Section: Genomics
Topic: Agricultural sciences, Genetics/genomics, Population biology

Trends in genome diversity of small populations under a conservation program: a case study of two French chicken breeds

Corresponding author(s): Tixier-Boichard, Michèle (michele.boichard@inrae.fr)

10.24072/pcjournal.474 - Peer Community Journal, Volume 4 (2024), article no. e99.

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Livestock biodiversity is declining globally at rates unprecedented in human history. Of all avian species, chickens are among the most affected ones because many local breeds have a small effective population size that makes them more susceptible to demographic and genetic stochasticity. The maintenance of genetic diversity and control over genetic drift and inbreeding by conservation programs are fundamental to ensure the long-term survival and adaptive potential of a breed. However, while the benefits of a conservation program are well understood, they are often overlooked. We here used temporal whole-genome sequencing data to assess the effects of a conservation program on the genetic diversity (Δπ), deleterious variation (ΔL), and inbreeding (ΔF) of two local French chicken breeds, the Barbezieux and Gasconne. We showed that when the conservation program is consistent over time and does not undergo any major organisational changes (i.e., Barbezieux), the loss of genetic diversity is limited. This was true for both pedigree and genomic inbreeding but also for the genetic load estimated from functionally important genome-wide variants. However, when a conservation program is interrupted or re-initiated from scratch (i.e., Gasconne), the loss of genetic diversity can hardly be limited as a result of the bottleneck effect associated with the re-sampling. Our results reinforce the imperative to establish and sustain existing conservation programs that aim to keep populations with a relatively small effective population size from the brink of extinction. Moreover, we conclude by encouraging the use of molecular data to more effectively monitor inbreeding at the genome level while improving fitness by tracking protein-coding and non-coding deleterious variants.

Published online:
DOI: 10.24072/pcjournal.474
Type: Article de recherche
Mots clés : Conservation program, Inbreeding, Genetic diversity, Genetic load, Chicken

Bortoluzzi, Chiara 1, 2; Restoux, Gwendal 2; Rouger, Romuald 3; Desnoues, Benoit 4; Petitjean, Florence 5; Bosse, Mirte 6, 1; Tixier-Boichard, Michèle 2

1 Wageningen University & Research - Animal Breeding and Genomics, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
2 Université Paris-Saclay, INRAE, AgroParisTech, GABI, 78350, Jouy-en-Josas, France
3 Centre INRAE Val de Loire, UMR-BOA, SYSAAF, 37380 Nouzilly, France
4 Syndicat des Selectionneurs Avicoles et Aquacoles Français (SYSAAF), Unité Mixte de Recherche-UMR Biologie des Oiseaux et Aviculture-BOA, Val de Loire, 37380, Nouzilly, France
5 Centre de Sélection de Béchanne, Hameau de Béchanne, 01370 Saint-Etienne-Du-Bois, France
6 VU University - Amsterdam Institute for Life and Environment (A-LIFE), De Boelelaan 1108, 1081 HZ Amsterdam, The Netherlands
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Trends in genome diversity of small populations under a conservation program: a case study of two {French} chicken breeds},
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Bortoluzzi, Chiara; Restoux, Gwendal; Rouger, Romuald; Desnoues, Benoit; Petitjean, Florence; Bosse, Mirte; Tixier-Boichard, Michèle. Trends in genome diversity of small populations under a conservation program: a case study of two French chicken breeds. Peer Community Journal, Volume 4 (2024), article  no. e99. doi : 10.24072/pcjournal.474. https://peercommunityjournal.org/articles/10.24072/pcjournal.474/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.genomics.100369

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Abascal, F.; Corvelo, A.; Cruz, F.; Villanueva-Cañas, J. L.; Vlasova, A.; Marcet-Houben, M.; Martínez-Cruz, B.; Cheng, J. Y.; Prieto, P.; Quesada, V.; Quilez, J.; Li, G.; García, F.; Rubio-Camarillo, M.; Frias, L.; Ribeca, P.; Capella-Gutiérrez, S.; Rodríguez, J. M.; Câmara, F.; Lowy, E.; Cozzuto, L.; Erb, I.; Tress, M. L.; Rodriguez-Ales, J. L.; Ruiz-Orera, J.; Reverter, F.; Casas-Marce, M.; Soriano, L.; Arango, J. R.; Derdak, S.; Galán, B.; Blanc, J.; Gut, M.; Lorente-Galdos, B.; Andrés-Nieto, M.; López-Otín, C.; Valencia, A.; Gut, I.; García, J. L.; Guigó, R.; Murphy, W. J.; Ruiz-Herrera, A.; Marques-Bonet, T.; Roma, G.; Notredame, C.; Mailund, T.; Albà, M. M.; Gabaldón, T.; Alioto, T.; Godoy, J. A. Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx, Genome Biology, Volume 17 (2016) no. 1 | DOI

