Giant pandas in captivity undergo short-term adaptation in nerve-related pathways

Abstract

Behaviors in captive animals, including changes in appetite, activity level, and social interaction, are often seen as adaptive responses. However, these behaviors may become progressively maladaptive, leading to stress, anxiety, depression, and other negative reactions in animals. In this study, we investigated the whole-genome sequencing data of 39 giant panda individuals, including 11 in captivity and 28 in the wild. To eliminate the mountain range effect and focus on the factor of captivity only, we first performed a principal component analysis. We then enumerated the 21,474,180 combinations of wild giant pandas (11 chosen from 28) and calculated their distances from the 11 captive individuals. The 11 wild individuals with the closest distances were used for the subsequent analysis. The linkage disequilibrium (LD) patterns demonstrated that the population was almost eliminated. We identified 505 robust selected genomic regions harboring at least one SNP, and the absolute frequency difference was greater than 0.6 between the two populations. GO analysis revealed that genes in these regions were mainly involved in nerve-related pathways. Furthermore, we identified 22 GO terms for which the selection strength significantly differed between the two populations, and there were 10 nerve-related pathways among them. Genes in the differentially abundant regions were involved in nerve-related pathways, indicating that giant pandas in captivity underwent minor genomic selection. Additionally, we investigated the relationship between genetic variation and chromatin conformation structures. We found that nucleotide diversity (θπ) in the captive population was correlated with chromatin conformation structures, which included A/B compartments, topologically associated domains (TADs) and TAD-cliques. For each GO term, we then compared the expression level of genes regulated by the above four factors (AB index, TAD intactness, TAD clique and PEI) with the corresponding genomic background. The retained 10 GO terms were all coordinately regulated by the four factors, and three of them were associated with nerve-related pathways. This study revealed that giant pandas in captivity undergo short-term adaptation in nerve-related pathways. Furthermore, it provides new insights into the molecular mechanism of gene expression regulation under short-term adaptation to environmental change.