30,000 maternal line pigs and phenotypic records from >45,000 sows and >90,000 litters. Second, we will evaluate the genetic architecture and usefulness of behavioral and physiological phenotypes. Finally, we will biologically validate genomic methods and traits to improve heat tolerance in lactating sows by collecting in-depth phenotypes in sows with divergent genomic breeding values (low vs high heat tolerance) under heat challenge. This proposal is expected to positively impact the welfare and performance of lactating sows and piglets thereby increasing the profitability of the global swine industry and improve food security.' />
Source: PURDUE UNIVERSITY submitted to NRP
IMPROVING THE WELFARE AND PRODUCTIVITY OF LACTATING SOWS DURING HEAT STRESS EVENTS THROUGH GENOMICS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
AFRI COMPETITIVE GRANT
Reporting Frequency
Annual
Accession No.
1021657
Grant No.
2020-67015-31575
Cumulative Award Amt.
$485,000.00
Proposal No.
2019-05551
Multistate No.
(N/A)
Project Start Date
Jun 1, 2020
Project End Date
May 31, 2023
Grant Year
2020
Program Code
[A1201]- Animal Health and Production and Animal Products: Animal Breeding, Genetics, and Genomics
Recipient Organization
PURDUE UNIVERSITY
(N/A)
WEST LAFAYETTE,IN 47907
Performing Department
Animal Sciences
Non Technical Summary
Breeding programs have improved the genetic potential of swine resulting in greater performance. However, performance improvements have been accompanied by a 55-70% increase in heat production for lactating sows and have reduced their ability to cope with high temperatures. Decreased heat tolerance negatively impacts the sow's ability to raise her litter and the effects of heat stress on animal agriculture are expected to worsen and result in more economic losses, especially as the number and severity of heat waves increase globally. Therefore, there is a critical need for researchers to develop new selection techniques and management practices to alleviate the negative effects of heat stress. The overall goal of this proposal is to identify novel traits and validate genomic selection methods to improve heat tolerance while improving lactating sow performance. To achieve this goal, we will first investigate the genomic background of the heat stress response and the predictive performance of genomic selection in lactating sows using genotypes from >30,000 maternal line pigs and phenotypic records from >45,000 sows and >90,000 litters. Second, we will evaluate the genetic architecture and usefulness of behavioral and physiological phenotypes. Finally, we will biologically validate genomic methods and traits to improve heat tolerance in lactating sows by collecting in-depth phenotypes in sows with divergent genomic breeding values (low vs high heat tolerance) under heat challenge. This proposal is expected to positively impact the welfare and performance of lactating sows and piglets thereby increasing the profitability of the global swine industry and improve food security.
Animal Health Component
30%
Research Effort Categories
Basic
70%
Applied
30%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3033599108060%
3153510102040%
Knowledge Area
303 - Genetic Improvement of Animals; 315 - Animal Welfare/Well-Being and Protection;

Subject Of Investigation
3510 - Swine, live animal; 3599 - Swine, general/other;

Field Of Science
1080 - Genetics; 1020 - Physiology;
Goals / Objectives
The success of genomic selection for improved heat tolerance in lactating sows depends on the availability of phenotypes that are heritable, can be measured on a large number of animals and that represent well the behavioral and physiological mechanisms of heat stress response in lactating sows. Defining the optimal phenotypes that can be collected at a cost-effective manner in a large number of animals is a priority for the swine industry in order to fully utilize genomic selection. Therefore, it is of utmost value to investigate the usefulness of phenotypes routinely measured in breeding and commercial pig herds and define novel indicator-traits that might better capture the genetic variability for heat tolerance in lactating sows. These traits and statistical models need to be biologically validated through comprehensive (in-depth) phenotyping of animals with divergent genetic merit for the traits identified.It is our central hypothesis that behavioral and physiological mechanisms associated with heat stress response in lactating sows is controlled, to some extent, by genetic components, and sufficient genetic variation exists to enable successful implementation of genomic selection to improve heat tolerance in lactating sows. The overall goal of this integrated proposal is to investigate and biologically validate genomic selection methods and identify novel traits to optimize selection for improving heat tolerance while maintaining or increasing productivity of lactating sows under heat stress conditions. The specific objectives are:Objective 1: To investigate the genomic background of heat stress response and the predictive performance of genomic selection in lactating sows, using large-scale data already available in breeding and commercial farms. As part of this objective, we will leverage existing data to investigate genetic parameters and predictive performance of genomic breeding values for indicator traits of heat tolerance in growing/finishing pigs (of maternal pig lines) and lactating sows based on growth traits and reproductive performance (both group of traits measured in all the animals). The genetic correlation between heat tolerance in growing/finishing animals and lactating sows of maternal pig lines (i.e. Landrace and Large White) will also be analyzed. In addition, we will investigate candidate genes with differential effects in ranging climatic levels (e.g. temperature and humidity) and associated metabolic pathways. This will provide a better understanding of the genetic background of heat stress response in lactating sows and will result in more cost-effective approaches to genetically improve heat tolerance in lactating sows. The activities within the next objectives (#2 and #3) will biologically validate these models through data collection of more in-depth phenotypes and comprehensive phenotyping of animals with divergent genetic merit for heat tolerance, identified based on these models.Objective 2: To evaluate the genetic architecture and potential usefulness for genomic selection of behavioral and physiological traits associated with heat stress response in lactating sows. We will collect novel phenotypes (various behavioral and physiological traits) on 1,000 lactating sows, over two summer periods, that are better indicators of heat stress response. Genetic parameters (including genetic correlation with the phenotypes from Objective #1), genomic predictions, genome-wide association studies and gene-set enrichment analysis will be performed. These phenotypes will be collected in pig breeding and commercial farms that have agreed to collaborate with us.Objective 3: To biologically validategenomic methods and novel traits to improve heat tolerance in lactating sows.A group of divergently selected animals (n = 32, defined based on power analyses and individuals selected based on genomic breeding values for heat tolerance) will be transported from North Carolina or Texas to the USDA-ARS state-of-the-art facilities (West Lafayette, IN) to measure heat production throughout the entire lactation, as well as various other production, reproduction, behavioral and physiological traits. This will serve as a validation of the genomic methods and traits proposed in the previous objectives (#1 and #2) and will enable the identification of alternative traits to be measured at a cost-effective manner in large-scale in breeding programs aiming to improve heat tolerance in lactating sows. In addition, it will greatly contribute to a better understanding of the impacts of selection of improved heat tolerance in the productive efficiency of lactating sows. The information generated (e.g. genetic parameters) will enable multi-trait selection for improved heat tolerance while maintaining or increasing productive and reproductive performance.Taken together, these objectives will enable us to make recommendations to the US pig industry on the optimal indicator traits and genomic selection approaches to improve heat tolerance in lactating sows. This will be based on the feasibility to collect the data in a large number of animals, the trait(s) heritability, biological mechanisms captured by the phenotype, and predictive performance of genomic selection. In summary, this proposal will provide a better understanding of the genetic background of behavioral and physiological mechanisms affecting heat stress responses in lactating sows and propose guidelines for the optimal implementation of genomic selection for heat tolerance in pigs.
