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

<div><p></p><p>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 <i>Oncorhynchus tshawytscha</i>, the Y chromosome possesses a growth hormone pseudogene (<i>ghp</i>) that is linked to the sex-determination locus and is derived from the functional autosomal growth hormone 2 gene (<i>gh2</i>). 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 <i>gh2</i> and <i>ghp</i> in 315 individuals from 19 Chinook Salmon populations ranging from Russia to Alaska, British Columbia, and California. The <i>ghp</i> 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, <i>gh2</i> variants from the most common haplotype were found in 46.7% of individuals. We detected more sites of variation in <i>ghp</i> (nine positions, five haplotypes) than in <i>gh2</i> (three positions, five haplotypes), but these were restricted to just four genotypes for <i>ghp</i>, compared with nine for <i>gh2</i>. Selection may have caused a single Y chromosome to become fixed among most populations in this species, while the variation at the <i>gh2</i> locus is maintained under diploid autosomal conditions. Since the <i>ghp</i> locus variants are not likely to be directly associated with strong functions, other linked Y<i>-</i>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.</p><p>Received January 15, 2015; accepted June 3, 2015</p></div