Perturbation drives changing metapopulation dynamics in a top marine predator

Funding: O.E.G. was supported by the Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council (grant no. HR09011). E.L.C. was supported by a Newton Fellowship (Royal Society of London), Marie Curie Fellowship (EU Horizon2020) and a Rutherford Discovery Fellowship (Royal Society of New Zealand). A.J.H. and D.J.F.R. were supportedby NERC (grant no. SMRU 10/001).Metapopulation theory assumes a balance between local decays/extinctions and local growth/new colonisations. Here we investigate whether recent population declines across part of the UK harbour seal range represent normal metapopulation dynamics or are indicative of perturbations potentially threatening the metapopulation viability, using 20 years of population trends, location tracking data (n = 380), and UK-wide, multi-generational population genetic data (n = 269). First, we use microsatellite data to show that two genetic groups previously identified are distinct metapopulations: northern and southern. Then, we characterize the northern metapopulation dynamics in two different periods, before and after the start of regional declines (pre-/peri-perturbation). We identify source-sink dynamics across the northern metapopulation, with two putative source populations apparently supporting three likely sink populations, and a recent metapopulation-wide disruption of migration coincident with the perturbation. The northern metapopulation appears to be in decay, highlighting that changes in local populations can lead to radical alterations in the overall metapopulation's persistence and dynamics.PostprintPeer reviewe

Genetic population structure of harbour seals in the United Kingdom and neighbouring waters

Natural Environment Research Council (GrantNumber(s): SMRU1001; Grant recipient(s): Ailsa Hall)1.  In the United Kingdom (UK), several harbour seal (Phoca vitulina) populations have been declining over the past decade. In order to understand the effect of these changes in abundance, this study seeks to determine the population structure of harbour seals in the UK, and in Scotland in particular, on a wider and finer spatial scale than has previously been reported. 2.  Harbour seals were genotyped from 18 different localities throughout the UK and neighbouring localities in mainland Europe, at 12 microsatellite loci. Results from Bayesian and frequency based tests of population structure suggested an initial structural division into two main groups consisting of localities in northern UK and southern UK-mainland Europe, respectively. 3.  These two clusters were further divided into four geographically distinct genetic clusters. 4.  An overall agreement between the genetic results and the existing management areas for UK harbour seals was observed, but it is also clear that an adaptive management approach should be adopted, in which the delineation of the current management areas is maintained until further genetic and ecological information has been accumulated and analysed.Publisher PDFPeer reviewe

A workflow used to design low density SNP panels for parentage assignment and traceability in aquaculture species and its validation in Atlantic salmon

This project has received funding from the European Union's Horizon 2020 research and innovation program under grant agreement No 654008.Accurate parentage assignment is key for the development of a successful breeding program, allowing pedigree reconstruction from mixed families and control of inbreeding. In the present study we developed a workflow for the design of an efficient single nucleotide polymorphism (SNP) panel for paternity assignment and validated it in Atlantic salmon (Salmo salar L.). A total of 86,468 SNPs were identified from Restriction Site Associated DNA Sequencing (RAD-seq) libraries, and reduced to 1517 following the application of quality control filters and stringent selection criteria. A subsample of SNPs were chosen for the design of high-throughput SNP assays and a training set of known parents and offspring was then used to achieve further filtering. A panel comprising 94 SNPs balanced across the salmon genome were identified, providing 100% assignment accuracy in known pedigrees. Additionally, the panel was able to assign individuals to one of three farmed salmon populations used in this study with 100% accuracy. We conclude that the workflow described is suitable for the design of cost effective parentage assignment and traceability tools for aquaculture species.PostprintPeer reviewe

