Antarctic marine species have evolved in one of the coldest and most temperature-stable marine environments on Earth. They have long been classified as being stenothermal, or having a poor capacity to resist warming. Here we show that their ability to acclimate their physiology to elevated temperatures is poor compared with species from temperate latitudes, and similar to those from the tropics. Those species that have been demonstrated to acclimate take a very long time to do so, with Antarctic fish requiring up to 21-36 days to acclimate, which is 2-4 times as long as temperate species, and invertebrates requiring between 2 and 5 months to complete whole-animal acclimation. Investigations of upper thermal tolerance (CT(max)) in Antarctic marine species have shown that as the rate of warming is reduced in experiments, CT(max) declines markedly, ranging from 8 to 17.5 °C across 13 species at a rate of warming of 1 °C day(-1), and from 1 to 6 °C at a rate of 1 °C month(-1). This effect of the rate of warming on CT(max) also appears to be present at all latitudes. A macrophysiological analysis of long-term CT(max) across latitudes for marine benthic groups showed that both Antarctic and tropical species were less resistant to elevated temperatures in experiments and thus had lower warming allowances (measured as the difference between long-term CT(max) and experienced environmental temperature), or warming resistance, than temperate species. This makes them more at risk from warming than species from intermediate latitudes. This suggests that the variability of environmental temperature may be a major factor in dictating an organism's responses to environmental change.
RNA-Seq transcriptome data were generated from mantle tissue of the great scallop, Pecten maximus. The consensus data were produced from a time course series of animals subjected to a 56-day thermal challenge at 3 different temperatures. A total of 26,064 contigs were assembled de novo, providing a useful resource for both the aquaculture community and researchers with an interest in mollusc shell production.
The co-authors of this paper hereby state their intention to work together to launch the Genomic Observatories Network (GOs Network) for which this document will serve as its Founding Charter. We define a Genomic Observatory as an ecosystem and/or site subject to long-term scientific research, including (but not limited to) the sustained study of genomic biodiversity from single-celled microbes to multicellular organisms.An international group of 64 scientists first published the call for a global network of Genomic Observatories in January 2012. The vision for such a network was expanded in a subsequent paper and developed over a series of meetings in Bremen (Germany), Shenzhen (China), Moorea (French Polynesia), Oxford (UK), Pacific Grove (California, USA), Washington (DC, USA), and London (UK). While this community-building process continues, here we express our mutual intent to establish the GOs Network formally, and to describe our shared vision for its future. The views expressed here are ours alone as individual scientists, and do not necessarily represent those of the institutions with which we are affiliated.
Isolated and established in culture from the Antarctic in 1988, the nematode Panagrolaimus davidi has proven to be an ideal model for the study of adaptation to the cold. Not only is it the best-documented example of an organism surviving intracellular freezing but it is also able to undergo cryoprotective dehydration. As part of an ongoing effort to develop a molecular understanding of this remarkable organism, we have assembled both a transcriptome and a set of genomic scaffolds. We provide an overview of the transcriptome and a survey of genes involved in temperature stress. We also explore, in silico, the possibility that P. davidi will be susceptible to an environmental RNAi response, important for further functional studies.
Metabolic rate is a key component of energy budgets that scales with body size and varies with large-scale environmental geographical patterns. Here we conduct an analysis of standard metabolic rates (SMR) of marine ectotherms across a 70° latitudinal gradient in both hemispheres that spanned collection temperatures of 0-30 °C. To account for latitudinal differences in the size and skeletal composition between species, SMR was mass normalized to that of a standard-sized (223 mg) ash-free dry mass individual. SMR was measured for 17 species of calcified invertebrates (bivalves, gastropods, urchins and brachiopods), using a single consistent methodology, including 11 species whose SMR was described for the first time. SMR of 15 out of 17 species had a mass-scaling exponent between 2/3 and 1, with no greater support for a 3/4 rather than a 2/3 scaling exponent. After accounting for taxonomy and variability in parameter estimates among species using variance-weighted linear mixed effects modelling, temperature sensitivity of SMR had an activation energy (Ea) of 0.16 for both Northern and Southern Hemisphere species which was lower than predicted under the metabolic theory of ecology (Ea 0.2-1.2 eV). Northern Hemisphere species, however, had a higher SMR at each habitat temperature, but a lower mass-scaling exponent relative to SMR. Evolutionary trade-offs that may be driving differences in metabolic rate (such as metabolic cold adaptation of Northern Hemisphere species) will have important impacts on species abilities to respond to changing environments.
