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Showing papers in "The Biological Bulletin in 2017"


Journal ArticleDOI
TL;DR: A model for early transcriptional regulation of protein degradation and cell adhesion response that may ultimately lead to the bleaching and stress response is proposed.
Abstract: Corals respond to heat pulses that cause bleaching with massive transcriptional change, but the immediate responses to stress that lead up to these shifts have never been detailed Understanding these early signals could be important for identifying the regulatory mechanisms responsible for bleaching and how these mechanisms vary between more and less resilient corals Using RNA sequencing (RNAseq) and sampling every 30 minutes during a short-term heat shock, we found that components of the transcriptome were significantly upregulated within 90 min and after a temperature increase of +2 °C The developmental transcription factor, Kruppel-like factor 7, was highly expressed within 60 min, and stress-related transcription factors such as Elk-3 were highly expressed starting at 240 min The sets of genes enriched for early transcriptional response to heat stress included heat shock proteins, small GTPases, and proteasome genes Retrovirus-related Pol polyproteins from transposons were significantly expressed throughout the whole experiment Lastly, we propose a model for early transcriptional regulation of protein degradation and cell adhesion response that may ultimately lead to the bleaching and stress response

62 citations


Journal ArticleDOI
TL;DR: The current literature is reviewed, publicly available transcriptomic data is analyzed, and hypotheses about the origins and development of spider eyes are discussed, highlighting that there are many new things to discover from spider eyes, and yet these opportunities are set against a backdrop of deep homology with other arthropod lineages.
Abstract: Spiders are among the world's most species-rich animal lineages, and their visual systems are likewise highly diverse. These modular visual systems, composed of four pairs of image-forming "camera" eyes, have taken on a huge variety of forms, exhibiting variation in eye size, eye placement, image resolution, and field of view, as well as sensitivity to color, polarization, light levels, and motion cues. However, despite this conspicuous diversity, our understanding of the genetic underpinnings of these visual systems remains shallow. Here, we review the current literature, analyze publicly available transcriptomic data, and discuss hypotheses about the origins and development of spider eyes. Our efforts highlight that there are many new things to discover from spider eyes, and yet these opportunities are set against a backdrop of deep homology with other arthropod lineages. For example, many (but not all) of the genes that appear important for early eye development in spiders are familiar players known from the developmental networks of other model systems (e.g., Drosophila). Similarly, our analyses of opsins and related phototransduction genes suggest that spider photoreceptors employ many of the same genes and molecular mechanisms known from other arthropods, with a hypothesized ancestral spider set of four visual and four nonvisual opsins. This deep homology provides a number of useful footholds into new work on spider vision and the molecular basis of its extant variety. We therefore discuss what some of these first steps might be in the hopes of convincing others to join us in studying the vision of these fascinating creatures.

41 citations


Journal ArticleDOI
TL;DR: The potential for a shared evolutionary lineage between the radiolar photoreceptors of serpulids and sabellids is explored and these unique innovations in the broader context of metazoan eye evolution are considered.
Abstract: Fan worms, represented by sabellid and serpulid polychaetes, have an astonishing array of unusual eyes and photoreceptors located on their eponymous feeding appendages. Here we organize the previous descriptions of these eyes in serpulids and report new anatomical, molecular, and physiological data regarding their structure, function, and evolution and the likely identity of their phototransduction machinery. We report that, as in sabellids, serpulids display a broad diversity of radiolar eye arrangements and ocellar structures. Furthermore, the visual pigment expressed in the eyes of Spirobranchus corniculatus, a species of the charismatic Christmas tree worms, absorbs light maximally at 464 nm in wavelength. This visual pigment closely matches the spectrum of downwelling irradiance in shallow coral reef habitats and lends support to the hypothesis that these radiolar photoreceptors function as a silhouette-detecting "burglar alarm" that triggers a rapid withdrawal response when the worm is threatened by potential predators. Finally, we report on the transcriptomic sequencing results for the radiolar eyes of S. corniculatus, which express invertebrate c-type opsins in their ciliary radiolar photoreceptors, closely related to the opsin found in the radiolar eyes of the sabellid Acromegalomma interruptum. We explore the potential for a shared evolutionary lineage between the radiolar photoreceptors of serpulids and sabellids and consider these unique innovations in the broader context of metazoan eye evolution.

29 citations


Journal ArticleDOI
TL;DR: It is found that regeneration starts with a rapid healing response characterized by hemocyte aggregation and infiltration of immunocytes, followed by increased activity of hemoblasts, recruitment of macrophage-like cells for clearing the tissues of debris, and their subsequent disappearance from the circulation concomitant with the maturation of a single regenerated adult.
Abstract: Whole-body regeneration (WBR)-the formation of an entire adult from only a small fragment of its own tissue-is extremely rare among chordates. Exceptionally, in the colonial ascidian Botrylloides leachii (Savigny, 1816) a fully functional adult is formed from their common vascular system after ablation of all adults from the colony in just 10 d, thanks to their high blastogenetic potential. While previous studies have identified key genetic markers and morphological changes, no study has yet focused on the hematological aspects of regeneration despite the major involvement of the remaining vascular system and the contained hemocytes in this process. To dissect this process, we analyzed colony blood flow patterns using time-lapse microscopy to obtain a quantitative description of the velocity, reversal pattern, and average distance traveled by hemocytes. We also observed that flows present during regeneration are powered by temporally and spatially synchronized contractions of the terminal ampullae. In addition, we revised previous studies of B. leachii hematology as well as asexual development using histological sectioning and compared the role played by hemocytes during WBR. We found that regeneration starts with a rapid healing response characterized by hemocyte aggregation and infiltration of immunocytes, followed by increased activity of hemoblasts, recruitment of macrophage-like cells for clearing the tissues of debris, and their subsequent disappearance from the circulation concomitant with the maturation of a single regenerated adult. Overall, we provide a detailed account of the hematological properties of regenerating B. leachii colonies, providing novel lines of inquiry toward the decipherment of regeneration in chordates.

