Comparative Population Genomics and Biophysical Modeling of Shrimp Migration in the Gulf of Mexico Reveals Current-Mediated Connectivity

The Gulf of Mexico experiences frequent perturbations, both natural and anthropogenic. To better understand the impacts of these events, we must inventory natural variability within the ecosystem, communities, species, and populations, and contextualize these findings in relation to physical features. Here, we present an integrated study of comparative population genomics and biophysical oceanography. Targeting three species of mesopelagic shrimp common to the Gulf of Mexico midwater (Acanthephyra purpurea, Systellaspis debilis, and Robustosergia robusta), we analyzed genetic diversity and population connectivity as proxies for species health and resilience, respectively. We also simulated a range of vertical migratory behaviors for the shrimp to infer the relationship between diel vertical migration and horizontal transmission between the Gulf of Mexico and the greater Atlantic Ocean. This study aims to establish biological baselines and characterize these values in terms of the prevailing oceanographic feature of the midwater: the Gulf Loop Current. Generally, the oplophorid species (A. purpurea and S. debilis) exhibit lower genetic diversity and higher interpopulation homogeneity compared to the sergestid (R. robusta). Biophysical simulations suggest the differences in vertical migratory regimes between these two groups have important implications for horizontal transport out of the Gulf of Mexico. Because of the difference in vertical migration patterns, access to the Gulf Loop Current varies across taxa and impacts inter-basin migration. Our findings suggest a negative correlation between surface abundance and genetic diversity in these three shrimp species. We hypothesize that this correlation may be due to the relationships between surface abundance and access to the fastest moving waters of the Gulf Loop Current

Comparative mitogenomics of the Decapoda reveals evolutionary heterogeneity in architecture and composition

The emergence of cost-effective and rapid sequencing approaches has resulted in an exponential rise in the number of mitogenomes on public databases in recent years, providing greater opportunity for undertaking large-scale comparative genomic and systematic research. Nonetheless, current datasets predominately come from small and disconnected studies on a limited number of related species, introducing sampling biases and impeding research of broad taxonomic relevance. This study contributes 21 crustacean mitogenomes from several under-represented decapod infraorders including Polychelida and Stenopodidea, which are used in combination with 225 mitogenomes available on NCBI to investigate decapod mitogenome diversity and phylogeny. An overview of mitochondrial gene orders (MGOs) reveals a high level of genomic variability within the Decapoda, with a large number of MGOs deviating from the ancestral arthropod ground pattern and unevenly distributed among infraorders. Despite the substantial morphological and ecological variation among decapods, there was limited evidence for correlations between gene rearrangement events and species ecology or lineage specific nucleotide substitution rates. Within a phylogenetic context, predicted scenarios of rearrangements show some MGOs to be informative synapomorphies for some taxonomic groups providing strong independent support for phylogenetic relationships. Additional comparisons for a range of mitogenomic features including nucleotide composition, strand asymmetry, unassigned regions and codon usage indicate several clade-specific trends that are of evolutionary and ecological interest

Vision and Bioluminescence in the Deep-Sea Benthos

During a NOAA-OER funded research cruise, novel collecting techniques were used to collect live, deep-sea benthic animals for studies of bioluminescence and vision. True color images and emission spectra of bioluminescence were obtained from a number of species, including the spiral octocoral Iridogorgia sp., the sea fan Chrysogorgia sp., the sea pen Umbellula sp., and the caridean shrimp Heterocarpusoryx. Electrophysiological studies were conducted on 3 species of decapod crustaceans collected with methods that limited light damage to their photoreceptors. The caridean shrimp, Bathypalaemonella, collected from 1920m, was always found in association with the bioluminescent spiral octocoral Iridogorgia. While moribund at the surface, enough data were obtained from one specimen to show different wave forms in response to short and long wavelength light, indicative of two different classes of photoreceptor cells. The chirostylid crab, Uroptychusnitidus, found in association with the bioluminescent sea fan, Chrysogorgia sp., also appears to possess two visual pigments, and if further analysis of data supports this preliminary observation, will be the 4th species of deep-sea, non-bioluminescent crustaceans possessing two visual pigments found in association with bioluminescent cnidarians. These four species also share another characteristic–the presence of one or two very long claws, which the crab species are known to use to pick items (possibly plankton stuck in the mucus) off their cnidarian hosts. These data support the previously presented hypothesis (Frank et al. 2012), that these crustaceans may be utilizing their dual visual pigment systems to distinguish between prey and host, based on spectral differences between pelagic and benthic bioluminescence.