Understanding the environmental responses of an invasive species is critical in predicting how ecosystem composition may be transformed in the future, especially under climate change. In this study, Crassostrea gigas, a species well adapted to the highly variable intertidal environment, was exposed to the chronic environmental challenges of temperature (19 and 24°C) and pH (ambient seawater and a reduction of 0.4 pH units) in an extended 3-month laboratory-based study. Physiological parameters were measured (condition index, shell growth, respiration, excretion rates, O:N ratios, and ability to repair shell damage) alongside molecular analyses. Temperature was by far the most important stressor, as demonstrated by reduced condition indexes and shell growth at 24°C, with relatively little effect detected for pH. Transcriptional profiling using candidate genes and SOLiD sequencing of mantle tissue revealed that classical "stress" genes, previously reported to be upregulated under acute temperature challenges, were not significantly expressed in any of the treatments, emphasizing the different response between acute and longer term chronic stress. The transcriptional profiling also elaborated on the cellular responses underpinning the physiological results, including the identification of the PI3K/AKT/mTOR pathway as a potentially novel marker for chronic environmental challenge. This study represents a first attempt to understand the energetic consequences of cumulative thermal stress on the intertidal C. gigas which could significantly impact on coastal ecosystem biodiversity and function in the future.
Future oceans are predicted to contain less oxygen than at present. This is because oxygen is less soluble in warmer water and predicted stratification will reduce mixing. Hypoxia in marine environments is thus likely to become more widespread in marine environments and understanding species-responses is important to predicting future impacts on biodiversity. This study used a tractable model, the Antarctic clam, Laternula elliptica, which can live for 36 years, and has a well-characterized ecology and physiology to understand responses to hypoxia and how the effect varied with age. Younger animals had a higher condition index, higher adenylate energy charge and transcriptional profiling indicated that they were physically active in their response to hypoxia, whereas older animals were more sedentary, with higher levels of oxidative damage and apoptosis in the gills. These effects could be attributed, in part, to age-related tissue scaling; older animals had proportionally less contractile muscle mass and smaller gills and foot compared with younger animals, with consequential effects on the whole-animal physiological response. The data here emphasize the importance of including age effects, as large mature individuals appear to be less able to resist hypoxic conditions and this is the size range that is the major contributor to future generations. Thus, the increased prevalence of hypoxia in future oceans may have marked effects on benthic organisms abilities to persist and this is especially so for long-lived species when predicting responses to environmental perturbation.
The Ice krill, Euphausia crystallorophias is one of the species at the base of the Southern Ocean food chain. Given their significant contribution to the biomass of the Southern Ocean, it is vitally important to gain a better understanding of their physiology and, in particular, anticipate their responses to climate change effects in the warming seas around Antarctica.
Juvenile stages are often thought to be less resistant to thermal challenges than adults, yet few studies make direct comparisons using the same methods between different life history stages. We tested the resilience of juvenile stages compared to adults in 4 species of Antarctic marine invertebrate over 3 different rates of experimental warming. The species used represent 3 phyla and 4 classes, and were the soft-shelled clam Laternula elliptica, the sea cucumber Cucumaria georgiana, the sea urchin Sterechinus neumayeri, and the seastar Odontaster validus. All four species are widely distributed, locally abundant to very abundant and are amongst the most important in the ecosystem for their roles. At the slowest rate of warming used (1°C 3 days(-1)) juveniles survived to higher temperatures than adults in all species studied. At the intermediate rate (1°C day(-1)) juveniles performed better in 3 of the 4 species, with no difference in the 4(th), and at the fastest rate of warming (1°C h(-1)) L. elliptica adults survived to higher temperatures than juveniles, but in C. georgiana juveniles survived to higher temperatures than adults and there were no differences in the other species. Oxygen limitation may explain the better performance of juveniles at the slower rates of warming, whereas the loss of difference between juveniles and adults at the fastest rate of warming suggests another mechanism sets the temperature limit here.
