Multi-tissue metabolic and transcriptomic responses to a short-term heat stress in swine.

BACKGROUND: Heat stress (HS) is an increasing threat for pig production with a wide range of impacts. When submitted to high temperatures, pigs will use a variety of strategies to alleviate the effect of HS. While systemic adaptations are well known, tissue-specific changes remain poorly understood. In this study, thirty-two pigs were submitted to a 5-day HS at 32 °C. RESULTS: Transcriptomic and metabolomic analyses were performed on several tissues. The results revealed differentially expressed genes and metabolites in different tissues. Specifically, 481, 1774, 71, 1572, 17, 164, and 169 genes were differentially expressed in muscle, adipose tissue, liver, blood, thyroid, pituitary, and adrenal glands, respectively. Regulatory glands (pituitary, thyroid, and adrenal) had a lower number of regulated genes, perhaps indicating an earlier sensitivity to HS. In addition, 7, 8, 2, and 8 metabolites were differentially produced in muscle, liver, plasma, and urine, respectively. The study also focused on the oxidative stress pathway in muscle and liver by performing a correlation analysis between genes and metabolites. CONCLUSIONS: This study has identified various adaptation mechanisms in swine that enable them to cope with heat stress (HS). These mechanisms include a global decrease in energetic metabolism, as well as changes in metabolic precursors that are linked with protein and lipid catabolism and anabolism. Notably, the adaptation mechanisms differ significantly between regulatory (pituitary, thyroid and adrenal glands) and effector tissues (muscle, adipose tissue, liver and blood). Our findings provide new insights into the comprehension of HS adaptation mechanisms in swine.

Comparative analysis of whole blood transcriptomics between European and local Caribbean pigs in response to feed restriction in a tropical climate.

BACKGROUND: Feed restriction occurs frequently during pig growth, either due to economic reasons or stressful environmental conditions. Local breeds are suggested to have better tolerance to periods of feed restriction. However, the mechanisms underlying the response to feed restriction in different breeds is largely unknown. The aims of the present study were (1) to compare the blood transcriptome profile in response to feed restriction and refeeding of two contrasted breeds, Large White (LW), which has been selected for high performance, and Creole (CR), which is adapted to tropical conditions, and (2) to investigate the effect of a moderate feed restriction and refeeding on whole blood transcriptome. Analysis of blood transcriptome allows to study the response to feed restriction and refeeding in a dynamic way. RNAseq was performed on blood samples of growing LW and CR pigs at two time points: after 3 weeks of feed restriction and after 3 weeks of refeeding. The data was compared with samples from control animals offered the same diet on an ad libitum basis throughout the whole experiment. RESULTS: In terms of performance (body weight and feed efficiency), CR pigs were less impacted by feed restriction than LW. The transcriptional response to feed restriction and refeeding between CR and LW was contrasted both in terms of number of DEGs and enriched pathways. CR demonstrated a stronger transcriptional response to feed restriction whereas LW had a stronger response to refeeding. Differences in the transcriptional response to feed restriction between CR and LW were related to cell stress response (Aldosterone Signalling, Protein ubiquitination, Unfolded Protein Signalling) whereas after refeeding, differences were linked to thermogenesis, metabolic pathways and cell proliferation (p38 MAPK, ERK/MAPK pathway). In both breeds, transcriptional changes related to the immune response were found after restriction and refeeding. CONCLUSIONS: Altogether, the present study indicates that blood transcriptomics can be a useful tool to study differential genetic response to feed restriction in a dynamic way. The results indicate a differential response of blood gene expression to feed restriction and refeeding between breeds, affecting biological pathways that are in accordance with performance and thermoregulatory results.

Soil ingestion, a key determinant of exposure to environmental contaminants. The case study of chlordecone exposure in free-range pigs in the French West Indies.

