Genome-wide scan for selection signatures and genes related to heat tolerance in domestic chickens in the tropical and temperate regions in Asia

Abstract

Heat stress is one of the major environmental stressors challenging the global poultry industry. Identifying the genes responsible for heat tolerance is fundamentally important for direct breeding programs. To uncover the genetic basis underlying the ambient temperature adaptation of chickens, we analyzed a total of 59 whole genomes from indigenous chickens that inhabit South Asian tropical regions and temperate regions from Northern China. We applied F_ST and π-ratio to scan selective sweeps and identified 34 genes with a signature of positive selection in chickens from tropical regions. Several of these genes are functionally implicated in metabolism (FABP2, RAMP3, SUGCT, and TSHR) and vascular smooth muscle contractility (CAMK2), and they may be associated with adaptation to tropical regions. In particular, we found a missense mutation in thyroid-stimulating hormone receptor (41020238:G>A) that shows significant differences in allele frequency between the chicken populations of the two regions. To evaluate whether the missense mutation in TSHR could enhance the heat tolerance of chickens, we constructed segregated chicken populations and conducted heat stress experiments using homozygous mutations (AA) and wild-type (GG) chickens. We found that GG chickens exhibited significantly higher concentrations of alanine aminotransferase, lactate dehydrogenase, and creatine kinase than AA chickens under heat stress (35 ± 1°C) conditions (P < 0.05). These results suggest that TSHR (41020238:G>A) can facilitate heat tolerance and adaptation to higher ambient temperature conditions in tropical climates. Overall, our results provide potential candidate genes for molecular breeding of heat-tolerant chickens.

Keywords: TSHR; adaptation; chicken; genome sequencing; heat tolerance.

Figure 1

Geographic distribution, population relationships, and genetic diversity of chickens. (A) Geographic distribution of samples used in this study. (B) Population nucleotide diversity. (C) Principal component analysis. (D) ML tree constructed based on autosomal data.

Figure 2

The putative selected genomic regions in tropical populations were identified using both fixation statistics (F_ST) and π-ratio (Temperate/Tropical) approaches with a sliding window strategy (50-kb windows with 25-kb steps).

Figure 3

Allele frequency distribution of TSHR (41020238:G>A) in domestic chickens from temperate (10 breeds) and tropical regions (16 breeds).

Figure 4

Schematic representation of the thyroid stimulating hormone receptor (TSHR) and carboxypeptidase Z (CPZ) domain organization. LRR_5: leucine-rich repeat domain; 7tm_1: seven-(pass)-transmembrane domain receptors, also known as G protein-coupled receptors (GPCRs); Fz: cysteine-rich domain of CPZ; Peptidase_M14:peptidase M14-like domain of CPZ; M14-C_like: CPZ regulatory-like domain.