Pigs and Humans: 10,000 Years of Interaction

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Click here to sign up. Submission Websites List. For the academic login, please select your organization on the next page. You will be redirected to verify your credentials. Corresponding Author Max F. Significant progress on pig genetics and genomics research has been witnessed in recent years due to the integration of advanced molecular biology techniques, bioinformatics and computational biology, and the collaborative efforts of researchers in the swine genomics community.

Progress on expanding the linkage map has slowed down, but the efforts have created a higher-resolution physical map integrating the clone map and BAC end sequence. Additionally, expression studies using high-throughput microarrays and other gene expression techniques have made significant advancements. The number of identified non-coding RNAs is rapidly increasing and their exact regulatory functions are being explored. A publishable draft build 10 of the swine genome sequence was available for the pig genomics community by the end of December Build 9 of the porcine genome is currently available with Ensembl annotation; manual annotation is ongoing.

A recent community-wide effort to create a 60K porcine SNP chip has greatly facilitated whole-genome association analyses, haplotype block construction and linkage disequilibrium mapping, which can contribute to whole-genome selection. These recent technological advances and where they may lead are reviewed. Archaeological evidence from figurines and bones revealed that the domestication of the pig Sus scrofa occurred as early as 9, years ago in the Middle East, and some evidence indicated the domestication of the pig could date back even earlier in China [Department of Animal Science Oklahoma State University, ; Clutton-Brock, ].

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After transformation of pigs from hunted wild animals to fully managed domestic ones, relationships between humans and pigs became closer, yet more diverse and complex [Albarella et al. Humans have developed a variety of pig breeds for meat production and a source of fat during the co-evolution of both species.

Enormous progress has been made for swine breeding with the utilization of classic genetics and quantitative genetics approaches. Many studies identified candidate genes and quantitative trait loci QTL significantly associated with economically important traits and some of them have been utilized in the commercial pig industry [Rothschild et al. It is predicted that even more progress can be achieved after pig genomics information is better understood and then integrated into marker-assisted selection.

Coordinated efforts to better understand the pig genome were initiated in the early s with gene identification and mapping efforts. The annotated build 9 of the porcine genome was made available in September The publishable build 10 was completed by the end of December with Ensembl annotation to come a few months later. At the same time, significant progress has been made on gene expression using high-throughput arrays and functional studies of the pig genome [Tuggle et al. Swine genome science has come of age and the advances in swine genomics promise to greatly benefit the pig industry and consumers in the future.

The steps to expand the linkage map have slowed down in recent years, partially due to the advances in the genome sequencing project and high-density porcine SNP chip development. Instead, efforts have moved to developing the pig-human comparative map and integrating the linkage, physical and cytogenetic maps.

Driven by the pig genome sequencing project, a new human-pig comparative map mainly consisting of ESTs and BAC-end sequences was constructed as a first step towards sequencing the pig genome [Meyers et al. A large-scale porcine BAC physical map was furthermore developed and used for the selection of BACs to construct a minimal tiling path for genome sequencing and targeted gap filling [Rogatcheva et al.

Eventually, an updated physical map integrating the clone map and BAC end sequence data was reported [Humphray et al. As one of the principal and most accurate mapping techniques, FISH is still being used for porcine gene mapping in a few studies. An advanced 12,rad RH map was also developed, and it allows for even greater precision for mapping within and across species [Yerle et al.

The utilization of these valuable tools has led to the rapid increase in the number of genes mapped to pig chromosomes during the last decade. For pork production to be cost-effective, it requires an efficient growth rate, a low feed-to-gain ratio, high levels of reproductive success and survivability and increased pig health.

Consumers are also looking for pork products with good carcass merit and high meat quality. Using pig resource families founded by commercial and exotic pig breeds, researchers have identified quantitative trait loci QTL affecting these traits. A large number of QTL have been reported on nearly all chromosomes for growth, carcass and meat quality traits and several chromosomes for reproduction and feet and leg structure. The QTL affecting immune response and disease resistance traits are far less numerous, but this is an area where gene expression studies are particularly valuable.

