Rare, long-distance dispersal underpins genetic connectivity in the pink sea fan, Eunicella verrucosa.

Characterizing patterns of genetic connectivity in marine species is of critical importance given the anthropogenic pressures placed on the marine environment. For sessile species, population connectivity can be shaped by many processes, such as pelagic larval duration, oceanographic boundaries and currents. This study combines restriction-site associated DNA sequencing (RADseq) and passive particle dispersal modelling to delineate patterns of population connectivity in the pink sea fan, Eunicella verrucosa, a temperate octocoral. Individuals were sampled from 20 sites covering most of the species' northeast Atlantic range, and a site in the northwest Mediterranean Sea to inform on connectivity across the Atlantic-Mediterranean transition. Using 7510 neutral SNPs, a geographic cline of genetic clusters was detected, partitioning into Ireland, Britain, France, Spain (Atlantic), and Portugal and Spain (Mediterranean). Evidence of significant inbreeding was detected at all sites, a finding not detected in a previous study of this species based on microsatellite loci. Genetic connectivity was characterized by an isolation by distance pattern (IBD) (r 2 = 0.78, p < 0.001), which persisted across the Mediterranean-Atlantic boundary. In contrast, exploration of ancestral population assignment using the program ADMIXTURE indicated genetic partitioning across the Bay of Biscay, which we suggest represents a natural break in the species' range, possibly linked to a lack of suitable habitat. As the pelagic larval duration (PLD) is unknown, passive particle dispersal simulations were run for 14 and 21 days. For both modelled PLDs, inter-annual variations in particle trajectories suggested that in a long-lived, sessile species, range-wide IBD is driven by rare, longer dispersal events that act to maintain gene flow. These results suggest that oceanographic patterns may facilitate range-wide stepping-stone genetic connectivity in E. verrucosa and highlight that both oceanography and natural breaks in a species' range should be considered in the designation of ecologically coherent MPA networks.

mapmixture: An R package and web app for spatial visualisation of admixture and population structure.

The mapmixture R package and interactive web app are tools to aid visualisation of admixture and population structure in geographic space. The purpose of mapmixture is to enable and encourage molecular ecologists, and in particular population geneticists and phylogeneticists, to plot their admixture, ancestry or assignment results on a map when location information is available. mapmixture accepts data in the format typically generated by admixture analyses and visualises proportions to each genetic cluster per site as pie charts on a projected (optional) map. Combining this site-based map presentation approach with the routine individual-based presentation of admixture (structure) barplots will enhance interpretation of genetic-geographic patterns. Additionally, in the context of science communication, this enables clearer transfer of spatial genetic information to readers or listeners, and especially to audiences that do not have a background in genetics but who are able to use the genetic information as evidence in conservation management. The latest version of mapmixture is available on GitHub (https://github.com/tom-jenkins/mapmixture), which details installation instructions and examples of how to use the package and interactive web app.

The First Genome of the Cold-Water Octocoral, the Pink Sea Fan, Eunicella verrucosa.

Cold-water corals form an important part of temperate benthic ecosystems by increasing three-dimensionality and providing an important ecological substrate for other benthic fauna. However, the fragile three-dimensional structure and life-history characteristics of cold-water corals can leave populations vulnerable to anthropogenic disturbance. Meanwhile, the ability of temperate octocorals, particularly shallow-water species, to respond to adjustments in their environment linked to climate change has not been studied. This study reports the first genome assembly of the pink sea fan (Eunicella verrucosa), a temperate shallow-water octocoral species. We produced an assembly of 467 Mb, comprising 4,277 contigs and an N50 of 250,417 bp. In total, 213 Mb (45.96% of the genome) comprised repetitive sequences. Annotation of the genome using RNA-seq data derived from polyp tissue and gorgonin skeleton resulted in 36,099 protein-coding genes after 90% similarity clustering, capturing 92.2% of the complete Benchmarking Universal Single-Copy Orthologs (BUSCO) ortholog benchmark genes. Functional annotation of the proteome using orthology inference identified 25,419 annotated genes. This genome adds to the very few genomic resources currently available in the octocoral community and represents a key step in allowing scientists to investigate the genomic and transcriptomic responses of octocorals to climate change.

Predicting habitat suitability and range shifts under projected climate change for two octocorals in the north-east Atlantic.