28 citations


Journal ArticleDOI
TL;DR: The gray whale genomes reported here will enable comparative studies of natural selection in cetaceans, and the SNP markers should be highly informative for future studies of gray whale evolution, population structure, demography, and relatedness.
Abstract: Genetic and genomic approaches have much to offer in terms of ecology, evolution, and conservation. To better understand the biology of the gray whale Eschrichtius robustus (Lilljeborg, 1861), we sequenced the genome and produced an assembly that contains ∼95% of the genes known to be highly conserved among eukaryotes. From this assembly, we annotated 22,711 genes and identified 2,057,254 single-nucleotide polymorphisms (SNPs). Using this assembly, we generated a curated list of candidate genes potentially subject to strong natural selection, including genes associated with osmoregulation, oxygen binding and delivery, and other aspects of marine life. From these candidate genes, we queried 92 autosomal protein-coding markers with a panel of 96 SNPs that also included 2 sexing and 2 mitochondrial markers. Genotyping error rates, calculated across loci and across 69 intentional replicate samples, were low (0.021%), and observed heterozygosity was 0.33 averaged over all autosomal markers. This level of variability provides substantial discriminatory power across loci (mean probability of identity of 1.6 × 10-25 and mean probability of exclusion >0.999 with neither parent known), indicating that these markers provide a powerful means to assess parentage and relatedness in gray whales. We found 29 unique multilocus genotypes represented among our 36 biopsies (indicating that we inadvertently sampled 7 whales twice). In total, we compiled an individual data set of 28 western gray whales (WGSs) and 1 presumptive eastern gray whale (EGW). The lone EGW we sampled was no more or less related to the WGWs than expected by chance alone. The gray whale genomes reported here will enable comparative studies of natural selection in cetaceans, and the SNP markers should be highly informative for future studies of gray whale evolution, population structure, demography, and relatedness.

27 citations


Journal ArticleDOI
TL;DR: It is suggested that the Antarctic Polar Front is a strong but imperfect barrier to dispersal, and fluctuations in location and strength of the APF and ACC due to climate shifts may have profound consequences for levels of admixture or endemism in this region of the world.
Abstract: The Antarctic Polar Front (APF) is one of the most well-defined and persistent oceanographic features on the planet and serves as a barrier to dispersal between the Southern Ocean and lower latitudes. High levels of endemism in the Southern Ocean have been attributed to this barrier, whereas the accompanying Antarctic Circumpolar Current (ACC) likely promotes west-to-east dispersal. Previous phylogeographic work on the brittle star Astrotoma agassizii Lyman, 1875 based on mitochondrial genes suggested isolation across the APF, even though populations in both South American waters and the Southern Ocean are morphologically indistinguishable. Here, we revisit this finding using a high-resolution 2b-RAD (restriction-site-associated DNA) single-nucleotide polymorphism (SNP)-based approach, in addition to enlarged mitochondrial DNA data sets (16S rDNA, COI, and COII), for comparison to previous work. In total, 955 biallelic SNP loci confirmed the existence of strongly divergent populations on either side of the Drake Passage. Interestingly, genetic admixture was detected between South America and the Southern Ocean in five individuals on both sides of the APF, revealing evidence of recent or ongoing genetic contact. We also identified two differentiated populations on the Patagonian Shelf with six admixed individuals from these two populations. These findings suggest that the APF is a strong but imperfect barrier. Fluctuations in location and strength of the APF and ACC due to climate shifts may have profound consequences for levels of admixture or endemism in this region of the world.

22 citations


Journal ArticleDOI
TL;DR: This study shows that within a single 10-min trial E. scolopes learns to inhibit its predatory behavior, and after three trials it can retain this memory for at least 12 d, the first demonstrated of learning and memory in this species as well as the first demonstration of associative learning in any squid.
Abstract: Learning and memory in cephalopod molluscs have received intensive study because of cephalopods’ complex behavioral repertoire and relatively accessible nervous systems. While most of this research has been conducted using octopus and cuttlefish species, there has been relatively little work on squid. Euprymna scolopes Berry, 1913, a sepiolid squid, is a promising model for further exploration of cephalopod cognition. These small squid have been studied in detail for their symbiotic relationship with bioluminescent bacteria, and their short generation time and successful captive breeding through multiple generations make them appealing models for neurobiological research. However, little is known about their behavior or cognitive ability. Using the well-established “prawn-in-the-tube” assay of learning and memory, we show that within a single 10-min trial E. scolopes learns to inhibit its predatory behavior, and after three trials it can retain this memory for at least 12 d. Rapid learning and ver...