Future directions in research on beaked whales

Until the 1990s, beaked whales were one of the least understood groups of large mammals. Information on northern bottlenose whales (Hyperoodon ampullatus) and Baird’s beaked whales (Berardius bairdii) was available from data collected during whaling, however, little information existed on the smaller species other than occasional data gleaned from beach-cast animals. Recent research advances have been plentiful. Increasing global survey effort, together with morphometric and genetic analyses have shown at least 22 species in this group. Longitudinal field studies of at least four species (H. ampullatus, B. bairdii, Ziphius cavirostris, Mesoplodon densirostris) have become established over the last three decades. Several long-term studies support photo-identification catalogs providing insights into life history, social structure and population size. Tag-based efforts looking at diving, movements and acoustics have provided detail on individual behavior as well as population structure and ranges. Passive acoustic monitoring has allowed long-term and seasonal monitoring of populations. Genetic studies have uncovered cryptic species and revealed contrasting patterns of genetic diversity and connectivity amongst the few species examined. Conservation concern for these species was sparked by mass strandings coincident with military mid-frequency sonar use. Fat and gas emboli have been symptomatic indicators of mortalities related to sonar exposure, suggesting that their vulnerability stems from the physiological exertion of extreme diving for medium-sized whales. Behavioral response experiments have now shown that beaked whales appear to cease foraging and delay their return to foraging and/or leave the area in association with exposure to mid-frequency signals at low acoustic levels. Future priorities for these species will be to (1) continue field-studies to better understand smaller-scale habitat use, vital rates and social structure; (2) develop better detection methods for larger-scale survey work; (3) improve methodology for monitoring energetics, individual body condition and health; (4) develop tools to better understand physiology; (5) use recent genetic advances with improved sample databanks to re-examine global and local beaked whale relationships; (6) further quantify anthropogenic impacts (both sonar and other noise) and their population consequences (7) apply acquired data for realistic mitigation of sonar and other anthropogenic impacts for beaked whale conservation.Publisher PDFPeer reviewe

Biogeography in the deep : hierarchical population genomic structure of two beaked whale species

Funding for this research was provided by the Office of Naval Research, Award numbers N000141613017 and N000142112712. ABO was supported by a partial studentship from the University of St Andrews, School of Biology; OEG by the Marine Alliance for Science and Technology for Scotland (Scottish Funding Council grant HR09011); ELC by a Rutherford Discovery Fellowship from the Royal Society of New Zealand Te Aparangi; NAS by a Ramon y Cajal Fellowship from the Spanish Ministry of Innovation; MLM by the European Union’s Horizon 2020 Research and Innovation Programme (Marie Skłodowska-Curie grant 801199); CR by the Marine Institute (Cetaceans on the Frontier) and the Irish Research Council; and MTO by the Hartmann Foundation.The deep sea is the largest ecosystem on Earth, yet little is known about the processes driving patterns of genetic diversity in its inhabitants. Here, we investigated the macro- and microevolutionary processes shaping genomic population structure and diversity in two poorly understood, globally distributed, deep-sea predators: Cuvier’s beaked whale (Ziphius cavirostris) and Blainville’s beaked whale (Mesoplodon densirostris). We used double-digest restriction associated DNA (ddRAD) and whole mitochondrial genome (mitogenome) sequencing to characterise genetic patterns using phylogenetic trees, cluster analysis, isolation-by-distance, genetic diversity and differentiation statistics. Single nucleotide polymorphisms (SNPs; Blainville’s n = 43 samples, SNPs=13988; Cuvier’s n = 123, SNPs= 30479) and mitogenomes (Blainville’s n = 27; Cuvier’s n = 35) revealed substantial hierarchical structure at a global scale. Both species display significant genetic structure between the Atlantic, Indo-Pacific and in Cuvier’s, the Mediterranean Sea. Within major ocean basins, clear differentiation is found between genetic clusters on the east and west sides of the North Atlantic, and some distinct patterns of structure in the Indo-Pacific and Southern Hemisphere. We infer that macroevolutionary processes shaping patterns of genetic diversity include biogeographical barriers, highlighting the importance of such barriers even to highly mobile, deep-diving taxa. The barriers likely differ between the species due to their thermal tolerances and evolutionary histories. On a microevolutionary scale, it seems likely that the balance between resident populations displaying site fidelity, and transient individuals facilitating gene flow, shapes patterns of connectivity and genetic drift in beaked whales. Based on these results, we propose management units to facilitate improved conservation measures for these elusive species.Publisher PDFPeer reviewe

