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. 2024 Aug 5;16(8):evae174.
doi: 10.1093/gbe/evae174.

Draft Genome of Akame (Lates Japonicus) Reveals Possible Genetic Mechanisms for Long-Term Persistence and Adaptive Evolution with Low Genetic Diversity

Yasuyuki Hashiguchi  1 , Tappei Mishina  2   3 , Hirohiko Takeshima  4 , Kouji Nakayama  5 , Hideaki Tanoue  6 , Naohiko Takeshita  7 , Hiroshi Takahashi  7
Affiliations

Draft Genome of Akame (Lates Japonicus) Reveals Possible Genetic Mechanisms for Long-Term Persistence and Adaptive Evolution with Low Genetic Diversity

Yasuyuki Hashiguchi et al. Genome Biol Evol. .

Abstract

It is known that some endangered species have persisted for thousands of years despite their very small effective population sizes and low levels of genetic polymorphisms. To understand the genetic mechanisms of long-term persistence in threatened species, we determined the whole genome sequences of akame (Lates japonicus), which has survived for a long time with extremely low genetic variations. Genome-wide heterozygosity in akame was estimated to be 3.3 to 3.4 × 10-4/bp, one of the smallest values in teleost fishes. Analysis of demographic history revealed that the effective population size in akame was around 1,000 from 30,000 years ago to the recent past. The relatively high ratio of nonsynonymous to synonymous heterozygosity in akame indicated an increased genetic load. However, a detailed analysis of genetic diversity in the akame genome revealed that multiple genomic regions, including genes involved in immunity, synaptic development, and olfactory sensory systems, have retained relatively high nucleotide polymorphisms. This implies that the akame genome has preserved the functional genetic variations by balancing selection, to avoid a reduction in viability and loss of adaptive potential. Analysis of synonymous and nonsynonymous nucleotide substitution rates has detected signs of positive selection in many akame genes, suggesting adaptive evolution to temperate waters after the speciation of akame and its close relative, barramundi (Lates calcarifer). Our results indicate that the functional genetic diversity likely contributed to the long-term persistence of this species by avoiding the harmful effects of the population size reduction.

Keywords: akame; balancing selection; draft genome; genetic diversity; genetic load; inbreeding depression.

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Conflict of interest statement

Conflict of Interest The authors declare that there is no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Sampling locations of the two akame individuals (Kochi and Miyazaki) used in this study.
Fig. 2.
Fig. 2.
Historical Nes inferred by PSMC analysis for akame (Kochi and Miyazaki) and barramundi (India, Thailand, and Indonesia). Fine lines denote bootstrap replicates. The green and white bars below indicate the last three interglacial and glacial periods, respectively. LGP, last glacial period.
Fig. 3.
Fig. 3.
a) A relationship between genomic heterozygosity and ratio of heterozygosity at 0-fold relative to 4-fold degenerate sites in the individuals of akame and barramundi. b) Ratios of functional effect categories of SNVs in the individuals of akame and barramundi. Functional effect categories in each SNV were identified using the SnpEff program (Cingolani et al. 2012). Functional effect categories: High, nonsense and splicing donor/acceptor site variants; Moderate, missense variants; Low, synonymous and stop retained variants. c) Boxplot of the ROH lengths in Kochi and Miyazaki akame individuals. d) Cumulative fraction of the genome made up of ROHs at least 100 kb long.
Fig. 4.
Fig. 4.
a) A sliding-window plot of nucleotide diversity (red: left y axis) and mean FST (light blue: right y axis) for 10-kb nonoverlapping windows in the akame genome. The mitochondrial genome was excluded from the analysis. Dashed line indicates the cutoff value of nucleotide diversity (mean + 4 SD: 0.0020). Abbreviations of the representative polymorphic genes in the nucleotide diversity peak regions (nucleotide diversity within the coding region >0.01) are shown in the figure (see Table 2 for details). In addition, the genomic locations of the MHC, OR, and two protocadherin gene clusters within the nucleotide diversity-peak regions are indicated by blue arrows. b) A violin plot of FST values in the background and nucleotide diversity-peak regions. Distribution of FST values in the nucleotide diversity-peak regions was significantly shifted toward lower values compared with background regions (P < 2.2 × 10−16, two-tailed Mann–Whitney test). Numbers of windows in each category are shown in parentheses. c) Summary of the functional annotation clustering of the 221 genes within the nucleotide diversity-peak regions. The number of genes in each cluster is shown in the graph. Numbers on the right of the bars indicate fold enrichment. The names of significantly enriched (FDR-adjusted P-value < 0.05) clusters are indicated in bold. A full list of the annotation clusters is provided in supplementary table S6, Supplementary Material online.
Fig. 5.
Fig. 5.
Analysis of selection in akame genes. a) FDR-adjusted P-value distributions of the RELAX tests of akame (above) and barramundi (below). Red and blue bars indicate the numbers of genes with intensified (k > 1) and relaxed (k < 1) selective pressures, respectively. For visualization, the numbers of genes with a P-value of >0.95 were excluded from the histograms. b) Two branch-specific models to test differences in selective pressures between akame and barramundi. Phylogenetic relationship of the five fish species was reconstructed by the maximum-likelihood methods using concatenated one-to-one orthologous gene set (supplementary fig. S8, Supplementary Material online; see Materials and Methods). c) Scatter plot of the synonymous–nonsynonymous nucleotide substitution rate ratio (ω = dN/dS) in the branches of akame (ω2, x axis) and barramundi (ω1, y axis) estimated by Model 2 in each orthologous gene set. For visualization, genes with ω1 and/or ω2 values estimated as infinity were excluded from the plot. Genes with ω1 and/or ω2 estimated as 0 were included in the plot by adjusting them to replace 1 × 10−4. Diagonal line indicates ω1 = ω2.
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