20 citations


Journal ArticleDOI
TL;DR: Although aesthetasc ablation attenuated flicking behavior in a chemical stimulus-independent manner, success in detection and short-range localization of food did not rely on the presence of aesthetASC sensilla, confirming the existence of a non-aesthetasc alternative pathway for feeding.
Abstract: Shrimp are an essential ecological component of marine ecosystems, and have commercial importance for human consumption and aquaculture. Like other decapod crustaceans, shrimp rely on chemical senses to detect and localize food resources by means of chemosensilla that are located mainly on the cephalothoracic appendages. Using the shrimp Palaemon adspersus, a model organism with omnivorous feeding behavior, we aimed to provide comparative information on the role of aesthetascs, antennular sensilla, and flicking behavior in food detection. To this end, we examined i) the morphology of antennular sensilla by field emission scanning electron microscopy, ii) the shrimp's sensitivity to a number of food-related compounds (amino acids and sugars) by means of whole-animal bioassays, and iii) the contribution of the aesthetasc sensilla to food detection. Our results showed that, aside from the aesthetascs, only three other main morphotypes of setae with chemoreceptive features were present in the antennules, thus accounting for relatively simple sensillar equipment. Nevertheless, we found broad-spectrum sensitivity of the shrimp to a number of amino acids (i.e., isoleucine, leucine, methionine, phenylalanine, glycine, tryptophan, cysteine, and tyrosine) and carbohydrates (trehalose, maltose, cellobiose, and fructose) that was consistent with the omnivorous or scavenging habits of the animal. Although aesthetasc ablation attenuated flicking behavior in a chemical stimulus-independent manner, success in detection and short-range localization of food did not rely on the presence of aesthetasc sensilla. This finding confirms the existence of a non-aesthetasc alternative pathway for feeding, with functional redundancy in simple generalist feeder models such as shrimp.

18 citations


Journal ArticleDOI
TL;DR: It is shown that high temperature causes coral bleaching independent of pCO2, and underscores the potential role of the coral host in driving intraspecific variation in coral Bleaching.
Abstract: This study tested the bleaching response of the Pacific coral Seriatopora caliendrum to short-term exposure to high temperature and elevated partial pressure of carbon dioxide (pCO2). Juvenile colonies collected from Nanwan Bay, Taiwan, were used in a factorial experimental design in which 2 temperatures (∼27.6 °C and ∼30.4 °C) and 2 pCO2 values (∼47.2 Pa and ∼90.7 Pa) were crossed to evaluate, over 12 days, the effects on the densities and physiology of the symbiotic dinoflagellates (Symbiodinium) in the corals. Thermal bleaching, as defined by a reduction of Symbiodinium densities at high temperature, was unaffected by high pCO2. The division, or mitotic index (MI), of Symbiodinium remaining in thermally bleached corals was about 35% lower than in control colonies, but they contained about 53% more chlorophyll. Bleaching was highly variable among colonies, but the differences were unrelated to MI or pigment content of Symbiodinium remaining in the coral host. At the end of the study, all of the ...

13 citations


Journal ArticleDOI
TL;DR: A general overview of the molecular aspects ofCopepod vision is presented by identifying phototransduction genes from newly generated and publicly available RNA-sequencing data and assemblies from 12 taxonomically diverse copepod species and identifying a set of 10 expressed transcripts that serve as a set to target genes for future studies ofcopepod phototranduction.
Abstract: Copepod crustaceans are an abundant and ecologically significant group whose basic biology is guided by numerous visually guided behaviors. These behaviors are driven by copepod eyes, including naupliar eyes and Gicklhorn’s organs, which vary widely in structure and function among species. Yet little is known about the molecular aspects of copepod vision. In this study we present a general overview of the molecular aspects of copepod vision by identifying phototransduction genes from newly generated and publicly available RNA-sequencing data and assemblies from 12 taxonomically diverse copepod species. We identify a set of 10 expressed transcripts that serve as a set of target genes for future studies of copepod phototransduction. Our more detailed evolutionary analyses of the opsin gene responsible for forming visual pigments found that all of the copepod species investigated express two main groups of opsins: middle-wavelength-sensitive (MWS) opsins and pteropsins. Additionally, there is evidenc...

13 citations


Journal ArticleDOI
TL;DR: The results provide the first direct evidence that temperature can affect the extent of behavioral alteration brought about by certain parasite species, and the consequences of increased trophic transmission remain elusive; the supposedly key anti-predatory behavior was not significantly affected by exposure of gammarids to different temperatures.
Abstract: Understanding the effect of temperature on ecologically important species has become a major challenge in the context of global warming. However, the consequences of climate change cannot be accurately predicted without taking into consideration biotic interactions. Parasitic infection, in particular, constitutes a widespread biotic interaction, and parasites impact their hosts in multiple ways, eventually leading to consequences for communities and ecosystems. We explored the effect of temperature on the anti-predator behavior of a keystone freshwater invertebrate, the amphipod Gammarus fossarum. Gammarids regularly harbor manipulative acanthocephalan parasites that modify their anti-predator behavior in ways that potentially increase the probability of trophic transmission to their definitive hosts. We investigated the impact of temperature on gammarids infected by two acanthocephalan parasites, Pomphorhynchus tereticollis and Polymorphus minutus. Uninfected and naturally infected gammarids were...

