Functional differences between the extraordinary eyes of deep-sea hyperiid amphipods.

The ocean's midwater is a uniquely challenging yet predictable and simple visual environment. The need to see without being seen in this dim, open habitat has led to extraordinary visual adaptations. To understand these adaptations, we compared the morphological and functional differences between the eyes of three hyperiid amphipods-Hyperia galba, Streetsia challengeri and Phronima sedentaria. Combining micro-CT data with computational modelling, we mapped visual field topography and predicted detection distances for visual targets viewed in different directions through mesopelagic depths. Hyperia's eyes provide a wide visual field optimized for spatial vision over short distances, while Phronima's and Streetsia's eyes have the potential to achieve greater sensitivity and longer detection distances using spatial summation. These improvements come at the cost of smaller visual fields, but this loss is compensated for by a second pair of eyes in Phronima and by behaviour in Streetsia. The need to improve sensitivity while minimizing visible eye size to maintain crypsis has likely driven the evolution of hyperiid eye diversity. Our results provide an integrative look at how these elusive animals have adapted to the unique visual challenges of the mesopelagic.

A transcriptome-based phylogeny for Polynoidae (Annelida: Aphroditiformia).

Polynoidae is the most diverse radiation of Aphroditiformia and one of the most successful groups of all Annelida in terms of diversity and habitats colonized. With such an unmatched diversity, phylogenetic investigations have struggled to understand their evolutionary relationships. Previous phylogenetic analyses have slowly increased taxon sampling and employed methodologies, but despite their diversity and biological importance, large genomic sampling is limited. To investigate the internal relationships within Polynoidae, we conducted the first phylogenomic analyses of the group based on 12 transcriptomes collected from species inhabiting a broad array of habitats, including shallow and deep waters, as well as hydrothermal vents, anchialine caves and the midwater. Our phylogenomic analyses of Polynoidae recovered congruent tree topologies representing the clades Polynoinae, Macellicephalinae and Lepidonotopodinae. Members of Polynoinae and Macellicephalinae clustered in well-supported and independent clades. In contrast, Lepidonotopodinae taxa were always recovered nested within Macellicephalinae. Though our sampling only covers a small proportion of the species known for Polynoidae, our results provide a robust phylogenomic framework to build from, emphasizing previously hypothesized relationships between Macellicephalinae and Lepidonotopodinae taxa, while providing new insights on the origin of enigmatic cave and pelagic lineages.

A new computational model illuminates the extraordinary eyes of Phronima.

Vision in the midwater of the open ocean requires animals to perform visual tasks quite unlike those of any other environment. These tasks consist of detecting small, low contrast objects and point sources against a relatively dim and uniform background. Deep-sea animals have evolved many extraordinary visual adaptations to perform these tasks. Linking eye anatomy to specific selective pressures, however, is challenging, not least because of the many difficulties of studying deep-sea animals. Computational modelling of vision, based on detailed morphological reconstructions of animal eyes, along with underwater optics, offers a chance to understand the specific visual capabilities of individual visual systems. Prior to the work presented here, comprehensive models for apposition compound eyes in the mesopelagic, the dominant eye form of crustaceans, were lacking. We adapted a model developed for single-lens eyes and used it to examine how different parameters affect the model's ability to detect point sources and extended objects. This new model also allowed us to examine spatial summation as a means to improve visual performance. Our results identify a trade-off between increased depth range over which eyes function effectively and increased distance at which extended objects can be detected. This trade-off is driven by the size of the ommatidial acceptance angle. We also show that if neighbouring ommatidia have overlapping receptive fields, spatial summation helps with all detection tasks, including the detection of bioluminescent point sources. By applying our model to the apposition compound eyes of Phronima, a mesopelagic hyperiid amphipod, we show that the specialisations of the large medial eyes of Phronima improve both the detection of point sources and of extended objects. The medial eyes outperformed the lateral eyes at every modelled detection task. We suggest that the small visual field size of Phronima's medial eyes and the strong asymmetry between the medial and lateral eyes reflect Phronima's need for effective vision across a large depth range and its habit of living inside a barrel. The barrel's narrow aperture limits the usefulness of a large visual field and has allowed a strong asymmetry between the medial and lateral eyes. The model provides a useful tool for future investigations into the visual abilities of apposition compound eyes in the deep sea.

