Shannon B. Johnson

Monterey Bay Aquarium Research Institute

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Robert C. Vrijenhoek

Monterey Bay Aquarium Research Institute

Greg W. Rouse

Scripps Institution of Oceanography

Verena Tunnicliffe

University of Victoria

Shana K. Goffredi

Occidental College

Lonny Lundsten

Monterey Bay Aquarium Research Institute

Corinna Breusing

University of Rhode Island

Craig M. Young

University of Oregon

Anders Warén

Swedish Museum of Natural History

Julio B.J. Harvey

University of California, Santa Cruz

Lynne M. Christianson

Monterey Bay Aquarium Research Institute

Cooperative Institutions

Monterey Bay Aquarium Research Institute

Rutgers, The State University of New Jersey

University of California, San Diego

Oceanography Society

Moss Landing Marine Laboratories

Scripps Institution of Oceanography

University of California, Santa Cruz

Woods Hole Oceanographic Institution

National Oceanic and Atmospheric Administration

University of Hawaiʻi at Mānoa

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Population structure and connectivity in Indo-Pacific deep-sea mussels of the Bathymodiolus septemdierum complex

Conservation Genetics (2015)

Corinna Breusing Shannon B. Johnson Verena Tunnicliffe Robert C. Vrijenhoek

Abstract Current pressures to mine polymetallic sulfide deposits pose threats to the animal communities found at deep-sea hydrothermal vents. Management plans aimed at preserving these unusual communities require knowledge of historical and contemporary forces that shaped the distributions and connectivity of associated species. As most vent research has focused on the eastern Pacific and mid-Atlantic ridge systems less is known about Indo-Pacific vents, where mineral extraction activities are imminent. Deep-sea mussels (Bivalvia: Mytilidae) of the genus Bathymodiolus include the morphotypic species B. septemdierum , B. brevior , B. marisindicus , and B. elongatus which are among the dominant vent taxa in western Pacific back-arc basins and the Central Indian Ridge. To assess their interpopulational relationships, we examined multilocus genotypes based on DNA sequences from four nuclear and four mitochondrial genes, and allozyme variation encoded by eleven genes. Bayesian assignment methods grouped mussels from seven widespread western Pacific localities into a single cluster, whereas the Indian Ocean mussels were clearly divergent. Thus, we designate two regional metapopulations. Notably, contemporary migration rates among all sites appeared to be low despite limited population differentiation, which highlights the necessity of obtaining realistic data on recovery times and fine-scale population structure to develop and manage conservation units effectively. Future studies using population genomic methods to address these issues in a range of species will help to inform management plans aimed at mitigating potential impacts of deep-sea mining in the Indo-Pacific region.

Indo-Pacific

10.1007/s10592-015-0750-0

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Citations (46)

Hidden diversity of Ctenophora revealed by new mitochondrial COI primers and sequences

Authorea (Authorea) (2021)

Lynne M. Christianson Shannon B. Johnson Darrin T. Schultz Steven H. D. Haddock

The mitochondrial gene cytochrome-c-oxidase subunit 1 (COI) is useful in many taxa for phylogenetics, population genetics, metabarcoding, and rapid species identifications. However, the phylum Ctenophora (comb jellies) has historically been difficult to study due to divergent mitochondrial sequences and the corresponding inability to amplify COI with degenerate and standard COI ‘barcoding’ primers. As a result, there are very few COI sequences available for ctenophores, despite over 200 described species in the phylum. Here, we designed new primers and amplified the COI fragment from members of all major groups of ctenophores, including many undescribed species. Phylogenetic analyses of the resulting COI sequences revealed high diversity within many groups that was not evident from more conserved 18S rDNA sequences, in particular among the Lobata. The COI phylogenetic results also revealed unexpected community structure within the genus Bolinopsis , suggested new species within the genus Bathocyroe , and supported the ecological and morphological differences of some species such as Lampocteis cruentiventer and similar lobates ( Lampocteis sp. ‘V’ stratified by depth, and ‘A’ differentiated by color). The newly described primers reported herein provide important tools to enable researchers to illuminate the diversity of ctenophores worldwide via quick molecular identifications, improve the ability to analyze environmental DNA by improving reference libraries and amplifications, and enable a new breadth of population genetic studies.

DNA Barcoding

10.22541/au.161516405.50876931/v1

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The morphological diversity of Osedax worm borings (Annelida: Siboglinidae)

Journal of the Marine Biological Association of the United Kingdom (2014)

Nicholas D. Higgs Adrian G. Glover Thomas G. Dahlgren Craig R. Smith Yoshihiro Fujiwara

Marine worms in the genus Osedax , have specialized ‘root’ tissues used to bore into the bones of decomposing vertebrate skeletons and obtain nutrition. We investigated the borings of nine Osedax species, using micro computed tomography to quantitatively describe the morphology of the borings and provide three-dimensional reconstructions of the space occupied by Osedax root tissues inside the bone. Each Osedax species displayed a consistent boring morphology in any given bone, but these differed between bones. In bones where multiple species coexisted there was limited evidence for spatial niche partitioning by Osedax root tissues inside the bones investigated here. The new morphological data may be applied to Osedax traces in fossil bones, showing that borings can be used to indicate minimum species richness in these bones.