Ingested soil may expose free-range animals to environmental pollutants. In pigs, soil ingestion is few described whereas their burrowing behaviour suggests that it could be high. Although highly productive pigs are generally reared indoor, free-range farming is increasing in view of ethical considerations for animal welfare and is a common practice for subsistence agriculture systems. The experiment lasted 8 weeks (2 for adaptation, 6 for measurements) with 24 growing pigs of Guadeloupean Creole (CR) or Large White (LW) breeds. Pigs were assigned to 3 outdoor treatments: high pasture HP (>60 days of regrowth), low pasture LP (35 days of regrowth), and sweet potato SP (sweet potato field). Titanium (soil marker) and chromium (faecal output marker) contents of faeces, vegetation and soil samples were used to estimate individual daily soil ingestions. The average, 10th and 90th percentiles were 440, 200 and 726 g of dry soil per 100 kg body weight, respectively, without significant differences between the 3 outdoor treatments or the 2 breeds but with a significant period (i.e. week of measurements) × treatment interaction (P < 0.001). In the French West Indies, animals may be exposed to chlordecone (CLD), a very persistent organochlorine insecticide. Simulations of CLD tissue contamination due to ingestion of contaminated soil were carried out and compared to the maximum residue limit. These results show that grazing management needs to be adapted to effectively limit soil ingestion by pigs and the impact of a contaminated environment on the sustainability of pig systems.

Plasticity of feeding behaviour traits in response to production environment (temperate vs. tropical) in group-housed growing pigs.

Heat stress affects pig metabolism, health and welfare, resulting in reduced growth and important economic losses. The present experiment aimed to evaluate the effects of two climatic environments [temperate (TEMP) vs. tropical humid (TROP)] on feeding behaviour in growing pigs. The feeding behaviour traits were measured with automated feeders and included: daily feed intake, daily eating time, feeding rate, daily number of meals, feed intake per meal, and feeding time per meal. Pigs came from a backcross population between Large White (LW, heat sensitive) and Creole (CR, heat tolerant) pigs. The same 10 F1 LW × CR boars (sire families [SF]) were mated with related LW sows in each environment. Feeding behaviour was recorded for a total of 1,296 pigs (n = 634 pigs for TEMP and n = 662 pigs for TROP) between 11 and 23 weeks of age. Growth performance and thermoregulatory responses (rectal and skin temperatures) were also measured. Results show that TROP conditions affect feeding behaviour traits: animals had more meals per day but these meals were smaller both in duration and in size, resulting in lower daily feed intake and less time eating per day. Significant SF by environment (GxE) interactions were found for all feeding behaviour traits. When SF were distributed into robust and sensitive groups (previously defined according to performance and thermoregulatory traits), results showed group by environment interactions for all feeding traits, except meal frequency. Moreover, a significant difference in feeding rate between robust and sensitive group was detected in TEMP, suggesting that feeding rate may be a good candidate to evaluate heat tolerance.

The Genetics of Thermoregulation in Pigs: A Review.

Heat stress (HS) affects pig performance, health and welfare, resulting in a financial burden to the pig industry. Pigs have a limited number of functional sweat glands and their thermoregulatory mechanisms used to maintain body temperature, are challenged by HS to maintain body temperature. The genetic selection of genotypes tolerant to HS is a promising long-term (adaptation) option that could be combined with other measures at the production system level. This review summarizes the current knowledge on the genetics of thermoregulation in pigs. It also discusses the different phenotypes that can be used in genetic studies, as well as the variability in thermoregulation between pig breeds and the inheritance of traits related to thermoregulation. This review also considers on-going challenges to face for improving heat tolerance in pigs.

Agroecological practices to support tropical livestock farming systems: a Caribbean and Latin American perspective.

With global climate changes currently occurring, and particularly given the severe energy and food shortages occurring throughout tropical regions, agroecological (AE) systems are drawing renewed attention as an efficient alternative to intensive models of production, particularly unsuitable in regions of the world such as the Caribbean or Latin America. There is a pressing need to focus on livestock farming systems (LFS) and characterize their potential contributions to global sustainability. A multidisciplinary approach is needed to address these multiple and complex problems. Traditionally, LFS have shown their sustainability high potential. The purpose of this work is to highlight solutions to minimize inputs, by describing some success and diverse case studies through the Caribbean. These systems were analyzed at different levels: animal/function, farm/family, and territory/society. This produced a set of guidelines that help to increase the efficiency of tropical systems, particularly those concerned with (1) choosing the best-suited genotypes, while enhancing population biodiversity; (2) matching the farming system to the available resources, feed, and by-products; (3) steering the whole farming system through reproduction management with no hormonal treatment, while facilitating system reproducibility and increasing performances; (4) controlling health constraints instead of annihilating risks and implement an integrated management design to reduce chemical treatments or increase the use of nutraceuticals; and (5) mitigating climate constraints by using soft techniques. In the second part of this work, some integrated systems are described. The Tosoly farm of Colombia, for instance, is conceived as a totally integrated crop-livestock system, allowing the additional production of energy at the farm level. Thus, it epitomizes the positive impact that livestock can exert upon the environment. The case study of Haiti indicates how AE practices can help in designing a pro-poor sustainable milk production system. It concerns an entire dairy sector built all over the country on the basis of micro-units of milk production and processing.