Project Methods
THIS IS A SUBSTANTIALLY SUMMARIZED VERSION OF THE METHODOLOGY SECTION (DUE TO THE WORD LIMIT IN THE REEport PLATFORM).Objective 1:To investigate the genomic background and predictive performance of the lactating sow heat stress response, using large-scale datasets already available in breeding and commercial farms.As part of this objective, we will leverage large-scale existing data to investigate genetic parameters, candidate genes and metabolic pathways, and predictive performance of genomic breeding values for indicator traits of heat tolerance in lactating sows based on growth and reproductive performance. The datasets used in this step will be provided by two US large pig breeding companies withoperations in various US states. The records are from three main genetic groups:Landrace, Large White or crossbreed animals involving at least one of these two maternal line. There are currently records for >26,000 Landrace (> 51,000 litters) and >20,000 Large White (> 42,000 litters) sows.Genotypic data for >34,000 animals will be available for the analyses.The statistical models used for the analyses will be defined by testing all the environmental effects recorded that could be influencing the traits under analysis, using a backwards selection procedure. Variance components will be estimated using gibbs3f90 (Misztalet al.,2002).All the available phenotypes, genotypes and pedigree records will be used in the analyses. Heritability, genetic correlations and genomic breeding values will be estimated using random regression for sows' reaction norms to environmental stressors. Both single-trait and bivariate animal models (with all trait combinations) will be fitted. Genomic estimated breeding values for heat tolerance based on each variable will be estimated using the blup90iod2 software. Genomic prediction accuracy for each trait will be assessed by dividing the dataset in training and validation populations (e.g., Oliveiraet al.,2019).The random regression coefficients will be transformed in indexes for each heat load level. The program postGSf90 will be used to estimate the marker effects and relative proportion of genetic variance explained by each marker. Subsequently, wewill investigate candidate genes with differential effects in ranging THI levels and associated metabolic pathways.Objective 2: To evaluate the genetic architecture and potential usefulness for genomic selection of behavioral and physiological traits associated with heat stress response in lactating sows.Thermoregulatory and performance phenotypes will be collected on 1,000 lactating sows over two summer periods as indicators of the sow heat stress response. In this step, we will focus on data collection in a single breed (Large White), but will collect data on multiple parities (1-5). Thermoregulatory data collection will be performed over 4 subsequent days between the 10thand 21stday of lactation (period of highest sow metabolic heat production; Johnsonet al.,2019) four times daily (8:00 am, 12:00 pm, 4:00 pm, and 8:00 pm). Thermoregulatory measures will include skin temperature, vaginal temperature, and respiration rate.Performance measures will also be collected. All the data collected in the 1,000 sows will be used to estimate variance components, genetic parameters (heritability and genetic correlations), genomic predictions, GWAS and functional analyses for all the traits mentioned above. The genetic relationship between the indicator traits of heat tolerance described in Objectives #1 and #2 will also be assessed. All the calculations will be done as described before.Objective 3: Biologically validategenomic methods and novel traits to improve heat tolerance in lactating sows.A group of 32 sows with divergent genomic breeding values (GEBV) for heat tolerance (HT; n = 16) or heat sensitivity (HS; n = 16; based on the indicator traits from Objectives #1 and #2) will be comprehensively phenotyped during their whole lactation for various in-depth indicators of behavioral and physiological mechanisms of the heat stress response. Sows will be transported in 2 groups (n = 16 sows/group), 10 weeks apart, from the breeding farms located in North Carolina and Texas to the USDA-ARS Livestock Behavior Unit in West Lafayette, IN. Within each 16-sow group, 8 sows will be 2 weeks pre-farrowing and 8 sows will be 6 weeks pre-farrowing to allow for continuous testing in the USDA-ARS facilities. From 1 d prior to expected farrowing until weaning, all sows will be exposed to cyclic heat stress (HS) temperatures of 28 to 32°C. At 0800 h daily, ambient temperature will increase by 1°C each hour until 1200 h when 32°C will be achieved. This ambient temperature will be held constant for 4 h until 1600 h whereby it will be reduced gradually by 1°C each hour for 4 h until 2000 h where it will be held constant at 28°C overnight.Sows and their litters will be weighed on d 1, 10, and 21 post-farrowing and all sows will be providedad libitumaccess to water and feed throughout the entire trial. Sow feed intake will be monitored on d 4, 8, 14, and 18 of lactation. A back fat and loin eye measurement will be taken on all sows at d 1 post-farrowing, d 10 post-farrowing and d 21 post-farrowing to assess body condition.Future sow reproductive performance data will also be collected.Starting at 7 days prior to farrowing and then throughout the entire lactation period, vaginal temperatures will be recorded in all sows at 10 min intervals 24 hours/day using vaginal implants fitted with calibrated thermochron temperature recorders. In addition to vaginal temperatures, sow respiration rate and skin temperature will be monitored four times daily throughout the entire pre-farrowing (day -7 to day -1) and lactation periods (days 0 to 21 post-farrowing) at 0800, 1200, 1600, and 2000 hours.On d 4, 8, 14, and 18 of lactation, indirect calorimetry will be performed on all sows and their litters as well as on median weight piglets from the sentinel sow's litter as previously described in great detail (Johnsonet al.,2019).Total heat production will be measured at different days oflactation so as to characterize the temporal pattern of total heat production as lactation progressed in individual lactating sows. Total heat production will be determined for the sows and litters as well as the individual sows themselves as previously described (Johnsonet al.,2019).Observing changes in behavior can indicate if an animal is experiencing thermal discomfort (i.e., non-nutritive sow drinker manipulation as an indicator of motivation to dissipate heat).Therefore, in addition to thermoregulatory and performance measures, all sows and litters will be videotaped to record behavior using ceiling mounted cameras (Panasonic WV-CP254H, Matsushita Electrix Industrial CO. Ltd., Osaka, Japan) connected to a digital video recorder system. Sow behavior will be video-recorded upon placement into the farrowing stall (day -7), and then behavior of both the sow and her piglets will be recorded for 24-hour periods on days 0 (day of farrowing) to 3, 5, 7, 9, 13, and the day prior to weaning (day 20). Behaviors to be assessed will focus on those indicative of thermal comfort or distress of the sow and are described in an ethogram. All analyses will be performed using MIXED procedure in SAS® (version 9.4, SAS Institute Inc., Cary, NC). The definition of the most appropriate phenotypes to be used for genomic selection for heat tolerance is lactating sows will be based on: the feasibility to collect the data in a large number of animals, the trait(s) heritability, biological mechanisms captured by the phenotype, and predictive performance of genomic selection.