Understanding the relationship between life-history variation and population structure in marine invertebrates is not straightforward. This is particularly true of polar species due to the difficulty of obtaining samples and a paucity of genomic resources from which to develop nuclear genetic markers. Such knowledge, however, is essential for understanding how different taxa may respond to climate change in the most rapidly warming regions of the planet. We therefore used over two hundred polymorphic Amplified Fragment Length Polymorphisms (AFLPs) to explore population connectivity at three hierachical spatial scales in the direct developing Antarctic topshell Margarella antarctica. To previously published data from five populations spanning a 1500 km transect along the length of the Western Antarctic Peninsula, we added new AFLP data for four populations separated by up to 6 km within Ryder Bay, Adelaide Island. Overall, we found a nonlinear isolation-by-distance pattern, suggestive of weaker population structure within Ryder Bay than is present over larger spatial scales. Nevertheless, significantly positive F st values were obtained in all but two of ten pairwise population comparisons within the bay following Bonferroni correction for multiple tests. This is in contrast to a previous study of the broadcast spawner Nacella concinna that found no significant genetic differences among several of the same sites. By implication, the topshells direct-developing lifestyle may constrain its ability to disperse even over relatively small geographic scales.
Insects in the field are exposed to multiple bouts of cold, and there is increasing evidence that the fitness consequences of repeated cold exposure differ from the impacts of a single cold exposure. We tested the hypothesis that different kinds of cold exposure (in this case, single short, prolonged and repeated cold exposure) would result in differential gene expression. We exposed 3 day old adult female wild-type Drosophila melanogaster (Diptera: Drosophilidae) to -0.5°C for a single 2 h exposure, a single 10 h exposure, or five 2 h exposures on consecutive days, and extracted RNA after 6 h of recovery. Global gene expression was quantified using an oligonucleotide microarray and validated with real-time PCR using different biological replicates. We identified 76 genes upregulated in response to multiple cold exposure, 69 in response to prolonged cold exposure and 20 genes upregulated in response to a single short cold exposure, with a small amount of overlap between treatments. Three genes--Turandot A, Hephaestus and CG11374--were upregulated in response to all three cold exposure treatments. Key functional groups upregulated include genes associated with muscle structure and function, the immune response, stress response, carbohydrate metabolism and egg production. We conclude that cold exposure has wide-ranging effects on gene expression in D. melanogaster and that increased duration or frequency of cold exposure has impacts different to those of a single short cold exposure. This has important implications for extrapolating laboratory studies of insect overwintering that are based on only a single cold exposure.
Fish scales are an important reservoir of calcium and phosphorus and together with the skin function as an integrated barrier against environmental changes and external aggressors. Histological studies have revealed that the skin and scales regenerate rapidly in fish when they are lost or damaged. In the present manuscript the histological and molecular changes underlying skin and scale regeneration in fed and fasted sea bream (Sparus auratus) were studied using a microarray 3 and 7 days after scale removal to provide a comprehensive molecular understanding of the early stages of these processes.