Effect of chronic and acute heat challenges on fecal microbiota composition, production, and thermoregulation traits in growing pigs1,2.

The present study aimed at investigating the impact of heat challenges on gut microbiota composition in growing pigs and its relationship with pigs' performance and thermoregulation responses. From a total of 10 F1 sire families, 558 and 564 backcross Large White × Créole pigs were raised and phenotyped from 11 to 23 wk of age in temperate (TEMP) and in tropical (TROP) climates, respectively. In TEMP, all pigs were subjected to an acute heat challenge (3 wk at 29 °C) from 23 to 26 wk of age. Feces samples were collected at 23 wk of age both in TEMP and TROP climate (TEMP23 and TROP23 samples, respectively) and at 26 wk of age in TEMP climate (TEMP26 samples) for 16S rRNA analyses of fecal microbiota composition. The fecal microbiota composition significantly differed between the 3 environments. Using a generalized linear model on microbiota composition, 182 operational taxonomic units (OTU) and 2 pathways were differentially abundant between TEMP23 and TEMP26, and 1,296 OTU and 20 pathways between TEMP23 and TROP23. Using fecal samples collected at 23 wk of age, pigs raised under the 2 climates were discriminated with 36 OTU using a sparse partial least square discriminant analysis that had a mean classification error-rate of 1.7%. In contrast, pigs in TEMP before the acute heat challenge could be discriminated from the pigs in TEMP after the heat challenge with 32 OTU and 9.3% error rate. The microbiota can be used as biomarker of heat stress exposition. Microbiota composition revealed that pigs were separated into 2 enterotypes. The enterotypes were represented in both climates. Whatever the climate, animals belonging to the Turicibacter-Sarcina-Clostridium sensu stricto dominated enterotype were 3.3 kg heavier (P < 0.05) at 11 wk of age than those belonging to the Lactobacillus-dominated enterotype. This latter enterotype was related to a 0.3 °C lower skin temperature (P < 0.05) at 23 wk of age. Following the acute heat challenge in TEMP, this enterotype had a less-stable rectal temperature (0.34 vs. 0.25 °C variation between weeks 23 and 24, P < 0.05) without affecting growth performance (P > 0.05). Instability of the enterotypes was observed in 34% of the pigs, switching from an enterotype to another between 23 and 26 wk of age after heat stress. Despite a lower microbial diversity, the Turicibacter-Sarcina-Clostridium sensu stricto dominated enterotype was better adapted to heat stress conditions with lower thermoregulation variations.

Genotype by environment interactions for performance and thermoregulation responses in growing pigs1,2.

