Genomic Analyses for Selective Signatures and Genes Involved in Hot Adaptation Among Indigenous Chickens From Different Tropical Climate Regions

Abstract

Climate change, especially weather extremes like extreme cold or extreme hot, is a major challenge for global livestock. One of the animal breeding goals for sustainable livestock production should be to breed animals with excellent climate adaptability. Indigenous livestock and poultry are well adapted to the local climate, and they are good resources to study the genetic footprints and mechanism of the resilience to weather extremes. In order to identify selection signatures and genes that might be involved in hot adaptation in indigenous chickens from different tropical climates, we conducted a genomic analysis of 65 indigenous chickens that inhabit different climates. Several important unique positively selected genes (PSGs) were identified for each local chicken group by the cross-population extended haplotype homozygosity (XP-EHH). These PSGs, verified by composite likelihood ratio, genetic differentiation index, nucleotide diversity, Tajima's D, and decorrelated composite of multiple signals, are related to nerve regulation, vascular function, immune function, lipid metabolism, kidney development, and function, which are involved in thermoregulation and hot adaptation. However, one common PSG was detected for all three tropical groups of chickens via XP-EHH but was not confirmed by other five types of selective sweep analyses. These results suggest that the hot adaptability of indigenous chickens from different tropical climate regions has evolved in parallel by taking different pathways with different sets of genes. The results from our study have provided reasonable explanations and insights for the rapid adaptation of chickens to diverse tropical climates and provide practical values for poultry breeding.

Keywords: hot adaptation; indigenous chicken; parallelism; selection signature; tropical climate.

FIGURE 1

Population structure and relationships of tropical chickens. (A) geographic variation of monthly mean surface temperature for the location of chickens used in the study. (B) neighbor-joining tree. (C) principal component analysis (PCA) with the first (PC1) and second (PC2) principal components. (D) genetic structure of all chicken groups using ADMIXTURE program with K = 2 and K = 3. Indonesian chickens (ID), Indian chickens (IN), Saudi Arabian chickens (SA), and chickens of northern China (NCN).

FIGURE 2

Selection Sweeps analysis. (A) XP-EHH analysis (ID chickens to NCN chickens). (B) XP-EHH analysis (IN chickens to NCN chickens). (C) XP-EHH analysis (SA chickens to NCN chickens). (D) XP-EHH analysis (ID.IN.SA chickens to NCN chickens). Sliding window analyses with 40-kb window and 20-kb increment, using 99th percentile cutoff.

FIGURE 3

Selective signatures and haplotype analysis in CYP19A1 gene identified by Indonesian chickens. (A) the CYP19A1 gene is additionally validated by CLR, Fst, π, Tajima’s D, and DCMS. (B) haplotype analysis at the CYP19A1 gene. Gallus gallus spadiceus from China and Thailand (RJF), Chantecler chickens (CA), Tibetan chicken (TB), chickens of southern China (SCN), commercial chickens (C), Iranian chickens (IR), and Ethiopian chickens (ET).

FIGURE 4

A putative selective sweep region associated with hot tolerance in Indian chickens. (A) five sweep statistics plotted over a 280-Kb region on chromosome 9 detected by Indian chickens. From top to bottom, the vertical axis shows the values of CLR, Fst, π, Tajima’s D, and DCMS. (B) the degree of haplotype sharing around the region. (C) allele frequency of the mutant MINDY4B loci. Blue, orange, and gray represented homozygous mutant, heterozygous mutant, and homozygous wild type, respectively.

FIGURE 5

Genomic candidate regions with high selection signals in Saudi Arabian chickens. (A) CLR, Fst, π, Tajima’s D, and DCMS analysis of a 40-Kb region on chromosome 7 identified by Saudi Arabian chickens. (B) haplotype sharing in the region. (C) allele frequency of the mutant OSGEPL1 loci. The meaning of different colors is the same as that in Figure 4.

FIGURE 6

Genomic candidate gene detected XP-EHH analyses of four chicken groups. (A) venn diagram showing the PSGs overlap among XP-EHH_ID-to-NCN, XP-EHH_IN-to-NCN, XP-EHH_SA-to-NCN, and XP-EHH_{ID.IN.SA-to-NCN}. (B) CLR, Fst, π, Tajima’s D, and DCMS analysis of TGFB3 identified by XP-EHH analyses of four chicken groups.