Strange eyes, stranger brains: exceptional diversity of optic lobe organization in midwater crustaceans.

Nervous systems across Animalia not only share a common blueprint at the biophysical and molecular level, but even between diverse groups of animals the structure and neuronal organization of several brain regions are strikingly conserved. Despite variation in the morphology and complexity of eyes across malacostracan crustaceans, many studies have shown that the organization of malacostracan optic lobes is highly conserved. Here, we report results of divergent evolution to this 'neural ground pattern' discovered in hyperiid amphipods, a relatively small group of holopelagic malacostracan crustaceans that possess an unusually wide diversity of compound eyes. We show that the structure and organization of hyperiid optic lobes has not only diverged from the malacostracan ground pattern, but is also highly variable between closely related genera. Our findings demonstrate a variety of trade-offs between sensory systems of hyperiids and even within the visual system alone, thus providing evidence that selection has modified individual components of the central nervous system to generate distinct combinations of visual centres in the hyperiid optic lobes. Our results provide new insights into the patterns of brain evolution among animals that live under extreme conditions.

Loss of metagenesis and evolution of a parasitic life style in a group of open-ocean jellyfish.

Loss or stark reduction of the free-swimming medusa or jellyfish stage is common in the cnidarian class Hydrozoa. In the hydrozoan clade Trachylina, however, many species do not possess a sessile polyp or hydroid stage. Trachylines inhabiting freshwater and coastal ecosystems (i.e., Limnomedusae) possess a metagenetic life cycle involving benthic, sessile polyp and free-swimming medusa. In contrast, the paradigm is that open ocean inhabiting, oceanic trachylines (in the orders Narcomedusae and Trachymedusae) develop from zygote to medusa via a free-swimming larva, forgoing the polyp stage. In some open-ocean trachylines, development includes a sessile stage that is an ecto- or endoparasite of other oceanic organisms. We expand the molecular-based phylogenetic hypothesis of trachylines significantly, increasing taxon and molecular marker sampling. Using this comprehensive phylogenetic hypothesis in conjunction with character state reconstructions we enhance understanding of the evolution of life cycles in trachyline hydrozoans. We find that the polyp stage was lost at least twice independently, concurrent with a transition to an oceanic life style. Further, a sessile, polypoid parasitic stage arose once, rather than twice as current classification would imply, in the open ocean inhabiting Narcomedusae. Our results also support the hypothesis that interstitial species of the order Actinulida are directly descended from direct developing, oceanic trachylines.

Synonymization of two, monotypic black-coral-commensal scale worm genera, Antipathipolyeunoa Pettibone, 1991 and Parahololepidella Pettibone, 1969 (Polynoidae, Aphroditiformia).

Parahololepidella Pettibone, 1969 is a polynoid genus commensal with the antipatharian genus Tanacetipathes Opresko, 2001. These scale worms are elongate with numerous segments and small elytra. To date, the only other known polynoid associated with Tanacetipathes is Antipathipolyeunoa Pettibone, 1991. By re-examining the holotype of Antipathipolyeunoa, we have identified several overlooked characters that no longer distinguish this genus from Parahololepidella. Based on the presence of chaetae on the tentacular segment and elytral irregularity on posterior segments, we propose synonymizing Antipathipolyeunoa with Parahololepidella.

Diversification of acorn worms (Hemichordata, Enteropneusta) revealed in the deep sea.

Enteropneusts (phylum Hemichordata), although studied extensively because of their close relationship to chordates, have long been considered shallow-water, burrowing animals. The present paper more than doubles the number of enteropneust species recorded in the deep sea based on high-resolution imaging and sampling with remotely operated vehicles. We provide direct evidence that some enteropneusts are highly mobile-using changes in posture and currents to drift between feeding sites-and are prominent members of deep, epibenthic communities. In addition, we provide ecological information for each species. We also show that despite their great morphological diversity, most deep-living enteropneusts form a single clade (the rediagnosed family Torquaratoridae) on the basis of rDNA sequences and morphology of the proboscis skeleton and stomochord. The phylogenetic position of the torquaratorids indicates that the group, after evolving from near-shore ancestors, radiated extensively in the deep sea.

