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 individuals 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 P. nobilis, Pinna rudis and P. nobilis × P. 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 with 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, they all carried a TLR‐7 of P. rudis origin, whereas sensitive P. nobilis were not introgressed, at least at TLR loci. Small contributions of TLR‐6 and TLR‐4 single‐nucleotide polymorphisms to the clustering of resistant and susceptible individuals could be detected, but their specific role in resistance remains highly speculative. This study provides new information on the diversity of TLR genes within the P. nobilis species after MME and additional insights into adaptation to H. pinnae that should contribute to the conservation of this Mediterranean endemic species.

Morphometric Analysis of the Critically Endangered Fan Mussel (Pinna nobilis L.) in Maliakos Gulf (Central Aegean)

“…P. nobilis has recently been classified as critically endangered on the IUCN Red List of threatened species. One of the main challenges faced by P. nobilis populations is the impact of a protozoan parasite called Haplosporidium pinnae [2]. This parasite has caused mass mortality events and increased the risk of extinction in many of the habitats where this species is found.…”

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

“…The large fan-shell genus Pinna is represented by two species in the Mediterranean Sea: the endemic P. nobilis Linnaeus 1758 [1], and the (sub)tropical Atlantic P. rudis Linnaeus 1758 [2]. P. rudis is recognised as the sister taxon of P. nobilis [3], and hybrids nobilis × rudis are also known [4]. Notwithstanding its broader geographical range, in the Mediterranean Sea P. rudis is less common than P. nobilis, being mainly restricted to the warmest southwestern regions of the basin [5].…”