Not out of the Mediterranean: Atlantic populations of the gorgonian Paramuricea clavata are a separate sister species under further lineage diversification

21 pages, 4 figures, 1 table, supporting information https://doi.org/10.1002/ece3.9740.-- Data Availability Statement: Raw RNA-seq data and mt-mutS sequences have been uploaded to NCBI's SRA (BioProject ID: PRJNA847883) and GenBank databases (Accessions numbers: ON804207-ON804214), respectively. Final sequence alignments and microsatellite data are available on DRYAD (https://doi.org/10.5061/dryad.r7sqv9sfm)

The accurate delimitation of species boundaries in nonbilaterian marine taxa is notoriously difficult, with consequences for many studies in ecology and evolution. Anthozoans are a diverse group of key structural organisms worldwide, but the lack of reliable morphological characters and informative genetic markers hampers our ability to understand species diversification. We investigated population differentiation and species limits in Atlantic (Iberian Peninsula) and Mediterranean lineages of the octocoral genus Paramuricea previously identified as P. clavata. We used a diverse set of molecular markers (microsatellites, RNA-seq derived single-copy orthologues [SCO] and mt-mutS [mitochondrial barcode]) at 49 locations. Clear segregation of Atlantic and Mediterranean lineages was found with all markers. Species-tree estimations based on SCO strongly supported these two clades as distinct, recently diverged sister species with incomplete lineage sorting, P. cf. grayi and P. clavata, respectively. Furthermore, a second putative (or ongoing) speciation event was detected in the Atlantic between two P. cf. grayi color morphotypes (yellow and purple) using SCO and supported by microsatellites. While segregating P. cf. grayi lineages showed considerable geographic structure, dominating circalittoral communities in southern (yellow) and western (purple) Portugal, their occurrence in sympatry at some localities suggests a degree of reproductive isolation. Overall, our results show that previous molecular and morphological studies have underestimated species diversity in Paramuricea occurring in the Iberian Peninsula, which has important implications for conservation planning. Finally, our findings validate the usefulness of phylotranscriptomics for resolving evolutionary relationships in octocorals

This work was funded by program BIOMARES, a Pew Marine Fellowship, and FCT – Foundation for Science and Technology UIDB/04326/2020, UIDP/04326/2020, LA/P/0101/2020, PTDC/BIA-CBI/6515/2020; EU-BiodivERsA BiodivRestore-253 (FCT: DivRestore/0013/2020); EU Horizon 2020 research and innovation program (MERCES: Grant no. 689518); as well as the Inaqua Conservation Fund (Oceanário de Lisboa and National Geographic Channel) and National Geographic Society/Waitt Grant no. W153-11. This article is also a product of the French network on Marine Connectivity (GDR MarCo). M.C. was supported by postdoctoral fellowships of projects HABMAR (Grant no. MAR-01.04.02-FEAMP-0018) co-financed by the European Maritime and Fisheries Fund of the Operational Program MAR 2020 for Portugal (Portugal 2020), and BiodivAMP (Grant no. FA_06_2017_045) financed by the Directorate-General for Sea Policy of the Ministry of Economy and Sea for Portugal under the Operational Program Fundo Azul. JBL was funded by assistant researcher contract framework of the RD Unit—UID/Multi/04423/2019 – Interdisciplinary Centre of Marine and Environmental Research—financed by the European Regional Development Fund (ERDF) through COMPETE2020—Operational Program for Competitiveness and Internationalization (POCI) and national funds through FCT/MCTES (PIDDAC). JB was funded by a FCT PhD scholarship SFRH/BD/72501/2010

With the institutional support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S)

Peer reviewed