Genetic diversity, connectivity and gene flow along the distribution of the emblematic Atlanto-Mediterranean sponge Petrosia ficiformis (Haplosclerida, Demospongiae)

ABSTRACT Background: Knowledge about the distribution of the genetic variation of marine species is fundamental to address species conservation and management strategies, especially in scenarios with mass mortalities. In the Mediterranean Sea, Petrosia ficiformis is one of the species most affected by temperature-related diseases. Our study aimed to assess its genetic structure, connectivity, and bottleneck signatures to understand its evolutionary history and to provide information to help design conservation strategies of sessile marine invertebrates. Results: We genotyped 280 individuals from 19 locations across the entire distribution range of P. ficiformis in the Atlanto-Mediterranean region at 10 microsatellite loci. High levels of inbreeding were detected in most locations (especially in the Macaronesia and the Western Mediterranean) and bottleneck signatures were only detected in Mediterranean populations, although not coinciding entirely with those with reported die-offs. We detected strong significant population differentiation, with the Atlantic populations being the most genetically isolated, and show that six clusters explained the genetic structure along the distribution range of this sponge. Although we detected a pattern of isolation by distance in P. ficiformis when all locations were analyzed together, stratified Mantel tests revealed that other factors could be playing a more prominent role than isolation by distance. Indeed, we detected a strong effect of oceanographic barriers impeding the gene flow among certain areas, the strongest one being the Almeria-Oran front, hampering gene flow between the Atlantic Ocean and the Mediterranean Sea. Finally, migration and genetic diversity distribution analyses suggest a Mediterranean origin for the species. Conclusions: In our study Petrosia ficiformis showed extreme levels of inbreeding and population differentiation, which could all be linked to the poor swimming abilities of the larva. However, the observed moderate migration patterns are highly difficult to reconcile with such poor larval dispersal, and suggest that, although unlikely, dispersal may also be achieved in the gamete phase. Overall, because of the high genetic diversity in the Eastern Mediterranean and frequent mass mortalities in the Western Mediterranean, we suggest that conservation efforts should be carried out specifically in those areas of the Mediterranean to safeguard the genetic diversity of the species.ACKNOWLEDGEMENTS The authors wish to warmly thank Maurizio Pansini, Thanos Dailianis, Thierry Perez, Peter Wirtz, and Tatjana Bakran-Petricioli (to JRX) Laura Steindler and Eduardo Serrano, Juan Moles Joan Giménez, and Carlos Angulo-Preckler (to AR) for sending specimens from their research locations. We are also indebted to the two reviewers and the Associate Editor Prof. Sally Leys who greatly improved our manuscript. AR and ST also wish to thank Martín Taboada Riesgo for the support along the study. FUNDING This research was funded by the Spanish Government project MARSYMBIOMICS CTM2013–43287-P, the Catalan Government grant 2014SGR-336 for Consolidated Research Groups, the European project SponGES (Grant Agreement No. 679849), and internal funds of the NHM to AR (SDF14032). AR and RPP were funded by Juan de la Cierva fellowships of the Spanish Government during half the study. The funding bodies did not have any role in the design of the study and collection, analysis, interpretation of data or in writing the manuscript. AVAILABILITY OF DATA AND MATERIAL The complete matrix of genotypes can be accessed in PANGAEA under https://doi.org/10.1594/PANGAEA.882098. The coordinates and locations for each population are listed in Table 1