10.1017/s0025315414000770

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Scanning Electron Microscopic Aids for Identification of Larval and Post-Larval Bivalves

Journal of Shellfish Research (2018)

Richard A. Lutz Jacob D. Goodwin Brad S. Baldwin Gavin Burnell Michael Castagna

The identification of bivalve larvae and early postlarvae in plankton and benthic samples has long been a challenge, hampering both basic and applied research efforts in marine, estuarine, and freshwater environments. The usefulness of published optical micrographs of the early life-history stages of bivalves is limited because of the great morphological similarity of the imaged articulated shells, particularly at the early (straight-hinge) developmental stages. While a number of techniques have been refined in recent years and show promise for use in routine identifications of larval and post-larval bivalves (e.g., single-step nested multiplex polymerase chain reaction; in situ hybridization protocols through color coding with taxon-specific, dye-labeled DNA probes; coupled fluorescence in situ hybridization and cell sorting; and image analysis techniques using species-specific shell birefringence patterns under polarized light), no adequate comprehensive reference source exists that accurately depicts the morphology and morphometry of the shells of larval and post-larval stages of target bivalve species in a consistent format to assist in identification of such stages. To this end, scanning electron micrograph (SEM) sequences are presented of the disarticulated shell valves of laboratory-reared larval and post-larval stages of 56 species of bivalve molluscs from a wide spectrum of marine, estuarine, and freshwater habitats. Emphasis is placed on the usefulness of the morphology and morphometrics of consistently-oriented, disarticulated shell valves and associated hinge structures in discriminating the early life-history stages of these various bivalve species. Although the scanning electron micrograph sequences presented accurately depict the gross morphologies/ morphometrics and hinge structures of the disarticulated shell valves of the larvae and/or postlarvae of the 56 species of bivalves, it is important to emphasize that a scanning electron microscope is not necessary to observe even fine hinge structures associated with the early ontogenetic stages of these species. Such structures are readily visible using a wide range of optical compound microscopes equipped with high-intensity reflected light sources, although the disarticulated shell valves must be viewed in several planes of focus to discern the often subtle details seen clearly in the scanning electron micrographs. These morphological characters provide researchers with invaluable aids for the routine identification of the early life-history stages of these species isolated from plankton and benthic samples.

Marine invertebrates

10.2983/035.037.0202

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Optical Imaging and Molecular Sequencing of a Preserved Collection of Bivalve Larvae

Journal of Shellfish Research (2018)

Jacob D. Goodwin Richard A. Lutz Shannon B. Johnson Victor S. Kennedy Scott M. Gallager

From the 1980s through 1995, scientists at numerous marine, coastal, estuarine, and freshwater laboratories spawned bivalves to provide larvae for use in identifying species based on larval hinge structures and gross shell morphometry. These larvae were preserved in 95% ethanol and stored in sample vials, many of which dried out over the years. Advantage was taken of 50 of 56 species from this collection (and two additional species that were not in the collection for a total of 52 species) to explore the use of optical techniques (polarized light and a full-wave compensation plate) to highlight birefringence patterns of larval shells to discriminate individual species. Representative images of various developmental stages of 77% (40/52) of the larval bivalve species in the collection were successfully imaged. Similarities across birefringence patterns were observed at the taxonomic ordinal and familial level. Molecular polymerase chain reaction techniques were used in an effort to sequence many of the dried-out specimens and they successfully identified 19% (10/52) of the larval bivalve species with matches in GenBank. Here it has been demonstrated that optical techniques are efficient for imaging dried-out larval bivalve shells for classification purposes and we present successful sequences of 10 species of bivalve larvae from the preserved collection.

Marine species

10.2983/035.037.0203

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Bone‐eating Osedax females and their ‘harems’ of dwarf males are recruited from a common larval pool

Molecular Ecology (2008)

Robert C. Vrijenhoek Shannon B. Johnson Greg W. Rouse

Abstract Extreme male dwarfism occurs in Osedax (Annelida: Siboglinidae), marine worms with sessile females that bore into submerged bones. Osedax are hypothesized to use environmental sex determination, in which undifferentiated larvae that settle on bones develop as females, and subsequent larvae that settle on females transform into dwarf males. This study addresses several hypotheses regarding possible recruitment sources for the males: (i) common larval pool — males and females are sampled from a common pool of larvae; (ii) neighbourhood — males are supplied by a limited number of neighbouring females; and (iii) arrhenotoky — males are primarily the sons of host females. Osedax rubiplumus were sampled from submerged whalebones located at 1820‐m and 2893‐m depths in Monterey Bay, California. Immature females typically did not host males, but mature females maintained male ‘harems’ that grew exponentially in the number of males as female size increased. Allozyme analysis of the females revealed binomial proportions of nuclear genotypes, an indication of random sexual mating. Analysis of mitochondrial DNA sequences from the male harems and their host females allowed us to reject the arrhenotoky and neighbourhood hypotheses for male recruitment. No significant partitioning of mitochondrial diversity existed between the male and female sexes, or between subsamples of worms collected at different depths or during different years (2002–2007). Mitochondrial sequence diversity was very high in these worms, suggesting that as many as 10 6 females contributed to a common larval pool from which the two sexes were randomly drawn.