Animal physiology, ecology and evolution are affected by temperature and it is expected that community structure will be strongly influenced by global warming. This is particularly relevant in the tropics, where organisms are already living close to their upper temperature limits and hence are highly vulnerable to rising temperature. Here we present data on upper temperature limits of 34 tropical marine ectotherm species from seven phyla living in intertidal and subtidal habitats. Short term thermal tolerances and vertical distributions were correlated, i.e., upper shore animals have higher thermal tolerance than lower shore and subtidal animals; however, animals, despite their respective tidal height, were susceptible to the same temperature in the long term. When temperatures were raised by 1°C hour(-1), the upper lethal temperature range of intertidal ectotherms was 41-52°C, but this range was narrower and reduced to 37-41°C in subtidal animals. The rate of temperature change, however, affected intertidal and subtidal animals differently. In chronic heating experiments when temperature was raised weekly or monthly instead of every hour, upper temperature limits of subtidal species decreased from 40°C to 35.4°C, while the decrease was more than 10°C in high shore organisms. Hence in the long term, activity and survival of tropical marine organisms could be compromised just 2-3°C above present seawater temperatures. Differences between animals from environments that experience different levels of temperature variability suggest that the physiological mechanisms underlying thermal sensitivity may vary at different rates of warming.
The Antarctic krill Euphausia superba is a keystone species in the Antarctic food chain. Not only is it a significant grazer of phytoplankton, but it is also a major food item for charismatic megafauna such as whales and seals and an important Southern Ocean fisheries crop. Ecological data suggest that this species is being affected by climate change and this will have considerable consequences for the balance of the Southern Ocean ecosystem. Hence, understanding how this organism functions is a priority area and will provide fundamental data for life history studies, energy budget calculations and food web models.
The gilthead sea bream, Sparus auratus, and the European sea bass, Dicentrarchus labrax, are two of the most important marine species cultivated in Southern Europe. This study aimed at increasing genomic resources for the two species and produced and annotated two sets of 30,000 expressed sequence tags (EST) each from 14 normalized tissue-specific cDNA libraries from sea bream and sea bass. Clustering and assembly of the ESTs formed 5268 contigs and 12,928 singletons for sea bream and 4573 contigs and 13,143 singletons for sea bass, representing 18,196 and 17,716 putative unigenes, respectively. Assuming a similar number of genes in sea bass, sea bream and in the model fish Gasterosteus aculeatus genomes, it was estimated that approximately two thirds of the sea bream and the sea bass transcriptomes were covered by the unigene collections. BLAST sequence similarity searches (using a cut off of e-value <10(-5)) against fully the curated SwissProt (and TrEMBL) databases produced matches of 28%(37%) and 43%(53%) of the sea bream and sea bass unigene datasets respectively, allowing some putative designation of function. A comparative approach is described using human Ensembl peptide ID homologs for functional annotation, which increased the number of unigenes with GO terms assigned and resulted in more GO terms assigned per unigene. This allowed the identification of tissue-specific genes using enrichment analysis for GO pathways and protein domains. The comparative annotation approach represents a good strategy for transferring more relevant biological information from highly studied species to genomic resource poorer species. It was possible to confirm by interspecies mRNA-to-genomic alignments 25 and 21 alternative splice events in sea bream and sea bass genes, respectively. Even using normalized cDNA from relatively few pooled individuals it was possible to identify 1145 SNPs and 1748 microsatellites loci for genetic marker development. The EST data are being applied to a range of projects, including the development microarrays, genetic and radiation hybrid maps and QTL genome scans. This highlights the important role of ESTs for generating genetic and genomic resources of aquaculture species.
The Antarctic clam, Laternula elliptica, is an infaunal stenothermal bivalve mollusc with a circumpolar distribution. It plays a significant role in bentho-pelagic coupling and hence has been proposed as a sentinel species for climate change monitoring. Previous studies have shown that this mollusc displays a high level of plasticity with regard to shell deposition and damage repair against a background of genetic homogeneity. The Southern Ocean has amongst the lowest present-day CaCO3 saturation rate of any ocean region, and is predicted to be among the first to become undersaturated under current ocean acidification scenarios. Hence, this species presents as an ideal candidate for studies into the processes of calcium regulation and shell deposition in our changing ocean environments.