Species distribution models have become a valuable tool to predict the distribution of species across geographic space and time. In this study, maximum entropy models were constructed for two temperate shallow-water octocoral species, the pink sea fan (Eunicella verrucosa) and dead man's fingers (Alcyonium digitatum), to investigate and compare habitat suitability. The study area covered the north-east Atlantic from the Bay of Biscay to the British Isles and southern Norway; this area includes both the northern range of E. verrucosa and the middle-northern range of A. digitatum. The optimal models for each species showed that, overall, slope, temperature at the seafloor and wave orbital velocity were important predictors of distribution in both species. Predictions of habitat suitability showed areas of present-day (1951-2000) suitable habitat where colonies have not yet been observed, particularly for E. verrucosa, where areas beyond its known northern range limit were identified. Moreover, analysis with future layers (2081-2100) of temperature and oxygen concentration predicted a sizable increase in habitat suitability for E. verrucosa beyond these current range limits under the Representative Concentration Pathway 8.5 scenario. This suggests that projected climate change may induce a potential range expansion northward for E. verrucosa, although successful colonisation would also be conditional on other factors such as dispersal and interspecific competition. For A. digitatum, this scenario of projected climate change may result in more suitable habitat in higher latitudes, but, as with E. verrucosa, there is a degree of uncertainty in the model predictions. Importantly, the results from this study highlight present-day areas of high habitat suitability which, if combined with knowledge on population density, could be used to identify priority areas to enhance protection and ensure the long-term survival of these octocoral species in the region.

The complete mitochondrial genome of the pink sea fan, Eunicella verrucosa (Pallas, 1766).

The pink sea fan, Eunicella verrucosa (Pallas, 1766), inhabits rocky substrates across the northeast Atlantic and the western Mediterranean. Across much of its range it has been detrimentally affected by fishing. DNA from 17 E. verrucosa specimens was amplified by phi29-induced rolling circle amplification. Following purification by sodium acetate-ethanol precipitation, the circular genomic DNA was sequenced on an Illumina MiSeq v2. Specimens originated from sites along the west coast of Ireland, southwest Wales, southwest/southern England, northwest France, southern Portugal, and the Mediterranean coast of northeast Spain. All samples had identical mitochondrial genome sequences of 19,267 bp and included 14 protein-coding genes (including the mutS gene), two ribosomal RNA subunits (12S and 16S) and one methionine tRNA gene. Two genes (nad2 and nad5) overlapped by 13 bp; all other genes were separated by non-coding intergenic regions. All protein-coding genes had the same start codon (ATG) and a TAA or TAG stop codon, except for cox1 that terminated with the incomplete stop codon T--. The mitochondrial genome of E. verrucosa (MW588805) showed 99.72% similarity with that of a related sea fan species, Eunicella cavolini, with six SNPs and a 49 bp deletion between nad5 and nad4 in E. verrucosa distinguishing the two.

Whole genome genotyping reveals discrete genetic diversity in north-east Atlantic maerl beds.

Maerl beds are vital habitats for a diverse array of marine species across trophic levels, but they are increasingly threatened by human activities and climate change. Furthermore, little is known about the genetic diversity of maerl-forming species and the population structure of maerl beds, both of which are important for understanding the ability of these species to adapt to changing environments and for informing marine reserve planning. In this study, we used a whole genome genotyping approach to explore the population genomics of Phymatolithon calcareum, a maerl-forming red algal species, whose geographical distribution spans the north-east Atlantic, from Norway to Portugal. Our results, using 14,150 genome-wide SNPs (single nucleotide polymorphisms), showed that P. calcareum maerl beds across the north-east Atlantic are generally structured geographically, a pattern likely explained by low dispersal potential and limited connectivity between regions. Additionally, we found that P. calcareum from the Fal Estuary, south-west England, is genetically distinct from all other P. calcareum sampled, even from The Manacles, a site located only 13 km away. Further analysis revealed that this finding is not the result of introgression from two closely related species, Phymatolithon purpureum or Lithothamnion corallioides. Instead, this unique diversity may have been shaped over time by geographical isolation of the Fal Estuary maerl bed and a lack of gene flow with other P. calcareum populations. The genomic data presented in this study suggest that P. calcareum genetic diversity has accumulated over large temporal and spatial scales, the preservation of which will be important for maximizing the resilience of this species to changes in climate and the environment. Moreover, our findings underline the importance of managing the conservation of maerl beds across western Europe as distinct units, at a site-by-site level.

Historical translocations and stocking alter the genetic structure of a Mediterranean lobster fishery.

