The characterization of toll-like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression.      

Abstract

The fan mussel Pinna nobilis is currently on the brink of extinction due to a multifactorial disease mainly caused to the highly pathogenic parasite Haplosporidium pinnae, meaning that the selection pressure outweighs the adaptive potential of the species. Hopefully, rare specimens have been observed somehow resistant to the parasite, stretching the need to identify the traits underlying this better fitness. Among the candidate to explore at first intention are fast evolving immune genes, of which toll-like receptor (TLR). In this study, we examined the genetic diversity at 14 TLR loci across Pinna nobilis, Pinna rudis and Pinna nobilis x Pinna rudis hybrid genomes, collected at four physically distant regions, that were found to be either resistant or sensitive to the parasite Haplosporidium pinnae. We report a high genetic diversity, mainly observed at cell surface TLRs compared to that of endosomal TLRs. However, the TLR-7 and TLR-1 exhibited unexpected level of diversity and haplotype phylogeny, respectively. The lack of population structure, associated with a high genetic diversity and elevated dN/dS ratio were interpreted as balancing selection, though both directional and purifying selection were detected. Overall, we observed small contributions of putatively selected SNPs involved in the resistance. However, the most contributing SNPs were carried by two TLR-6 loci and might be used as potent biomarkers of distinguish between resistant and sensitive P. nobilis individuals. Moreover, more than 10% of P. nobilis individuals were found introgressed with P. rudis. Noteworthy, all introgressed P. nobilis observed as resistant to H. pinnae carried a TLR-7 of P. rudis origin. This study contributes to the ongoing efforts towards conservation carried out to prevent from extinction this Mediterranean endemic species.

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

“…Moreover, considering the findings of Coupé et al [47] that some P. nobilis individuals that introgressed with P. rudis were resistant to infection by Haplosporidium pinnae, the expansion of P. rudis in the Mediterranean could lead to an increased frequency of hybridisation and introgression with P. nobilis. This, in turn, could confer resistance to H. pinnae, a primary etiological agent of mass mortality events, thereby potentially promoting the recovery and survival of the fan mussel.…”

“…The initial investigations into the causes of the MME of P. nobilis primarily concentrated on the search for protozoa [29,30,32,33,[40][41][42], and histological analysis on the first affected individuals of P. nobilis revealed the presence of a haplosporidian-like parasite (Haplosporidium pinnae) within the digestive gland [29,30,40], initially believed to be host-specific for fan mussels. Subsequent studies identified several bacterial species as potential pathogens contributing to the MME of P. nobilis [13,[35][36][37]39,[43][44][45][46], indicating that the disease is a multifactorial pathology [13,47,48]. Scarpa et al [13] also reported the finding of H. pinnae in other bivalve species collected before 2016.…”

A Tale of Two Sisters: The Southerner Pinna rudis Is Getting North after the Regional Extinction of the Congeneric P. nobilis (Mollusca: Bivalvia)

“…The search for survivors is requiring a large sampling effort, partly supported by citizen science. In this context, an unusual number of P. rudis individuals, apparently unaffected by pathogens [21], has been recorded in various, newly discovered locations across the Mediterranean, indicating that the species is expanding its range northward and eastward [22][23][24][25].…”