Insights on Pinna nobilis population genetic structure in the Aegean and Ionian Sea

Abstract

The fan mussel Pinna nobilis Linnaeus, 1758 is an endemic species of the Mediterranean Sea, protected by international agreements. It is one of the largest bivalves in the world, playing an important role in the benthic communities; yet it has been recently characterized as Critically Endangered by the IUCN, due to mass mortality events. In this context, the assessment of the genetic variation of the remaining P. nobilis populations and the evaluation of connectivity among them are crucial elements for the conservation of the species. For this purpose, samples were collected from six regions of the Eastern Mediterranean Sea; the Islands of Karpathos, Lesvos and Crete; the Chalkidiki and Attica Peninsulas; and the Amvrakikos Gulf. Sampling was performed either by collecting tissue from the individuals or by using a non-invasive method, i.e., by scraping the inside of their shells aiming to collect their mucus and thus avoid stress induction to them. Conventional molecular techniques with the use of the COI and 16S rRNA mitochondrial markers were selected for the depiction of the intra-population genetic variability. The analyses included 104 samples from the present study and publicly available sequences of individuals across the whole Mediterranean Sea. The results of this work (a) suggest the use of eDNA as an efficient sampling method for protected bivalves and (b) shed light to the genetic structure of P. nobilis population in the Eastern Mediterranean; this latter knowledge might prove to be fundamental for the species conservation and hence the ecosystem resilience. The haplotype analyses reinforced the evidence that there is a certain degree of connectivity among the distinct regions of the Mediterranean; yet there is evidence of population distinction within the basin, namely between the Western and the Eastern basins. The combination of both genetic markers in the same analysis along with the inclusion of a large number of individuals produced more robust results, revealing a group of haplotypes being present only in the Eastern Mediterranean and providing insights for the species’ most suitable conservation management.

Reconstructing the Evolutionary History of Pinna nobilis: New Genetic Signals from the Past of a Species on the Brink of Extinction

“…Furthermore, authors set the genetic boundary between the western and eastern Mediterranean basins in the Ionian Sea, thus suggesting that, for P. nobilis, the Sicilian straits do not represent a boundary for larval dispersal. These results were then corroborated by Sarafidou et al [51], who analysed the residual genetic variation in the surviving populations after the MME from sites in the Aegean and Ionian Seas. Furthermore, based on the COI analyses, and consistent with what was previously hypothesised by Sanna et al [14], Wesselman et al [58] suggested that P. nobilis is characterised by a single mitochondrial haplogroup that experienced a recent population expansion starting from a small, original population.…”

“…Consequently, we reconstructed, with the utmost accuracy, the pre-MME phylogeographic patterns of P. nobilis in the Mediterranean Sea, shedding light on the origin of the genetic structuring between the western and eastern P. nobilis populations hypothesised in Sanna et al [14] and recently corroborated by Sarafidou et al [51] based on the analysis of Aegean and Ionian populations surviving after the MME. By utilising samples from populations not yet affected by the mass mortality of P. nobilis, we were able to study the evolutionary patterns of the species without the bias of the evolutionary forces that affected the genetic landscape of the populations due to the MME.…”

“…Thus, the entire Mediterranean basin might have been interested by a level of haplotype sharing among western and eastern populations higher than those identified until now. This potential scenario is supported by a recent study on surviving populations from the Aegean and Ionian seas [51], which revealed haplotype sharing between the western Mediterranean and Ionian Sea based on the analysis of a concatenated mitochondrial fragment, including COI and ribosomal 16S genes.…”

“…Only a few populations of P. nobilis survived the MME based on the most recent publications; however, we are aware that some populations disappear within a few months (e.g., Croatian populations, Čižmek et al [35]) [49]. These populations are primarily situated in estuaries and isolated coastal lagoons in France, Italy, Spain [50], Greece [51], and the Sea of Marmara [52]. Notably, even if there are no recent surveys concerning the status of P. nobilis along the Tunisian coastlines, some unpublished studies indicate thriving populations in the Kerkennah Islands, Monastir Bay, and Bizerte Lagoon [53].…”

“…In such a context, several molecular studies have been performed on the genetic variability of P. nobilis so far [14,22,25,49,51,[57][58][59][60][61]. The primary objective of the majority of these papers was to infer the genetic variability of P. nobilis after the protection plans started in the 1990s.…”