Heterozygote advantage of hybrid varieties from red crucian carp and white crucian carp revealed by genome wide association analysis

Abstract

Distant hybridization in fish reshapes genetic materials of hybrid varieties, thereby providing heterosis in growth process. However, genetic basis of growth advantage remains poorly understood. In this study, we conducted whole-genome resequencing, RNA-seq analyses, and genome-wide association studies (GWAS) on 400 individuals from white crucian carp (Carassius cuvieri, WCC), red crucian carp (Carassius auratus red var., RCC), and their hybrids (WR and WR-II). We identified 14,169,714 filtered single nucleotide polymorphisms (SNPs), with an average SNP density of less than 700 bp across genome. 18 SNPs were significantly associated with growth traits, and 306 genes were annotated in genomic regions around the SNP loci. Lead SNP-associated candidate genes, including SLC35F3, HERC2 and MAP2K2, showed higher expression levels, correlating positively with WR-II's growth advantage. Heterozygous frequencies for WCC and RCC were zero, except for a 20 % frequency in RCC for body depth (BD)-associated lead SNP. Excluding BD-associated SNP, WR-II had higher heterozygous frequencies (24 %–33.3 %) than WR (1.9 %–15.4 %) across four lead SNPs, except for the body length-associated SNP variants (80.8 % for WR and 52.2 % for WR-II). Among individuals with dominant growth, genotype frequencies for two heterozygous SNPs were higher in WR-II (28.6 %) than in WR (21.2 %), and for three heterozygous SNPs, the frequencie was significantly higher in WR-II (14.3 %) compared to WR (1.9 %) (p < 0.05). Notably, WR had no individuals with four heterozygous SNPs, while WR-II had 9.5 %. These results suggest that hybridization increases allelic heterozygosity, contributing to growth advantage by upregulating gene expression. Our findings provide valuable insights into genetic basis of heterosis in hybrid varieties.