The evolution of the major histocompatibility complex in upstream versus downstream river populations of the longnose dace

• Published in: Ecology and evolution 2017-05, Vol.7 (10), p.3297-3311
• Main Authors: Crispo, Erika, Tunna, Haley R., Hussain, Noreen, Rodriguez, Silvia S., Pavey, Scott A., Jackson, Leland J., Rogers, Sean M.
• Format: Article
• Language: English
• Subjects: Amino acids; Biological evolution; Contaminants; diversifying selection; Downstream effects; Ecological conditions; Evolutionary genetics; Gene sequencing; Genetic resources; heterozygote advantage; Immune response; Immune system; Major histocompatibility complex; negative frequency‐dependent selection; next‐generation sequencing; Original Research; overdominance; Population structure; Populations; Rhinichthys cataractae; Rivers
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.2839

Populations in upstream versus downstream river locations can be exposed to vastly different environmental and ecological conditions and can thus harbor different genetic resources due to selection and neutral processes. An interesting question is how upstream–downstream directionality in rivers affects the evolution of immune response genes. We used next‐generation amplicon sequencing to identify eight alleles of the major histocompatibility complex (MHC) class II β exon 2 in the cyprinid longnose dace (Rhinichthys cataractae) from three rivers in Alberta, upstream and downstream of municipal and agricultural areas along contaminant gradients. We used these data to test for directional and balancing selection on the MHC. We also genotyped microsatellite loci to examine neutral population processes in this system. We found evidence for balancing selection on the MHC in the form of increased nonsynonymous variation relative to neutral expectations, and selection occurred at more amino acid residues upstream than downstream in two rivers. We found this pattern despite no population structure or isolation by distance, based on microsatellite data, at these sites. Overall, our results suggest that MHC evolution is driven by upstream–downstream directionality in fish inhabiting this system. Amino acids of the MHC II beta subunit, exon 2, were found to be under balancing selection in longnose dace. Results are from OmegaMap which simultaneously estimates selection and recombination.