Composition and metabolic potential of microbiomes associated with mesopelagic animals from Monterey Canyon.

There is growing recognition that microbiomes play substantial roles in animal eco-physiology and evolution. To date, microbiome research has largely focused on terrestrial animals, with far fewer studies on aquatic organisms, especially pelagic marine species. Pelagic animals are critical for nutrient cycling, yet are also subject to nutrient limitation and might thus rely strongly on microbiome digestive functions to meet their nutritional requirements. To better understand the composition and metabolic potential of midwater host-associated microbiomes, we applied amplicon and shotgun metagenomic sequencing to eleven mesopelagic animal species. Our analyses reveal that mesopelagic animal microbiomes are typically composed of bacterial taxa from the phyla Proteobacteria, Firmicutes, Bacteroidota and, in some cases, Campylobacterota. Overall, compositional and functional microbiome variation appeared to be primarily governed by host taxon and depth and, to a lesser extent, trophic level and diel vertical migratory behavior, though the impact of host specificity seemed to differ between migrating and non-migrating species. Vertical migrators generally showed lower intra-specific microbiome diversity (i.e., higher host specificity) than their non-migrating counterparts. These patterns were not linked to host phylogeny but may reflect differences in feeding behaviors, microbial transmission mode, environmental adaptations and other ecological traits among groups. The results presented here further our understanding of the factors shaping mesopelagic animal microbiomes and also provide some novel, genetically informed insights into their diets.

The remarkable squidworm is an example of discoveries that await in deep-pelagic habitats.

An intriguing new annelid, Teuthidodrilus samae (Annelida, Cirratuliformia) gen. and sp. nov., was observed and collected during deep-water column exploration of the western Celebes Sea. The Celebes Sea is a deep pocket basin, effectively isolated from surrounding deep water, and is part of the Coral Triangle, a focal area for conservation because of its high diversity and unique geological history. Collected specimens reached 94 mm in length and possessed 10 anterior appendages that were as long or longer than the body. Two characters distinguish T. samae from other polychaetes: notochaetae forming broad, concavo-convex paddles and six pairs of free-standing, oppositely branched nuchal organs. Phylogenetic analysis of five genes and a 29-character morphological matrix showed that T. samae is an acrocirrid (primarily benthic polychaetes) belonging to the morphologically diverse swimming clade. Pelagic animals within primarily benthic clades are of particular interest in evolutionary biology, because their adaptations to life in the water column inform us of the evolutionary possibilities and constraints within the clade and indirectly of the selective pressures at work in this unfamiliar habitat. This new genus illustrates how much we have to learn about even the large, abundant inhabitants of deep-pelagic communities.

Metachronal Swimming with Flexible Legs: A Kinematics Analysis of the Midwater Polychaete Tomopteris.

Aquatic animals have developed a wide array of adaptations specific to life underwater, many of which are related to moving in the water column. Different swimming methods have emerged, such as lift-based flapping, drag-based body undulations, and paddling. Patterns occur across scales and taxa, where animals with analogous body features use similar locomotory methods. Metachronal paddling is one such wide-spread propulsion mechanism, occurring in taxa as diverse as ctenophores, crustaceans, and polychaetes. Sequential movement of multiple, near identical appendages, allows for steady swimming through phase-offsets between adjacent propulsors. The soft-bodied, holopelagic polychaete Tomopteris has two rows of segmental appendages (parapodia) positioned on opposite sides along its flexible body that move in a metachronal pattern. The outer one-third of their elongate parapodia consist of two paddle-like pinnules that can be spread or, when contracted, fold together to change the effective width of the appendage. Along with metachronal paddling, tomopterid bodies undulate laterally, and by using high speed video and numerical modeling, we seek to understand how these two behaviors combine to generate effective swimming. We collected animals using deep-diving remotely operated vehicles, and recorded video data in shore- and ship-based imaging laboratories. Kinematics were analyzed using landmark tracking of features in the video data. We determined that parapodia are actively moved to generate thrust and pinnules are actively spread and contracted to create differences in drag between power and recovery strokes. At the same time, the body wave increases the parapodium stroke angle and extends the parapodia into undisturbed water adjacent to the body, enhancing thrust. Based on kinematics measurements used as input to a 1D numerical model of drag-based swimming, we found that spreading of the pinnules during the power stroke provides a significant contribution to propulsion, similar to the contribution provided by the body wave. We conclude that tomopterids combine two different propulsive modes, which are enabled by their flexible body plan. This makes their anatomy and kinematics of interest not only for biologists, but also for soft materials and robotics engineers.