The role of isolation on contrasting phylogeographic patterns in two cave crustaceans

Background: The underlying mechanisms and processes that prompt the colonisation of extreme environments, such as caves, constitute major research themes of evolutionary biology and biospeleology. The special adaptations required to survive in subterranean environments (low food availability, hypoxic waters, permanent darkness), and the geographical isolation of caves, nominate cave biodiversity as ideal subjects to answer long-standing questions concerning the interplay amongst adaptation, biogeography, and evolution. The present project aims to examine the phylogeographic patterns exhibited by two sympatric species of surface and cave-dwelling peracarid crustaceans (Asellus aquaticus and Niphargus hrabei), and in doing so elucidate the possible roles of isolation and exaptation in the colonisation and successful adaptation to the cave environment. Results: Specimens of both species were sampled from freshwater hypogean (cave) and epigean (surface) habitats in Hungary, and additional data from neighbouring countries were sourced from Genbank. Sequencing of mitochondrial and nuclear loci revealed, through haplotype network reconstruction (TCS) and phylogenetic inference, the genetic structure, phylogeographic patterns, and divergence-time estimates of A. aquaticus and N. hrabei surface and cave populations. Contrasting phylogeographic patterns were found between species, with A. aquaticus showing strong genetic differentiation between cave and surface populations and N. hrabei lacking any evidence of genetic structure mediated by the cave environment. Furthermore, N. hrabei populations show very low levels of genetic differentiation throughout their range, which suggests the possibility of recent expansion events over the last few thousand years. Conclusions: Isolation by cave environment, rather than distance, is likely to drive the genetic structuring observed between immediately adjacent cave and surface populations of A. aquaticus, a predominantly surface species with only moderate exaptations to subterranean life. For N. hrabei, in which populations exhibit a fully ‘cave-adapted’ (troglomorphic) phenotype, the lack of genetic structure suggests that subterranean environments do not pose a dispersal barrier for this surface-cave species

Transcriptomic effects of dispersed oil in a non-model decapod crustacean

Background. Oil spills are major environmental disasters. Dispersants help control spills, as they emulsify oil into droplets to speed bioremediation. Although dispersant toxicity is controversial, the genetic consequences and damages of dispersed oil exposure are poorly understood. We used RNA-seq to measure gene expression of flatback mudcrabs (Eurypanopeus depressus, Decapoda, Brachyura, Panopeidae) exposed to dispersed oil. Methods. Our experimental design included two control types, oil-only, and oil-dispersant treatments with three replicates each. We prepared 100 base pair-ended libraries from total RNA and sequenced them in one Illumina HiSeq2000 lane. We assembled a reference transcriptome with all replicates per treatment, assessed quality with novel metrics, identified transcripts, and quantified gene expression with open source software. Results. Our mudcrab transcriptome included 500,008 transcripts from 347,082,962 pair-end raw reads. In oil-only treatments, we found few significant differences. However, in oil-dispersant treatments, over 4000 genes involved with cellular differentiation, primordial cellular component upkeep, apoptosis, and immune response were downregulated. A few muscle structure and development genes were upregulated. Discussion. Our results provide evidence that exposure to chemically dispersed oil causes a generalized cellular shutdown and muscular repair attempts. Our results suggest current oil-spill treatment procedures could be detrimental to crustaceans and indicate additional research is needed to evaluate the impact of oil spills in gene expression. Finally, traditional quality metrics such as N50s have limitations to explain the nature of RNA-seq compared to new methods in non-model decapod crustaceans

