Toll-like receptor polymorphism in fan mussels

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 H. pinnae.
We report a high genetic diversity, mainly observed at cell surface TLRs
compared to that of endosomal TLRs. However, the endosomal TLR-7 exhibited
unexpected level of diversity and haplotype phylogeny. The lack of
population structure, associated with a high genetic diversity and
elevated dN/dS ratio, was interpreted as balancing selection, though both
directional and purifying selection were detected. Interestingly, roughly
40% of the P. nobilis identified as resistant to H. pinnae were
introgressed with P. rudis TLR. Specifically, all these P. nobilis carried
a TLR-7 of P. rudis origin. On the contrary, sensitive P. nobilis were not
introgressed, at least at TLR loci, highlighting that TLR-7 might be a
potent effector of resistance. Small contributions of TLR-6 and TLR-4
single nucleotide polymorphism to the cluster of resistant and sensitive
groups could be detected, but their specific role in the resistance
remains highly speculative. This study brings additional knowledge on the
molecular processes of resistance to H. pinnae and will likely contribute
to the conservation efforts carried out to prevent from extinction this
Mediterranean endemic species.