Heat stress affects pig health, welfare, and production, and thus the economic viability of the pig sector in many countries. Breeding for heat tolerance is a complex issue, increasingly important due to climate change and the development of pig production in tropical areas. Characterizing genetic determinism of heat tolerance would help building selection schemes dedicated to high performance in tropical areas. The main objective of our study was to estimate the genetic parameters for production and thermoregulation traits in two highly related growing pig populations reared in temperate (TEMP) or tropical humid (TROP) environment. Pigs came from a backcross population between Large White (LW, heat sensitive) and Creole (CR, heat tolerant) pigs. Phenotypic data were obtained on a total of 1,297 pigs using the same procedures in both environments, for body weight (BW, at weeks 11 and 23), daily feed intake (ADFI), backfat thickness (BFT, at weeks 19 and 23), cutaneous temperature (CT, at weeks 19 and 23), and rectal temperature (RT, at weeks 19, 21, and 23). Feed conversion ratio (FCR) and residual feed intake (RFI) were computed for the whole test period (11 to 23 wk). Criteria comparing the fits to the data revealed genotype × environment (G × E) interactions for most traits but not for FCR. The variance components were obtained using two different methods, a restricted maximum likelihood method and a Bayesian Markov chain Monte Carlo method, considering that traits are either similar or different in each environment. Regardless of the method, heritability estimates for production traits were moderate to high, except for FCR (lower than 0.18). Heritability estimates for RT were low to moderate, ranging from 0.04 to 0.34. The genetic correlations of each trait between environments generally differed from 1, except for FCR and ADG. For most thermoregulation traits, they also did not differ significantly from zero, suggesting that the main genetic bases of heat tolerance may vary in different environment. Within environments, the unfavorable genetic correlations between production traits and RT suggest an antagonism between the ability to maintain inner temperature and the ability to increase ADFI and ADG. However, greater RT were also associated to leaner pigs and better feed efficiency. Nevertheless, due to large inaccuracies of these estimations, larger cohorts would be needed to decide about the best breeding schemes to choose for tropical pig production.

Effect of feed restriction and refeeding on performance and metabolism of European and Caribbean growing pigs in a tropical climate.

Reduction in feed intake is a common physiological response of growing pigs facing stressful environmental conditions. The present experiment aims to study (1) the effects of a short-term feed restriction and refeeding on pig performance and metabolism and (2) the differential response between two breeds, Large White (LW), which has been selected for high performance, and Creole (CR), which is adapted to tropical conditions. A trial of 36 castrated male pigs (18 LW and 18 CR) was carried out. For each breed, half of the animals were restrictively fed at 50% of the standard feed allowance for 6 days and then fed normally for the next 14 days. Growth performance, thermoregulatory responses, plasma hormones and metabolites were measured. Results showed that, for all traits, the difference in response between the two breeds was small and rarely significant, which may be due to the short duration of the feed restriction. Irrespective of breed, feed restriction induced a reduction of growth rate and feed efficiency that was rapidly compensated for upon refeeding. Feed restriction also reduced skin temperature, rectal temperature and respiratory rate, as well as blood urea and cholesterol, which are of interest as potential biomarkers for feed restriction.

1HNMR-Based metabolomic profiling method to develop plasma biomarkers for sensitivity to chronic heat stress in growing pigs.

The negative impact of heat stress (HS) on the production performances in pig faming is of particular concern. Novel diagnostic methods are needed to predict the robustness of pigs to HS. Our study aimed to assess the reliability of blood metabolome to predict the sensitivity to chronic HS of 10 F1 (Large White × Creole) sire families (SF) reared in temperate (TEMP) and in tropical (TROP) regions (n = 56±5 offsprings/region/SF). Live body weight (BW) and rectal temperature (RT) were recorded at 23 weeks of age. Average daily feed intake (AFDI) and average daily gain were calculated from weeks 11 to 23 of age, together with feed conversion ratio. Plasma blood metabolome profiles were obtained by Nuclear Magnetic Resonance spectroscopy (1HNMR) from blood samples collected at week 23 in TEMP. The sensitivity to hot climatic conditions of each SF was estimated by computing a composite index of sensitivity (Isens) derived from a linear combination of t statistics applied to familial BW, ADFI and RT in TEMP and TROP climates. A model of prediction of sensitivity was established with sparse Partial Least Square Discriminant Analysis (sPLS-DA) between the two most robust SF (n = 102) and the two most sensitive ones (n = 121) using individual metabolomic profiles measured in TEMP. The sPLS-DA selected 29 buckets that enabled 78% of prediction accuracy by cross-validation. On the basis of this training, we predicted the proportion of sensitive pigs within the 6 remaining families (n = 337). This proportion was defined as the predicted membership of families to the sensitive category. The positive correlation between this proportion and Isens (r = 0.97, P < 0.01) suggests that plasma metabolome can be used to predict the sensitivity of pigs to hot climate.

Effect of heat stress on blood rheology in different pigs breeds.