Morphological convergence and adaptation in cave and pelagic scale worms (Polynoidae, Annelida).

Across Annelida, accessing the water column drives morphological and lifestyle modifications-yet in the primarily "benthic" scale worms, the ecological significance of swimming has largely been ignored. We investigated genetic, morphological and behavioural adaptations associated with swimming across Polynoidae, using mitogenomics and comparative methods. Mitochondrial genomes from cave and pelagic polynoids were highly similar, with non-significant rearrangements only present in cave Gesiella. Gene orders of the new mitogenomes were highly similar to shallow water species, suggestive of an underlying polynoid ground pattern. Being the first phylogenetic analyses to include the holopelagic Drieschia, we recovered this species nested among shallow water terminals, suggesting a shallow water ancestry. Based on these results, our phylogenetic reconstructions showed that swimming evolved independently three times in Polynoidae, involving convergent adaptations in morphology and motility patterns across the deep sea (Branchipolynoe), midwater (Drieschia) and anchialine caves (Pelagomacellicephala and Gesiella). Phylogenetic generalized least-squares (PGLS) analyses showed that holopelagic and anchialine cave species exhibit hypertrophy of the dorsal cirri, yet, these morphological modifications are achieved along different evolutionary pathways, i.e., elongation of the cirrophore versus style. Together, these findings suggest that a water column lifestyle elicits similar morphological adaptations, favouring bodies designed for drifting and sensing.

Distribution, associations and role in the biological carbon pump of Pyrosoma atlanticum (Tunicata, Thaliacea) off Cabo Verde, NE Atlantic.

Gelatinous zooplankton are increasingly acknowledged to contribute significantly to the carbon cycle worldwide, yet many taxa within this diverse group remain poorly studied. Here, we investigate the pelagic tunicate Pyrosoma atlanticum in the waters surrounding the Cabo Verde Archipelago. By using a combination of pelagic and benthic in situ observations, sampling, and molecular genetic analyses (barcoding, eDNA), we reveal that: P. atlanticum abundance is most likely driven by local island-induced productivity, that it substantially contributes to the organic carbon export flux and is part of a diverse range of biological interactions. Downward migrating pyrosomes actively transported an estimated 13% of their fecal pellets below the mixed layer, equaling a carbon flux of 1.96-64.55 mg C m-2 day-1. We show that analysis of eDNA can detect pyrosome material beyond their migration range, suggesting that pyrosomes have ecological impacts below the upper water column. Moribund P. atlanticum colonies contributed an average of 15.09 ± 17.89 (s.d.) mg C m-2 to the carbon flux reaching the island benthic slopes. Our pelagic in situ observations further show that P. atlanticum formed an abundant substrate in the water column (reaching up to 0.28 m2 substrate area per m2), with animals using pyrosomes for settlement, as a shelter and/or a food source. In total, twelve taxa from four phyla were observed to interact with pyrosomes in the midwater and on the benthos.

Ultra-black Camouflage in Deep-Sea Fishes.

At oceanic depths >200 m, there is little ambient sunlight, but bioluminescent organisms provide another light source that can reveal animals to visual predators and prey [1-4]. Transparency and mirrored surfaces-common camouflage strategies under the diffuse solar illumination of shallower waters-are conspicuous when illuminated by directed bioluminescent sources due to reflection from the body surface [5, 6]. Pigmentation allows animals to absorb light from bioluminescent sources, rendering them visually undetectable against the dark background of the deep sea [5]. We present evidence suggesting pressure to reduce reflected bioluminescence led to the evolution of ultra-black skin (reflectance <0.5%) in 16 species of deep-sea fishes across seven distantly related orders. Histological data suggest this low reflectance is mediated by a continuous layer of densely packed melanosomes in the exterior-most layer of the dermis [7, 8] and that this layer lacks the unpigmented gaps between pigment cells found in other darkly colored fishes [9-13]. Using finite-difference, time-domain modeling and comparisons with melanosomes found in other ectothermic vertebrates [11, 13-21], we find the melanosomes making up the layer in these ultra-black species are optimized in size and shape to minimize reflectance. Low reflectance results from melanosomes scattering light within the layer, increasing the optical path length and therefore light absorption by the melanin. By reducing reflectance, ultra-black fish can reduce the sighting distance of visual predators more than 6-fold compared to fish with 2% reflectance. This biological example of efficient light absorption via a simple architecture of strongly absorbing and highly scattering particles may inspire new ultra-black materials.

