The study by Jacques et al. (2024) addresses a critical concern in the context of genetic diversity erosion in domesticated animal populations.  The research uses data from the cryopreserved resources from the French National Cryobank to manage genetic diversity in livestock species. The authors employ a comprehensive methodology to propose novel biodiversity metrics to characterize the status of genetic diversity of cryopreserved collections including cattle, sheep, goat, horse, donkey, and pig livestock species.  The findings reveal significant variations of genetic diversity at species and breed levels. Breeds with a large commercial distribution had more donors in the collection than local breeds. The authors propose a practical framework for assessing germplasm collections, providing a valuable tool for planning and managing collections at both national and international levels.  The study also highlights the usefulness of the Gini-Simpson and effective donor numbers indices to plan a more efficient sampling, whereas the index of diversity impact can be employed in the selection of the most suitable donors for immediate use, based on pedigree but also using genetic markers. 

In resume, this study makes a significant contribution to the field by offering a framework for the assessment of germplasm collections. Its innovative metrics provide insights that could guide strategic decision-making in planning, managing, and utilizing cryopreserved resources. This research is relevant and can benefit conservationists, and population genetics working towards the preservation and sustainable use of genetic resources in livestock species.

Reference

Jacques, A., Duclos, D., Danchin-Burge, C., Mercat, M. J.,  Tixier-Boichard M., Restoux, G. (2024). Assessing the potential of germplasm collections for the management of genetic diversity: the case of the French National Cryobank. bioRxiv 2023.07.19.549644. ver. 3 peer-reviewed and recommended by Peer Community in Animal Science. https://doi.org/10.1101/2023.07.19.549644

The adaptability of livestock to changing environments is based in particular on their genetic characteristics but also on the farming conditions to which they are subjected. However, this last point is poorly documented and little is known about its contribution to environmental challenges. The study by Quéméner and colleagues [1] addresses this question by assessing the effect of two hygiene conditions (good vs poor) on the distribution of cell populations present in adipose and muscle tissues of pigs divergently selected for feed efficiency [2].

The working hypothesis is that degraded housing conditions would be at the origin of an hyper stimulation of the immune system that can influence the homeostasis of adipose tissue and skeletal muscle and consequently modulate the cellular content of these tissues. Cellular compositions are thus interesting intermediate phenotypes for quantifying complex traits. The study uses pigs divergently selected for residual feed intake (RFI+ and RFI-) to assess whether there is a genetic effect associated with the observed phenotypes. 

The study characterized different stromal cell populations based on the expression of surface markers: CD45 to separate hematopoietic lineages and markers associated with the stem properties of mesenchymal cells: CD56, CD34, CD38 and CD140a. The authors observed that certain subpopulations are differentially enriched according to the hygiene condition (good vs poor) in adipose and skeletal tissue (CD45-CD56-) sometimes with an associated (genetic) lineage effect. This pioneering study validates a number of tools for characterizing cell subpopulations present in porcine adipose and muscle tissue. It confirms that housing conditions can have an effect on intermediate phenotypes such as intra-tissue cell populations. This pioneering work will pave the way to better understand the effects of livestock systems on tissue biology and animal phenotypes and to characterize the nature and function of progenitor cells present in muscle and adipose tissue.

[1] Quéméner A, Dessauge F, Perruchot MH, Le Floc’h N, Louveau I. 2022. The impact of housing conditions on porcine mesenchymal stromal/stem cell populations differ between adipose tissue and skeletal muscle. bioRxiv 2021.06.08.447546, ver. 3 peer-reviewed and recommended by Peer Community in Animal Science. https://doi.org/10.1101/2021.06.08.447546 

[2] Gilbert H, Bidanel J-P, Gruand J, Caritez J-C, Billon Y, Guillouet P, Lagant H, Noblet J, Sellier P. 2007. Genetic parameters for residual feed intake in growing pigs, with emphasis on genetic relationships with carcass and meat quality traits. Journal of Animal Science 85:3182–3188. https://doi.org/10.2527/jas.2006-590.

