Genetic homogeneity of the critically endangered fan mussel, Pinna nobilis, throughout lagoons of the Gulf of Lion (North-Western Mediterranean Sea)

Abstract

The fan mussel, Pinna nobilis, endemic to the Mediterranean Sea, is a critically endangered species facing mass mortality events in almost all of its populations, following the introduction of the parasite Haplosporidium pinnae. Such a unique pandemic in a marine organism, which spreads rapidly and with mortality rates reaching up to 100%, could lead to the potential extinction of the species. Only few regions, involving lagoon habitats, remain healthy throughout the entire Mediterranean Sea. This study describes the genetic structure of P. nobilis across the Gulf of Lion, including confined locations such as lagoons and ports. A total of 960 samples were collected among 16 sites distributed at 8 localities, and then genotyped using 22 microsatellite markers. Genetic diversity was high in all sites with mean allele numbers ranging between 10 and 14.6 and with observed heterozygosities (Ho) between 0.679 and 0.704. No genetic differentiation could be identified (FST ranging from 0.0018 to 0.0159) and the percentages of related individuals were low and similar among locations (from 1.6 to 6.5%). Consequently, all fan mussels, over the entire coastline surveyed, including those in the most geographically isolated areas, belong to a large genetically homogeneous population across the Gulf of Lion. Considering the ongoing mass mortality context, this result demonstrates that almost all of the genetic diversity of P. nobilis populations is still preserved even in isolated lagoons, which might represent a refuge habitat for the future of the species.

Investigating population dynamics from parentage analysis in the highly endangered fan mussel Pinna nobilis

“…As a parallel, low but significant genetic differentiation was found between years in the bay of Peyrefite, which also supports the hypothesis of a rapid turnover within the population. Even if low, values were in the same order of magnitude as what was found between Port‐St‐Louis and the Côte des Albères, which are separated by approximately 200 km (Peyran, Boissin, et al, 2021). Such differences, as well as the small heterozygote deficiency observed in 2015 and 2018, may reflect some temporal Wahlund effect that could be due to successive cohorts presenting slight variations in allele frequencies.…”

“…In addition, the area is known to undergo intense air-sea interactions leading to strong winds and large sea states that can have substantial impacts on coastal habitats (Renault et al, 2012), which could be responsible for the lower survival in the bay of Peyrefite. (Peyran, Boissin, et al, 2021). Such differences, as well as the small heterozygote deficiency observed in 2015 and 2018, may reflect some temporal Wahlund effect that could be due to successive cohorts presenting slight variations in allele frequencies.…”

“…In this context, it is now, more than ever, necessary to have better information about the demographic dynamics of the species in order to implement effective conservation plans. Previous studies on P. nobilis population genetics showed low genetic differentiation that implied connectivity among populations (González-Wangüemert et al, 2019;Peyran, Boissin, et al, 2021;Wesselmann et al, 2018). However, none of these studies focused on recruitment processes which drive the replenishment of the local population.…”

“…Following this tragic situation, the status of the species was reevaluated and upgraded to “critically endangered” on the IUCN red list (Kersting et al, 2019). Currently, only very few populations remain unaffected in marine habitats (Acarli et al, 2020; Çinar et al, 2021; García‐March, Tena, et al, 2020) or in lagoons (Cabanellas‐Reboredo et al, 2019; Catanese et al, 2018; Peyran, Morage, et al, 2021) that should be considered as targets for conservation priorities as they could act as refuges and source populations for the species recovery.…”

“…Previous studies on P . nobilis population genetics showed low genetic differentiation that implied connectivity among populations (González‐Wangüemert et al, 2019; Peyran, Boissin, et al, 2021; Wesselmann et al, 2018). However, none of these studies focused on recruitment processes which drive the replenishment of the local population.…”