Stocking is often used to supplement wild populations that are overexploited or have collapsed, yet it is unclear how this affects the genetic diversity of marine invertebrate populations. During the 1970s, a lobster stock enhancement program was carried out around the island of Corsica in the Mediterranean using individuals translocated from the Atlantic coast of France. This included the release of thousands of hatchery-reared postlarval lobsters and several adult individuals, but no monitoring plan was established to assess whether these animals survived and recruited to the population. In this study, we sampled European lobster (Homarus gammarus) individuals caught around Corsica and tested whether they showed Atlantic ancestry. Due to a natural marked phylogeographic break between Atlantic and Mediterranean lobsters, we hypothesized that lobsters with dominant (>0.50) Atlantic ancestry were descended from historical stocking releases. Twenty Corsican lobsters were genotyped at 79 single nucleotide polymorphisms, and assignment analysis showed that the majority (13) had dominant Atlantic ancestry. This suggests that the hatchery stocking program carried out in Corsica during the 1970s, using individuals translocated from the Atlantic coast of France, has likely augmented local recruitment but at a cost of altering the genetic structure of the Corsican lobster population.

Crossing the pond: genetic assignment detects lobster hybridisation.

American lobsters (Homarus americanus) imported live into Europe as a seafood commodity have occasionally been released or escaped into the wild, within the range of an allopatric congener, the European lobster (H. gammarus). In addition to disease and competition, introduced lobsters threaten native populations through hybridisation, but morphological discriminants used for species identification are unable to discern hybrids, so molecular methods are required. We tested an array of 79 single nucleotide polymorphisms (SNPs) for their utility to distinguish 1,308 H. gammarus from 38 H. americanus and 30 hybrid offspring from an American female captured in Sweden. These loci provide powerful species assignment in Homarus, enabling the robust identification of hybrid and American individuals among a survey of European stock. Moreover, a subset panel of the 12 most powerful SNPs is sufficient to separate the two pure species, even when tissues have been cooked, and can detect the introduced component of hybrids. We conclude that these SNP loci can unambiguously identify hybrid lobsters that may be undetectable via basic morphology, and offer a valuable tool to investigate the prevalence of cryptic hybridisation in the wild. Such investigations are required to properly evaluate the potential for introgression of alien genes into European lobster populations.

Harnessing genomics to fast-track genetic improvement in aquaculture.

Aquaculture is the fastest-growing farmed food sector and will soon become the primary source of fish and shellfish for human diets. In contrast to crop and livestock production, aquaculture production is derived from numerous, exceptionally diverse species that are typically in the early stages of domestication. Genetic improvement of production traits via well-designed, managed breeding programmes has great potential to help meet the rising seafood demand driven by human population growth. Supported by continuous advances in sequencing and bioinformatics, genomics is increasingly being applied across the broad range of aquaculture species and at all stages of the domestication process to optimize selective breeding. In the future, combining genomic selection with biotechnological innovations, such as genome editing and surrogate broodstock technologies, may further expedite genetic improvement in aquaculture.

Single nucleotide polymorphisms reveal a genetic cline across the north-east Atlantic and enable powerful population assignment in the European lobster.

Resolving stock structure is crucial for fisheries conservation to ensure that the spatial implementation of management is commensurate with that of biological population units. To address this in the economically important European lobster (Homarus gammarus), genetic structure was explored across the species' range using a small panel of single nucleotide polymorphisms (SNPs) previously isolated from restriction-site-associated DNA sequencing; these SNPs were selected to maximize differentiation at a range of both broad and fine scales. After quality control and filtering, 1,278 lobsters from 38 sampling sites were genotyped at 79 SNPs. The results revealed a pronounced phylogeographic break between the Atlantic and Mediterranean basins, while structure within the Mediterranean was also apparent, partitioned between lobsters from the central Mediterranean and the Aegean Sea. In addition, a genetic cline across the north-east Atlantic was revealed using both putatively neutral and outlier SNPs, but the precise driver(s) of this clinal pattern-isolation by distance, secondary contact, selection across an environmental gradient, or a combination of these factors-remains undetermined. Putatively neutral markers differentiated lobsters from Oosterschelde, an estuary on the Dutch coast, a finding likely explained by past bottlenecks and limited gene flow with adjacent North Sea populations. Building on the findings of our spatial genetic analysis, we were able to test the accuracy of assigning lobsters at various spatial scales, including to basin of origin (Atlantic or Mediterranean), region of origin and sampling location. The predictive model assembled using 79 SNPs correctly assigned 99.7% of lobsters not used to build the model to their basin of origin, but accuracy decreased to region of origin and again to sampling location. These results are of direct relevance to managers of lobster fisheries and hatcheries, and provide the basis for a genetic tool for tracing the origin of European lobsters in the food supply chain.