Villain et al., (2023) investigated the structure of vocalisations in piglets in relation to human-animal-relationship. They first established a positive relationship by habituating piglets to be positively handled at weaning or later on after weaning. They then compared the reactions of piglets previously positively handled at weaning to that of non-handled piglets during tests in presence of a human (interacting or not), and also before and after the conditioning period when all piglets received positive contacts. They showed that the duration and frequency of grunts emitted in the presence of the human depends on previous contacts. More specifically, grunts are shorter and higher pitched in pigs that have been positively handled, in line with a positive human-animal relationship which is also observed through proximity of the piglets with the human. The authors concluded that the structure of pig vocalisation can reflect the quality of their relationship with humans. 

The authors also showed that not only the response to humans is modified by positive contacts but also the general mood of piglets, with piglets positively handled at weaning emitting shorter grunts than non-handled piglets, whatever the context. 

Another interesting finding is the temporality of behaviour of pigs habituated to positive contacts: during the first tests, they stay close to the human, probably being reassured by the proximity of the human. Then, when tests are repeated, they explore more the test room, using the human as an exploratory basis as already reported in the literature. 

The hypotheses of the study are clear. The methods are reported in details so that the work is reproducible. The interpretation of results is sound. The manuscript is clearly written. 

This paper brings new and original knowledge in the field of animals’ emotional responses and human-animal relationship: on the structure of grunts in relation to positive affects (positive emotion, positive mood) and on the temporality of the responses to human presence.

I recommend this manuscript for its originality and quality.

Isabelle Veissier

Villain, A.S., Guérin, C., Tallet, C., 2023. The use of pigs vocalisation structure to assess the quality of human-pig relationship. bioRxiv 2022.03.15.484457, ver. 5 peer-reviewed and recommended by Peer Community in Animal Science. https://doi.org/10.1101/2022.03.15.484457

"Ensuring ethical animal welfare research: Are more ethics review committees the solution?" by Birte Nielsen and colleagues [1] provides food for thought on the ethical assessment of experiments involving farm animals. While regulations can provide a precise framework, they differ from country to country and do not consider several cases, mainly when the experimentation involves non- or minimally invasive manipulations. It is also the case when research projects use farmed animals that do not fall within the scope of the regulations on animal experimentation but have undergone practices that can be authorised on farms but may raise ethical questions (tail docking, live castration, tooth filing, beak trimming, dehorning). On the other hand, the heterogeneity of the criteria taken into account by the ethics committees, when they exist (and this can differ greatly from one country to another), do not necessarily correspond to the criteria of the journals, the reviewers and the bodies brought in to evaluate the research project, or to the regulations specific to each country.  

All these paradoxes lead the authors to propose solutions, the most straightforward and spontaneous of which is to ask ourselves questions about this issue upstream of the experimental design required to answer a given scientific question. While increasing the number of ethical review committees may be an insufficient option, the authors insist on the importance of improving committee members' training, taking into consideration jurisdictions' differences between countries and spending more time on ethics evaluation during manuscripts' reviewing. In addition, the upstream assessment of research projects by ethics committees, specific to an institution (research institute, universities, companies), a scientific publisher or even a dedicated international ethical review board may also be a good option.

The ethical evaluation of research projects is a question at the heart of our research activities, for which we do not have all the answers. As with scientific reviewing, we must take on the role of evaluator or be evaluated ourselves, using criteria and feelings that are not always consensual. The heterogeneity of evaluation systems within the scientific community, the lack of training for scientists in the fundamentals of ethical evaluation, and the different perceptions of the animal condition between countries and cultures can lead to a reciprocal lack of understanding between evaluator and evaluated, and sometimes a feeling of injustice, as some research may be easy to conduct in one country but difficult in another. Indeed, it is exciting to read the exchanges between the authors and the three reviewers who assessed this opinion paper to appreciate the diversity of points of view and see specific points of divergence.

In addition to animal experimentation, the judgment handed down on 30 June 2023 by the French court penalising a pig farmer for the abusive use of an authorised breeding practice (tail docking) is a perfect illustration of the fact that the ethical assessment of practices and handling of farm animals now extends far beyond the scientific world and is becoming an increasingly important factor in the relationship between society and animal breeding. Failure to consider this evolution, whether in experimentation or animal husbandry, may have legal consequences and increase the lack of understanding between our practices and how society perceives them. The questions raised and the solutions proposed in the article by Nielsen et al. are central to our concerns, not only for the scientific community but also to meet the expectations of all stakeholders.