Journal ArticleDOI
TL;DR: The findings emphasize the role of stress regime when predicting adaptive responses of symbiotic cnidarians to changing climates, because genetic variation may exist for some forms of stress-induced bleaching but not others.
Abstract: Rising ocean temperatures disrupt the symbiosis between corals and their microalgae, accelerating global decline of coral reef ecosystems. Because of the difficulty of performing laboratory experiments with corals, the sea anemone Aiptasia has emerged as an important model system for molecular studies of coral bleaching and symbiosis. Here, we investigate natural variation in bleaching responses among different genetic lineages of Aiptasia. Both heat- and cold-induced paths to symbiosis breakdown were analyzed. Significant genetic variation in response to acute heat stress was observed, with severe bleaching of two Aiptasia strains from Hawaii but minimal bleaching of strains from the U.S. South Atlantic, including the strain used to generate the Aiptasia reference genome. Both strains from Hawaii hosted Symbiodinium type B1, whereas strains from the U.S. South Atlantic hosted type A4 or B2. In contrast to the results from exposures to acute heat stress, negligible variation was observed in response to a pulsed cold shock despite moderate bleaching across all strains. These results support our hypothesis that bleaching responses to distinct stressors are independent. Our findings emphasize the role of stress regime when predicting adaptive responses of symbiotic cnidarians to changing climates, because genetic variation may exist for some forms of stress-induced bleaching but not others.

Journal ArticleDOI
TL;DR: The genetic and morphometric population structures of the semiterrestrial crab Armases angustipes from along the Brazilian coast were examined, revealing low genetic variability and lack of phylogeographic structure; geometric morphometrics showed statistically significant morphological differentiation and geographic structuring.
Abstract: The genetic and morphometric population structures of the semiterrestrial crab Armases angustipes from along the Brazilian coast were examined. The influence of the Central South Equatorial Current on larval dispersal of A. angustipes also was evaluated. Six populations were sampled from estuarine areas in Sao Luis do Maranhao, Maranhao; Natal, Rio Grande do Norte; Maceio, Alagoas; Ilheus, Bahia; Aracruz, Espirito Santo; and Guaratuba, Parana. Patterns of genetic differentiation were assessed using DNA sequence data corresponding to parts of the mitochondrial cytochrome c oxidase subunit 1. Geometric morphometric techniques were used to evaluate morphological variation in shape and size of the carapace and right cheliped propodus. Our results revealed low genetic variability and lack of phylogeographic structure; geometric morphometrics showed statistically significant morphological differentiation and geographic structuring. Our data indicate the absence of possible barriers to gene flow for this mobile species, and no clear correlation of morphological or genetic variation with ocean currents and/or geographic distance. Our results also suggest that historical geological and climatological events and/or possible bottleneck effects influenced the current low genetic variability among the populations of A. angustipes.

Journal ArticleDOI
TL;DR: These findings suggest that light detection by the eyes of A. irradians is conferred primarily by photoreceptors that express Gαo or Gαq, that the corneal cells of scallops may contain sensory receptors and/or receive neural input, and that G protein labeling is useful for visualizing substructures and identifying specific populations of cells within the nervous systems of invertebrates.
Abstract: A multitude of image-forming eyes are spread across the bodies of certain invertebrates. Recent efforts have characterized how these eyes function, but less progress has been made toward describing the neural structures associated with them. Scallops, for example, have a distributed visual system that includes dozens of eyes whose optic nerves project to the lateral lobes of the parietovisceral ganglion (PVG). To identify sensory receptors and chemical synapses associated with the scallop visual system, we studied the expression of four G protein α subunits (Gαi, Gαo, Gαq, and Gαs) in the eyes and PVG of the bay scallop Argopecten irradians (Lamarck, 1819). In the eyes of A. irradians, we noted expression of Gαo by the ciliary photoreceptors of the distal retina, expression of Gαq by the rhabdomeric photoreceptors of the proximal retina, and the expression of Gαo and Gαq by the cells of the cornea; we did not, however, detect expression of Gαi or Gαs in the eyes. In the PVG of A. irradians, we noted widespread expression of Gαi, Gαo, and Gαq. The expression of Gαs was limited to fine neurites in the lateral and ventral central lobes, as well as large unipolar neurons in the dorsal central lobes. Our findings suggest that light detection by the eyes of A. irradians is conferred primarily by photoreceptors that express Gαo or Gαq, that the corneal cells of scallops may contain sensory receptors and/or receive neural input, and that G protein labeling is useful for visualizing substructures and identifying specific populations of cells within the nervous systems of invertebrates.

