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

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

Population structure and genetic connectivity reveals distinctiveness of Irish harbour seals (<i>Phoca vitulina</i>) and implications for conservation management

Funding: This research was funded by the Galway-Mayo Institute of Technology (scholarship, now Atlantic Technological University), under research grants from the Irish National Parks and Wildlife Service (NPWS, grant ref. SPU G07-2017) and the Marine Environment Section of the Department of Housing, Local Government, and Heritage (DHLGH). The contribution from SMRU (sampling and genetic analyses and DJFR) was funded by NERC National Public Good- National Capability funding (NE/R015007/1), Nature Scot, and the Scottish Government.The identification of discrete intraspecific units, such as genetically informed management units (MUs), is important to effectively develop and implement conservation strategies for protected species. Harbour seals (Phoca vitulina) occurring in Irish waters are currently viewed as a single nationwide panmictic population (and hence MU), although this assumption is not based on any knowledge of population structure because of the lack of available genetic data. Thus, the present study used mitochondrial control region sequences and between nine and 11 microsatellite loci from harbour seals from Ireland and Northern Ireland (up to n = 123) and adjacent UK/European waters (up to n = 289) to provide insights into the genetic population structure and diversity of harbour seals in the areas studied. Within the island of Ireland, genetic analyses revealed the presence of three genetically distinct local populations, characterized by high genetic diversity, hereby defined as: East Ireland (EI), North-west & Northern Ireland (NWNI), and South-west Ireland (SWI). Using previously published and newly generated data, a subsequent wider scale analysis revealed that the EI and SWI local populations were genetically distinct from neighbouring UK/European areas, whereas seals from the NWNI area could not be distinguished from a previously identified Northern UK metapopulation. Migration rate estimates showed that NWNI receives migrants from North-west Scotland, with NWNI acting as a genetic source for both SWI and EI. The present study provides the most comprehensive genetic assessment of harbour seals in European waters to date, with findings indicating that conservation strategies for harbour seals in Irish waters should be amended to accommodate at least three genetically distinct local populations/MUs. The use of approaches considering both ecological and genetic parameters is recommended for future assessments and delineation of units of ecological relevance for conservation management purposes.PostprintPeer reviewe

Speciation in the deep : genomics and morphology reveal a new species of beaked whale Mesoplodon eueu

This work was supported by ONR grants N000141613017 to E.L.C. and N.A. and N00014-18-1-2808 to C.S.B.; funds from the NMNH Rebecca G. Mead and James G. Mead Marine Mammal Endowment, NSF (USA) grant no. DEB-1457735 to M.S.S., P.A.M. and J.G.; Brothers Hartmann Foundation grant no. AB28148 to M.T.O.; NMFS, BOEM, and USA Navy funding to D.Ch. under the Atlantic Marine Assessment Program for Protected Species. M.L.M. was funded under the Marie Skłodowska-Curie grant agreement no 801199; E.L.C. by a Rutherford Discovery Fellowship from the Royal Society of New Zealand Te Apārangi. Irish Whale and Dolphin Group Cetacean Stranding scheme is part-funded by the National Parks and Wildlife Service.The deep sea has been described as the last major ecological frontier, as much of its biodiversity is yet to be discovered and described. Beaked whales (ziphiids) are among the most visible inhabitants of the deep sea, due to their large size and worldwide distribution, and their taxonomic diversity and much about their natural history remain poorly understood. We combine genomic and morphometric analyses to reveal a new Southern Hemisphere ziphiid species, Ramari's beaked whale, Mesoplodon eueu, whose name is linked to the Indigenous peoples of the lands from which the species holotype and paratypes were recovered. Mitogenome and ddRAD-derived phylogenies demonstrate reciprocally monophyletic divergence between M. eueu and True's beaked whale (M. mirus) from the North Atlantic, with which it was previously subsumed. Morphometric analyses of skulls also distinguish the two species. A time-calibrated mitogenome phylogeny and analysis of two nuclear genomes indicate divergence began circa 2 million years ago (Ma), with geneflow ceasing 0.35–0.55 Ma. This is an example of how deep sea biodiversity can be unravelled through increasing international collaboration and genome sequencing of archival specimens. Our consultation and involvement with Indigenous peoples offers a model for broadening the cultural scope of the scientific naming process.Publisher PDFPeer reviewe

Marine mammal conservation : over the horizon

S.E.N. acknowledges funding from the Natural Environment Research Council (NE/L002434/1). S.E.N. and B.J.G. also acknowledge support from the European Union (INDICIT; EU grant agreement no. 110661/2018/794561/SUB/ENV. C2). E.C. has a doctoral fellowship from the World Wildlife Foundation - Education for Nature. M.I.D.C. was supported by the UK Department for Business and Industrial Strategy (BEIS; project number OESEA-16-78). D.J.F.R. was supported by National Capability funding from the UK Natural Environment Research Council (NERC) to the Sea Mammal Research Unit (SMRU) (grant no. SMRU1001). A.B.O. acknowledges funding from the Office of Naval Research (award no. N000141613017). D.M.P. was supported by the Whale Habitat Professorship Endowment Fund, Marine Mammal Institute, Oregon State University. K.A.S. was supported by a Royal Society of New Zealand Te Aparangi Rutherford Discovery Fellowship.Marine mammals can play important ecological roles in aquatic ecosystems, and their presence can be key to community structure and function. Consequently, marine mammals are often considered indicators of ecosystem health and flagship species. Yet, historical population declines caused by exploitation, and additional current threats, such as climate change, fisheries bycatch, pollution and maritime development, continue to impact many marine mammal species, and at least 25% are classified as threatened (Critically Endangered, Endangered or Vulnerable) on the IUCN Red List. Conversely, some species have experienced population increases/recoveries in recent decades, reflecting management interventions, and are heralded as conservation successes. To continue these successes and reverse the downward trajectories of at-risk species, it is necessary to evaluate the threats faced by marine mammals and the conservation mechanisms available to address them. Additionally, there is a need to identify evidence-based priorities of both research and conservation needs across a range of settings and taxa. To that effect we: (1) outline the key threats to marine mammals and their impacts, identify the associated knowledge gaps and recommend actions needed; (2) discuss the merits and downfalls of established and emerging conservation mechanisms; (3) outline the application of research and monitoring techniques; and (4) highlight particular taxa/populations that are in urgent need of focus.Publisher PDFPeer reviewe

Speciation in the deep: genomics and morphology reveal a new species of beaked whale

Earth’s deep oceans remains less well understood than the surface of Mars. Beaked whales (ziphiids) are among the most visible inhabitants of the abyss, due to their large size and worldwide distribution, yet their diversity and ecology remain obscure. We combine genomic and morphometric analyses to reveal a new Southern Hemisphere ziphiid species, Ramari’s beaked whale, Mesoplodon eueu, whose name is linked to the Indigenous people of the lands from which the species holotype and paratypes were recovered. Mitogenome and ddRAD-derived phylogenies demonstrate reciprocally monophyletic divergence between M. eueu and North Atlantic True’s beaked whale (M. mirus), with which it was subsumed. Revised morphometric analyses of skulls separate the species. A time-calibrated mitogenome phylogeny and analysis of two nuclear genomes indicate divergence began ca 2 million years ago (Ma), with geneflow ceasing 0.35-0.55 Ma. This is an example of how deep-sea biodiversity can be unravelled through increasing international collaboration and genome sequencing of archival specimens. Our consultation and involvement with Indigenous groups offers a model for broadening the cultural scope of the scientific naming process.,See article supplementary materials for methods and sample IDs.