[2] Bertorelle, G.; Raffini, F.; Bosse, M.; Bortoluzzi, C.; Iannucci, A.; Trucchi, E.; Morales, H. E.; van Oosterhout, C. Genetic Load: Genomic Estimates and Applications in Non-Model Animals, Nature Reviews Genetics, Volume 23 (2022) no. 8, pp. 492-503 | DOI

[3] Blesbois, E.; Seigneurin, F.; Grasseau, I.; Limouzin, C.; Besnard, J.; Gourichon, D.; Coquerelle, G.; Rault, P.; Tixier-Boichard, M. Semen Cryopreservation for Ex Situ Management of Genetic Diversity in Chicken: Creation of the French Avian Cryobank, Poultry Science, Volume 86 (2007) no. 3, pp. 555-564 | DOI

[4] Bortoluzzi, C. Trends in Genome Diversity of Small Populations under a Conservation Program: A Case Study of Two French Chicken Breeds, Zenodo, 2024 | DOI

[5] Bortoluzzi, C.; Bosse, M.; Derks, M. F.; Crooijmans, R. P.; Groenen, M. A.; Megens, H.-J. The Type of Bottleneck Matters: Insights into the Deleterious Variation Landscape of Small Managed Populations, Evolutionary applications, Volume 13 (2020) no. 2, pp. 330-341 | DOI

[6] Bortoluzzi, C.; Crooijmans, R. P.; Bosse, M.; Hiemstra, S. J.; Groenen, M. A.; Megens, H.-J. The Effects of Recent Changes in Breeding Preferences on Maintaining Traditional Dutch Chicken Genomic Diversity, Heredity, Volume 121 (2018) no. 6, pp. 564-578 | DOI

[7] Bortoluzzi, C.; Restoux, G.; Rouger, R.; Desnoues, B.; Petitjean, F.; Bosse, M.; Tixier-Boichard, M. Trends in Genome Diversity of Small Populations under a Conservation Program: A Case Study of Two French Chicken Breeds, Zenodo, 2024 | DOI

[8] Bosse, M.; Megens, H.-J.; Derks, M. F.; de Cara, '. M.; Groenen, M. A. Deleterious Alleles in the Context of Domestication, Inbreeding, and Selection, Evolutionary applications, Volume 12 (2019) no. 1, pp. 6-17 | DOI

[9] Bosse, M.; Megens, H.-J.; Madsen, O.; Crooijmans, R. P.; Ryder, O. A.; Austerlitz, F.; Groenen, M. A.; de Cara, M. A. R. Using Genome-Wide Measures of Coancestry to Maintain Diversity and Fitness in Endangered and Domestic Pig Populations, Genome research, Volume 25 (2015) no. 7, pp. 970-981 | DOI

[10] Bosse, M.; Megens, H.-J.; Madsen, O.; Paudel, Y.; Frantz, L. A.; Schook, L. B.; Crooijmans, R. P.; Groenen, M. A. Regions of Homozygosity in the Porcine Genome: Consequence of Demography and the Recombination Landscape, PLoS genetics, Volume 8 (2012) no. 11, p. e1003100 | DOI

[11] Bouffartigue, B.; Charvolin-Lemaire, E.; Danvy, S. S.; Duclos, D.; Ducos, A.; Gourdine, J.-L.; Hazard, D.; Journeaux, L.; Lauvie, A.; Naves, M.; others Étude concernant l’actualisation, la définition et les exemples de valorisation des races locales, rustiques, menacées. Volet 2–Races rustiques. Définition de critères simples pour qualifier une race de rustique Établissement d’une liste de races ovines rustiques, Inrae (2023)

[12] Browning, B.; Browning, S. R. Improving the Accuracy and Efficiency of Identity-by-Descent Detection in Population Data, Genetics, Volume 194 (2013) no. 2, pp. 459-471 | DOI