Journal ArticleDOI
TL;DR: Results indicated that i) antioxidant gene expression is modulated in the course of the blastogenetic cycle and upon exposure to Cd, and ii) hemocytes synthesize both enzymatic and nonenzymatic antioxidants, in line with the idea that they represent a major detoxification system for ascidians.
Abstract: Botryllus schlosseri is a cosmopolitan colonial ascidian that undergoes cyclical generation changes, or take-overs, during which adult zooids are resorbed and replaced by their buds. At take-over, adult tissues undergo diffuse apoptosis and effete cells are massively ingested by circulating phagocytes, with a consequent increase in oxygen consumption and in production of reactive oxygen species (ROS). The latter are responsible for the death of phagocytes involved in the clearance of apoptotic cells and corpses by phagocytosis-induced apoptosis. However, the majority of phagocytes and hemocytes do not die, even if they experience oxidative stress. This fact suggests the presence of detoxification mechanisms assuring their protection. To test this assumption, we searched for transcripts of genes involved in detoxification in the transcriptome of B. schlosseri. We identified and characterized transcripts for Cu/Zn superoxide dismutase (SOD), γ-glutamyl-cysteine ligase modulatory subunit (GCLM), glutathione synthase (GS), and two glutathione peroxidases (i.e., GPx3 and GPx5), all involved in protection from ROS. We also carried out a phylogenetic analysis of the putative amino acid sequences, confirming their similarity to their vertebrate counterparts, and studied the location of their mRNAs by in situ hybridization on hemocyte monolayers. We also analyzed gene transcription during the colonial blastogenetic cycle, which is the interval of time between one take-over and the next, by qRT-PCR. In addition, we investigated the effects of cadmium (Cd), an inducer of oxidative stress, on gene transcription. Our results indicated that i) antioxidant gene expression is modulated in the course of the blastogenetic cycle and upon exposure to Cd, and ii) hemocytes synthesize both enzymatic and nonenzymatic antioxidants, in line with the idea that they represent a major detoxification system for ascidians.

Journal ArticleDOI
TL;DR: The identified mRNAs that could encode four different opsins and several components of a potential Gq-mediated phototransduction pathway in the central nervous system of the Caribbean mantis shrimp Neogonodactylus oerstedii suggest that there are previously undiscovered cerebral photoreceptors in stomatopods.
Abstract: Visual pigments, each composed of an opsin protein covalently bound to a chromophore molecule, confer light sensitivity for vision. The eyes of some species of stomatopod crustaceans, or mantis shrimp, can express dozens of different opsin genes. The opsin diversity, along with spectral filters and unique tripartite eye structure, bestow upon stomatopods unusually complex visual systems. Although opsins are found in tissues outside typical image-forming eyes in other animals, extraocular opsin expression in stomatopods, animals well known for their diversity of opsins, was unknown. Caudal photoreception in the central nervous system of decapod crustaceans, a group closely related to stomatopod crustaceans, is thought to be opsin based. However, electrophysiological data suggest that stomatopods do not have caudal photoreceptors. In this study, we identified mRNAs that could encode four different opsins and several components of a potential Gq-mediated phototransduction pathway in the central nervous system of the Caribbean mantis shrimp Neogonodactylus oerstedii. The four opsins are abundantly expressed in the cerebral ganglion, or brain, with little or no expression in the remainder of the ventral nerve cord. Our data suggest that there are previously undiscovered cerebral photoreceptors in stomatopods.

Journal ArticleDOI
TL;DR: It is argued that calcite prism growth in euheterodonts is dominated by abiotic constraints whereas, in pteriomorphs (such as oysters, pterioids, and mussels), it is under strong biological control.
Abstract: Multiple groups of bivalve molluscs produce calcitic shell layers, many of these broadly classified as "prismatic." Various pteriomorphian bivalves (such as oysters, pterioids, and mussels) secrete prismatic microstructures with high organic content and clear, strong biological control. However, we present the results of a detailed analysis by scanning electron microscopy (SEM), thermogravimetric analysis, and electron backscatter diffraction to characterize the calcitic prisms in two different clades within the euheterodont bivalves: the extant Chama arcana and the extinct rudists. These results show that the form of prisms constructed is both closely similar between the two taxa and significantly different from those of the pteriomorph bivalves. Most notably, C. arcana and the extinct rudists lack the clear organic outer envelopes and uniform polygonal, cross-sectional appearance. Instead, they form interdigitating crystals of very varied diameters, with some crystals encapsulating others. We advocate retaining the term "fibrillar prisms" to classify these euheterodont microstructures. These fibrillar prisms are more closely similar to abiotic speleothem deposits than to the calcitic prisms of pteriomorph bivalves. We argue that calcite prism growth in euheterodonts is dominated by abiotic constraints whereas, in pteriomorphs (such as oysters, pterioids, and mussels), it is under strong biological control.