Progress 06/01/20 to 05/31/23

Outputs
Target Audience: This project had a broad target audience throughout its duration, including: 1. Animal scientists from the US and worldwide: despite the COVID19 pandemic, all the three objectives of the project were successfully completed on time. All the results obtained were already published or submitted for publication in open access journals. In addition, the results have been presented in national and international conferences, including the World Congress on genetics Applied to Livestock Production, National Swine Improvement Federation Annual Meeting, andthe Annual Meeting of the American Society of Animal Science, in various invited seminars at US and international universities (e.g., Iowa State University, Michigan State University, University of Florida, Federal University of Vicosa, Federal University of Bahia, University of San Agustin - Peru). The results were also presented at the Leman conference in Minesotta, which is a conference targetted at veterinarians. 2. Pig breeding companies: All the results obtained have been shared with US swine breeding companies and are being implemented in their genomic evaluations for heat tolerance of maternal line pigs. 3. Various undergraduate and graduate students from Purdue University and North Carolina State University have been trained on this project. The knowledge generated has also been incorporated in the classes taught at both Universities. 4. Pig farmers: the results obtained were presented in pig producer meetings such as the National Swine Improvement Federal, the Purdue Ag Week, and the MidwestSwine Meeting Day. 5. Other scientists: the resources generated through this project have also been leveraged for additional grant proposals and collaborations with researchers at the university of Nebraska-Linconl, University of Missouri, University of Nevada-Reno, and Federal University of Vicosa (Brazil). Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? As indicated in the personnel section, various undergraduate and graduate students and two postdocs were trained through this project. They were trained in the collection of physiological and behavioral indicators of heat stress and various genetic and genomic analyses of great importance to the field of animal breeding. All the results obtained have been written in scientific paper format and submitted for publication (or already published) to be shared with a broader community. The trainnees also had the opportunity to present the results of the project in national and international conferences. All the team also interacted with swine geneticists working in breeding companies, which was another great training opportunity. How have the results been disseminated to communities of interest? All the results obtained have been openly shared through journal publications, presentations in scientific and extension conferences of regional, national, and international scope and through invited lectures in other Universities delivered by the Principal Investigators. The team has also interacted with swine geneticists and veterinarians working in breeding companies and shared the results obtained. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? We have successfully completed all the activities proposed in this project. Various peer-reviewed papers have been published in open access journals, recently submitted for publication, and various conference proceedings have been presented as well. The results obtained are being implemented in swine breeding programs and the results have been presented in research and extension meetings. We have also developed two genetically-divergent populations that were used for the third objective of this project and will continue being used for subsequent research projects. A summary of the main findings obtained in the proposal are provided below: 1) Definition of environmental variables and critical periods to evaluate heat tolerance in pigs from maternal lines based on single-step genomic reaction norms: The definition of critical periods and climatic variables to be used as the environmental gradient in the reaction norm models is a key step for genetically evaluating heat tolerance (HT). Therefore, the main objectives of this study were to define the best critical periods and environmental descriptors (based on public weather station information) to evaluate HT and estimate variance components for HT in Large White pigs. Relative humidity (for BFT, MDP, NBD, WN, and WW) and maximum temperature (for OTW, TNB, NBA, IBF, and IWE) are the recommended environmental gradients based on the three analyzed criteria. The acute HS (average of 30 days before measurement date) is the critical period recommended for OTW, BFT, and MDP. For WN, WW, IBF, and IWE, a period ranging from 34 days prior to farrowing up to weaning is recommended. For TNB, NBA, and NBD, the critical period from 20 days prior to breeding up to 30 days into gestation is recommended. The average heritability estimates for HT (based on reaction norm slope) ranged from 0.04 (IBF) to 0.42 (BFT). The correlation values for WN, WW, IBF, and IWE indicate that these traits are largely affected by GxE interactions, while the remaining traits had moderate (OTW, TNB, and NBA) or weak (MDP, BFT, and NBD) GxE interactions. Re-ranking of individuals were observed for all traits, except MDP, BFT, and NBD. Additionally, a small re- ranking was observed for TNB. A largely comprehensive landscape of GxE interactions is provided in this study, and relevant recommendations of critical periods and climatic gradients were made for several traits in order to evaluate HS in maternal- line pigs. These observations demonstrate that HT in maternal-line pigs is heritable and genetic progress can be achieved through genetic and genomic selection. 