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

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 obser...

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Autores principales: Coupé, Stéphane, Giantsis, Ioannis A., Vázquez Luis, Maite, Scarpa, Fabio, Foulquié, Mathieu, Prévot, Jean‐Marc, Casu, Marco, Lattos, Athanasios, Michaelidis, Basile, Sanna, Daria, García‐March, José Rafa, Tena‐Medialdea, José, Vicente, Nardo, Bunet, Robert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10401143/
https://www.ncbi.nlm.nih.gov/pubmed/37546570
http://dx.doi.org/10.1002/ece3.10383
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author Coupé, Stéphane
Giantsis, Ioannis A.
Vázquez Luis, Maite
Scarpa, Fabio
Foulquié, Mathieu
Prévot, Jean‐Marc
Casu, Marco
Lattos, Athanasios
Michaelidis, Basile
Sanna, Daria
García‐March, José Rafa
Tena‐Medialdea, José
Vicente, Nardo
Bunet, Robert
author_facet Coupé, Stéphane
Giantsis, Ioannis A.
Vázquez Luis, Maite
Scarpa, Fabio
Foulquié, Mathieu
Prévot, Jean‐Marc
Casu, Marco
Lattos, Athanasios
Michaelidis, Basile
Sanna, Daria
García‐March, José Rafa
Tena‐Medialdea, José
Vicente, Nardo
Bunet, Robert
author_sort Coupé, Stéphane
collection PubMed
description 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.
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spelling pubmed-104011432023-08-05 The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression Coupé, Stéphane Giantsis, Ioannis A. Vázquez Luis, Maite Scarpa, Fabio Foulquié, Mathieu Prévot, Jean‐Marc Casu, Marco Lattos, Athanasios Michaelidis, Basile Sanna, Daria García‐March, José Rafa Tena‐Medialdea, José Vicente, Nardo Bunet, Robert Ecol Evol Research Articles 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. John Wiley and Sons Inc. 2023-08-04 /pmc/articles/PMC10401143/ /pubmed/37546570 http://dx.doi.org/10.1002/ece3.10383 Text en © 2023 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Coupé, Stéphane
Giantsis, Ioannis A.
Vázquez Luis, Maite
Scarpa, Fabio
Foulquié, Mathieu
Prévot, Jean‐Marc
Casu, Marco
Lattos, Athanasios
Michaelidis, Basile
Sanna, Daria
García‐March, José Rafa
Tena‐Medialdea, José
Vicente, Nardo
Bunet, Robert
The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression
title The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression
title_full The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression
title_fullStr The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression
title_full_unstemmed The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression
title_short The characterization of toll‐like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression
title_sort characterization of toll‐like receptor repertoire in pinna nobilis after mass mortality events suggests adaptive introgression
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10401143/
https://www.ncbi.nlm.nih.gov/pubmed/37546570
http://dx.doi.org/10.1002/ece3.10383
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