[13] Browning, B.; Tian, X.; Zhou, Y.; Browning, S. R. Fast Two-Stage Phasing of Large-Scale Sequence Data, The American Journal of Human Genetics, Volume 108 (2021) no. 10, pp. 1880-1890 | DOI

[14] Caballero, A.; Toro, M. A. Interrelations between Effective Population Size and Other Pedigree Tools for the Management of Conserved Populations, Genetics research, Volume 75 (2000) no. 3, pp. 331-343 | DOI

[15] Danecek, P.; Auton, A.; Abecasis, G.; Albers, C. A.; Banks, E.; DePristo, M. A.; Handsaker, R. E.; Lunter, G.; Marth, G. T.; Sherry, S. T.; McVean, G.; Durbin, R. The variant call format and VCFtools, Bioinformatics, Volume 27 (2011) no. 15, pp. 2156-2158 | DOI

[16] Davydov, E. V.; Goode, D. L.; Sirota, M.; Cooper, G. M.; Sidow, A.; Batzoglou, S. Identifying a High Fraction of the Human Genome to Be under Selective Constraint Using GERP++, PLoS computational biology, Volume 6 (2010) no. 12, p. e1001025 | DOI

[17] de Cara, M. Á. R.; Villanueva, B.; Toro, M. Á.; Fernández, J. Purging deleterious mutations in conservation programmes: combining optimal contributions with inbred matings, Heredity, Volume 110 (2013) no. 6, pp. 530-537 | DOI

[18] Derks, M. F.; Megens, H.-J.; Bosse, M.; Lopes, M. S.; Harlizius, B.; Groenen, M. A. A Systematic Survey to Identify Lethal Recessive Variation in Highly Managed Pig Populations, Bmc Genomics, Volume 18 (2017) no. 1, pp. 1-12 | DOI

[19] Díez-del-Molino, D.; Sánchez-Barreiro, F.; Barnes, I.; Gilbert, M. T. P.; Dalén, L. Quantifying Temporal Genomic Erosion in Endangered Species, Trends in Ecology & Evolution, Volume 33 (2018) no. 3, pp. 176-185 | DOI

[20] FAO The State of the World's Biodiversity for Food and Agriculture. J. Bélanger & D. Pilling (eds.), FAO Commission on Genetic Resources for Food and Agriculture Assessments, Rome, 2019 | DOI

[21] Fernández, B. J.; Toro, M. A. The use of mathematical programming to control inbreeding in selection schemes, Journal of Animal Breeding and Genetics, Volume 116 (1999) no. 6, pp. 447-466 | DOI

[22] Fernández, J.; Meuwissen, T.; Toro, M.; Mäki-Tanila, A. Management of genetic diversity in small farm animal populations, Animal, Volume 5 (2011) no. 11, pp. 1684-1698 | DOI

[23] Fernández, J.; Toro, M. A.; Caballero, A. Managing Individuals' Contributions to Maximize the Allelic Diversity Maintained in Small, Conserved Populations, Conservation Biology, Volume 18 (2004) no. 5, pp. 1358-1367 | DOI

[24] Gross, C.; Bortoluzzi, C.; de Ridder, D.; Megens, H.-J.; Groenen, M. A.; Reinders, M.; Bosse, M. Prioritizing Sequence Variants in Conserved Non-Coding Elements in the Chicken Genome Using chCADD, PLoS genetics, Volume 16 (2020) no. 9, p. e1009027 | DOI

[25] Habel, J. C.; Husemann, M.; Finger, A.; Danley, P. D.; Zachos, F. E. The Relevance of Time Series in Molecular Ecology and Conservation Biology, Biological Reviews, Volume 89 (2014) no. 2, pp. 484-492 | DOI

[26] Harris, R. S. Improved Pairwise Alignment of Genomic DNA, The Pennsylvania State University, 2007

[27] Huber, C. D.; Kim, B. Y.; Lohmueller, K. E. Population Genetic Models of GERP Scores Suggest Pervasive Turnover of Constrained Sites across Mammalian Evolution, PLoS genetics, Volume 16 (2020) no. 5, p. e1008827 | DOI

[28] Kardos, M.; Taylor, H. R.; Ellegren, H.; Luikart, G.; Allendorf, F. W. Genomics Advances the Study of Inbreeding Depression in the Wild, Evolutionary applications, Volume 9 (2016) no. 10, pp. 1205-1218 | DOI

