Low Variation in a Y-Chromosomal Growth Hormone Pseudogene Relative to its Functional Autosomal Progenitor Gene in Chinook Salmon

Abstract

Most fish species do not have single-chromosome-based sex determination or display cytologically distinguishable sex chromosomes. The selective forces acting on homologous sequences in diploid autosomal versus haploid sex-chromosomal regions are expected to be distinct and thus to differentially influence genetic variation. In Chinook Salmon Oncorhynchus tshawytscha, the Y chromosome possesses a growth hormone pseudogene (ghp) that is linked to the sex-determination locus and is derived from the functional autosomal growth hormone 2 gene (gh2). Thus, examining these two paralogues provides a model with which to study the forces affecting the persistence of genetic variation between sex-linked and autosomal loci among individuals in Chinook Salmon populations. We characterized single-nucleotide polymorphisms in a 1.6-kb contiguous homologous region in gh2 and ghp in 315 individuals from 19 Chinook Salmon populations ranging from Russia to Alaska, British Columbia, and California. The ghp sequence was highly similar among individuals and populations, with variant haplotypes being detected in only 5.4% of individuals and restricted to just two populations. In contrast, gh2 variants from the most common haplotype were found in 46.7% of individuals. We detected more sites of variation in ghp (nine positions, five haplotypes) than in gh2 (three positions, five haplotypes), but these were restricted to just four genotypes for ghp, compared with nine for gh2. Selection may have caused a single Y chromosome to become fixed among most populations in this species, while the variation at the gh2 locus is maintained under diploid autosomal conditions. Since the ghp locus variants are not likely to be directly associated with strong functions, other linked Y-chromosomal loci may have important functions that, when selected, cause Y chromosomes to either be damaged and rapidly eliminated or to have enhanced fitness and sweep through the species. Whether such loci include the sex-determination locus itself or other functional loci is not yet known.

Received January 15, 2015; accepted June 3, 2015

ACKNOWLEDGMENTS

The authors would like to thank Benjamin Goh and Janine Supernault for technical assistance, Sally Otto for helpful comments on the manuscript, and the very many fisheries biologists who provided samples from throughout the study area.