2) Genomic parameters for automatically-measured vaginal temperature, respiration efficiency, and other thermotolerance indicators in maternal-line pigs measured in lactating sows under heat stress conditions: The main objectives of this study were to estimate genetic parameters for various HS indicators in a commercial population of Landrace x Large White lactating sows measured under HS conditions. The main indicators evaluated were: skin surface temperatures (SST), vaginal temperature (TV), respiration rate (RR), panting score (PS), body condition scores (BCS), hair density (HD), body size (BS), ear size, and respiration efficiency (Reff). Traits based on TV presented moderate heritability (from 0.15 to 0.29). Low heritability estimates were found for SST traits (from 0.04 to 0.06), RR (0.06), PS (0.05 ± 0.01), and Reff (0.03). Moderate to high heritability values were estimated for BCS (0.29 for caliper; and 0.25 for visual), HD (0.25), BS (0.33), ear area (EA; 0.40), and ear length (EL; 0.32). High genetic correlations were estimated among SST traits (> 0.78), and among TV traits (> 0.75). Similarly, high genetic correlations were also observed between RR and PS (0.87), BCS measures (0.92), and ear measures (0.95). These results indicate that overlapping sets of genes influence these traits. Low to moderate positive genetic correlations were observed between SST and TV (from 0.25 to 0.76). Low to moderate negative genetic correlation were observed between TV and BCS (from -0.27 to -0.55). Respiration efficiency was positive and moderately correlated with RR (0.36), PS (0.56), and BCS (0.56 and 0.50). All other traits combinations were lowly genetic correlated, suggesting that different sets of genes play a role in each trait. All traits evaluated are heritable, with different intensities, and genetic progress is possible for all of them. The results for the genetic correlations evidenced the complex relationship between these traits and confirms the importance of a thermotolerance subindex to select heat tolerant individuals. 3) Genomic analyses of longitudinal variability in automatically-recorded vaginal temperature in lactating sows under heat stress conditions: Vaginal temperature (TV) is a sensitive HS indicator and is able to lessen animal behaviors disruptions, allowing to obtain continuous records. However, very little is currently known about TV especially in lactating sows. In this study, we estimated genetic parameters for TV along time (measured each 10 min) and environment gradients (EGs) in lactating sows, and identified genetic regions associated with HS using the automatically collected TV in 1,645 lactating sows under HS conditions. Heritability estimates of TV along time (0.18 - 0.60) and EGs (0.08 - 0.18) had different curves and ranges. Time around 8:30 AM and from 18:00 PM until midnight showed high heritability and repeatability and could be the best times for TV data collection and selection purposes. Our study uncovered genetic parameters of TV and identified six novel overlapping genomic regions and unique functions of each HS stage that are associated with TV under HS conditions in lactating sows. Immunity, stress, metabolism, and hormone were enriched multiple times, which signify response to HS is complex and many resilience related pathways and functions activated. 4) Biological validation of heat tolerance: To biologically validate genomic methods and novel traits to improve heat tolerance in lactating sows. In the completion of this third objective, we biologically validated genomic methods and novel traits to improve heat tolerance in lactating sows. Sows were selected for heat stress tolerance and heat stress sensitivity based upon results and accomplishments described in objectives 1 and 2. A total of 20 gestating sows selected for divergent heat stress tolerance and 20 sows selected for divergent heat stress sensitivity were tested during lactation to evaluate their biological response to heat stress. Biological responses to heat stress sensitivity and tolerance included body temperature response, measures of milk production, and growth rate. Biological validation of the genomic method established that sows selected for heat stress tolerant had biological measures consistent with greater milk production under heat stress conditions whereas sows selected for heat stress sensitivity had biological measures consistent with decreased milk production under heat stress conditions. Despite this, core body temperature of heat stress sensitive and tolerant sows was similar, and this was likely driven by improved heat loss mechanisms employed by heat stress tolerant sows. The established improvements in both measures of milk production and thermoregulatory capacity for heat stress tolerant sows appears to demonstrate that heat stress tolerance could be genomically selected for while maintaining or improving measures of productivity. Results from this objective have positive implications towards improving both the welfare and productivity of pigs raised under heat stress conditions, which may improve the sustainability and profitability of pig production in a changing climate.

Publications

  • Type: Journal Articles Status: Published Year Published: 2023 Citation: 2) Johnson, J.S., Wen, H., Freitas, P.H., Maskal, J.M., Hartman, S.O., Byrd, M., Graham, J.R., Ceja, G., Tiezzi, F., Maltecca, C. and Huang, Y., 2023. Evaluating phenotypes associated with heat tolerance and identifying moderate and severe heat stress thresholds in lactating sows housed in mechanically or naturally ventilated barns during the summer under commercial conditions. Journal of Animal Science, 101, p.skad129. https://doi.org/10.1093/jas/skad129
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: 10) Freitas, P.H.F., J.S. Johnson, H. Wen, J.M. Maskal, M.K. Byrd, F. Tiezzi, Y. Huang, A.P. Schinckel, and Luiz F. Brito. 2022. Genome-wide association analyses for various thermotolerance indicators in maternal-line pigs. 2022 World Congress on Genetics Applied to Livestock Production (WCGALP). Rotterdam, Netherlands.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: 11) Wen, H., J.S. Johnson, P.H.F. Freitas, J.M. Maskal, M.K. Byrd, F. Tiezzi, Y. Huang, A.P. Schinckel, and Luiz F. Brito. 2022. Genetic parameter estimation of various body temperature and respiration rate indicators in maternal-line pigs under heat stress conditions. 2022 World Congress on Genetics Applied to Livestock Production (WCGALP). Rotterdam, Netherlands.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: 17) C. Maltecca, F. Tiezzi, J. Johnson, L. Brito. Elucidating The Biology of Sow Tolerance to Heat Stress. PAG 2022, San Diego, CA, USA.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: rito, L. F. & Johnson, J. S. 2022. Improving climatic resilience in pigs through physiological genomics. ASAS Midwest. Omaha, NE, USA.
