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Genetic variation of the major histocompatibility complex (MHC class II β gene) in the threatened Gila trout, Oncorhynchus gilae gilae

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Abstract

Gila trout (Oncorhynchus gilae gilae) was federally protected in 1973 because of severe declines in abundance and geographic range size. At present, four relict genetic lineages of the species remain in mountain streams of New Mexico and Arizona, USA. Management actions aimed at species recovery, including hatchery production and restocking of formerly occupied streams, have been guided by information from non-functional genetic markers. In this study, we investigated genetic variation at exon 2 of the major histocompatibility complex (MHC) class II β gene that is involved in pathogen resistance and thus presumably under natural selection. Phylogenetic analysis revealed trans-species polymorphism and a significantly high ratio of non-synonymous to synonymous amino acid changes consistent with the action of historical balancing selection that maintained diversity at this locus in the past. However, Gila trout exhibited low allelic diversity (five alleles from 142 individuals assayed) compared to some other salmonid fishes, and populations that originated exclusively from hatcheries possessed three or fewer MHC alleles. Comparative analysis of genetic variation at MHC and six presumably neutrally evolving microsatellite loci revealed that genetic drift cannot be rejected as a primary force governing evolution of MHC in contemporary populations of Gila trout. Maintenance of diversity at MHC will require careful implementation of hatchery breeding protocols and continued protection of wild populations to prevent loss of allelic diversity due to drift.

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Acknowledgements

This work is part of a multi-agency effort to conserve and recover the Gila trout in its native range. We are indebted to personnel of the US Fish & Wildlife Service, the USDA Forest Service, the New Mexico Department of Game and Fish, and the Arizona Department of Game and Fish; especially J. Brooks, K. Young, J. Monzingo, D. Propst, and J. Seals for providing samples used in this study (collected under their permits). J. Wares provided a pilot MHC data set that motivated this study. We are grateful to M. Osborne, W. Wilson, and D. Alò for assistance in the laboratory. W. Wilson made crucial suggestions on analysis of selection on the peptide-binding region and recombination and S. Poe provided guidance on phylogenetic analysis. D. Karapatakis and the Savannah River Ecology Laboratory provided software and assistance necessary for GIS mapping of Gila trout range via funding from the Environmental Remediation Sciences Division of the Office of Biological and Environmental Research, U.S. Department of Energy through the Financial Assistance Award No. DE-FC09-96SR 18546 to the University of Georgia Research Foundation. We are grateful to R. Miller, W. Wilson, M. Osborne, J. Cook, and especially D. Propst for comments and suggestions on the manuscript. Funding for this study was provided by the National Science Foundation (NSF) DEB-0133233 (TFT). Opinions, findings and conclusions or recommendations expressed in this paper are those of the authors and do not necessarily reflect the views of the NSF. Additional funding to MBP was provided by T & E, Inc., the University of New Mexico (UNM) Biology and Graduate Professional Student Associations, the UNM Department of Biology, and the UNM Office of Graduate Studies.

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Peters, M.B., Turner, T.F. Genetic variation of the major histocompatibility complex (MHC class II β gene) in the threatened Gila trout, Oncorhynchus gilae gilae . Conserv Genet 9, 257–270 (2008). https://doi.org/10.1007/s10592-007-9336-9

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  • DOI: https://doi.org/10.1007/s10592-007-9336-9

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