Editorial: Deep Pelagic Ecosystem Dynamics in a Highly Impacted Water Column: The Gulf of Mexico After Deepwater Horizon

The intermediate-sized midwater fauna (fishes, shrimps, and cephalopods; “micronekton” collectively) are dominant components of the pelagic ocean, which is by far the largest ecosystem type on Earth by several metrics (volume, organismal numbers, biomass, and productivity). Deep-pelagic micronekton, those animals residing in the water column below 200 m depth during the day, are the direct link between plankton and oceanic top predators, and through the linked processes of feeding and daily vertical migration facilitate one of Earth\u27s most important ecosystem services to humans, carbon sequestration. Despite increasing recognition of this importance, a disconnect exists between stewardship and human impact; only a miniscule fraction of the deep-pelagic ocean has been studied in detail, while anthropogenic threats to that system are increasing rapidly. Perhaps nowhere on Earth is that dichotomy more demonstrable than the Gulf of Mexico (Gulf hereafter), a complex, high-diversity ecosystem under intense human usage and subjected to arguably the worst marine pollution event in human history. Assessment of the impacts of the Deepwater Horizon disaster to the deep-pelagic biota was impeded from the start by the lack of pre-event information, both in terms of baselines (faunal composition, abundance, and distribution) and in terms of understanding natural variability, against which impacts of anthropogenic disturbance could be detected and quantified. In this Research Topic, we present a description of three interlinked research programs (ONSAP, DEEPEND, and DEEPEND|RESTORE, described below) that began in 2010 and continue as of this writing. These programs were designed to investigate key aspects of the Gulf pelagic ecosystem, including its faunal structure, biophysical drivers of that structure, organismal and community ecology, natural variability, and potential resilience to disturbance. The contributed papers are grouped below by major themes, indicated in the conceptual model (Figure 1) of DEEPEND (Deep Pelagic Nekton Dynamics; www.deependconsortium.org), the largest of the three aforementioned research programs

Phylogenetics links monster larva to deep-sea shrimp.

Mid-water plankton collections commonly include bizarre and mysterious developmental stages that differ conspicuously from their adult counterparts in morphology and habitat. Unaware of the existence of planktonic larval stages, early zoologists often misidentified these unique morphologies as independent adult lineages. Many such mistakes have since been corrected by collecting larvae, raising them in the lab, and identifying the adult forms. However, challenges arise when the larva is remarkably rare in nature and relatively inaccessible due to its changing habitats over the course of ontogeny. The mid-water marine species Cerataspis monstrosa (Gray 1828) is an armored crustacean larva whose adult identity has remained a mystery for over 180 years. Our phylogenetic analyses, based in part on recent collections from the Gulf of Mexico, provide definitive evidence that the rare, yet broadly distributed larva, C. monstrosa, is an early developmental stage of the globally distributed deepwater aristeid shrimp, Plesiopenaeus armatus. Divergence estimates and phylogenetic relationships across five genes confirm the larva and adult are the same species. Our work demonstrates the diagnostic power of molecular systematics in instances where larval rearing seldom succeeds and morphology and habitat are not indicative of identity. Larval-adult linkages not only aid in our understanding of biodiversity, they provide insights into the life history, distribution, and ecology of an organism

Light Organ Photosensitivity in Deep-Sea Shrimp May Suggest a Novel Role in Counterillumination