  • Type: Journal Articles Status: Published Year Published: 2023 Citation: Freitas, P.H.F., Johnson, J.S., Wen, H. et al. Genetic parameters for automatically-measured vaginal temperature, respiration efficiency, and other thermotolerance indicators measured on lactating sows under heat stress conditions. Genet Sel Evol 55, 65 (2023). https://doi.org/10.1186/s12711-023-00842-x
  • Type: Journal Articles Status: Under Review Year Published: 2023 Citation: Hui Wen, Jay S. Johnson, Pedro H. F. Freitas, Jacob M. Maskal, Leonardo S. Gloria, Andre C. Araujo, Victor B. Pedrosa, Francesco Tiezzi, Christian Maltecca, Yijian Huang, Allan P. Schinckel, Luiz F. Brito. Longitudinal genomic analyses of automatically-recorded vaginal temperature in lactating sows under heat stress conditions based on random regression models. Genetics Selection and Evolutions Journal - Under Review
  • Type: Conference Papers and Presentations Status: Published Year Published: 2023 Citation: Hui Wen, Jay. S. Johnson, Leonardo S. Gloria, Jacob M. Maskal, Andre C. Araujo, Felipe E. de Carvalho, Artur Oliveira Rocha, Yijian Huang, Luiz F. Brito. Definition and genetic parameters estimation for climatic resilience indicators derived from longitudinal vaginal temperature records in lactating sows under heat stress conditions. Journal of Animal Science. ASAS annual meeting
  • Type: Conference Papers and Presentations Status: Published Year Published: 2023 Citation: Sharlene Hartman, Jay S. Johnson, Victor B. Pedrosa, Allan P. Schinckel, Jeremy N. Marchant, Leonardo S. Gloria, and Luiz F. Brito. Genomic-based genetic parameters of behavioral ethogram traits in lactating sows under heat stress conditions and their relationship with direct indicators of heat tolerance. Journal of Animal Science. ASAS annual meeting.
  • Type: Journal Articles Status: Submitted Year Published: 2023 Citation: Pedro Henrique F. Freitas, Jay S. Johnson, Francesco Tiezzi, Yijian Huang, Allan P. Schinckel, Luiz F. Brito. Genomic predictions and GWAS for heat tolerance in pigs based on reaction norm models with performance records and data from public weather stations considering alternative temperature gradient. Journal of Animal Breeding and Genetics. Under Review
  • Type: Conference Papers and Presentations Status: Published Year Published: 2023 Citation: Johnson, J.S. 2023. Improving swine heat stress resilience in a changing climate. Michigan State University. September 12, 2023.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2023 Citation: Byrd, M.K., L. Brito, H. Wen, P. Frietas, S. Hartman, J. Maskal, Y. Huang, F. Tiezzi, C. Maltecca, A.P. Schinckel, and J.S. Johnson. 2023. Evaluating indirect measures of milk production in heat stressed lactating sows genomically selected for improved thermotolerance. J. Anim. Sci. Accepted.


Progress 06/01/21 to 05/31/22

Outputs
Target Audience:1. Animal scientists from the US and worldwide: The first and second objectives of the project has been fully completed (as planned) and all the experiments of the third and last objective have been completed as well (we are at the data analyses stage). All the results have either been published already in open access journals, submitted for publication, or in preparation stage. In addition, the results have been presented in national and international conferences, including the World Congress on genetics Applied to Livestock Production and the Annual Meeting of the American Society of Animal Science. 2. Pig breeding companies: All the results obtained have been shared with US swine breeding companies and will be implemented in their genomic evaluations for heat tolerance of maternal line pigs. 3. Undergraduate and graduate students from Purdue University and North Carolina State University have been trained on this project. The knowledge generated is also being incorporated in the classes taught at both Universities. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?As indicated in the personnel section, various undergraduate and graduate students and one postdoc were trained through this project. They were trained in the collection of physiological and behavioral indicators of heat stress and various genetic and genomic analyses of great importance to the field of animal breeding. All the results obtained are being written in scientific paper format to be (or have already been) shared with a broader community. The trainnees also had the opportunity to present the results of the project in national and international conferences.All the team also interacted with swine geneticists working in breeding companies, which was another great training opportunity. How have the results been disseminated to communities of interest?All the results obtained are being openly shared through journal publications, presentations in scientific and extension conferences of regional, national, and international scope and through invited lectures in other Universities delivered by the Principal Investigators. The team has also interacted with swine geneticists working in breeding companies and shared the results obtained. What do you plan to do during the next reporting period to accomplish the goals?In the next (and last) reporting period, we will complete to analyse the datasets from Objective #3 of the project, and complete and submit journal publications with theremaining results of the project. We will also prepare a detailed final report of the project.

