Abstract
Selection for cold tolerance in chickens is important for improving production performance and animal welfare. The identification of chicken breeds with higher cold tolerance and production performance will help to target candidates for the selection. The thyroid gland plays important roles in thermal adaptation, and its function is influenced by breed differences and transcriptional plasticity, both of which remain largely unknown in the chicken thyroid transcriptome. In this study, we subjected Bashang Long-tail (BS) and Rhode Island Red (RIR) chickens to either cold or warm environments for 21 weeks and investigated egg production performance, body weight changes, serum thyroid hormone concentrations, and thyroid gland transcriptome profiles. RIR chickens had higher egg production than BS chickens under warm conditions, but BS chickens produced more eggs than RIRs under cold conditions. Furthermore, BS chickens showed stable body weight gain under cold conditions while RIRs did not. These results suggested that BS breed is a preferable candidate for cold-tolerance selection and that the cold adaptability of RIRs should be improved in the future. BS chickens had higher serum thyroid hormone concentrations than RIRs under both environments. RNA-Seq generated 344.3 million paired-end reads from 16 sequencing libraries, and about 90% of the processed reads were concordantly mapped to the chicken reference genome. Differential expression analysis identified 46–1,211 genes in the respective comparisons. With regard to breed differences in the thyroid transcriptome, BS chickens showed higher cell replication and development, and immune response-related activity, while RIR chickens showed higher carbohydrate and protein metabolism activity. The cold environment reduced breed differences in the thyroid transcriptome compared with the warm environment. Transcriptional plasticity analysis revealed different adaptive responses in BS and RIR chickens to cope with the cold, and showed higher responsiveness in BS compared with RIR chickens, suggesting greater adaptability of the thyroid in BS chickens. Moreover, 10,053 differential splicing events were revealed among the groups, with RNA splicing and processing, gene expression, transport, and metabolism being the main affected biological processes, identifying a valuable alternative splicing repertoire for the chicken thyroid. A short isoform of TPO (encoding thyroid peroxidase) containing multiple open reading frames was generated in both breeds by skipping exons 4 and 5 in the cold environment. These findings provide novel clues for future studies of the molecular mechanisms underlying cold adaptation and/or acclimation in chickens.
Highlights
Cold stress is one of the most prominent environmental challenges for homeothermic animals, with potentially negative effects on their reproduction, health, wellbeing, and feed efficiency [1,2,3]
The egg production performance from 18–39 weeks was higher in Rhode Island Red (RIR) compared with Bashang Long-tail (BS) birds in the warm environment (130.7 vs. 91.1 eggs/bird, p < 1.0×10−7), while BS birds produced more eggs than RIR birds in the cold environment (70.5 vs. 57.7 eggs/bird, p = 5.2×10−4)
These results suggest better cold tolerance of BS chickens, which are preferred for selection for cold tolerance
Summary
Cold stress is one of the most prominent environmental challenges for homeothermic animals, with potentially negative effects on their reproduction, health, wellbeing, and feed efficiency [1,2,3]. Consumer demand for high-quality food from animals is coupled with an increasing emphasis on animal welfare [4], and free-range production systems are becoming more widespread, potentially subjecting the animals to more frequent and serious cold stress. Homeothermic animals protect themselves from the cold by increasing heat production and decreasing heat loss via a variety of physiological changes in multiple organs and systems [5]. Thyroid size and activity were shown to increase in birds acclimated to low temperatures [15,16,17]. These findings suggest important roles for the thyroid in cold acclimation and/or adaptation
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