Asymmetric and parallel subgenome selection co-shape common carp domestication

Abstract

Background: The common carp (Cyprinus carpio) might best represent the domesticated allopolyploid animals. Although subgenome divergence which is well-known to be a key to allopolyploid domestication has been comprehensively characterized in common carps, the link between genetic architecture underlying agronomic traits and subgenome divergence is unknown in the selective breeding of common carps globally.

Results: We utilized a comprehensive SNP dataset in 13 representative common carp strains worldwide to detect genome-wide genetic variations associated with scale reduction, vibrant skin color, and high growth rate in common carp domestication. We identified numerous novel candidate genes underlie the three agronomically most desirable traits in domesticated common carps, providing potential molecular targets for future genetic improvement in the selective breeding of common carps. We found that independently selective breeding of the same agronomic trait (e.g., fast growing) in common carp domestication could result from completely different genetic variations, indicating the potential advantage of allopolyploid in domestication. We observed that candidate genes associated with scale reduction, vibrant skin color, and/or high growth rate are repeatedly enriched in the immune system, suggesting that domestication of common carps was often accompanied by the disease resistance improvement.

Conclusions: In common carp domestication, asymmetric subgenome selection is prevalent, while parallel subgenome selection occurs in selective breeding of common carps. This observation is not due to asymmetric gene retention/loss between subgenomes but might be better explained by reduced pleiotropy through transposable element-mediated expression divergence between ohnologs. Our results demonstrate that domestication benefits from polyploidy not only in plants but also in animals.

Keywords: Allopolyploid; High growth rate; Scale reduction; Selection sweep; Vibrant skin color.

Fig. 1

The population genetic structure of the 13 worldwide common carp strains based on 1.92 million genome-wide SNPs. a Sampling locations of common carps included in this study. Number in parentheses is number of individuals in each common carp strain (Additional file 2: Table S1). b Principal component analysis. c Bayesian model-based genetic clustering analysis. The number of populations (K) was predefined from 2 to 13, with the best-fit scenario of K = 2. d The maximum-likelihood phylogeny

Fig. 2

Genome-wide selection signatures associated with scale reduction in common carp domestication. a Genome-wide selection signals. Tracks A and B are Tajima’s D in the scale-reduced domesticated group and fully scaled wild group, respectively; Tracks C and D are CLR scores in the scale-reduced domesticated group and fully scaled wild group, respectively; Track E is F_ST between the scale-reduced domesticated group and fully scaled wild group; Track F is the synteny between subgenomes A and B. Chromosomes with signatures of selection are highlighted with larger font size of names (Additional file 2: Table S4). b Genomic regions with selection sweep signals on chromosome A09. Tajima’s D and CLR scores are calculated in the scale-reduced domesticated group (red lines) and the fully scaled wild group (blue lines), respectively. F_ST is calculated between the scale-reduced domesticated group and the fully scaled wild group (gray line), between the scale-reduced domesticated group and the fully scaled (wild and domesticated) group (orange line), and between the scale-reduced domesticated group and the fully scaled domesticated group (pink line). Light blue vertical bars with indicate the selection regions. Genes in the genomic regions (light blue vertical bars) with selection sweep signals are listed. c Genotypes of SNPs showing higher genetic differentiation between scale-reduced and fully scaled common carps in genomic regions with selection sweep signals on chromosome A09. d The GO in genomic regions with selection sweep signals related to scale reduction. e Genotypes of SNPs in the gene abca12 and extended haplotype homozygosity (EHH) around the crucial SNP “A09:8573491” and “A09:8589164.” f Genotypes of SNPs in the gene morc3a and EHH around the crucial SNP “A09:11711312”

Fig. 3

Genome-wide selection signatures associated with skin color variation in common carp domestication. a Genome-wide selection signals. Tracks A and B are Tajima’s D in the skin-vibrant domesticated group and the skin-caesious wild group, respectively; Tracks C and D are CLR scores in the skin-vibrant domesticated group and the skin-caesious wild group, respectively; Track E is F_ST between the skin-vibrant domesticated group and the skin-caesious wild group; Track F is the synteny between subgenomes A and B. Chromosomes with signatures of selection are highlighted with larger font size of names (Additional file 2: Table S4). b Genomic regions with selection sweep signals on chromosomes of A06 and B06. Tajima’s D and CLR scores are calculated in the skin-vibrant domesticated group (red lines) and the skin-caesious wild group (blue lines), respectively. F_ST is calculated between the skin-vibrant domesticated group and the skin-caesious wild group (gray line), between the skin-vibrant domesticated group and the skin-caesious (wild and domesticated) group (orange line), and between the skin-vibrant group and the skin-caesious Asian wild group (pink line). Light blue vertical bars which indicate the selection regions. Genes in the genomic regions (light blue vertical bars) with selection sweep signals are listed. Lines between chromosomes of A06 and B06 show synteny between the two paralogous chromosomes. c The GO in genomic regions with selection sweep signals related to skin color variation. d Genotypes of SNPs in three pairs of paralogous genes on A06 and B06 and extended haplotype homozygosity around the crucial SNPs in each of the six genes. e Expression in skin of the three pairs of ohnologs with selection signals associated with color variation in common carps (Additional file 2: Table S10)

Fig. 4

Genome-wide selection signatures associated with high growth rate in common carp domestication. Growth rate in wild and domesticated common carps from Asia (a) and Europe (b). Genome-wide selection signatures associated with high growth rate in domesticated common carps from Asia (c) and Europe (d). Tracks A and B are Tajima’s D in the high growth rate domesticated and wild group; Tracks C and D are CLR score in the high growth rate domesticated and wild group; Track E is F_ST between the high growth rate domesticated and wild group; Track F is the synteny between subgenome A and B (Additional file 2: Table S4). Chromosomes with signatures of selection are highlighted with larger font size of names. The GO in genomic regions with selection sweep signals related to high growth rate in domesticated common carps from Asia (e) and Europe (f)

Fig. 5

Ohnolog dynamics in genomic regions with selection sweep signals in common carp genomes. a Ohnolog dynamics in genomic regions with selection sweep signals related to scale reduction, skin color variation, and fast growth and genome-wide ohnolog dynamics in common carp genomes. The ratios of 1:0, 1:1, and others represent singleton genes, ohnologs, and multiple-copy genes in the genome of Yuxuan Yellow River carp (yxYR), German mirror carp (GM), and Hebao red carp (HB), respectively. b Expression of 121 ohnolog pairs between subgenomes in the muscle of the strain SP (Additional file 2: Table S15). c Ohnolog with twofold expression divergence. Expression divergence between 78 pairs of expressed ohnologs with TPM > 1 in at least one sample in the muscle of the strain SP. Log₂(TPM_{Subgenome B}/TPM_{Subgenome A}) indicates the degree of expression difference of the ohnolog pairs. N values indicate the number of ohnolog pairs with twofold expression divergence. d TE content and coverage in gene body (intron), upstream (1 Kb), and downstream (1 Kb) regions between the 122 pairs of ohnologs, 74 pairs of expressed ohnologs, 16 pairs of ohnologs with twofold upregulated expression in selected genes, and 10 pairs of ohnologs with twofold down-regulated expression in selected genes in GM genome, respectively