Extraocular photoreception, the ability to detect and respond to light outside of the eye, has not been previously described in deep-sea invertebrates. Here, we investigate photosensitivity in the bioluminescent light organs (photophores) of deep-sea shrimp, an autogenic system in which the organism possesses the substrates and enzymes to produce light. Through the integration of transcriptomics, in situ hybridization and immunohistochemistry we find evidence for the expression of opsins and phototransduction genes known to play a role in light detection in most animals. Subsequent shipboard light exposure experiments showed ultrastructural changes in the photophore similar to those seen in crustacean eyes, providing further evidence that photophores are light sensitive. In many deep-sea species, it has long been documented that photophores emit light to aid in counterillumination – a dynamic form of camouflage that requires adjusting the organ’s light intensity to “hide” their silhouettes from predators below. However, it remains a mystery how animals fine-tune their photophore luminescence to match the intensity of downwelling light. Photophore photosensitivity allows us to reconsider the organ’s role in counterillumination - not only in light emission but also light detection and regulation

Transcriptomic effects of dispersed oil in a non-model decapod crustacean

Background. Oil spills are major environmental disasters. Dispersants help control spills, as they emulsify oil into droplets to speed bioremediation. Although dispersant toxicity is controversial, the genetic consequences and damages of dispersed oil exposure are poorly understood. We used RNA-seq to measure gene expression of flatback mudcrabs (Eurypanopeus depressus, Decapoda, Brachyura, Panopeidae) exposed to dispersed oil. Methods. Our experimental design included two control types, oil-only, and oil-dispersant treatments with three replicates each. We prepared 100 base pair-ended libraries from total RNA and sequenced them in one Illumina HiSeq2000 lane. We assembled a reference transcriptome with all replicates per treatment, assessed quality with novel metrics, identified transcripts, and quantified gene expression with open source software. Results. Our mudcrab transcriptome included 500,008 transcripts from 347,082,962 pairend raw reads. In oil-only treatments, we found few significant differences. However, in oildispersant treatments, over 4000 genes involved with cellular differentiation, primordial cellular component upkeep, apoptosis, and immune response were downregulated. A few muscle structure and development genes were upregulated. Discussion. Our results provide evidence that exposure to chemically dispersed oil causes a generalized cellular shutdown and muscular repair attempts. Our results suggest current oil-spill treatment procedures could be detrimental to crustaceans and indicate additional research is needed to evaluate the impact of oil spills in gene expression. Finally, traditional quality metrics such as N50s have limitations to explain the nature of RNA-seq compared to new methods in non-model decapod crustaceans

Phylogeny of Stenopodidea (Crustacea: Decapoda) shrimps inferred from nuclear and mitochondrial genes reveals non-monophyly of the families Spongicolidae and Stenopididae, and most of their composite genera

The infraorder Stenopodidea is a relatively small group of marine decapod crustaceans including the well known cleaner shrimps, but their higher taxonomy has been rather controversial. This study provides the most comprehensive molecular phylogenetic analyses of Stenopodidea using sequence data from two mitochondrial (16S and 12S rRNA) and two nuclear (histone H3 and sodium–potassium ATPase α-subunit (NaK)) genes. We included all 12 nominal genera from the three stenopodidean families in order to test the proposed evolutionary hypothesis and taxonomic scheme of the group. The inferred phylogeny did not support the familial ranking of Macromaxillocarididae and rejected the reciprocal monophyly of Spongicolidae and Stenopididae. The genera Stenopus, Richardina, Spongiocaris, Odontozona, Spongicola and Spongicoloides are showed to be poly- or paraphyletic, with monophyly of only the latter three genera strongly rejected in the analysis. The present results only strongly support the monophyly of Microprosthema and suggest that Paraspongiola should be synonymised with Spongicola. The three remaining genera, Engystenopus, Juxtastenopus and Globospongicola, may need to be expanded to include species from other genera if their statuses are maintained. All findings suggest that the morphological characters currently adopted to define genera are mostly invalid and substantial taxonomic revisions are required. As the intergeneric relationships were largely unresolved in the present attempt, the hypothesis of evolution of deep-sea sponge-associated taxa from shallow-water free-living species could not be verified here. The present molecular phylogeny, nevertheless, provides some support that stenopoididean shrimps colonised the deep sea in multiple circumstances