Impacts
What was accomplished under these goals? We have already completed all the activities proposed for Objectives #1 and #2, as planned, and all the experiments with live animals from Objective #3 have been finalized too. Various peer-reviewed papers have been published in open access journals, recently submitted for publication, and various conference proceedings have been presented as well, including two 4-page manuscripts at the World Congress on Genetics Applied to Livestock Production. A summary of the main findings obtained in the current reporting yearis provided below: 1) Definition of environmental variables and critical periods to evaluate heat tolerance in pigs from maternal lines based on single-step genomic reaction norms: The definition of critical periods and climatic variables to be used as the environmental gradient in the reaction norm models is a key step for genetically evaluating heat tolerance (HT). Therefore, the main objectives of this study were to define the best critical periods and environmental descriptors (based on public weather station information) to evaluate HT and estimate variance components for HT in Large White pigs. The traits included in this study were: ultrasound backfat thickness (BFT; mm), ultrasound muscle depth (MDP; mm), piglet weaning weight (WW; kg), off-test weight (OTW; kg; measured at approximately 5.5 months of age), interval between farrowing (IBF; days), total number of piglets born (TNB), number of piglets born alive (NBA), number of piglets born dead (NBD), number of piglets weaned (WN), and weaning to estrus interval (IWE; days). The number of phenotypic records ranged from 6,059 (WN) to 172,984 (TNB), and genotypes were available for 8,686 animals. Seven climatic variables (maximum, minimum, and average temperatures; average relative humidity; dew point; discomfort index; and temperature-humidity index) were compared. Relative humidity (for BFT, MDP, NBD, WN, and WW) and maximum temperature (for OTW, TNB, NBA, IBF, and IWE) are the recommended environmental gradients based on the three analyzed criteria. The acute HS (average of 30 days before measurement date) is the critical period recommended for OTW, BFT, and MDP. For WN, WW, IBF, and IWE, a period ranging from 34 days prior to farrowing up to weaning is recommended. For TNB, NBA, and NBD, the critical period from 20 days prior to breeding up to 30 days into gestation is recommended. The average heritability estimates for HT (based on reaction norm slope) ranged from 0.04 (IBF) to 0.42 (BFT). The correlation values for WN, WW, IBF, and IWE indicate that these traits are largely affected by GxE interactions, while the remaining traits had moderate (OTW, TNB, and NBA) or weak (MDP, BFT, and NBD) GxE interactions. Re-ranking of individuals were observed for all traits, except MDP, BFT, and NBD. Additionally, a small re-ranking was observed for TNB. A largely comprehensive landscape of GxE interactions is provided in this study, and relevant recommendations of critical periods and climatic gradients were made for several traits in order to evaluate HS in maternal-line pigs. These observations demonstrate that HT in maternal-line pigs is heritable and genetic progress can be achieved through genetic and genomic selection. 2) Genomic parameters for automatically-measured vaginal temperature, respiration efficiency, and other thermotolerance indicators in maternal-line pigs measured in lactating sows under heat stress conditions: The main objectives of this study were to estimate genetic parameters for various HS indicators in a commercial population of Landrace x Large White lactating sows measured under HS conditions. The main indicators evaluated were: skin surface temperatures (SST), vaginal temperature (TV), respiration rate (RR), panting score (PS), body condition scores (BCS), hair density (HD), body size (BS), ear size, and respiration efficiency (Reff). Traits based on TV presented moderate heritability (from 0.15 to 0.29). Low heritability estimates were found for SST traits (from 0.04 to 0.06), RR (0.06), PS (0.05 ± 0.01), and Reff (0.03). Moderate to high heritability values were estimated for BCS (0.29 for caliper; and 0.25 for visual), HD (0.25), BS (0.33), ear area (EA; 0.40), and ear length (EL; 0.32). High genetic correlations were estimated among SST traits (> 0.78), and among TV traits (> 0.75). Similarly, high genetic correlations were also observed between RR and PS (0.87), BCS measures (0.92), and ear measures (0.95). These results indicate that overlapping sets of genes influence these traits. Low to moderate positive genetic correlations were observed between SST and TV (from 0.25to 0.76). Low to moderate negative genetic correlation were observed between TV and BCS (from -0.27 to -0.55). Respiration efficiency was positive and moderately correlated with RR (0.36), PS (0.56), and BCS (0.56 and 0.50). All other traits combinations were lowly genetic correlated, suggesting that different sets of genes play a role in each trait. All traits evaluated are heritable, with different intensities, and genetic progress is possible for all of them. The results for the genetic correlations evidenced the complex relationship between these traits and confirms the importance of a thermotolerance subindex to select heat tolerant individuals. 3) Genomic analyses of longitudinal variability in automatically-recorded vaginal temperature in lactating sows under heat stress conditions: Vaginal temperature (TV) is a sensitive HS indicator and is able to lessen animal behaviors disruptions, allowing to obtain continuous records. However, very little is currently known about TV especially in lactating sows. In this study, we estimated genetic parameters for TV along time (measured each 10 min) and environment gradients (EGs) in lactating sows, and identified genetic regions associated with HS using the automatically collected TV in 1,645 lactating sows under HS conditions. Heritability estimates of TV along time (0.18 - 0.60) and EGs (0.08 - 0.18) had different curves and ranges. Time around 8:30 AM and from 18:00 PM until midnight showed high heritability and repeatability and could be the best times for TV data collection and selection purposes.GXE is not significant in current population under HS conditions. However, the moderate genetic correlations between extreme EGs indicated that lactating sows could have different performance. Compared to other variance components, more variation was observed in the additive genetic variance of TV along time, whereas more variation was observed in the permanent environmental variance of TV along climate. Six genomic regions were identified in all analyses and the genes within these regions were mainly involved in immunity, energy metabolism, stress, and disease. Our study uncovered genetic parameters of TV and identified six novel overlapping genomic regions and unique functions of each HS stage that are associated with TV under HS conditions in lactating sows. Immunity, stress, metabolism, and hormone were enriched multiple times, which signify response to HS is complex and many resilience related pathways and functions activated. 4) Genome-wide association analyses for various thermotolerance indicators measured during lactation in maternal-line pigs: This study aimed to perform GWAS for six indicators of thermotolerance in lactating sows to identify genomic regions and candidate genes influencing these traits in commercial Landrace x Large White sows during lactation stage under heat stress conditions. Sixteen genomic regions were identified on chromosomes 1, 2, 3, 5, 6, 7, 8, 10, 12, 13, 14, and 16, with ten of these genomic regions related with known QTL associated with health and production traits. These findings highlight the importance of thermoregulation indicators on the performance and well-being of pigs, and consequently adding such traits to the current selection indexes.