10.1111/j.1365-294x.2008.03937.x

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Citations (33)

Mobile autonomous process sampling within coastal ocean observing systems

Limnology and Oceanography Methods (2010)

John P. Ryan Shannon B. Johnson Alana Sherman Kanna Rajan Frédéric Py

Predicting when and where key oceanic processes will be encountered is problematic in dynamic coastal waters where diverse physical, chemical, and biological factors interact in varied and rapidly changing combinations. Defining key processes often requires efficient sampling of specific water masses and prompt sample return for subsequent analyses. This compound challenge motivated our efforts to develop mobile autonomous process sampling (MAPS) for use with autonomous underwater vehicles (AUVs). With this system, features are recognized by artificial intelligence that integrates AUV sensor data to estimate probabilistic states for adaptive control of survey navigation and triggering of targeted water samplers. To demonstrate the utility of the MAPS/AUV system, we focused on intermediate nepheloid layers (INLs), episodic transport events that may play a role in zooplankton ecology. During multiple field tests in Monterey Bay, California, the MAPS/AUV system recognized, mapped, and sampled INLs. Invertebrate larvae contained in the water samples were subsequently characterized with molecular probes developed for high‐throughput screening. Preliminary results support the hypothesis that INLs function as vehicles for episodic larval transport. Applying MAPS within a greater coastal ocean observing system permitted description of regional oceanographic dynamics that influenced the patterns and scales of INL and larval transport.

Adaptive sampling

10.4319/lom.2010.8.394

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Citations (58)

Speciation of pelagic zooplankton: Invisible boundaries can drive isolation of oceanic ctenophores

Frontiers in Genetics (2022)

Shannon B. Johnson Jacob R. Winnikoff Darrin T. Schultz Lynne M. Christianson Wyatt L. Patry

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.

Reproductive isolation

Genetic algorithm

Lineage (genetic)

10.3389/fgene.2022.970314

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Atolla reynoldsi sp. nov. (Cnidaria, Scyphozoa, Coronatae, Atollidae): A New Species of Coronate Scyphozoan Found in the Eastern North Pacific Ocean

Animals (2022)

George I. Matsumoto Lynne M. Christianson Bruce H. Robison Steven H. D. Haddock Shannon B. Johnson

We have observed and collected unusual specimens of what we recognize as undescribed types of the genus Atolla over the past 15 years. Of these, there appear to be three potentially different types. One of these has now been genetically sequenced and compared both morphologically and molecularly with five other Atolla species that have been found in the eastern Pacific. This new variant is so morphologically distinct from other previously described Atolla species that we believe it can be described as a new species, Atolla reynoldsi sp. nov. This species along with two additional types may comprise a new genus. It is also clear that a more accurate and diagnostic morphological key for the genus Atolla needs to be developed. This paper will also provide some potential starting points for a new key to the genus.

Scyphozoa

Hydrozoa

10.3390/ani12060742

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Citations (7)

Genetic Diversity and Potential Function of Microbial Symbionts Associated with Newly Discovered Species of Osedax Polychaete Worms

Applied and Environmental Microbiology (2007)

Shana K. Goffredi Shannon B. Johnson Robert C. Vrijenhoek

ABSTRACT We investigated the genetic diversity of symbiotic bacteria associated with two newly discovered species of Osedax from Monterey Canyon, CA, at 1,017-m ( Osedax Monterey Bay sp. 3 “rosy” [ Osedax sp. MB3]) and 381-m ( Osedax Monterey Bay sp. 4 “yellow collar”) depths. Quantitative PCR and clone libraries of 16S rRNA gene sequences identified differences in the compositions and abundances of bacterial phylotypes associated with the newly discovered host species and permitted comparisons between adult Osedax frankpressi and juveniles that had recently colonized whalebones implanted at 2,891 m. The newly discovered Osedax species hosted Oceanospirillales symbionts that are related to Gammaproteobacteria associated with the previously described O. frankpressi and Osedax rubiplumus (S. K. Goffredi, V. J. Orphan, G. W. Rouse, L. Jahnke, T. Embaye, K. Turk, R. Lee, and R. C. Vrijenhoek, Environ. Microbiol. 7:1369-1378, 2005). In addition, Osedax sp. MB3 hosts a diverse and abundant population of additional bacteria dominated by Epsilonproteobacteria . Ultrastructural analysis of symbiont-bearing root tissues verified the enhanced microbial diversity of Osedax sp. MB3. Root tissues from the newly described host species and O. frankpressi all exhibited collagenolytic enzyme activity, which covaried positively with the abundance of symbiont DNA and negatively with mean adult size of the host species. Members of this unusual genus of bone-eating worms may form variable associations with symbiotic bacteria that allow for the observed differences in colonization and success in whale fall environments throughout the world's oceans.

Symbiotic bacteria

Phylotype

10.1128/aem.01986-06

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Citations (124)