Some valuable lessons learned from recent QTL mapping studies include: 1 Many traits result from a complex interaction of several different factors. A QTL study that focuses on a single phenotype measurement may result in an incomplete understanding of the multitude of factors that combine to produce the trait of interest.

Instead, a systematic study of factors that may contribute to the analyzed trait can help illustrate the underlying causes of a specific phenotype with better accuracy. For example, ovulation rate, follicle-stimulating hormone levels, uterine length, feed intake and environmental factors may likely add value to QTL affecting litter size. Due to funding limitations, sample sizes are frequently smaller than ideal. By combining the data from multiple QTL studies, possible experimental limitations can be corrected while increasing the power for detecting real QTL [Kim et al.

Development of new approaches will also improve multi-factorial and complex trait analysis for QTL [Rothschild et al. With the identification of a large number of pig SNPs and the application of high-throughput genotyping platforms, fine mapping within specific QTL areas is being carried out.

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On SSC2, fine mapping and haplotype analyses confirmed that the CAST gene was one of the important candidate genes influencing meat quality [Meyers et al. Fine mapping was also performed on SSC8 to identify 2 candidate genes responsible for ovulation rate [Campbell et al. Due to the availability of the newly developed high-density 60K porcine SNP chip, large-scale association studies are discovering many new QTL. The study of pig eQTL, which measures and treats each observation of gene expression from a microarray as a new trait, shows promise for traits with a strong environmental influence on gene expression.

A simulation study on selective transcriptional profiling and data analysis strategies for eQTL mapping in outbred pig populations was conducted, which suggested a strategy for future eQTL mapping analyses [Cardoso et al. The discovery of imprinted QTL provides an opportunity to further understand the genetic control of traits of interest in pigs. Linkage disequilibrium LD plays a vital role in QTL mapping, so genotyping of high-density SNPs in genes or chromosomal regions of interest is an essential prerequisite to discover the LD structure within a region. This information allows causative mutations, LD blocks and selective sweeps in a population to be discovered.

For example, as evidence that LD levels can be low even within a single gene, an absence of LD was observed between 2 mutations ArgHis and AspAsn in the MC4R gene, and both mutations were significantly associated with fatness and growth traits [Fan et al. Hence, high-density SNPs may give further clues about causative mutations in certain genes. Similarly, large-scale SNP analyses need to be validated in different populations and breeds due to the variability in some gene sequences and LD levels among different breeds.

For instance, studies of the sequence variation of 3 different genes showed no evidence of reduction in genetic variability among different pig breeds for FABP4 and IGF2 genes, but a significant reduction in genetic variability for FABP5 in different breeds [Ojeda et al. Chromosome-wise LD analyses showed a difference in LD among different commercial pig breeds, as well as in European and Chinese indigenous pig breeds [Du et al. The LD blocks were extended up to kb for European breeds and only 10 kb for Chinese breeds. The average extent of LD in the pig was a bit higher than in humans, which ranged from 10—30 kb.

Candidate gene analyses have been employed to investigate a variety of economic traits. The commercial pig industry is actively using many of these gene markers in combination with traditional performance information to improve production by marker-assisted selection MAS. While the traits listed above have received most of the attention, many traits of economic importance to the swine industry have been greatly overlooked. As QTL studies have become more prevalent, there is more interest in trying to determine QTL for non-traditional traits.

For example, recent studies using a high-throughput genotyping technique revealed that the genes CCR7 and CPT1A were associated with sow longevity traits [Mote et al.

Pigs Communicate With Humans in New Experiment - National Geographic

With the rapid advances of the porcine genome sequence and other related projects, a tremendous amount of data is being generated every day. Thus, large databases to store this information and make it publicly available are becoming more essential, as are online resources that enable analysis of this new data. Information is shown in table 1 about the online database resources beneficial for the pig genomics community. In recent years, a number of studies have been carried out to profile expression of the pig genome. There are over porcine cDNA libraries which have each contributed more than 1, sequences to UniGene.