Publications

  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Freitas, P. H. F., J. J. Johnson, S. Y. Chen, H. R. Oliveira, F. Tiezzi, S. F. Lazaro, Y. Huang, Y. Gu, A. Schinckel, and L. F. Brito. 2021. Definition of environmental variables and critical periods to evaluate heat tolerance in pigs from maternal lines based on single-step genomic reaction norms. Frontiers in Genetics. 23. https://doi.org/10.3389/fgene.2021.717409
  • Type: Journal Articles Status: Published Year Published: 2021 Citation: Chen, S. Y., P. H. F. Freitas, H. R. Oliveira, S. F. L�zaro, Y. J. Huang, J. T. Howard, Y. Gu, A. P. Schinckel, and L. F. Brito. 2021. Genotype-by-environment interactions for reproduction, body composition, and growth traits in maternal-line pigs based on single-step genomic reaction norms. Genetics Selection Evolution 53, 51. https://doi.org/10.1186/s12711-021-00645-y
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Tiezzi, F., L. F. Brito, J. Howard, Y. Huang, K. Gray, C. Schwab, J. Fix, and C. Maltecca. 2020. Genomics of heat tolerance in reproductive performance investigated in four independent maternal lines of pigs. Frontiers in Genetics, 11, 629. https://doi.org/10.3389/fgene.2020.00629
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Brito, L. F., H. R. Oliveira, B. R. McConn, A. P. Schinckel, A. Arrazola, J. Marchant-Forde, and J. S. Johnson. 2020. Large-scale Phenotyping of Livestock Welfare in Commercial Production Systems: A New Frontier in Animal Breeding. Frontiers in Genetics, 11, 793. https://doi.org/10.3389/fgene.2020.00793
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: Freitas, P.H.F., J.S. Johnson, H. Wen, J.M. Maskal, M.K. Byrd, F. Tiezzi, Y. Huang, A.P. Schinckel, and Luiz F. Brito. 2022. Genome-wide association analyses for various thermotolerance indicators in maternal-line pigs. 2022 World Congress on Genetics Applied to Livestock Production (WCGALP). Rotterdam, Netherlands.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: Wen, H., J.S. Johnson, P.H.F. Freitas, J.M. Maskal, M.K. Byrd, F. Tiezzi, Y. Huang, A.P. Schinckel, and Luiz F. Brito. 2022. Genetic parameter estimation of various body temperature and respiration rate indicators in maternal-line pigs under heat stress conditions. 2022 World Congress on Genetics Applied to Livestock Production (WCGALP). Rotterdam, Netherlands.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: Cleaver, K. N., B. A. Hill, J. S. Johnson, and L. F. Brito. 2021. Relationships Between Heat Stress and Behavioral Responses with Reproductive Traits of Maternal-line Gilts. Journal of Animal Science, 99, 148-148.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: Freitas, P.H.F., Johnson, J.S., Chen, S.Y., L�zaro, S.F., Huang, Y., Gu, Y., Schinckel, A.P., Tiezzi, F. and Brito, L.F., 2021. PSIV-5 Definition of environmental variables and critical periods to evaluate heat tolerance in maternal-line pigs based on single-step genomic reaction norms. Journal of Animal Science, 99(Supplement_3), 297-298.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2021 Citation: Cleaver, K. N., J. S. Johnson, B. A. Hill, and L. F. Brito. Relationships between heat stress and behavioral responses with reproductive traits of maternal-line gilts. 2021 Midwest Animal Science Meeting.
  • Type: Conference Papers and Presentations Status: Published Year Published: 2022 Citation: Brito, L.F. and Johnson, J. S. 2022. Improving climatic resilience in pigs through physiological genomics. Annual Meeting of the American Society of Animal Science  Midwest Section. Omaha, NE.


Progress 06/01/20 to 05/31/21

Outputs
Target Audience:1. Animal Scientists from the US and worldwide: The first objective of the project has been completed (as planned) and two manuscripts were prepared and submitted to the Journals (Genetic Selection and Evolution and Frontiers In Genetics). In addition, the results have been presented in two national conferences. 2. Pig breeding companies: Our first results have been shared with US swine breeding companies and will be implemented in their genomic evaluations for heat tolerance of maternal line pigs. 3. Undergraduate and graduate students from Purdue University and North Carolina State University have been trained on this project. The knowledge generated is also being incorporated in the classes taught at both Universities. Changes/Problems:There were no changes or problems with Objetive #1. For objective #2, we were not able to travel to the farms in North Carolina for data collection due to the COVID pandemic, as visitors were not allowed to enter the swine facilities or even travel out of state. However, we are planning to collect all the data this year (Summer/2021). We have a larger team and will start the data collection in the Jacksonville area (North Carolina) by June 1, 2021. There are no other changes so far and all the activities are being completed successfully. What opportunities for training and professional development has the project provided?The postdocs and undergraduate and graduate students involved in this project were trained in various genetic and genomic analyses of great importance to the field of animal breeding. The results were also written in scientific paper format to be shared with the broader community. All the team also interacted with swine geneticists working in breeding companies, which was another great training opportunity. How have the results been disseminated to communities of interest?The results have been disseminated through scientific publications, conference presentations, and direct interactions with industry stakeholders (e.g. swine geneticists working in breeidng companies). What do you plan to do during the next reporting period to accomplish the goals?For the next reporting period, we will finalize the publications from Objective #1 and complete the research planned for Objective #2. For instance, we will start the data collection of >1,000 sows for various behavioral and physiological indicators of heat stress in farms located in North Carolina, perform the genetic and genomic analyses, and we will select the genetically divergent animals for the experiments described in Objective #3.