[29] Kasper, C. Professionalising Conservation Programmes for Local Chicken Breeds, Peer Community in Genomics, Volume 100369 (2024) | DOI

[30] Kimura, M. Some Problems of Stochastic Processes in Genetics, The Annals of Mathematical Statistics (1957), pp. 882-901 | DOI

[31] Kleinman-Ruiz, D.; Soriano, L.; Casas-Marce, M.; Szychta, C.; nigo S'anchez, I.; Fern'andez, J.; Godoy, J. A. Genetic Evaluation of the Iberian Lynx Ex Situ Conservation Programme, Heredity, Volume 123 (2019) no. 5, pp. 647-661 | DOI

[32] Kumar, P.; Henikoff, S.; Ng, P. C. Predicting the Effects of Coding Non-Synonymous Variants on Protein Function Using the SIFT Algorithm, Nature protocols, Volume 4 (2009) no. 7, pp. 1073-1081 | DOI

[33] McKenna, A.; Hanna, M.; Banks, E.; Sivachenko, A.; Cibulskis, K.; Kernytsky, A.; Garimella, K.; Altshuler, D.; Gabriel, S.; Daly, M.; others The Genome Analysis Toolkit: A MapReduce Framework for Analyzing next-Generation DNA Sequencing Data, Genome research, Volume 20 (2010) no. 9, pp. 1297-1303 | DOI

[34] McLaren, W.; Gil, L.; Hunt, S. E.; Riat, H. S.; Ritchie, G. R.; Thormann, A.; Flicek, P.; Cunningham, F. The Ensembl Variant Effect Predictor, Genome biology, Volume 17 (2016) no. 1, pp. 1-14 | DOI

[35] McQuillan, R.; Leutenegger, A.-L.; Abdel-Rahman, R.; Franklin, C. S.; Pericic, M.; Barac-Lauc, L.; Smolej-Narancic, N.; Janicijevic, B.; Polasek, O.; Tenesa, A.; others Runs of Homozygosity in European Populations, The American Journal of Human Genetics, Volume 83 (2008) no. 3, pp. 359-372 | DOI

[36] Meuwissen, T. Maximizing the Response of Selection with a Predefined Rate of Inbreeding, Journal of animal science, Volume 75 (1997) no. 4, pp. 934-940 | DOI

[37] Muir, W. M.; Wong, G. K.-S.; Zhang, Y.; Wang, J.; Groenen, M. A.; Crooijmans, R. P.; Megens, H.-J.; Zhang, H.; Okimoto, R.; Vereijken, A.; others Genome-Wide Assessment of Worldwide Chicken SNP Genetic Diversity Indicates Significant Absence of Rare Alleles in Commercial Breeds, Proceedings of the National Academy of Sciences, Volume 105 (2008) no. 45, pp. 17312-17317 | DOI

[38] Ohta, T. Slightly Deleterious Mutant Substitutions in Evolution, Nature, Volume 246 (1973) no. 5428, pp. 96-98 | DOI

[39] van Oosterhout, C.; Speak, S. A.; Birley, T.; Bortoluzzi, C.; Percival-Alwyn, L.; Urban, L. H.; Groombridge, J. J.; Segelbacher, G.; Morales, H. E. Genomic erosion in the assessment of species extinction risk and recovery potential, bioRxiv, 2022 | DOI

[40] Orlando, L.; Librado, P. Origin and Evolution of Deleterious Mutations in Horses, Genes, Volume 10 (2019) no. 9, p. 649 | DOI

[41] Paris, C.; Servin, B.; Boitard, S. Inference of Selection from Genetic Time Series Using Various Parametric Approximations to the Wright-Fisher Model, G3: Genes, Genomes, Genetics, Volume 9 (2019) no. 12, pp. 4073-4086 | DOI

[42] Paten, B.; Earl, D.; Nguyen, N.; Diekhans, M.; Zerbino, D.; Haussler, D. Cactus: Algorithms for Genome Multiple Sequence Alignment, Genome research, Volume 21 (2011) no. 9, pp. 1512-1528 | DOI

[43] Purcell, S.; Neale, B.; Todd-Brown, K.; Thomas, L.; Ferreira, M. A.; Bender, D.; Maller, J.; Sklar, P.; De Bakker, P. I.; Daly, M. J.; others PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses, The American journal of human genetics, Volume 81 (2007) no. 3, pp. 559-575 | DOI