Journal ArticleDOI
TL;DR: It is speculated that Heliopora coerulea can produce biliverdin and accumulate it in the skeleton, while red corals and other Octocorallia species cannot, and will be fundamental to future ecological and physiological studies.
Abstract: Heliopora coerulea is the only species in the subclass Octocorallia that has a crystalline aragonite skeleton The skeleton has been reported to contain the blue pigment, biliverdin IXα, which is formed by heme oxygenase (HO) during heme decomposition There is little information regarding gene expression in H coerulea; therefore, the biosynthesis pathway for biliverdin IXα is poorly understood To identify the genes related to heme synthesis and degradation, metatranscripts of H coerulea and its symbiont Symbiodinium spp were sequenced and separated from the host- and symbiont-derived sequences From the metatranscriptome analyses, all genes for heme synthesis and three HOs were isolated from the host and symbiont From our phylogenetic and amino acid analysis, we noted that one of the HO isoforms in the host coral was predicted to possess HO activity However, biliverdin reductase, which reduces biliverdin to bilirubin, was not identified in the present study Similarly, biliverdin reductase was not identified in the transcripts of the red coral Corallium rubrum, a species that also belongs to Octocorallia However, genes related to heme synthesis and HO were found in C rubrum We speculate that Heliopora coerulea can produce biliverdin and accumulate it in the skeleton, while red corals and other Octocorallia species cannot Further information from molecular studies of H coerulea will provide insights into the synthesis of biliverdin IXα, the blue pigment in the hard crystalline aragonite skeleton, and will be fundamental to future ecological and physiological studies

Journal ArticleDOI
TL;DR: It is shown the importance of developing a strategy that circumvents the limitations of semiautomated annotation and applies this workflow to photosensitivity as a means to discover non-opsin photoreceptors, and there is potential for the discovery of new light-sensitive GPCRs.
Abstract: The rise of high-throughput RNA sequencing (RNA-seq) and de novo transcriptome assembly has had a transformative impact on how we identify and study genes in the phototransduction cascade of non-model organisms. But the advantage provided by the nearly automated annotation of RNA-seq transcriptomes may at the same time hinder the possibility for gene discovery and the discovery of new gene functions. For example, standard functional annotation based on domain homology to known protein families can only confirm group membership, not identify the emergence of new biochemical function. In this study, we show the importance of developing a strategy that circumvents the limitations of semiautomated annotation and apply this workflow to photosensitivity as a means to discover non-opsin photoreceptors. We hypothesize that non-opsin G-protein-coupled receptor (GPCR) proteins may have chromophore-binding lysines in locations that differ from opsin. Here, we provide the first case study describing non-opsin light-sensitive GPCRs based on tissue-specific RNA-seq data of the common bay scallop Argopecten irradians (Lamarck, 1819). Using a combination of sequence analysis and three-dimensional protein modeling, we identified two candidate proteins. We tested their photochemical properties and provide evidence showing that these two proteins incorporate 11-cis and/or all-trans retinal and react to light photochemically. Based on this case study, we demonstrate that there is potential for the discovery of new light-sensitive GPCRs, and we have developed a workflow that starts from RNA-seq assemblies to the discovery of new non-opsin, GPCR-based photopigments.

Journal ArticleDOI
TL;DR: Proteinase mRNA in tissues, other than the digestive gland, suggests potentially different roles besides digestion during ontogeny, and transcript changes reflect transcriptional regulation of the proteinases tested.
Abstract: During shrimp larval development, changes occur in molecular components. Enzyme activity and mRNA expression of proteinases were assayed in Penaeus vannamei during larval development, which consists of 5 nauplius stages, 3 protozoeal stages, 3 mysis stages, and 12 postlarval stages. Trypsin activity reached a maximum at the beginning of postlarval stages 1 and 2, and significantly decreased in subsequent postlarval stages. Chymotrypsin activity increased at the third protozoeal stage, then significantly decreased in subsequent stages. Identification of proteinase by mass spectrometry and inhibitors allowed us to track their appearance in zymograms and to distinguish between isoenzymes. Chymotrypsin BI and BII had a distinguishing pattern of appearance during larval development, which could compensate for the reduction in trypsin activity. The mRNA content of isotrypsin 21, chymotrypsin 1, and zinc proteinase was differentially expressed in larvae. Zinc proteinase and chymotrypsin 1 mRNA were expr...

Journal ArticleDOI
TL;DR: Shell morphology, especially shell thickness, is host specific and comparable in similar host species between the Atlantic and West Pacific lineages, and the most parsimonious explanation is that C. testudinaria maintained phenotypic plasticity since the lineages diverged 4–5 mya.
Abstract: Symbiotic relationships are often species specific, allowing symbionts to adapt to their host environments. Host generalists, on the other hand, have to cope with diverse environments. One coping strategy is phenotypic plasticity, defined by the presence of host-specific phenotypes in the absence of genetic differentiation. Recent work indicates that such host-specific phenotypic plasticity is present in the West Pacific lineage of the commensal barnacle Chelonibia testudinaria (Linnaeus, 1758). We investigated genetic and morphological host-specific structure in the genetically distinct Atlantic sister lineage of C. testudinaria. We collected adult C. testudinaria from loggerhead sea turtles, horseshoe crabs, and blue crabs along the eastern U.S. coast between Delaware and Florida and in the Gulf of Mexico off Mississippi. We find that shell morphology, especially shell thickness, is host specific and comparable in similar host species between the Atlantic and West Pacific lineages. We did not detect significant genetic differentiation related to host species when analyzing data from 11 nuclear microsatellite loci and mitochondrial sequence data, which is comparable to findings for the Pacific lineage. The most parsimonious explanation for these parallel patterns between distinct lineages of C. testudinaria is that C. testudinaria maintained phenotypic plasticity since the lineages diverged 4-5 mya.