The main objectives of the present work were to test the effects of heat stress on blood rheology and to determine whether the responses can change according to the pig breeds. Thirty-six pigs from three pig's lines (n = 12 for each line) with assumed different tolerance to heat stress were compared: Large White (LW, little tolerance), Creole (CR, good tolerance) and LW × CR pigs (produced from a cross between LW and CR lines). In a first period, all pigs were exposed to a 9-d period of thermo-neutral environment (24°C; d-9 to d-1; P0). At the end of P0, six pigs from each line were slaughtered (n = 18). Then in a second period, the remaining pigs (6/breed; n = 18) were exposed to a 5-d period of heat stress (32°C; d + 1 -d + 5; P1) and thereafter slaughtered at d + 5. Rectal and skin temperatures, as well as respiratory rate, were recorded on d-1 and d + 5. At slaughter, blood was sampled for hematological and hemorheological measurements. Heat stress caused a rise of the skin temperature and respiratory rate without any changes in the rectal temperature or on the hematological and hemorheological parameters when all pigs' lines were considered. We observed a pig line effect on blood viscosity at high shear rate (375 s-1) and red blood cell deformability at 30 Pa with CR pigs having lower blood viscosity and higher red blood cell deformability than LW pigs. While the changes of blood viscosity under heat stress did not reach statistical significance in LW and CR lines, blood viscosity (at 375 s-1) increased above the temperate values in the LW × CR line. Red blood cell deformability at 30 Pa was higher in CR pigs exposed to heat stress compared to LW pigs in the same condition. In conclusion, thermal loading caused physiological stress but did not widely change the hematological and hemorheological profiles. Although some blood rheological parameters seem to vary with the pig breeds, the responses to heat stress are very similar.

Integrating banana and ruminant production in the French West Indies.

Using a mechanistic model, we compared five alternative farming systems with the purpose of transforming monoculture (MON) banana farms into mixed farming systems (MFS) with ruminants feeding banana by-products (leaves, pseudostems and nonmarketable fruits) and forage from the fallow land. The paper presents the main structure of the model (land surface changes, available biomass for animals, stocking rates, productive or reproductive indicators), and impact assessment (change in farm productivity) is discussed. Five MFS with typical local ruminant production systems were used to compare MON to the strategies using forage from fallow and/or integrating Creole cattle (CC), Creole goats (CG) or Martinik sheep (MS) into banana farming. One hectare MON shifted into an MFS allows a stocking rate of 1,184, 285, and 418 kg of live weight per hectare for CC, CG and MS, respectively. Banana by-products seem to be better valorized by the CC scenario. However, parameters such as length of the cycle, local prices for cattle, goat and sheep meat, work time and farmer's skills in ruminant management may have been taken into account by the farmer when choosing the ruminant species to rear.

Effect of heat challenge on peripheral blood mononuclear cell viability: comparison of a tropical and temperate pig breed.

We evaluated the effect of heat challenge on cell viability, concanavalin A-induced proliferation and heat shock protein (HSPs) mRNA expression in peripheral mononuclear blood cells (PBMC) isolated from Creole (CR) and Large White (LW) pigs. The PBMCs were cultured for 9 h at 37 °C before being subjected to heat challenge: (1) at 42 °C or 45 °C for 2, 4, 6 and 9 h to monitor cell viability;(2) at 45 °C for 2 and 9 h followed by stimulation for 24 h at 37 °C with concanavalin A to evaluate mitogen-induced proliferation; and (3) at 45 °C for 3, 6 and 9 h to measure induction of HSP70.2 and HSP90 mRNA. Cell viability was affected by breed and temperature (P < 0.01), and the viability decrease caused by heat challenge was greater for LW than CR pigs. For mitogen-stimulated PBMCs, incubation at 45 °C reduced lymphoblastogenesis equally in both breeds (P < 0.01). Although heat challenge for 3 and 6 h at 45°C induced expression of HSP70.2 and HSP90 mRNA, no breed difference was observed. In conclusion, differences in heat resistance between these two breeds at the whole organism level are reflected at the cellular level. Neither HSP70.2 nor HSP90 mRNA expression levels explain this effect.