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Accepted manuscript version, licensed CC BY-NC-ND 4.0. Source at https://doi.org/10.1038/s41598-018-37129-x .

Late developmental stages of the marine copepods in the genus Calanus can spend extended periods in a dormant stage (diapause) that is preceded by the accumulation of large lipid stores. We assessed how lipid metabolism during development from the C4 stage to adult is altered in response to predation risk and varying food availability, to ultimately understand more of the metabolic processes during development in Calanus copepods. We used RNA sequencing to assess if perceived predation risk in combination with varied food availability affects expression of genes associated with lipid metabolism and diapause preparation in C. finmarchicus . The lipid metabolism response to predation risk differed depending on food availability, time and life stage. Predation risk caused upregulation of lipid catabolism with high food, and downregulation with low food. Under low food conditions, predation risk disrupted lipid accumulation. The copepods showed no clear signs of diapause preparation, supporting earlier observations of the importance of multiple environmental cues in inducing diapause in C. finmarchicus . This study demonstrates that lipid metabolism is a sensitive endpoint for the interacting environmental effects of predation pressure and food availability. As diapause may be controlled by lipid accumulation, our findings may contribute towards understanding processes that can ultimately influence diapause timing.

Background Pteropods are planktonic gastropods that are considered as bio-indicators to monitor impacts of ocean acidification on marine ecosystems. In order to gain insight into their adaptive potential to future environmental changes, it is critical to use adequate molecular tools to delimit species and population boundaries and to assess their genetic connectivity. We developed a set of target capture probes to investigate genetic variation across their large-sized genome using a population genomics approach. Target capture is less limited by DNA amount and quality than other genome-reduced representation protocols, and has the potential for application on closely related species based on probes designed from one species. Results We generated the first draft genome of a pteropod, Limacina bulimoides, resulting in a fragmented assembly of 2.9 Gbp. Using this assembly and a transcriptome as a reference, we designed a set of 2899 genome-wide target capture probes for L. bulimoides. The set of probes includes 2812 single copy nuclear targets, the 28S rDNA sequence, ten mitochondrial genes, 35 candidate biomineralisation genes, and 41 non-coding regions. The capture reaction performed with these probes was highly efficient with 97% of the targets recovered on the focal species. A total of 137,938 single nucleotide polymorphism markers were obtained from the captured sequences across a test panel of nine individuals. The probes set was also tested on four related species: L. trochiformis, L. lesueurii, L. helicina, and Heliconoides inflatus, showing an exponential decrease in capture efficiency with increased genetic distance from the focal species. Sixty-two targets were sufficiently conserved to be recovered consistently across all five species. Conclusion The target capture protocol used in this study was effective in capturing genome-wide variation in the focal species L. bulimoides, suitable for population genomic analyses, while providing insights into conserved genomic regions in related species. The present study provides new genomic resources for pteropods and supports the use of target capture-based protocols to efficiently characterise genomic variation in small non-model organisms with large genomes.

Two Calanus species, C. glacialis and C. finmarchicus, due to different life strategies and environmental preferences act as an ecological indicators of Arctic Atlantification. Their high lipid content makes them important food source for higher trophic levels of Arctic ecosystems including the most abundant Northern Hemisphere's seabird, the little auk (Alle alle). Recent studies indicate a critical need for the use of molecular methods to reliably identify these two sympatric Calanus species. We performed genetic and morphology-based identification of 2600 Calanus individuals collected in little auks foraging grounds and diet in summer seasons 2019–2021 in regions of Svalbard with varying levels of Atlantification. Genetic identification proved that 40% of Calanus individuals were wrongly classified as C. finmarchicus according to morphology-based identification in both types of samples. The diet of little auks consisted almost entirely of C. glacialis even in more Atlantified regions. Due to the substantial bias in morphology-based identification, we expect that the scale of the northern expansion of boreal C. finmarchicus may have been largely overestimated and that higher costs for birds exposed to Atlantification could be mostly driven by a decrease in the size of C. glacialis rather than by shift from C. glacialis to C. finmarchicus.

Copepods of the zooplankton genus Calanus play a key role in marine ecosystems in the northern seas. Although being among the most studied organisms on Earth, due to their ecological importance, genomic resources for Calanus spp. remain scarce, mostly due to their large genome size (from 6 to 12 Gbps). As an alternative to whole‐genome sequencing in Calanus spp., we sequenced and de novo assembled transcriptomes of five Calanus species: Calanus glacialis, C. hyperboreus, C. marshallae, C. pacificus, and C. helgolandicus. Functional assignment of protein families based on clusters of orthologous genes (COG) and gene ontology (GO) annotations showed analogous patterns of protein functions across species. Phylogenetic analyses using maximum likelihood (ML) of 191 protein‐coding genes mined from RNA‐seq data fully resolved evolutionary relationships among seven Calanus species investigated (five species sequenced for this study and two species with published datasets), with gene and site concordance factors showing that 109 out of 191 protein‐coding genes support a separation between three groups: the C. finmarchicus group (including C. finmarchicus, C. glacialis, and C. marshallae), the C. helgolandicus group (including C. helgolandicus, C. sinicus, and C. pacificus) and the monophyletic C. hyperboreus group. The tree topology obtained in ML analyses was similar to a previously proposed phylogeny based on morphological criteria and cleared certain ambiguities from past studies on evolutionary relationships among Calanus species. This study contributes and improve the currently available transcriptomic resources for Calanus spp. and explore de novo transcriptome data as an alternative to whole genome sequencing to infer evolutionary relationships within the genus Calanus. Here, we sequenced, assembled, and annotated de novo transcriptomes of two species for the first time (C. hyperboreus and C. marshallae), and three species with some but limited transcriptomic data available (C. glacialis, C. helgolandicus, and C. pacificus).