Journal ArticleDOI
TL;DR: It is found that oysters continued to produce defended shells in response to predators when resources were limited, even though they grew smaller, lighter shells when deprived of food in control conditions, suggesting that predation is an important pressure in this system.
Abstract: Many prey react to predation risk by altering their phenotype to reduce their chances of being consumed but incur reductions in growth and fecundity when reacting to predators. To determine...

Journal ArticleDOI
TL;DR: The visual system of L. polyphemus is now arguably the best understood among chelicerates, and as such, it is a critical resource for furthering the understanding of the evolution and diversification of visual systems in arthropods.
Abstract: The American horseshoe crab Limulus polyphemus (Linnaeus, 1758) is one of four extant species of xiphosuran chelicerates, the sister group to arachnids. Because of their position in the arthropod family tree and because they exhibit many plesiomorphic characteristics, Xiphosura are considered a proxy for the euchelicerate ancestor and therefore important for understanding the evolution and diversification of chelicerates and arthropods. Limulus polyphemus is the most extensively studied xiphosuran, and its visual system has long been a focus of studies critical for our understanding of basic mechanisms of vision and the evolution of visual systems in arthropods. Building upon a wealth of information about the anatomy and physiology of its visual system, advances in genetic approaches have greatly expanded possibilities for understanding its biochemistry. This review focuses on studies of opsin expression in L. polyphemus, which have been significantly advanced by the availability of transcriptomes and a recent high-quality assembly of its genome. These studies show that the repertoire of expressed opsins in L. polyphemus is far larger than anticipated, that the regulation of their expression in rhabdoms is far more complex than anticipated, and that photosensitivity may be distributed widely throughout the L. polyphemus central nervous system. The visual system of L. polyphemus is now arguably the best understood among chelicerates, and as such, it is a critical resource for furthering our understanding of the evolution and diversification of visual systems in arthropods.

Journal ArticleDOI
TL;DR: This is the first report of Siderastrea stellata and its variability in the Gulf of Mexico that is supported by morphological and molecular analyses.
Abstract: The genus Siderastrea exhibits high levels of morphological variability. Some of its species share similar morphological characteristics with congeners, making their identification difficult. Siderastrea stellata has been reported as an intermediary of S. siderea and S. radians in the Brazilian reef ecosystem. In an earlier study conducted in Mexico, we detected Siderastrea colonies with morphological features that were not consistent with some siderastreid species previously reported in the Gulf of Mexico. Thus, we performed a combined morphological and molecular analysis to identify Siderastrea species boundaries from the Gulf of Mexico. Some colonies presented high morphologic variability, with characteristics that corresponded to Siderastrea stellata. Molecular analysis, using the nuclear ITS and ITS2 region, corroborated the morphological results, revealing low genetic variability between S. radians and S. stellata. Since the ITS sequences did not distinguish between Siderastrea species, we used the ITS2 region to differentiate S. stellata from S. radians. This is the first report of Siderastrea stellata and its variability in the Gulf of Mexico that is supported by morphological and molecular analyses.

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TL;DR: Overall, it appears that once larvae of C. teleta have completed development of the internal structures and physiology required for juvenile life during the precompetent period, they then upregulate the expression of chemosensory proteins and neurotransmitter receptors that will enable them to detect and transduce a settlement cue signal.
Abstract: Marine invertebrate larvae typically take hours to weeks after being released into the plankton before becoming "competent" to metamorphose. The mechanisms that govern this transition between the precompetent and metamorphically competent states are unknown. We studied gene expression patterns in precompetent and competent larvae of the salt-marsh-dwelling polychaete worm Capitella teleta (Blake, Grassle & Eckelbarger, 2009)-a species in which precompetent larvae are unusually easy to distinguish from competent larvae-to determine differences in gene expression associated with the onset of metamorphic competence. More than 1530 genes were more highly expressed in precompetent larvae, while more than 1060 genes were more highly expressed in competent larvae. Competent larvae downregulated the expression of genes belonging to gene ontologies relating to growth and development and upregulated those associated with ligand-binding transmembrane channels with possible chemo- and mechanosensory functions. Most of these channels were annotated as being from the degenerin/epithelial sodium channel family or the G-protein-coupled receptor family; proteins from these families can have chemosensory functions. Serotonin and GABA (γ-aminobutyric acid) receptors are among the genes that were upregulated in competent larvae; both have been shown to induce larvae of C. teleta and other marine invertebrates to metamorphose and are thought to be components of the signal transduction pathway that leads to metamorphosis. Overall, it appears that once larvae of C. teleta have completed development of the internal structures and physiology required for juvenile life during the precompetent period, they then upregulate the expression of chemosensory proteins and neurotransmitter receptors that will enable them to detect and transduce a settlement cue signal.

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TL;DR: Polychaetes exhibit diverse feeding strategies and diets, with some species possessing hardened teeth or jaws of varying complexity as mentioned in this paper, and some species possess complex, rigid, articulating articulations.
Abstract: Polychaetes exhibit diverse feeding strategies and diets, with some species possessing hardened teeth or jaws of varying complexity. Species in the order Eunicida have complex, rigid, artic...