Microscopic monogonont rotifers, including the euryhaline species Brachionus plicatilis, are typically found in water bodies where environmental factors restrict population growth to short periods lasting days or months. The survival of the population is ensured via the production of resting eggs that show a remarkable tolerance to unfavorable conditions and remain viable for decades. The aim of this study was to generate Expressed Sequence Tags (ESTs) for molecular characterisation of processes associated with the formation of resting eggs, their survival during dormancy and hatching.
The Antarctic limpet, Nacella concinna, exhibits the classical heat shock response, with up-regulation of duplicated forms of the inducible heat shock protein 70 (HSP70) gene in response to experimental manipulation of seawater temperatures. However, this response only occurs in the laboratory at temperatures well in excess of any experienced in the field. Subsequent environmental sampling of inter-tidal animals also showed up-regulation of these genes, but at temperature thresholds much lower than those required to elicit a response in the laboratory. It was hypothesised that this was a reflection of the complexity of the stresses encountered in the inter-tidal region. Here, we describe a further series of experiments comprising both laboratory manipulation and environmental sampling of N. concinna. We investigate the expression of HSP70 gene family members (HSP70A, HSP70B, GRP78 and HSC70) in response to a further suite of environmental stressors: seasonal and experimental cold, freshwater, desiccation, chronic heat and periodic emersion. Lowered temperatures (-1.9 degrees C and -1.6 degrees C), generally produced a down-regulation of all HSP70 family members, with some up-regulation of HSC70 when emerging from the winter period and increasing sea temperatures. There was no significant response to freshwater immersion. In response to acute and chronic heat treatments plus simulated tidal cycles, the data showed a clear pattern. HSP70A showed a strong but very short-term response to heat whilst the duplicated HSP70B also showed heat to be a trigger, but had a more sustained response to complex stresses. GRP78 expression indicates that it was acting as a generalised stress response under the experimental conditions described here. HSC70 was the major chaperone invoked in response to long-term stresses of varying types. These results provide intriguing clues not only to the complexity of HSP70 gene expression in response to environmental change but also insights into the stress response of a non-model species.
Insects provide tractable models for enhancing our understanding of the physiological and cellular processes that enable survival at extreme low temperatures. They possess three main strategies to survive the cold: freeze tolerance, freeze avoidance or cryoprotective dehydration, of which the latter method is exploited by our model species, the Arctic springtail Megaphorura arctica, formerly Onychiurus arcticus (Tullberg 1876). The physiological mechanisms underlying cryoprotective dehydration have been well characterised in M. arctica and to date this process has been described in only a few other species: the Antarctic nematode Panagrolaimus davidi, an enchytraied worm, the larvae of the Antarctic midge Belgica antarctica and the cocoons of the earthworm Dendrobaena octaedra. There are no in-depth molecular studies on the underlying cold survival mechanisms in any species.
Brittle stars are included within a whole range of species, which contribute to knowledge in the medically important area of tissue regeneration. All brittle stars regenerate lose limbs, but the rate at which this occurs is highly variable and species-specific. One of the slowest rates of arm regeneration reported so far is that of the Antarctic Ophionotus victoriae. Additionally, O. victoriae also has an unusual delay in the onset of regeneration of about 5months. Both processes are of interest for the areas of regeneration biology and adaptation to cold environments. One method of understanding the details of regeneration events in brittle stars is to characterise the genes involved. In the largest transcriptome study of any ophiuroid to date, we describe the results of mRNA pyrosequencing from pooled samples of regenerating arms of O. victoriae. The sequencing reads resulted in 18,000 assembled contiguous sequences of which 19% were putatively annotated by blast sequence similarity searching. We focus on the identification of major gene families and pathways with potential relevance to the regenerative processes including the Wnt/?-catenin pathway, Hox genes, the SOX gene family and the TGF beta signalling pathways. These data significantly increase the amount of ophiuroid sequences publicly available and provide candidate transcripts for the further investigation of the unusual regenerative process in this Antarctic ophiuroid.
