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.