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Patterns of Historical Balancing Selection on the Salmonid Major Histocompatibility Complex Class II β Gene

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Abstract

Allelic variation in the major histocompatibility class (MHC) IIB gene of salmonids is analyzed for patterns indicative of natural selection acting at the molecular level. Sequence data for the second exon of this MHC gene were generated for 11 species in three salmonid genera: Oncorhynchus, Salmo, and Salvelinus. Phylogenetic analysis of nucleotide sequences revealed: (1) monophyletic grouping of alleles from each genus, (2) transspecies evolution of alleles within Salmo and Salvelinus, and (3) differential patterns of transspecies evolution within the genus Oncorhynchus. Within Oncorhynchus, five of seven species had alleles that were species-specific or nearly so, while the remaining two, O. mykiss and O. clarkii, retained ancestral polymorphisms. The different patterns in Oncorhynchus and the other two genera could be due to historical demographic effects or functional differences in MHC molecules in the three genera, but the two hypotheses could not be distinguished with the current dataset. An analysis of recombination/gene conversion identified numerous recombinant alleles, which is consistent with what has been found in other vertebrate taxa. However, these gene conversion events could not account for the species-specific allelic lineages observed in five of the Oncorhynchus species. Analyses of the relative rates of nonsynonymous and synonymous substitutions revealed the signature of selection on the class IIB gene in all 11 of the salmonid species for both the ABS and the non-ABS codons. Codon-based analyses of selection identified seven codons that have experienced selection in the majority of the species. More than half of these sites were mammalian ABS codons, but several were not, suggesting subtle functional differences in the mammalian and teleost fish MHC molecules.

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Acknowledgments

We thank J. Candy (DWO; Canada), D. Hankin and E. Loudenslager (HSU; USA), P. Moran (NWFSC-NOAA; USA), M. Peacock (UNR; USA), C. Smith (ADFG; USA), J. Wenburg (USFWS; USA), and members of the Southwest Fisheries Science Center for samples. The manuscript benefited greatly from discussion with C. Lemaire and S. M. Blankenship. C. Gallardo provided laboratory assistance.

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Authors and Affiliations

  1. NOAA Southwest Fisheries Science Center and Department of Ocean Sciences, University of California, 110 Shaffer Road, Santa Cruz, CA, 95060, USA

    Andres Aguilar & John Carlos Garza

  2. School of Natural Sciences, University of California, P.O. Box 2039, Merced, CA, 95344, USA

    Andres Aguilar

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  1. Andres Aguilar
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  2. John Carlos Garza
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Correspondence to Andres Aguilar.

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[Reviewing Editor: Dr. Willie Swenson.]

GenBank accession numbers: EF432115–EF432188

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Aguilar, A., Garza, J.C. Patterns of Historical Balancing Selection on the Salmonid Major Histocompatibility Complex Class II β Gene. J Mol Evol 65, 34–43 (2007). https://doi.org/10.1007/s00239-006-0222-8

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