GWAS and Selective Sweep Analysis Reveal the Genetic Basis of Papilla Number in the Sea Cucumber (Apostichopus japonicus)

Sea cucumber (<i>Apostichopus japonicus</i>) is a commercially important mariculture species in northern China. Papilla number has been recognized as a key economic trait in sea cucumbers. Notably, significant variation in papilla count exists among different populations. The genetic mechanisms controlling papilla development are not fully understood. In this study, 72 individuals from six geographically distinct sea cucumber populations (Group N1) and 35 individuals from their offspring (Group N2) were analyzed using reduced-representation genome sequencing (RRGS) and whole-genome resequencing (WGS), respectively. Genome-wide association studies (GWAS) and selective sweep analysis were conducted to identify the biological pathways and genetic basis underlying variation in papilla number. The GWAS analysis identified two single-nucleotide polymorphism (SNP) loci on chromosomes 4 and 14 in the Group N1 that were significantly associated with papilla number. Within the vicinity of two SNPs, 48 genes were annotated as putative candidate genes, six of which have been reported to be associated with growth in <i>A. japonicus</i> or other aquatic animals. Selective sweep analysis identified 23 candidate genes in the JZ vs. YT within Group N1 and 39 candidate genes in the G1 vs. G3 within Group N2. Notably, functional enrichment analysis revealed that the Calcium signaling pathway was significantly enriched in both Group N1 and Group N2. This pathway has been demonstrated to regulate key cellular processes such as cell proliferation and differentiation through the activation of downstream signaling cascades. The intersection of results from parental Group N1 and progeny Group N2 yielded a total of six key biological pathways, including biological process, cellular process, cellular anatomical entity, cellular component, membrane, and binding. Collectively, our findings contribute to a deeper understanding of the genetic mechanisms underlying papilla number variation in <i>A. japonicus</i> and provide valuable insights for genomic selection in breeding programs.