Biogeography in the deep: hierarchical population genomic structure of two beaked whale species

The deep sea is the largest ecosystem on Earth, yet little is known about the processes driving patterns of genetic diversity in its inhabitants. Here, we investigated the macro- and microevolutionary processes shaping genomic population structure and diversity in two poorly understood, globally distributed, deep-sea predators: Cuvier’s beaked whale (Ziphius cavirostris) and Blainville’s beaked whale (Mesoplodon densirostris). We used double-digest restriction associated DNA (ddRAD) and whole mitochondrial genome (mitogenome) sequencing to characterise genetic patterns using phylogenetic trees, cluster analysis, isolation-by-distance, genetic diversity and differentiation statistics. Single nucleotide polymorphisms (SNPs; Blainville’s n=43 samples, SNPs=13988; Cuvier’s n=123, SNPs= 30479) and mitogenomes (Blainville’s n=27; Cuvier’s n=35) revealed substantial hierarchical structure at a global scale. Both species display significant genetic structure between the Atlantic, Indo-Pacific and in Cuvier’s, the Mediterranean Sea. Within major ocean basins, clear differentiation is found between genetic clusters on the east and west sides of the North Atlantic, and some distinct patterns of structure in the Indo-Pacific and Southern Hemisphere. We infer that macroevolutionary processes shaping patterns of genetic diversity include biogeographical barriers, highlighting the importance of such barriers even to highly mobile, deep-diving taxa. The barriers likely differ between the species due to their thermal tolerances and evolutionary histories. On a microevolutionary scale, it seems likely that the balance between resident populations displaying site fidelity, and transient individuals facilitating gene flow, shapes patterns of connectivity and genetic drift. Based on these results, we propose management units to facilitate improved conservation measures for these elusive species

DNA in the deep : comparative molecular ecology for the conservation of beaked whales

Beaked whales (Ziphiidae) are an incredibly diverse and elusive family, and behavioural responses linked to certain anthropogenic sounds have resulted in mass stranding events. The substantial knowledge gaps regarding abundance and population structure for most ziphiids highlight that more information is required for their effective management and conservation. To this end, next-generation DNA sequencing was used to investigate beaked whale ecology and evolution, showcasing the utility of reduced representation sequencing in non-model organisms. Single nucleotide polymorphisms (SNPs) were derived using double-digest restriction site associated DNA sequencing (ddRAD) from a newly established international beaked whale tissue and DNA archive. Globally, hierarchical genetic structure and diversity of cosmopolitan Cuvier’s and Blainville’s beaked whales (Ziphius cavirostris and Mesoplodon densirostris, “Cuvier’s” and “Blainville’s”) were investigated. Biogeographic barriers and differing life and evolutionary histories have contributed to the observed patterns, and the findings are evaluated in the context of management units for conservation. Regionally, population structure and demographic history were characterised for four North Atlantic beaked whales: Cuvier’s, Blainville’s, Sowerby’s beaked whales (M. bidens) and northern bottlenose whales (Hyperoodon ampullatus). Fluctuations in effective population size (Ne) were likely responses to climatic change. With these findings, potential responses of beaked whale populations to future climate change are discussed. Locally, genetic Essential Biodiversity Variables (EBVs) were calculated for paired ‘disturbed’ and ‘semi-pristine’ populations of Cuvier’s and Blainville’s in three well studied populations: the Bahamas, Canary Islands and Mediterranean Sea (Cuvier’s only). At least one ‘disturbed’ site was found in each region with reduced genetic variation and at risk of genetic erosion. In summary, genetic population structure has been identified in many ziphiids. These populations have different levels of genetic diversity, different demographic responses to historic climatic change and it is likely that they have different abilities to adapt to future anthropogenic and climate impacts and should be managed on a population level