Finally, although the authors do not directly address the question of genome editing and research using edited farm animals, this is and will be at the heart of future issues concerning the ethical evaluation of research projects. As with practices and manipulations, the intentionality of the modifications induced leads us to question and evaluate, in farmed species, their consequences on animal welfare and their relevance to society and the development of more sustainable and socially accepted animal husbandry.

Reference

[1] Nielsen, B. L., Golledge, H. D. R., Chou, J., Camerlink, I., Pongrácz, P., Ceballos, M., Whittaker, A. L., Olsson, I. S. (2023) Ensuring ethical animal welfare research: Are more ethics review committees the solution? OSF Preprints. Ver. 3 peer-reviewed and recommended by Peer Community in Animal Science. https://doi.org/10.31219/osf.io/s6459

One of the achievements of animal genetics is that it finds solutions along with the emergence of new needs of the animal husbandry community or the adoption of new laws. Muir and Cheng (2013) research serves as a classic example of using the innovations of animal genetics to meet new legal challenges, such as the restriction of beak cutting in laying hens. Muir and Cheng (2013) investigated the genetic diversity to deal with the cannibalism of intact chickens. In 2021, the European Citizens' Initiative urged the European Commission to legislate against the use of cages for farm animals in the livestock industry. Chapuis et al., (2024) presented a successful solution to the poultry industry about this (future) law by presenting a cost-efficient assignment SNP panel.

In animal breeding, access to pedigree information is necessary for genetic progress. Since the 1970s, the development of genomic science and  molecular techniques has shown their ability in this field. Despite the substantial reduction of genotyping costs in the last 20 years, the practical use of genome-wide genotyping for thousands of SNPs remains challenging. Therefore, the search for a small, cost-effective SNP panel is ongoing, with objectives including genetic diversity (Viale et al., 2017), product traceability (Dominik et al., 2021), species and hybrid identification (Harmoinen et al., 2021) and pedigree construction in wild populations (Ekblom et al., 2021). Furthermore, especially in recent decades, small panels of markers have been proposed for parentage assignment in different animals. For example, Domínguez-Viveros et al., (2020) developed panels with 42 to 63 markers for different sheep breeds in Mexico. Similar panels for parentage assignment have been proposed for salmon (May et al., 2020), rainbow trout (Liu et al., 2016), French sheep (Tortereau et al., 2017), Spanish sheep (Calvo et al., 2021), and European bison (Wehrenberg et al., 2024), with marker numbers of 142, 95, 180, 173, and 96, respectively. Massault et al., (2021) showed by simulation that a panel with at least 50 markers is sufficient for progeny assignment in pearl oysters. These examples highlight that extracting a small panel of markers (usually less than 200) from the total genotyping introduced in different species, can open new horizons for applying genomic information in animal breeding.

Chapuis et al. (2024) addressed the challenge of finding an efficient set of markers that can be used in the hybridization of two species of the Pekin duck and the Muscovy duck. They used KASPar technology to setup a panel, with SNPs existing in both species and their hybrids. This panel has sufficient polymorphism to use in practice. Thus, it can be considered as a step forward compared to previous work done on microsatellites. A final list of SNPs was constructed from a reference set comprising 600 K genotyping of Anas platyrhynchos, Cairina moschata and mule duck. 

In addition to developing of a cost-efficient assignment panel, the work of Chapuis et al. (2024) presented a factorial design to maintain genetic diversity while considering specificities of duck production. The use of factorial design in avian pedigreed populations is relatively novel, making this research particularly innovative. The study's approach to factorial design in populations with limited size may be generalized to similar poultry species. Furthermore, sufficient effective size of population is selected. So, the panel can be used in other populations outside the tested populations. A notable feature of this panel is the use of neutral SNPs, which ensures that markers will not be lost due to future selection pressures over time.

The paper of Chapuis et al. (2024) exemplifies the application of molecular genetics to address challenges in the poultry industry.  The use of kinship matrix instead of relationship matrix, taking into account the unique characteristics of duck production, could be another novelty of the paper. According to the reviewers' comments, the results can be beneficial in the future, particularly with the introduction of the specific factorial design.