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TL;DR: Investigation of whether the mRNA expression levels of selected mRNA-like genes are altered in the hyperplasic ovary of the ex-fissiparous freshwater planarian D. arabica aimed at investigating whether the transcript levels of human-like transcript (IL-1-like and TNF-α-like) were significantly higher than in the normal ovary, and amplified by real-time polymerase chain reaction some transcripts that could be similar to those amplified in human.
Abstract: The origin of infertility in the hyperplasic ovary of ex-fissiparous planarians remains poorly understood. In a previous study we demonstrated that a complex process of early autophagy, followed by apoptotic processes, occurs in the hyperplasic ovary of the freshwater planarian Dugesia arabica. The present study aimed to investigate whether the mRNA expression levels of selected mRNA-like genes are altered in the hyperplasic ovary of the ex-fissiparous freshwater planarian D. arabica compared to the normal ovary. Using human cytokine-specific primers including interleukin-1 (IL-1), interleukin-6 (IL-6), and tumor necrosis factor-alpha (TNF-α), we have successfully amplified by real-time polymerase chain reaction some transcripts that could be similar to those amplified in human. The transcript levels of the human-like transcript (IL-1-like and TNF-α-like) were significantly higher, 4.89- and 3.41-fold, respectively, in the hyperplasic ovary compared to the normal ovary (P 0.05). Immunohistochemical labeling supported the quantitative real-time PCR, showing that, like their respective mRNA expression levels, IL-1, IL-6, and TNF-α-like proteins are more highly expressed in the hyperplasic ovary than in the normal ovary.

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TL;DR: A conspicuous larval behavior consisting of repeated flexing of the postoral and posterodorsal larval arms was correlated with a larger, more complex musculature, indicating that larvalMusculature not associated with endoderm evolves in a manner that relates to differences in larvalbehavior.
Abstract: Within a common body plan, echinoid planktotrophic larvae are morphologically diverse, with variations in overall size, the length, and number of arms and the presence or absence of epiderm...

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TL;DR: The influence of size on desiccation tolerance in juveniles of the calyptraeid gastropod Crepipatella peruviana is investigated to determine the size at which they can first survive exposure to air.
Abstract: Desiccation is an important limiting factor in the intertidal zone. Generally decreasing seaward, desiccation stress can also be alleviated in wet microhabitats. Juvenile snails are generally more susceptible to desiccation than adults, and, for some species, juveniles must therefore hide in microhabitats to survive emersion. The transition from hiding in safe microhabitats to being able to survive fully exposed for the duration of low tide is not well documented. In this study, we investigated the influence of size on desiccation tolerance in juveniles of the calyptraeid gastropod Crepipatella peruviana to determine the size at which they can first survive exposure to air. Juveniles 2-13 mm long were exposed to 75% or 100% relative humidity for 0.5-6.5 hours. Juveniles smaller than 5 mm in shell length did not survive emersion at 75% relative humidity for even 0.5 hours; surprisingly, most also perished after short exposures to air at 100% relative humidity, suggesting that something other than desiccation stress may also be at play. In marked contrast, 82% of juveniles larger than 6 mm in shell length survived exposure to 75% relative humidity for the full 6.5 hours. In a field survey, no juveniles smaller than 9 mm were found on exposed rock but rather were found only in wet microhabitats. We suggest that the clearly defined size escape from desiccation may reflect a change in gill functioning or a newfound ability to retain water more effectively within the mantle cavity at low tide.

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TL;DR: It is concluded that very young (stage V) juvenile lobsters modify their shelter-seeking behavior based on prior experiences across several timescales, and Ecologically relevant variation in habitat exposure among postlarval and early juvenile lobster may influence successful recruitment in this culturally and commercially important fishery species.
Abstract: Shelter-seeking behaviors are vital for survival for a range of juvenile benthic organisms These behaviors may be innate or they may be affected by prior experience After hatching, American lobsters Homarus americanus likely first come into contact with shelter during the late postlarval (decapodid) stage, known as stage IV After the subsequent molt to the first juvenile stage (stage V), they are entirely benthic and are thought to be highly cryptic We hypothesized that postlarval (stage IV) experience with shelter would carry over into the first juvenile stage (stage V) and reduce the time needed for juveniles to locate and enter shelters (sheltering) We found some evidence of a carryover effect, but not the one we predicted: stage V juveniles with postlarval shelter experience took significantly longer to initiate sheltering We also hypothesized that stage V juveniles would demonstrate learning by relocating shelters more quickly with immediate prior experience Our findings were mixed In a maze, juveniles with immediate prior experience were faster to regain visual contact with shelter, suggesting that they had learned the location of the shelter In contrast, there was no significant effect of immediate prior experience on time to initiate sheltering in an open arena, or in the maze after juveniles had regained visual contact We conclude that very young (stage V) juvenile lobsters modify their shelter-seeking behavior based on prior experiences across several timescales Ecologically relevant variation in habitat exposure among postlarval and early juvenile lobsters may influence successful recruitment in this culturally and commercially important fishery species