[44] Rentzsch, P.; Witten, D.; Cooper, G. M.; Shendure, J.; Kircher, M. CADD: Predicting the Deleteriousness of Variants throughout the Human Genome, Nucleic acids research, Volume 47 (2019) no. D1, p. D886-D894 | DOI

[45] Restoux, G.; Rognon, X.; Vieaud, A.; Guemene, D.; Petitjean, F.; Rouger, R.; Brard-Fudulea, S.; Lubac-Paye, S.; Chiron, G.; Tixier-Boichard, M. Managing Genetic Diversity in Breeding Programs of Small Populations: The Case of French Local Chicken Breeds, Genetics Selection Evolution, Volume 54 (2022) no. 1, pp. 1-17 | DOI

[46] Robinson, J. A.; Räikkönen, J.; Vucetich, L. M.; Vucetich, J. A.; Peterson, R. O.; Lohmueller, K. E.; Wayne, R. K. Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction, Science Advances, Volume 5 (2019) no. 5 | DOI

[47] Santiago, E.; Caballero, A.; Köpke, C.; Novo, I. Estimation of the contemporary effective population size from SNP data while accounting for mating structure, Molecular Ecology Resources, Volume 24 (2023) no. 1 | DOI

[48] Scherf, B. D.; Pilling, D.; others The Second Report on the State of the World's Animal Genetic Resources for Food and Agriculture (2015)

[49] Storey, J. D.; Bass, A. J.; Dabney, A.; Robinson, D. Qvalue: Q-value Estimation for False Discovery Rate Control, R package version, Volume 2 (2015) no. 0, pp. 10-18129

[50] Tixier-Boichard, M.; Audiot, A.; Bernigaud, R.; Rognon, X.; Berthouly, C.; Magdelaine, P.; Coquerelle, G.; Grinand, R.; Boulay, M.; Ramanantseheno, D.; others Valorisation Des Races Anciennes de Poulets: Facteurs Sociaux, Technico-'economiques, génétiques et réglementaire, Les Actes du BRG, Volume 6 (2006), pp. 495-520

[51] van der Valk, T.; Díez-del-Molino, D.; Marques-Bonet, T.; Guschanski, K.; Dalén, L. Historical Genomes Reveal the Genomic Consequences of Recent Population Decline in Eastern Gorillas, Current Biology, Volume 29 (2019) no. 1 | DOI

[52] Vasimuddin, M.; Misra, S.; Li, H.; Aluru, S. Efficient Architecture-Aware Acceleration of BWA-MEM for Multicore Systems, 2019 IEEE International Parallel and Distributed Processing Symposium (IPDPS), IEEE, 2019, pp. 314-324 | DOI

[53] Verrier, E.; Tixier-Boichard, M.; Bernigaud, R.; Naves, M. Conservation and value of local livestock breeds: usefulness of niche products and/or adaptation to specific environments, Animal Genetic Resources Information, Volume 36 (2005), pp. 21-31 | DOI

[54] Wu, Z.; Bosse, M.; Rochus, C. M.; Groenen, M. A.; Crooijmans, R. P. Genomic Insight into the Influence of Selection, Crossbreeding, and Geography on Population Structure in Poultry, Genetics Selection Evolution, Volume 55 (2023) no. 1, p. 5 | DOI

[55] Xue, Y.; Prado-Martinez, J.; Sudmant, P. H.; Narasimhan, V.; Ayub, Q.; Szpak, M.; Frandsen, P.; Chen, Y.; Yngvadottir, B.; Cooper, D. N.; others Mountain Gorilla Genomes Reveal the Impact of Long-Term Population Decline and Inbreeding, Science, Volume 348 (2015) no. 6231, pp. 242-245 | DOI

[56] Zhang, G.; Li, C.; Li, Q.; Li, B.; Larkin, D. M.; Lee, C.; Storz, J. F.; Antunes, A.; Greenwold, M. J.; Meredith, R. W.; others Comparative Genomics Reveals Insights into Avian Genome Evolution and Adaptation, Science, Volume 346 (2014) no. 6215, pp. 1311-1320 | DOI

[57] Zheng, X.; Levine, D.; Shen, J.; Gogarten, S. M.; Laurie, C.; Weir, B. S. A high-performance computing toolset for relatedness and principal component analysis of SNP data, Bioinformatics, Volume 28 (2012) no. 24, pp. 3326-3328 | DOI

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