Genomic evidence for demographic fluctuations, genetic burdens and adaptive divergence in fourfinger threadfin Eleutheronema rhadinum

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Abstract Declining populations and bottlenecks lead to the accumulation of deleterious mutations in fish populations. These processes also trigger genetic purging, which is a key genetic factor in reducing the deleterious burdens and increasing population viability. However, there is a lack of empirical evidence on the interaction between demographic history and the genome-wide pattern of deleterious variations. Here, we generated genome resequencing data of Eleutheronema rhadinum from China and Thailand, representing the major distribution of the species’ southern regions. E. rhadinum had exceptionally low genome-wide variability and experienced dramatic population expansions followed by continuous declines. The geographical divergence, which occurred ~ 23,000 years ago, shaped different demographic trajectories and generated different regional patterns of deleterious mutations in China and Thailand populations. Several lines of evidence revealed that this geographical pattern of deleterious mutation was driven by the purging of highly deleterious mutations. We showed that purifying selection had inbreeding-associated fitness costs and was more efficient against missense mutations in the Thailand population, which had the lowest genetic burden of homozygous deleterious mutations. Multiple evolutionarily conserved protein domains were disrupted by the loss-of-function mutations, posing a high probability of gene functionality elimination. Moreover, thermal and salinity genes (Trpm3, Nek4, Gtf2f2, Cldn14) were identified in genomic divergence regions of E. rhadinum among China and Thailand populations. Our findings highlight the importance of demographic history factors shaping the geographical patterns of deleterious mutations. The results serve to deepen our understanding of the adaptive evolution and divergence of E. rhadinum with implications for other marine fish.