These libraries came from almost 50 categories of different tissues, such as muscle, brain, intestine, ovary, blood and embryonic tissue. Overall, data on pig gene expression is being produced at a rapid rate. The combination of expression data and the completed genome sequence will certainly contribute to the better understanding of the physiological complexity of the pig transcriptome and uncover genes and gene pathways that control traits of economic importance.

Many studies have shown that the differences that exist in the porcine transcriptome are dependent upon breed and developmental stage, among other factors, so there is much left to learn through expression studies. Microarray studies in particular have been used extensively to determine the biological basis for such traits as reproduction, muscle development, feed intake and host response to infection in pigs [Tuggle et al. The array is a 20,element oligonucleotide microarray with probes designed based on comparison of pig ESTs to known vertebrate proteins.

Affymetrix also sells a 23,probe porcine microarray. Another technique for expression profiling is SAGE, which is a sequencing-based method. The sequenced SAGE tags are a digital representation of cellular gene expression and have been used to identify genes differentially expressed at various stages of development. Successful examples using SAGE profiling for 2 critical embryo development stages and 3 skeletal development stages in 2 pig breeds have been reported [Blomberg and Zuelke, ; Tang et al.

ChIP-chip technology received its name because it determines the results from chromatin immunoprecipitation through use of a microarray. The approach responses Approaches yes or not , latency to approach, percentage of time inside the apparatus and in contact with the trough to trained and ambiguous cues were recorded and analysed.

Whereas training sessions were performed without the handler, CBT were performed with or without the presence of a human observer i. Unfamiliar humans men or women wore blue or green coveralls and were stockmen from the piggery who were not involved in the management of piglets from the present project. In addition, they never participated to a CBT more than once for a same piglet to ensure that they were really unfamiliar for piglets.

The observer was outside but close to the testing arena so piglets could see the top part of his body and his face. He remained motionless with his arms along the body and gazed at piglets. Piglets received twice each ambiguous cue with and without the observer presence i. CBT sessions in which piglets immediately failed trained cues and did not receive any ambiguous cues were removed from the subsequent analyses since it was considered that piglets were not enough concentrated or motivated during these sessions.

The last trained cue P or N , played before ambiguous cues, was balanced between trials since it can influence the interpretation of the ambiguous cue. Up to three ambiguous trials were played within one CBT session. If piglets did more than two errors on learnt cues, the CBT session ended. Thus, a maximum number of 11 trials were performed per CBT session. The SAS software version 9. All data were tested to see if they satisfied requirements for parametric testing.

Treatment effect on success in the task learning yes or no was analysed with a logistic model. In addition, the influence of the treatment and the presence of a human observer on the number of CBT sessions needed to play all ambiguous cues was evaluated using ANOVA for mixed models with treatment three levels, GEN, ROU or MIN, respectively , observer two levels, yes or no, respectively , and their interaction as fixed effects. Other data were analysed following the recommendations of Gygax [ 27 ]. Approaches yes or no were analysed using logistic regression with a binomial distribution. Latency to approach was analysed using ANOVA for mixed models, only for trials in which piglets approached.

Percentages of time spent inside the apparatus and in contact with the trough were analysed in the same way, only for trials in which piglets approached, after performing an angular transformation. The experimental unit was the trial but the hierarchical levels of group, piglet and CBT session were incorporated in the random effect and the piglet was specified as the subject to correctly assign available degrees of freedom to the fixed effects. In addition, the degree of freedom was corrected with the Kenward-Roger adjustment.

For the analysis of the discrimination of trained P and N cues during the last three training sessions, terms treated as fixed effects were cue two levels, P or N, respectively , treatment and their interaction. In addition, the effect of repeating ambiguous cues was evaluated by using the same models, but only with ambiguous cues, and by adding repetition two levels, 1 or 2, respectively and respective interactions as fixed effects. Adjusted means and confidence intervals for percentage of time were back-transformed to the original scale for presentation in figures.