Description and relationships of Chaetopterus pugaporcinus, an unusual pelagic polychaete (Annelida, Chaetopteridae).

An extraordinary new species, Chaetopterus pugaporcinus, is described from eight specimens collected from deep mesopelagic waters off Monterey Bay, California, by remotely operated vehicles. All specimens exhibit a consistent combination of both adult and larval characteristics, leaving in question the maturity of the specimens. All specimens lack ciliated larval bands and the stout, modified chaetae (cutting spines) typically found in segment A4 of chaetopterids. If the specimens described here are larvae, they are remarkable for their size, which ranged from 10 to 21 mm total length, nearly twice the length of the largest polychaete larvae previously reported and 5 to 10 times larger than known chaetopterid larvae. Then too, their lack of segment addition prior to settlement would be atypical. If adult, they are particularly unusual in their habitat choice and body form. Morphology of the uncini and comparison to larval morphology indicated a close relationship to either Chaetopterus or Mesochaetopterus. However, the lack of cutting spines and typical adult morphology made it impossible to determine to what genus this species should be allied. Thus, we carried out the first molecular phylogenetic analysis of the Chaetopteridae in order to appropriately place and name the new species. Three partial genes were sequenced for 21 annelid species. The sequencing also provides the first molecular evidence that Chaetopterus variopedatus sensu Hartman (1959) is not a single cosmopolitan species. The question of C. pugaporcinus being a delayed larva or a genuine holopelagic chaetopterid is discussed.

Time-calibrated molecular phylogeny of pteropods.

Pteropods are a widespread group of holoplanktonic gastropod molluscs and are uniquely suitable for study of long-term evolutionary processes in the open ocean because they are the only living metazoan plankton with a good fossil record. Pteropods have been proposed as bioindicators to monitor the impacts of ocean acidification and in consequence have attracted considerable research interest, however, a robust evolutionary framework for the group is still lacking. Here we reconstruct their phylogenetic relationships and examine the evolutionary history of pteropods based on combined analyses of Cytochrome Oxidase I, 28S, and 18S ribosomal rRNA sequences and a molecular clock calibrated using fossils and the estimated timing of the formation of the Isthmus of Panama. Euthecosomes with uncoiled shells were monophyletic with Creseis as the earliest diverging lineage, estimated at 41-38 million years ago (mya). The coiled euthecosomes (Limacina, Heliconoides, Thielea) were not monophyletic contrary to the accepted morphology-based taxonomy; however, due to their high rate heterogeneity no firm conclusions can be drawn. We found strong support for monophyly of most euthecosome genera, but Clio appeared as a polyphyletic group, and Diacavolinia grouped within Cavolinia, making the latter genus paraphyletic. The highest evolutionary rates were observed in Heliconoides inflatus and Limacina bulimoides for both 28S and 18S partitions. Using a fossil-calibrated phylogeny that sets the first occurrence of coiled euthecosomes at 79-66 mya, we estimate that uncoiled euthecosomes evolved 51-42 mya and that most extant uncoiled genera originated 40-15 mya. These findings are congruent with a molecular clock analysis using the Isthmus of Panama formation as an independent calibration. Although not all phylogenetic relationships could be resolved based on three molecular markers, this study provides a useful resource to study pteropod diversity and provides general insight into the processes that generate and maintain their diversity in the open ocean.

Sphaerodoridae (Annelida) of the deep Northwestern Atlantic, including remarkable new species of Euritmia and Sphaerephesia.

