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Haddock, S. H. D.

Publications and source records attributed to Haddock, S. H. D..

5 recordsLinked to original sources

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↗

Global genomics of the man-o'-war (Physalia) reveal biodiversity at the ocean surface

The open ocean is a vast, highly connected environment, and the organisms found there have been hypothesized to represent massive, well-mixed populations. Of these, the Portuguese man-o-war (Physalia) is uniquely suited to dispersal, sailing the ocean surface with a muscular crest. We tested the hypothesis of a single, panmictic Physalia population by sequencing 133 genomes, and found five distinct lineages, with multiple lines of evidence showing strong reproductive isolation despite range overlap. We then scored thousands of citizen-science photos and identified four recognizable morphologies linked to these lineages. Within lineages, we detected regionally endemic subpopulations, connected by winds and currents, and identified individual long-distance dispersal events. We find that, even in these sailing species, genetic variation is highly partitioned geographically across the open ocean. SummaryThe open ocean is a vast and highly connected environment. The organisms that live there have a significant capacity for dispersal and few geographic boundaries to separate populations. Of these, the Portuguese man-o-war or bluebottle (genus Physalia) is uniquely suited to long-distance travel, using its gas-filled float and muscular crest to catch the wind and sail the sea surface. Physalia are distributed across the globe, and like many pelagic organisms, have been hypothesized to represent a massive, well-mixed population that extends across ocean basins. We tested this hypothesis by sequencing whole genomes of 133 samples collected from waters of over a dozen countries around the globe. Our results revealed five distinct lineages, with multiple lines of evidence indicating strong reproductive isolation, despite regions of range overlap. We combined these data with an independent dataset of thousands of images of Physalia uploaded to the citizen-science website inaturalist.org, which we scored for morphological characters including sail size, tentacle arrangement, and color. From these images, we identified four recognizable morphologies, described their geographical distribution, and linked them to four of the lineages identified with genomic data. We conclude there are at least four species, three of which correspond to species proposed by scientists in the 18th and 19th centuries: P. physalis, P utriculus, and P. megalista, along with one as yet unnamed species Physalia sp. from the Tasman Sea. Within each species, we observe significant population structure, with evidence of persistent subpopulations at a regional scale, as well as evidence for individual long-distance dispersal events. Our findings indicate that, instead of one well-mixed, cosmopolitan species, there are in fact multiple Physalia species with distinct but overlapping ranges, each made up of regionally endemic subpopulations that are connected by major ocean currents and wind patterns.

zoology↗

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↗

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↗

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↗