Impacts
What was accomplished under these goals? During this first year of the project, we have completed the Objective #1. All the analyses were performed as described in the project. The results of this first objective have generated three scientific publications (Under review in the Journal Genetics Selection and Evolution and in the Journal Frontiers in Genetics; the third one is under review by the authors and will be submitted soon). A summary of the main findings is provided below: 1) Definition of environmental variables and critical periods to evaluate heat tolerance in pigs from maternal lines based on single-step genomic reaction norms: Heat stress (HS) is a major welfare and economic issue in the swine industry, especially as adverse climatic events become more common. Therefore, there is an urgent need to genetically improve animal climatic resilience. However, properly quantifying environmental HS is still a major challenge in livestock breeding programs. The definition of critical periods and climatic variables to be used as the environmental gradient in the reaction norm models is a key step for genetically evaluating heat tolerance (HT). Therefore, the main objectives of this study were to define the best critical periods and environmental descriptors (based on public weather station information) to evaluate HT and estimate variance components for HT in Large White pigs. The traits included in this study were: ultrasound backfat thickness (BFT; mm), ultrasound muscle depth (MDP; mm), piglet weaning weight (WW; kg), off-test weight (OTW; kg; measured at approximately 5.5 months of age), interval between farrowing (IBF; days), total number of piglets born (TNB), number of piglets born alive (NBA), number of piglets born dead (NBD), number of piglets weaned (WN), and weaning to estrus interval (IWE; days). The number of phenotypic records ranged from 6,059 (WN) to 172,984 (TNB), and genotypes were available for 8,686 animals. Seven climatic variables (maximum, minimum, and average temperatures; average relative humidity; dew point; discomfort index; and temperature-humidity index) were compared based on three criteria including the: 1) strongest GxE estimate as measured by the slope term, 2) variable yielding the highest theoretical accuracy of the genomic estimated breeding values (GEBV), and 3) variable yielding the highest distribution of GEBV per environmental value. Relative humidity (for BFT, MDP, NBD, WN, and WW) and maximum temperature (for OTW, TNB, NBA, IBF, and IWE) are the recommended environmental gradients based on the three analyzed criteria. The acute HS (average of 30 days before measurement date) is the critical period recommended for OTW, BFT, and MDP. For WN, WW, IBF, and IWE, a period ranging from 34 days prior to farrowing up to weaning is recommended. For TNB, NBA, and NBD, the critical period from 20 days prior to breeding up to 30 days into gestation is recommended. The average heritability estimates for HT (based on reaction norm slope) ranged from 0.04 (IBF) to 0.42 (BFT). The lowest genetic correlations between divergent environmental gradients were observed for WN (-0.27) and WW (-0.11). The correlation values for WN, WW, IBF, and IWE indicate that these traits are largely affected by genotype-by-environment (GxE) interactions, while the remaining traits had moderate (OTW, TNB, and NBA) or weak (MDP, BFT, and NBD) GxE interactions. Re-ranking of individuals were observed for all traits, except MDP, BFT, and NBD. Additionally, a small re-ranking was observed for TNB. A largely comprehensive landscape of GxE interactions is provided in this study, and relevant recommendations of critical periods and climatic gradients were made for several traits in order to evaluate HS in maternal-line pigs. These observations demonstrate that HT in maternal-line pigs is heritable and genetic progress can be achieved through genetic and genomic selection. 2) Genotype-by-environment interaction for reproduction, body composition, and growth traits in maternal-line pigs based on single-step genomic reaction norms:There is an increasing need for fitting genotype-by-environment (G×E) interactions in livestock breeding programs to improve productivity and animal welfare across different environmental and management conditions. This is even more relevant in pig breeding due to a focus on intensive breeding in nucleus farms and the global extension of commercial populations raised in more challenging environments. In this study, we used single-step homoscedastic and heteroscedastic genomic reaction norm models (RNMs) to evaluate G×E interactions in Large White pigs for reproduction (total number of piglets born, TNB; total number of piglets born alive, NBA; total number of piglets weaned, NW), growth (weaning weight, WW; off-test weight, OW), and body composition (ultrasound muscle depth, MD; ultrasound backfat thickness, BF) traits. Genotype information, including genomic markers located on the X chromosome, was obtained for 8,686 animals. Genomic-based genetic parameters and single-step genome-wide association studies (ssGWAS) were performed for all traits. The average performance of contemporary groups (CGs) was estimated and used as environmental gradient in the reaction norm analyses. We found that the need for considering heterogeneous residual variance in RNM was trait dependent. According to the estimated variance components of the RNM slope and genetic correlations across environmental gradients, there is clear G×E interactions for TNB and NBA, but of smaller magnitude for WW and absent for NW, OW, MD, and BF. On the basis of the explained genetic variances of moving genomic windows in ssGWAS, various relevant genomic regions associated with the RNM slope were observed for TNB, NBA, and WW, indicating the underlying biological mechanisms of environmental sensitivity. Dozens of novel candidate genes and genomic regions were identified for the studied traits. In particular, our results provided strong evidence regarding the biological contribution of the X chromosome to litter size traits in pigs, even based on a simplistic modelling approach. We provided a comprehensive landscape of G×E interaction in maternal line pigs by analyzing various economically relevant traits. Important genomic regions and candidate genes associated with reproductive performance were identified in various autosomes and on the X chromosome. Our findings will contribute to more accurately calculating genomic breeding values considering G×E, in order to genetically improve environmental robustness in maternal line pigs.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2021 Citation: Chen S.Y., P.H.F. Freitas, H.R. Oliveira, S.F. L�zaro, Y.J. Huang, J.T. Howard, Y. Gu, A.P. Schinckel, L.F. Brito. (2021) Genotype-by-environment interaction for reproduction, body composition, and growth traits in maternal-line pigs based on single-step genomic reaction norms. Genetics Selection and Evolution. Under review (second round of revisions).
  • Type: Journal Articles Status: Submitted Year Published: 2021 Citation: Freitas, P.H.F., Johnson, J.S., Chen, S., Oliveira, H.R., Tiezzi, F., L�zaro, S.F., Huang, Y., Gu, Y., Schinckel, A.P., Brito, L.F. (2021) Definition of environmental variables and critical periods to evaluate heat tolerance in pigs from maternal lines based on single-step genomic reaction norms. Frontiers in Genetics (Submitted).
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Brito LF, Oliveira HR, McConn BR, Schinckel AP, Arrazola A, Marchant-Forde JN and Johnson JS (2020) Large-Scale Phenotyping of Livestock Welfare in Commercial Production Systems: A New Frontier in Animal Breeding. Front. Genet. 11:793. doi: 10.3389/fgene.2020.00793
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2021 Citation: Freitas, P.H.F., Johnson, J.S., Chen, S., Oliveira, H.R., Tiezzi, F., L�zaro, S.F., Huang, Y., Gu, Y., Schinckel, A.P., Brito, L.F. (2021) Definition of environmental variables and critical periods to evaluate heat tolerance in pigs from maternal lines based on single-step genomic reaction norms. In: Annual Meeting of the American Society of Animal Sciences (ASAS), July, 2021.