalis larvae, especially descriptions of budding order, were often framed with the mature colony in mind. However, we use the simpler organization of larvae and the juvenile specimens to inform our understanding of the morphology, budding order, and colony organization in the mature specimen. Finally, we review what is known about the ecology and lifecyle of P. physalis.

zoology↗

Improved phylogenetic resolution within Siphonophora (Cnidaria) with implications for trait evolution

Siphonophores are a diverse group of hydrozoans (Cnidaria) that are found at all depths of the ocean - from the surface, like the familiar Portuguese man of war, to the deep sea. Siphonophores play an important role in ocean ecosystems, and are among the most abundant gelatinous predators. A previous phylogenetic study based on two ribosomal RNA genes provided insight into the internal relationships between major siphonophore groups, however there was little support for many deep relationships within the clade Codonophora. Here, we present a new siphonophore phylogeny based on new transcriptome data from 30 siphonophore species analyzed in combination with 13 publicly available genomic and transcriptomic datasets. We use this new phylogeny to reconstruct several traits that are central to siphonophore biology, including sexual system (monoecy vs. dioecy), gain and loss of zooid types, life history traits, and habitat. The phylogenetic relationships in this study are largely consistent with the previous phylogeny, but we find strong support for new clades within Codonophora that were previously unresolved. These results have important implications for trait evolution within Siphonophora, including favoring the hypothesis that monoecy arose twice.

evolutionary biology↗

Pairwise comparisons are problematic when analyzing functional genomic data across species

AbstractThere 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 be more similar 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 they reflect species relationships. These reanalyses concretely demonstrate 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.\n\nSignificanceComparisons of genome function between species are providing important insight into the evolutionary origins of diversity. Here we demonstrate that comparative functional genomics studies can come to the wrong conclusions if they do not take the relationships of species into account and instead rely on pairwise comparisons between species, as is common practice. We re-examined two previously published studies and found problems with pairwise comparisons that draw both their original conclusions into question. One study had found support for the ortholog conjecture and the other had concluded that the evolution of gene expression was different between animal phyla than within them. Our results demonstrate that to answer evolutionary questions about genome function, it is critical to consider evolutionary relationships.

genomics↗