Pigs and humans: 10, years of interaction | University College London

Piglets that completed the task learning successfully discriminated both positive and negative cues during the three last training sessions approaches: Since ambiguous cues were played following a successful P-N or N-P pair of trials and piglets failed to some trained cues, the number of CBT sessions required to play all the ambiguous cues varied between piglets from 4 to 15 sessions.

Analyses revealed that repeating ambiguous cues did not influence the percentage of approach of piglets The main effects on behavioural variables following each cue are summarised in Table 1. The results show that the interaction between cue and treatment had an impact on behavioural responses of piglets during CBT. In addition, the interaction between observer and treatment tended to have an impact on the proportion of approach.

Fig 2A and 2B describe the mean percentage of approach to the trough of piglets from each treatment for both trained and ambiguous cues during CBT in absence or presence of the human observer. Analyses showed that differences between treatments in the proportion of approach, regardless of the cue, were significant in the absence of the human observer F 2, Although there were no overall treatment effect in presence of the human observer F 2, Average proportion of approach i.

Nonetheless, because the effect of the interaction between observer and treatment was only a tendency, data were also pooled for a global analysis. Again, the proportion of approach was influenced by treatments following playback of AM cues F 2, However, the proportion of approach was not influenced by treatments neither following playbacks of trained P and N cues P cues: 1. The Table 1 shows an effect of the interaction between cue and treatment on the percentage of time spent inside the apparatus and in contact with the trough, meaning that changes in the approach behaviour of piglets from P to N cues progressed differently according to the treatment Fig 3A and 3B.

Indeed, the decrease of the approach behaviour from positive to negative cues of GEN piglets seems to be less pronounced than for MIN piglets. However, the analysis for each cue separately did not show any treatment effect. A Average percentage of time spent inside the apparatus and; B Average percentage of time spent in physical contact with the trough following playbacks of the five cues during cognitive bias tests for piglets from gentle GEN, light grey squares , rough ROU, black triangles and minimal contact MIN, dark grey diamonds treatments, regardless of the presence or not of the handler; C Average percentage of time spent inside the apparatus and; D Average percentage of time spent in physical contact with the trough following playbacks of the five cues during cognitive bias tests in the absence white circles or presence black circles of the human observer, regardless of the treatment.

The performance of piglets was lower when the observer was present since the number of CBT sessions required to play all the ambiguous cues was higher with than without the observer 4. Results show that the presence of a human observer during CBT influenced the percentage of time spent inside the apparatus and in contact with the trough Table 1. Overall, piglets spent less time inside the apparatus and in contact with the trough when the handler was present regardless of the cue time inside the apparatus: 0.

When considering cues separately, the effect was significant for P cues only time inside the apparatus: 0. In addition, as mentioned above, the interaction between observer and treatment tended to modulate the proportion of approach Table 1. The nature of the chronic experience with the handler induced a judgement bias confirming the hypothesis that the way humans behave with animals can modulate the emotional state of the animal and hence its welfare.

In addition, the presence of a human observer i. Piglets which received gentle contact over a long period of time were more likely to approach the trough in response to the ambiguous median auditory cue than piglets which received rough contact, piglets from minimal contact being intermediate. This decision-making suggests that piglets from gentle contact treatment expected the outcome to the ambiguous cues more likely to be the same as with the positive cue i.

Pigs and Humans: 10,000 Years of Interaction

The emotional state, at any given time, biases information processing [ 3 ] and influences how organisms perceive situations or stimuli. With experience, piglets handled gently may not only form a positive memory of humans and be more willing to approach or be approached by gentle or unfamiliar humans [ 16 , 17 ], but also perceive less negatively and be less wary and fearful under uncertain situations than piglets handled roughly.

These results corroborate with previous studies on human-pig relationship [ 28 , 29 ] that originally showed the impact of handling with different valences on pig behaviour and welfare. In pigs, aversive experience with humans involving electric shocks is susceptible to induce a chronic stress response, which translates in higher free corticosteroid concentrations even in the absence of negative handlers.

