Genomics reveals the role of admixture in the evolution of structure among sperm whale populations within the Mediterranean Sea

17 pages, 4 figures, 4 tables, supporting information https://doi.org/10.1111/mec.16898.-- Data availability statement: Sequences associated with ddRADseq analyses are deposited at GenBank under BioProject accession PRJNA936197. ddRADseq genotype files and relevant code are provided on Dryad at: https://doi.org/10.5061/dryad.dv41ns233. There are no restrictions on data availability

In oceanic ecosystems, the nature of barriers to gene flow and the processes by which populations may become isolated are different from the terrestrial environment, and less well understood. In this study we investigate a highly mobile species (the sperm whale, Physeter macrocephalus) that is genetically differentiated between an open North Atlantic population and the populations in the Mediterranean Sea. We apply high-resolution single nucleotide polymorphism (SNP) analysis to study the nature of barriers to gene flow in this system, assessing the putative boundary into the Mediterranean (Strait of Gibraltar and Alboran Sea region), and including novel analyses on structuring among sperm whale populations within the Mediterranean basin. Our data support a recent founding of the Mediterranean population, around the time of the last glacial maximum, and show concerted historical demographic profiles in both the Atlantic and the Mediterranean. In each region there is evidence for a population decline around the time of the founder event. The largest decline was seen within the Mediterranean Sea where effective population size is substantially lower (especially in the eastern basin). While differentiation is strongest at the Atlantic/Mediterranean boundary, there is also weaker but significant differentiation between the eastern and western basins of the Mediterranean Sea. We propose, however, that the mechanisms are different. While post-founding gene flow was reduced between the Mediterranean and Atlantic populations, within the Mediterranean an important factor differentiating the basins is probably a greater degree of admixture between the western basin and the North Atlantic and some level of isolation between the western and eastern Mediterranean basins. Subdivision within the Mediterranean Sea exacerbates conservation concerns and will require consideration of what distinct impacts may affect populations in the two basins

This work was supported by OceanCare (Switzerland), project Catodon of the Menkab, il respiro del mare association, and MPA Bergeggi Island. Sampling was supported by Loro Parque Foundation, the Fundación Biodiversidad, FCT (IF/00943/2013/CP1199/CT0001, UIDB/05634/2020 & UIDP/05634/2020), FRCT, the EC through research projects TRACE-PTDC/MAR/74071/2006, MAPCET-M2.1.2/F/012/2011, WATCH IT (Acores-01-0145-FEDER-000057) FEDER, COMPETE, QREN, POPH, ESF, Portuguese Ministry for Science and Education, OP Azores 2020, the regional government Xunta de Galicia – Dirección Xeral de Patrimonio Natural, research programme “Sperm whales of the Greek Seas” of the Pelagos Cetacean Research Institute partially supported by OceanCare since 2008, Oceanic Observatory of Madeira throughout the project M1420-01-0145-FEDER-000001-OOM and of the Oceano Azul Foundation throughout the Whale Tales Project (ODL/2019/003). Biagio Violi was funded by the Department of Earth and Life Sciences of Genoa University. Joan Giménez was supported by the Spanish National Program Juan de la Cierva-Formación (FJC2019-040016-I) and the Severo Ochoa Centre of Excellence accreditation (CEX2019-000928-S) given to the Institute of Marine Science (ICM-CSIC). Ana Dinis and Filipe Alves were funded by ARDITI throughout the project M1420-09-5369-FSE-000002 and by FCT throughout the projects UIDB/04292/2020 and UIDP/04292/2020 granted to MARE and project LA/P/0069/2020 granted to the Associate Laboratory ARNET. Mónica Almeida e Silva was cofunded by OP Azores 2020 (Fund 01-0145-FEDER-000140- MarAZ Researchers) of the EU. Cláudia Oliveira was funded by WATCH IT – Acores-01-0145-FEDER-000057, and service contract with SRMCT/DRAM under project INTERTAGUA (MAC2/1.1a/385). Okeanos is supported by FCT (UIDB/05634/2020 & UIDP/05634/2020) and the Regional Government of the Azores (M1.1.A/REEQ.CIENTÍFICOUI&D/2021/010). Alfredo Lopez was supported by the CESAM by FCT/MCTES (UIDP/50017/ 2020 + UIDB/ 50017/2020 + LA/P/0094/2020), through national funds and by national funds (OE), through FCT-I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19

Peer reviewed