The Arctic springtail, Megaphorura arctica, survives sub-zero temperatures in a dehydrated state via trehalose-dependent cryoprotective dehydration. Regulation of trehalose biosynthesis is complex; based in part on studies in yeast and fungi, its connection with oxidative stress caused by exposure of cells to oxidants, such as hydrogen peroxide (H?O?), or dehydration, is well documented. In this respect, we measured the amount of H?O? and antioxidant enzyme activities (superoxide dismutases: copper, zinc--CuZnSOD and manganese containing--MnSOD, and catalase--CAT), as the regulatory components determining H?O? concentrations, in Arctic springtails incubated at 5 °C (control) versus -2 °C (threshold temperature for trehalose biosynthesis). Because ecdysone also stimulates trehalose production in insects and regulates the expression of genes involved in redox homeostasis and antioxidant protection in Drosophila, we measured the levels of the active physiological form of ecdysone--20-hydroxyecdysone (20-HE). Significantly elevated H?O? and 20-HE levels were observed in M. arctica incubated at -2 °C, supporting a link between ecdysone, H?O?, and trehalose levels during cryoprotective dehydration. CAT activity was found to be significantly lower in M. arctica incubated at -2 °C versus 5 °C, suggesting reduced H?O? breakdown. Furthermore, measurement of the free radical composition in Arctic springtails incubated at 5 °C (controls) versus -2 °C by Electron Paramagnetic Resonance spectroscopy revealed melanin-derived free radicals at -2 °C, perhaps an additional source of H?O?. Our results suggest that H?O? and ecdysone play important roles in the cryoprotective dehydration process in M. arctica, linked with the regulation of trehalose biosynthesis.
We document differences in shell damage and shell thickness in a bivalve mollusc (Laternula elliptica) from seven sites around Antarctica with differing exposures to ice movement. These range from 60% of the sea bed impacted by ice per year (Hangar Cove, Antarctic Peninsula) to those protected by virtually permanent sea ice cover (McMurdo Sound). Patterns of shell damage consistent with blunt force trauma were observed in populations where ice scour frequently occurs; damage repair frequencies and the thickness of shells correlated positively with the frequency of iceberg scour at the different sites with the highest repair rates and thicker shells at Hangar Cove (74.2% of animals damaged) compared to the other less impacted sites (less than 10% at McMurdo Sound). Genetic analysis of population structure using Amplified Fragment Length Polymorphisms (AFLPs) revealed no genetic differences between the two sites showing the greatest difference in shell morphology and repair rates. Taken together, our results suggest that L. elliptica exhibits considerable phenotypic plasticity in response to geographic variation in physical disturbance.
Several recent empirical studies have challenged the prevailing dogma that broadcast-spawning species exhibit little or no population genetic structure by documenting genetic discontinuities associated with large-scale oceanographic features. However, relatively few studies have explored patterns of genetic differentiation over fine spatial scales. Consequently, we used a hierarchical sampling design to investigate the basis of a weak but significant genetic difference previously reported between Antarctic limpets (Nacella concinna) sampled from Adelaide and Galindez Islands near the base of the Antarctic Peninsula. Three sites within Ryder Bay, Adelaide Island (Rothera Point, Leonie and Anchorage Islands) were each sub-sampled three times, yielding a total of 405 samples that were genotyped at 155 informative Amplified Fragment Length Polymorphisms (AFLPs). Contrary to our initial expectations, limpets from Anchorage Island were found to be subtly, but significantly distinct from those sampled from the other sites. This suggests that local processes may play an important role in generating fine-scale population structure even in species with excellent dispersal capabilities, and highlights the importance of sampling at multiple spatial scales in population genetic surveys.
Several organisms display dormancy and developmental arrest at embryonic stages. Long-term survival in the dormant form is usually associated with desiccation, orthodox plant seeds and Artemia cysts being well documented examples. Several aquatic invertebrates display dormancy during embryonic development and survive for tens or even hundreds of years in a hydrated form, raising the question of whether survival in the non-desiccated form of embryonic development depends on pathways similar to those occurring in desiccation tolerant forms.
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