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Journal article
Biogeography in the deep: Hierarchical population genomic structure of two beaked whale species
Global ecology and conservation, Vol.40, e02308
12/2022
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Abstract
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.
•The deep sea is the largest yet one of the most poorly understood ecosystems on Earth.
•Genetic structure in two globally distributed deep sea predators were investigated.
•Genomic markers showed hierarchical structure among and within ocean basins.
•Biogeographical barriers are important at macroevolutionary scales for both species.
•Differences between species relate to life history traits and philopatry.
Details
- Title
- Biogeography in the deep: Hierarchical population genomic structure of two beaked whale species
- Creators
- Aubrie B. Onoufriou - University of St AndrewsOscar E. Gaggiotti - Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, UKNatacha Aguilar de Soto - BIOECOMAC Department of Animal Biology, Edaphology and Geology, University of La Laguna, San Cristóbal de La Laguna, Tenerife, Canary Islands, SpainMorgan L. McCarthy - Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Copenhagen, DenmarkPhillip A. Morin - Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, CA, USAMassimiliano Rosso - CIMA Research Foundation, Savona, ItalyMerel Dalebout - School of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, New South Wales, AustraliaNicholas Davison - Scottish Marine Animal Stranding Scheme, School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UKRobin W. Baird - Cascadia Research Collective, Olympia, WA, USAC. Scott Baker - Oregon State UniversitySimon Berrow - Marine and Freshwater Research Centre, Atlantic Technological University, Dublin Road, Galway, IrelandAndrew Brownlow - Scottish Marine Animal Stranding Scheme, School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UKDaniel Burns - Southern Cross UniversityFlorence Caurant - Observatoire Pelagis, UMS3462 La Rochelle University-CNRS, La Rochelle, FranceDiane Claridge - Bahamas Marine Mammal Research Organisation, Abaco, BahamasRochelle Constantine - University of AucklandFabien Demaret - Observatoire Pelagis, UMS3462 La Rochelle University-CNRS, La Rochelle, FranceSascha Dreyer - Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Copenhagen, DenmarkMartina Ðuras - Department of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Zagreb, Zagreb, CroatiaJohn W. Durban - Bahamas Marine Mammal Research Organisation, Abaco, BahamasAlexandros Frantzis - Pelagos Cetacean Research Institute, Vouliagmeni, GreeceLuis Freitas - Museu da Baleia da Madeira, Caniçal, Madeira, PortugalGabrielle Genty - Sea Mammal Research Unit, Scottish Oceans Institute, University of St Andrews, St Andrews, UKAna Galov - Department of Biology, Faculty of Science, University of Zagreb, Zagreb, CroatiaSabine S. Hansen - Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Copenhagen, DenmarkAndrew C. Kitchener - Department of Natural Sciences, National Museums Scotland, Edinburgh, UKVidal Martin - Society for the Study of the Cetaceans in the Canary Archipelago (SECAC), Lanzarote, Canary Islands, SpainAntonio A. Mignucci-Giannoni - Centro de Conservación de Manatíes del Caribe, Universidad Interamericana, Bayamón, Puerto RicoValeria Montano - School of Biology, University of St Andrews, St Andrews, UKAurelie Moulins - CIMA Research Foundation, Savona, ItalyCarlos Olavarría - Centro de Estudios Avanzados en Zonas Áridas (CEAZA), La Serena, ChileM. Michael Poole - Marine Mammal Research Program, Maharepa, Moorea, French PolynesiaCristel Reyes Suárez - BIOECOMAC Department of Animal Biology, Edaphology and Geology, University of La Laguna, San Cristóbal de La Laguna, Tenerife, Canary Islands, SpainEmer Rogan - School of Biological, Earth & Environmental Sciences, University College Cork, Cork, IrelandConor Ryan - Marine and Freshwater Research Centre, Atlantic Technological University, Dublin Road, Galway, IrelandAgustina Schiavi - BIOECOMAC Department of Animal Biology, Edaphology and Geology, University of La Laguna, San Cristóbal de La Laguna, Tenerife, Canary Islands, SpainPaola Tepsich - CIMA Research Foundation, Savona, ItalyJorge Urban R. - Departamento de Ciencias Marinas y Costeras, Universidad Autónoma de Baja California Sur, La Paz, B.C.S., MéxicoKristi West - Hawai'i Insitute of Marine Biology, University of Hawai'i at Manoa, Kaneohe, HI, USAMorten Tange Olsen - Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Copenhagen, DenmarkEmma L. Carroll - University of St Andrews
- Publication Details
- Global ecology and conservation, Vol.40, e02308
- Comment
- We are grateful for helpful discussion and comments on the manuscript provided by B. Taylor (SWFSC) and J. Onoufriou. We are also grateful for the discussion, comments, edits and samples provided by D. Kerem (IMMRAC). The authors would like to thank K. Andrews for providing the ddRAD protocol. We also thank G. Melo-Santos for the drawings of Cuvier’s and Blainville’s beaked whales in Figs. 1 and 2. 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 Foun- dation. Advanced whole genome assemblies were provided by J. Johnson of the Broad Institute (https://data.broadinstitute.org/ 200m_variation/). Many thanks to the New Zealand Cetacean Tissue Archive and Iwi, NMFS-Alaska Region Stranding Programs, NMFS-West Coast Region Stranding Programs, South Africa Museum (IZIKO), National Museum of Scotland, Nova Scotia Museum, SWFSC for allowing access to their Marine Mammal and Sea Turtle Research Collection, Smithsonian Museum of Natural History, and Coordinadora Para o Estudo dos Mamiferos Mari ̃nos (CEMMA) for providing samples. National Museums Scotland thanks the Neg- aunee Foundation for their generous support of a curatorial preparator, and the SeaWorld and Busch Gardens Conservation Fund which supported the collection of beaked whale samples. Thanks also to OceanCare (Switzerland) for their support of the research program led by the Pelagos Cetacean Research Institute and the National Parks and Wildlife Service of the Department of Housing, Local Government and Heritage for part funding the Irish Cetacean Stranding Scheme. The authors thank a long list of sample con- tributors, field teams and lab personnel for their participation: C. Dunn (BMMRO), J. Calambokidis (Cascadia Research Collective), L. Hickmott (Open Ocean Consulting), the late R. N. P. Goodall (RNP Goodall Foundation), L. Dolar (Silliman University), K. Medlock (Tasmanian Museum and Art Gallery), R. Pitman, the late W. Perrin, and J. Barlow of the Southwest Fisheries Science Center (SWFSC), the late P. Best, M. Ferreira (MATB), D. Veytia, M. Anderson, P. Covelo (CEMMA), P.S. Olsen, T.B. Brand, and L. Vinner (GeoGenetics Sequencing Core), J. Dines, N. Hauser, P. Jepson, J. Mead, Z. Lucas, M. Oremus, C. Potter and J. St. Leger. Special thanks for the University of La Laguna field team supporting this research at El Hierro: C. Yzoard, J. Alcazar, D. Miranda, J. Marrero, P. Arranz, A. Martin, and R. Vi ̃ne.
- Publisher
- Elsevier B.V
- Grant note
- 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.
- Identifiers
- 991013056512202368
- Copyright
- © 2022 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
- Academic Unit
- Faculty of Science and Engineering
- Language
- English
- Resource Type
- Journal article