References

Calvo JH, Serrano M, Tortereau F, Sarto P, Iguacel LP, Jiménez MA, Folch J, Alabart JL, Fabre S and Lahoz B (2021). Development of a SNP parentage assignment panel in some North-Eastern Spanish meat sheep breeds. Spanish Journal of Agricultural Research 18, e0406. https://doi.org/10.5424/sjar/2020184-16805    

Chapuis H, Brard-Fudulea S, Hazard A, Vignal A, Demars J, Rouger R, Teissier M, Gilbert H (2024). Cost-efficient assignment panel for ducks. Setup of a cost-efficient assignment panel for duck populations.: An illustration with experimental data. HAL, hal-04542880, ver. 2 peer-reviewed and recommended by Peer Community in Animal Science. https://hal.inrae.fr/hal-04542880 

Domínguez-Viveros J, Rodríguez-Almeida FA, Jahuey-Martínez FJ, Martínez-Quintana JA, Aguilar-Palma GN, Ordoñez-Baquera P (2020). Definition of a SNP panel for paternity testing in ten sheep populations in Mexico, Small Ruminant Research ,193,106262. https://doi.org/10.1016/j.smallrumres.2020.106262

Dominik S, Duff CJ, Byrne AI, Daetwyler H, Reverter A (2021). Ultra-small SNP panels to uniquely identify individuals in thousands of samples. Animal Production Science 61, 1796–1800. https://doi.org/10.1071/AN21123

Ekblom R, Aronsson M, Elsner-Gearing F, Johansson M, Fountain T, Persson J (2021). Sample identification and pedigree reconstruction in Wolverine (Gulo gulo) using SNP genotyping of non-invasive samples. Conservation Genetics Resources 13, 261–274. https://doi.org/10.1007/s12686-021-01208-5

Harmoinen J, von Thaden A, Aspi J, Kvist L, Cocchiararo B, Jarausch A, Gazzola A, Sin T, Lohi H, Hytönen MK, Kojola I, Stronen AV, Caniglia R, Mattucci F, Galaverni M, Godinho R, Ruiz-González A, Randi E, Muñoz-Fuentes V, Nowak C (2021). Reliable wolf-dog hybrid detection in Europe using a reduced SNP panel developed for non-invasively collected samples. BMC Genomics 22, 473. https://doi.org/10.1186/s12864-021-07761-5

Liu S, Palti Y, Gao G, Rexroad CE (2016). Development and validation of a SNP panel for parentage assignment in rainbow trout. Aquaculture 452, 178–182. https://doi.org/10.1016/j.aquaculture.2015.11.001

Massault C, Jones DB, Zenger KR, Strugnell JM, Barnard R, Jerry DR (2021). A SNP parentage assignment panel for the silver lipped pearl oyster (Pinctada maxima). Aquaculture Reports 20, 100687. https://doi.org/10.1016/j.aqrep.2021.100687

May SA, McKinney GJ, Hilborn R, Hauser L, Naish KA (2020). Power of a dual-use SNP panel for pedigree reconstruction and population assignment. Ecology and Evolution 10, 9522–9531. https://doi.org/10.1002/ece3.6645

Muir WM, Cheng HW(2013). Genetics and the Behaviour of Chickens: Welfare and Productivity. In Genetics and the Behaviour of Domestic Animals. Vol. 2 (2nd ed.). pp. 1–30.ISBN: 9780128100165

Tortereau F, Moreno CR, Tosser-Klopp G, Servin B, Raoul J (2017). Development of a SNP panel dedicated to parentage assignment in French sheep populations. BMC Genetics 18, 50. https://doi.org/10.1186/s12863-017-0518-2

Viale E, Zanetti E, Özdemir D, Broccanello C, Dalmasso A, De Marchi M, Cassandro M (2017). Development and validation of a novel SNP panel for the genetic characterization of Italian chicken breeds by next-generation sequencing discovery and array genotyping. Poultry Science 96, 3858–3866. https://doi.org/10.3382/ps/pex238

Wehrenberg G, Tokarska M, Cocchiararo B, Nowak C (2024). A reduced SNP panel optimised for non-invasive genetic assessment of a genetically impoverished conservation icon, the European bison. Scientific Reports 14, 1875. https://doi.org/10.1038/s41598-024-51495-9