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

• Published in: Ecology and evolution Vol. 13; no. 1; pp. e9740 - n/a
• Main Authors: Coelho, Márcio A. G., Pearson, Gareth A., Boavida, Joana R. H., Paulo, Diogo, Aurelle, Didier, Arnaud‐Haond, Sophie, Gómez‐Gras, Daniel, Bensoussan, Nathaniel, López‐Sendino, Paula, Cerrano, Carlo, Kipson, Silvija, Bakran‐Petricioli, Tatjana, Ferretti, Eliana, Linares, Cristina, Garrabou, Joaquim, Serrão, Ester A., Ledoux, Jean‐Baptiste
• Format: Journal Article
• Language: English
• Published: England John Wiley & Sons, Inc 01.01.2023; Wiley Open Access; John Wiley and Sons Inc
• Subjects: Atlantic‐Mediterranean transition; Biodiversity; Biodiversity and Ecology; Biogeography; Biomarkers; cryptic diversity; Environmental Sciences; Genetic markers; incomplete lineage sorting; Microsatellites; Mitochondria; Octocorallia; Paramuricea; Phylogenetics; phylotranscriptomics; Population differentiation; Reproductive isolation; Sibling species; Speciation; species delimitation; Species diversity; Sympatry; Iberian Peninsula; Mediterranean Sea; Portugal; Atlantic‐Mediterranean transition; species delimitation; Octocorallia; incomplete lineage sorting; cryptic diversity; phylotranscriptomics
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.9740

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. Demarcating the transition between intraspecies lineages and speciation requires accurate delimitation of species boundaries, which in many marine invertebrates such as corals is notoriously difficult, leading to misinterpretations of their ecology and evolution. This study investigates species boundaries, taxonomic affinity, and lineage diversification for key structural species of branching octocorals in the genus Paramuricea across the Atlantic‐Mediterranean biogeographic regions. We combine species tree methods (using RNA‐seq data) with population genetics (clustering methods using microsatellites) and phylogenetics (mitochondrial barcode) to show that the Atlantic and Mediterranean clades studied are recently diverged sister species on separate evolutionary trajectories (Paramuricea cf. grayi and P. clavata), also revealing a second putative (or ongoing) speciation event within Atlantic P. cf. grayi.