Longitudinal genomic analyses of automatically-recorded vaginal temperature in lactating sows under heat stress conditions based on random regression models

Authors: WEN, HUI - Purdue University; Johnson, Jay; FREITAS, PEDRO H. - Purdue University; MASKAL, JACOB - Purdue University; GLORIA, LEONARDO - Purdue University; ARAUJO, ANDRE - Purdue University; PEDROSA, VICTOR - Purdue University; TIEZZI, FRANCESCO - University Of Florence; MALTECCA, CHRISTIAN - North Carolina State University; HUANG, YIJIAN - Smithfield Foods, Inc; SCHINCKEL, ALLAN - Purdue University; BRITO, LUIZ - Purdue University

Submitted to: Genetics Selection Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/12/2023
Publication Date: 12/21/2023
Citation: Wen, H., Johnson, J.S., Freitas, P.F., Maskal, J.M., Gloria, L.S., Araujo, A.C., Pedrosa, V.B., Tiezzi, F., Maltecca, C., Huang, Y., Schinckel, A.P., Brito, L.F. 2023. Longitudinal genomic analyses of automatically-recorded vaginal temperature in lactating sows under heat stress conditions based on random regression models. Genetics Selection Evolution. https://doi.org/10.1186/s12711-023-00868-1.
DOI: https://doi.org/10.1186/s12711-023-00868-1

Interpretive Summary: Heat stress has a well-described negative impact on swine production. Producers utilize several techniques to improve swine heat stress resilience including cooling technologies and nutritional additives with positive outcomes. However, genomic selection may represent an effective strategy to improve swine productivity under heat stress conditions. As such, the study objective was to estimate genomic-based genetic parameters for automatically collected vaginal temperature to identify genes that may be used to select heat stress tolerant sows. It was determined that automatically collected vaginal temperature may be a promising indicator trait for breeding and selecting sows with improved heat tolerance. Results from this study provide novel information that will allow for the breeding of more heat stress resilience pigs that have improved welfare under hot conditions.

Technical Abstract: Background: Heat stress (HS) causes major economic losses and compromises animal welfare in the worldwide swine industry. Automatically and continuously recording vaginal temperature (TV) based on wearable sensors causes minimal disruptions to animal behavior and generates data that can be used to evaluate temporal body temperature changes under HS conditions. However, there are no genomic studies assessing TV in lactating sows from a longitudinal perspective. In this study, we estimated genomic-based genetic parameters for automatically-recorded TV in lactating sows based on random regression models and identified genomic regions and candidate genes associated with the HS indicators derived from automatically-recorded TV in 1,645 lactating sows under HS conditions. Results: Heritability estimates of TV over time (0.143 - 0.203) and across environmental gradients (EGs; 0.089 - 0.183) had different curve patterns and heritability estimate ranges. The repeatability estimates of TV across time (0.566 - 0.655) and EGs (0.543 - 0.773) were similar and moderate-to-high. TV measured from 1200h to 1600h had moderate heritability (0.200) and high repeatability (0.642), indicating that this period might be the best time for recording TV for genetic selection purposes. Significant genotype-by-environment interactions existed in the current population under HS conditions. Moderate genetic correlation values between extreme EG pairs indicated potential re-ranking of selection candidates across EGs. Two genomic regions located on SSC10 (Sus scrofa chromosome 10; 59.370 - 59.998 Mb) and SSC16 (21.548 - 21.966 Mb) were identified in all analyses and the genes (CDC123, CAMK1d, SEC61A2, and NUDT5) harboring these regions are mainly associated with immunity, protein transport, and energy metabolism. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses for unique genes identified across time or climate stages were performed and each period had unique genes with specific biological functions, including regulation of the nervous system, metabolism, and hormone production. Conclusions: Our findings indicate that TV is a promising indicator trait for breeding and selecting individuals with improved heat tolerance due to its moderate heritability and high repeatability. Moderate genotype-by-environment interactions for TV exist indicate potential re-ranking of selection candidates across EGs. TV is a highly polygenic trait controlled by multiple genomic regions with small effects. Two genomic regions located on SSC10 (59.370 - 59.998 Mb) and SSC16 (21.548 - 21.966 Mb) were identified across all HS stages. We also identified special biological functions for each HS stage that are associated with TV in lactating sows. Genes associated with the immune system, nervous system, metabolism, and hormone regulation were significantly enriched, indicating that HS response is regulated by various physiological, cellular, and behavioral mechanisms.