Y-chromosome haplotypes are associated with variation in size and age at maturity in male Chinook salmon

Abstract

Variation in size and age at maturity is an important component of life history that is influenced by both environmental and genetic factors. In salmonids, large size confers a direct reproductive advantage through increased fecundity and egg quality in females, while larger males gain a reproductive advantage by monopolizing access to females. In addition, variation in size and age at maturity in males can be associated with different reproductive strategies; younger smaller males may gain reproductive success by sneaking among mating pairs. In both sexes, there is a trade-off between older age and increased reproductive success and increased risk of mortality by delaying reproduction. We identified four Y-chromosome haplogroups that showed regional- and population-specific variation in frequency using RADseq data for 21 populations of Alaska Chinook salmon. We then characterized the range-wide distribution of these haplogroups using GT-seq assays. These haplogroups exhibited associations with size at maturity in multiple populations, suggesting that lack of recombination between X and Y-chromosomes has allowed Y-chromosome haplogroups to capture different alleles that influence size at maturity. Ultimately, conservation of life history diversity in Chinook salmon may require conservation of Y-chromosome haplotype diversity.

Keywords: Chinook salmon; GT‐seq; RADseq; Ychromosome; age at maturity; haplotype; size at maturity.

FIGURE 1

Frequency of Y‐chromosome haplogroups throughout Alaska based on RADseq and GT‐seq data. Locations of populations are approximate to prevent overlap of pie charts. Population names are given in Table 1. Note that the location for the Lower Yukon Test Fishery (population 3) indicates where fish were caught on their return to the Yukon River; these samples may represent fish from many populations that spawn throughout the Yukon River

FIGURE 2

Plot of haplotype clusters identified by phasing high LD loci from the RADseq dataset. Each individual is represented by two haplotypes corresponding to each chromosome of Ots17. For each SNP, the most common allele is in yellow and the least common allele is in red. Haplotypes were clustered into haplogroups, and six major haplotype clusters were identified; these are denoted by different colors along the sample dendrogram (y‐axis). The gray haplogroup represents X‐chromosomes, while four haplogroups (pink = Ots17‐MH1, green = Ots17‐MH2, blue = Ots17‐MH3, and purple = Ots17‐MH4) represent Ychromosomes; numeric designations only are labeled on plot. SNP position on Ots17 is given on the x‐axis. The position for SNPs that were successfully developed into GT‐seq assays are color‐coded in red on the x‐axis. The relative position of each SNP on chromosome 17 is shown on the top of the x‐axis

FIGURE 3

Logo plots showing allele frequencies within each of the male haplogroups and the X‐chromosome for the RADseq samples. For each SNP, the frequency of alleles within each haplotype (range = 0–1) is shown by the height of the allele. Alleles that are putatively fixed relative to the X‐chromosome are bounded by boxes. SNPs identified by tag number that were successfully converted to GT‐seq assays are in red on the top x‐axis. SNP positions on Ots17 are on the bottom x‐axis

FIGURE 4

Distribution of size at maturity for each Y‐chromosome haplogroup for Alaska Chinook salmon. Female (F) size at maturity is included for comparison. Samples sizes for each haplogroup are given above the boxplots. Length of each individual is shown by gray points. Within each region, Y‐chromosome haplogroups with statistically different lengths are represented by different letters. Haplogroups with two letters (i.e., ab) do not have statistically different size distributions from haplogroups with a or b

FIGURE 5

Distribution of (A) age at maturity and (B) size at age for each Y‐chromosome haplogroup in the Yukon River. Length of each individual is shown by gray points. Within each age class, Y‐chromosome haplogroups with statistically different lengths are represented by different letters. Sample sizes for each haplotype are given above the boxplots