This leads to lower growth rate, impairment of reproductive functions, and fear of humans [ 28 , 29 ]. In the present study, negative treatments were clearly less aversive than electric shocks but they were sufficient to have an impact on emotional states. Hence the impact of humans on the emotional state of the piglets as observed in the present study gives a coherent picture about the involvement of humans in animal welfare.

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Contrary to the present study, it seems that in some contexts, release from stressful situations may also lead to optimistic biases [ 13 , 30 , 31 ]. For instance, shearing, a routine husbandry procedure in sheep in which humans are involved, provokes an acute stress response and is accompanied by elevated plasma cortisol concentrations [ 32 ]. Although the link between this procedure and the perception of humans is poorly understood, it has been demonstrated that sheep exhibit positive judgement bias following release from shearing [ 30 ].

All these treatments were novel and applied on a relatively short period of time and the authors supposed that stressed animals may have sought something positive during CBT to counteract their negative experience. Hence, the situation was deeply different and piglets roughly handled may have shown free-floating negative mood throughout the experiment.

However, no judgement bias was observed for the ambiguous cues nearest positive cue and nearest negative cue. The paradigm supposes that a negative bias in response to an ambiguous cue closest to the positive cue may reflect a decreased expectation of positive event, a symptom of depression, whereas a negative bias in response to an ambiguous cue closest to the negative cue may indicate an increased expectation of negative events, a symptom of anxiety [ 4 ].

Using different probe degrees may have potentially provided not only an indicator of emotional states with different valences e. The absence of treatment effect prevented any conclusion about the potential arousal level anxiety vs depression of piglets. It is particularly noteworthy to see how the presence of a human observer i. Although piglets maintained their performance in discriminating cues, they spent less time inside the apparatus and in contact with the trough when the human observer was present.

It was originally shown that in absence of humans, isolated young pigs which have received minimal interactions with humans prefer access to sight and relative proximity with conspecifics as well as comfortable lying surface instead of a mirror [ 35 ].


However when a human is present, their preferences for comfort switch for social enrichments including mirror or conspecifics. Activities such as rest on a mat or exploration of objects e. In the present study, the presence of an observer was unfamiliar to piglets from all treatments since they were always trained without having a human in sight.

It seems that they were more anxious, or at least attentive towards the observer, and they were less willing to explore or seek for rewards than when the observer was absent. This may be explained by the loss of visual control over the observer when being in the apparatus. Roughly handled piglets should have been particularly wary and refuse to participate to CBT when the familiar rough handler was present but it was not the case. Perhaps the value of food rewards was higher than the risk to lose sight of the familiar rough handler for few seconds.

In addition, the way an animal perceive a same human being may vary according to the context. This new context, in which the negative handler was motionless outside of the pen may have induced a lower emotional response. Nevertheless, regardless of the treatment, the presence of the human observer did not bias the judgement of piglets since the way they interpreted the ambiguous situation, as observed by the choice of approaching or not and the latency to approach ambiguous cues, was not influenced by the presence of the handler.

This does not preclude that differences between treatments on the proportion of approach tended to appear more clear-cut in absence of the observer, reinforcing the idea that the presence of an observer, an unfamiliar situation for piglets, disturbed them. Some methodological aspects should also be discussed. Firstly, the present study demonstrates that piglets can be trained to discriminate auditory cues that differ quantitatively.

In the study of Douglas et al. In pigs, the various grunts and calls do not appear to have specific meanings, but the intensity, the frequency and the duration vary with the type of situations [ 37 , 38 ]. Thus, it has been supposed that pigs may discriminate more easily notes differing in frequencies Hz but also in repetition number in the available time.

Since high tonalities and longer sound durations are associated with experiences considered highly stressful in pigs [ 38 ], played cues could have a kind of meaning for pigs and influence their behavioural responses. Therefore, notes associated with positive and negative cues were balanced between treatments. Secondly, to optimise learning, pre-experiments showed that it was important to find a way to maintain a strong motivation to approach during positive trials and a strong motivation to avoid approaching during negative trials over time.