Absence of evidence is not evidence of absence: Nanopore sequencing and complete assembly of the European lobster (Homarus gammarus) mitogenome uncovers the missing nad2 and a new major gene cluster duplication.

BACKGROUND: The recently published complete mitogenome of the European lobster (Homarus gammarus) that was generated using long-range PCR exhibits unusual gene composition (missing nad2) and gene rearrangements among decapod crustaceans with strong implications in crustacean phylogenetics. Such atypical mitochondrial features will benefit greatly from validation with emerging long read sequencing technologies such as Oxford Nanopore that can more accurately identify structural variation. RESULTS: We re-sequenced the H. gammarus mitogenome on an Oxford Nanopore Minion flowcell and performed a long-read only assembly, generating a complete mitogenome assembly for H. gammarus. In contrast to previous reporting, we found an intact mitochondrial nad2 gene in the H. gammarus mitogenome and showed that its gene organization is broadly similar to that of the American lobster (H. americanus) except for the presence of a large tandemly duplicated region with evidence of pseudogenization in one of each duplicated protein-coding genes. CONCLUSIONS: Using the European lobster as an example, we demonstrate the value of Oxford Nanopore long read technology in resolving problematic mitogenome assemblies. The increasing accessibility of Oxford Nanopore technology will make it an attractive and useful tool for evolutionary biologists to verify new and existing unusual mitochondrial gene rearrangements recovered using first and second generation sequencing technologies, particularly those used to make phylogenetic inferences of evolutionary scenarios.

Meta-analysis of northeast Atlantic marine taxa shows contrasting phylogeographic patterns following post-LGM expansions.

BACKGROUND: Comparative phylogeography enables the study of historical and evolutionary processes that have contributed to shaping patterns of contemporary genetic diversity across co-distributed species. In this study, we explored genetic structure and historical demography in a range of coastal marine species across the northeast Atlantic to assess whether there are commonalities in phylogeographic patterns across taxa and to evaluate whether the timings of population expansions were linked to the Last Glacial Maximum (LGM). METHODS: A literature search was conducted using Web of Science. Search terms were chosen to maximise the inclusion of articles reporting on population structure and phylogeography from the northeast Atlantic; titles and abstracts were screened to identify suitable articles within the scope of this study. Given the proven utility of mtDNA in comparative phylogeography and the availability of these data in the public domain, a meta-analysis was conducted using published mtDNA gene sequences. A standardised methodology was implemented to ensure that the genealogy and demographic history of all mtDNA datasets were reanalysed in a consistent and directly comparable manner. RESULTS: Mitochondrial DNA datasets were built for 21 species. The meta-analysis revealed significant population differentiation in 16 species and four main types of haplotype network were found, with haplotypes in some species unique to specific geographical locations. A signal of rapid expansion was detected in 16 species, whereas five species showed evidence of a stable population size. Corrected mutation rates indicated that the majority of expansions were estimated to have occurred after the earliest estimate for the LGM (∼26.5 Kyr), while few expansions were estimated to have pre-dated the LGM. CONCLUSION: This study suggests that post-LGM expansion appeared to be common in a range of marine taxa, supporting the concept of rapid expansions after the LGM as the ice sheets started to retreat. However, despite the commonality of expansion patterns in many of these taxa, phylogeographic patterns appear to differ in the species included in this study. This suggests that species-specific evolutionary processes, as well as historical events, have likely influenced the distribution of genetic diversity of marine taxa in the northeast Atlantic.

Exceptional biodiversity of the cryptofaunal decapods in the Chagos Archipelago, central Indian Ocean.

The Chagos Archipelago is geographically remote and isolated from most direct anthropogenic pressures. Here, we quantify the abundance and diversity of decapod crustaceans inhabiting dead coral colonies, representing a standardised microhabitat, across the Archipelago. Using morphological and molecular techniques we recorded 1868 decapods from 164 nominal species within 54 dead coral colonies, but total species estimates (Chao1 estimator) calculate at least 217 species. Galatheids were the most dominant taxa, though alpheids and hippolytids were also very abundant. 32% of species were rare, and 46% of species were found at only one atoll. This prevalence of rarer species has been reported in other cryptofauna studies, suggesting these assemblages maybe comprised of low-abundance species. This study provides the first estimate of diversity for reef cryptofauna in Chagos, which will serve as a useful baseline for global comparisons of coral reef biodiversity.