Calanus finmarchicus and Calanus glacialis are keystone zooplankton species in North Atlantic and Arctic marine ecosystems because they form a link in the trophic transfer of nutritious lipids from phytoplankton to predators on higher trophic levels. These calanoid copepods spend several months of the year in deep waters in a dormant state called diapause, after which they emerge in surface waters to feed and reproduce during the spring phytoplankton bloom. Disruption of diapause timing could have dramatic consequences for marine ecosystems. In the present study, Calanus C5 copepodites were collected in a Norwegian fjord during diapause and were subsequently experimentally exposed to the water-soluble fraction of a naphthenic North Sea crude oil during diapause termination. The copepods were sampled repeatedly while progressing toward adulthood and were analyzed for utilization of lipid stores and for differential expression of genes involved in lipid metabolism. Our results indicate that water-soluble fraction exposure led to a temporary pause in lipid catabolism, suggested by (i) slower utilization of lipid stores in water-soluble fraction-exposed C5 copepodites and (ii) more genes in the β-oxidation pathway being downregulated in water-soluble fraction-exposed C5 copepodites than in the control C5 copepodites. Because lipid content and/or composition may be an important trigger for termination of diapause, our results imply that the timing of diapause termination and subsequent migration to the surface may be delayed if copepods are exposed to oil pollution during diapause or diapause termination. This delay could have detrimental effects on ecosystem dynamics.

In the Arctic shelf seas, the mesozooplankton biomass is dominated by the arctic copepod Calanus glacialis, but its boreal congeneric C. finmarchicus is expanding northwards. Even though it is already there, C. finmarchicus may not be able to truly establish itself in the Arctic seas and potentially replace C. glacialis. We compared metabolic and digestive enzyme activities of sympatric C. glacialis and C. finmarchicus from Isfjorden, Svalbard and off-shelf north of Svalbard. The seasonal regulation of anabolic and catabolic enzyme activities was generally similar for the two species, but with some interspecific differences corresponding to their ontogeny. Wake-up from overwintering started earlier in adults of C. glacialis than in C. finmarchicus, while the onset of dormancy started early in the overwintering stages of both species. Furthermore, C. glacialis showed an earlier and higher mobilization of lipase enzyme activities, indicating higher efficiency in assimilating dietary lipids compared to C. finmarchicus. Similar population sizes and population structures for C. finmarchicus off-shelf north of Svalbard and in Isfjorden support a similar origin. Still, C. finmarchicus was able to match regulation of enzyme activities to the bloom even though the bloom peaked approximately a month later off-shelf north of Svalbard, indicating that food availability is an important signal for the final step of termination of diapause. Even though the two species largely follow the same patterns of metabolic enzyme activities, the more efficient lipid anabolism of C. glacialis may give it an advantage over C. finmarchicus in high-Arctic unpredictable environments with short-pulsed primary production regimes.

In the North Atlantic and the Arctic Ocean, four species of the copepod genus Calanus dominate the zooplankton biomass. Because of their morphological resemblance, knowledge of their respective distribution range has long been biased by misidentification, until the recent use of molecular tools uncovered numerous areas of sympatry. As hybridization between Calanus finmarchicus and Calanus glacialis has been claimed in the East-Canadian Arctic based on microsatellites, we investigated further the potential for interbreeding in newly uncovered areas of sympatry. Calanus species and stage composition were analyzed during winter in two Norwegian subarctic fjords, using molecular markers developed specifically for species identification and hybrid detection between C. finmarchicus and C. glacialis. Overall, C. glacialis were the most abundant throughout the winter, followed by C. finmarchicus and Calanus hyperboreus with only a few records of Calanus helgolandicus. The presence of C. glacialis, C. hyperboreus, and C. finmarchicus’ nauplii was recorded, indicating that these species reproduce locally. In January and February, the simultaneous occurrence of males and females of both C. finmarchicus and C. glacialis suggested a potential for interspecies mating. However, genetic admixture tests performed on all 1126 individuals revealed no signal of hybridization, implying a strong reproductive isolation mechanism. We conclude that no evidence supports a potential for hybridization between C. finmarchicus and C. glacialis.

Abstract Genetic variation is instrumental for adaptation to changing environments but it is unclear how it is structured and contributes to adaptation in pelagic species lacking clear barriers to gene flow. Here, we applied comparative genomics to extensive transcriptome datasets from 20 krill species collected across the Atlantic, Indian, Pacific, and Southern Oceans. We compared genetic variation both within and between species to elucidate their evolutionary history and genomic bases of adaptation. We resolved phylogenetic interrelationships and uncovered genomic evidence to elevate the cryptic Euphausia similis var. armata into species. Levels of genetic variation and rates of adaptive protein evolution vary widely. Species endemic to the cold Southern Ocean, such as the Antarctic krill Euphausia superba, showed less genetic variation and lower evolutionary rates than other species. This could suggest a low adaptive potential to rapid climate change. We uncovered hundreds of candidate genes with signatures of adaptive evolution among Antarctic Euphausia but did not observe strong evidence of adaptive convergence with the predominantly Arctic Thysanoessa. We instead identified candidates for cold-adaptation that have also been detected in Antarctic fish, including genes that govern thermal reception such as TrpA1. Our results suggest parallel genetic responses to similar selection pressures across Antarctic taxa and provide new insights into the adaptive potential of important zooplankton already affected by climate change.