Sphaerodoridae (Annelida) is a seeming uncommon and minimally diverse group of polychaetes in the northwestern Atlantic, with only seven species reported from the United States, and none from the eastern coast of Canada, before the present study. Review of the large Smithsonian collection (National Museum of Natural History, Washington) revealed the presence of two morphologically extraordinary undescribed species and added a new record to the north-western Atlantic region. Euritmia carolensis sp. n. is characterised by bearing approximately 20 sessile spherical papillae arranged in three transverse rows per segment, ventrum with 4-6 larger papillae near the parapodial bases and parapodia without papillae; bearing 4-5 simple chaetae that are enlarged subdistally. Sphaerephesia amphorata sp. n. is distinguished from other congeners in the presence of four longitudinal rows of sessile, bottle-shaped macrotubercles with exceptionally long digitiform terminal papilla, and parapodia with four rounded and small papillae, bearing 4-7 compound chaetae, with blades 7-11 times as long as wide. Other encountered species are also herein re-described, including intraspecific variation and updated iconography. Comparison of material also allowed some systematic changes in the group, including the synonymisation of the genus Amacrodorum with Euritmia, and the transfer of Ephesiopsis shivae to Ephesiella. A key to the species reported from the Northwestern Atlantic is provided.

Nanostructures and Monolayers of Spheres Reduce Surface Reflections in Hyperiid Amphipods.

Transparent zooplankton and nekton are often nearly invisible when viewed under ambient light in the pelagic zone [1-3]. However, in this environment, where the light field is directional (and thus likely to cause reflections), and under the bioluminescent searchlights of potential predators, animals may be revealed by reflections from their body surface [4-7]. We investigated the cuticle surfaces of seven species of hyperiids (Crustacea; Amphipoda) using scanning electron microscopy and found two undocumented features that may reduce reflectance. We found that the legs of Cystisoma spp. (n = 5) are covered with an ordered array of nanoprotuberances 200 ± 20 nm SD in height that function optically as a gradient refractive index material [6, 8, 9]. Additionally, we observed that Cystisoma and six other species of hyperiids are covered with a monolayer of homogenous spheres (diameters ranging from 52 ± 7 nm SD on Cystisoma spp. to 320 ± 15 nm SD on Phronima spp.). Optical modeling using effective medium theory and transfer matrix methods demonstrated that both the nanoprotuberances and the monolayers reduce reflectance by as much as 100-fold, depending on the wavelength and angle of the incident light and the thickness of the gradient layer. Even though we only consider surface reflectance and not internal light scattering, our study demonstrates that these nanoprotuberances and spheres can improve crypsis in a featureless habitat where the smallest reflection can render an animal vulnerable to visual predation.

A unique apposition compound eye in the mesopelagic hyperiid amphipod Paraphronima gracilis.

The mesopelagic habitat is a vast space that lacks physical landmarks and is structured by depth, light penetration, and horizontal currents. Solar illumination is visible in the upper 1,000 m of the ocean, becoming dimmer and spectrally filtered with depth-generating a nearly monochromatic blue light field. The struggle to perceive dim downwelling light and bioluminescent sources and the need to remain unseen generate contrasting selective pressures on the eyes of mesopelagic inhabitants. Hyperiid amphipods are cosmopolitan members of the mesopelagic fauna with at least ten different eye configurations across the family-ranging from absent eyes in deep-living species to four enlarged eyes in mesopelagic individuals. The hyperiid amphipod Paraphronima gracilis has a pair of bi-lobed apposition compound eyes, each with a large upward-looking portion and a small lateral-looking portion. The most unusual feature of the P. gracilis eye is that its upward-looking portion is resolved into a discontinuous retina with 12 distinct groups, each serving one transverse row of continuously spaced facets. On the basis of eye morphology, we estimated spatial acuity (2.5° ± 0.11°, SEM; n = 25) and optical sensitivity (30 ± 3.4 µm(2) ⋅ sr, SEM; n = 25). Microspectrophotometry showed that spectral sensitivity of the eye peaked at 516 nm (±3.9 nm, SEM; n = 6), significantly offset from the peak of downwelling irradiance in the mesopelagic realm (480 nm). Modeling of spatial summation within the linear retinal groups showed that it boosts sensitivity with less cost to spatial acuity than more typical configurations.