Whereas some authors rationed pigs for cognitive bias experiments [ 22 , 25 ], others provided food ad libitum [ 24 ]. Rationing piglets proved to be efficient to maintain such level of motivation, even if it seems that it also motivated them to take risks incorrect responses to negative cues.

In addition, punishments used in negative trials were regularly changed to prevent from habituation. Training duration was adapted according to individual learning performances. It is supposed that this individual learning may have decrease inter-individual differences of approaches to learnt P and N cues during CBT. A potential criticism of the present study is about the low success rate in the task learning.

Compared to other studies in pigs, animals used in the present study were younger i. Perhaps discriminative learning is much more difficult for weaned piglets than for older pigs. In the same study, a significantly higher success rate i. Although these older animals were already used in other cognitive experiments [ 40 ], authors suggested that active-choice tasks, for which responses are operant for the two trained cues e. This study originally demonstrates that the emotional state of a farm animal such as piglets can be affected by the way humans interact with them.

Gentle interactions with humans induced more positive emotional states, as observed by the optimistic judgement bias of gently handled piglets compared to piglets which were roughly handled or received minimal contact. In addition, the presence of a human as an observer during cognitive bias tests caught the attention of piglets and affected their motivation to explore the apparatus and the trough, even though it did not significantly bias their judgement.

The demonstration of such cognitive and emotional abilities in farm animals should be taken into account in animal welfare research and management. Furthermore, it should modify our own perception of animals and may lead to the development of techniques by which humans can, not only decrease bad mood, but also trigger positive emotional states of animals. Many thanks to Marjolaine St-Louis and the piggery staff for their appreciated assistance and their enthusiastic participation during experiments.

The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. National Center for Biotechnology Information , U. PLoS One. Published online Aug 5. Georges Chapouthier, Editor. Author information Article notes Copyright and License information Disclaimer. Competing Interests: The authors have declared that no competing interests exist. Received Apr 16; Accepted Jun This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.

This article has been cited by other articles in PMC. Abstract The emotional state can influence decision-making under ambiguity. Introduction Domestic animals are considered to be sentient and endowed with cognitive and emotional abilities. Treatments Treatments were given from the third day post-weaning until the end of experiment.

Testing arena and apparatus design The testing arena was located in an experimental room separated from housing rooms and consisted of a 2. Open in a separate window. Fig 1. Overview of the testing arena and the apparatus. Statistical analyses The SAS software version 9. Fig 2. The nature of the experience with the handler biases the judgement of piglets towards AM cues. Fig 3. Percentages of time spent inside the apparatus and in contact with the trough are affected by the presence of a human observer, and to a lesser extent, by treatments.

Presence of the human observer The performance of piglets was lower when the observer was present since the number of CBT sessions required to play all the ambiguous cues was higher with than without the observer 4. Discussion The nature of the chronic experience with the handler induced a judgement bias confirming the hypothesis that the way humans behave with animals can modulate the emotional state of the animal and hence its welfare. Supporting Information S1 File Datasets used for the statistical analyses.

XLSX Click here for additional data file. Data Availability All relevant data are within the paper and its Supporting Information files. References 1. Human—animal interactions at abattoirs: Relationships between handling and animal stress in sheep and cattle. App Anim Behav Sci.

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Assessment of positive emotions in animals to improve their welfare. Physiol Behav. Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci Biobehav Rev. Cognitive bias as an indicator of animal emotion and welfare: Emerging evidence and underlying mechanisms. Darwinian models of depression: A review of evolutionary accounts of mood and mood disorders. Prog neuro-psychopharmacol biol psychiatry. Cognitive bias and affective state. Agitated honeybees exhibit pessimistic cognitive biases. Curr Biol.

A meta-analytic review of mood-congruent implicit memory in depressed mood. Clin Psychol Rev.