Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Diversity and population structure of indigenous chicken in Congo, using MHC-linked microsatellite LEI0258

Bigman Aganze Bigabwa A B C , Steven Ger Nyanjom B , Martina Kyallo C , John Juma C , Jean-Baka Domelevo Entfellner C and Roger Pelle https://orcid.org/0000-0003-1053-085X C *
+ Author Affiliations
- Author Affiliations

A Institut Supérieur Pédagogique de Bukavu, (ISP/Bukavu), PO Box 854, Bukavu, Democratic Republic of Congo.

B Department of Biochemistry, Jomo Kenyatta University of Agriculture and Technology, PO Box 62000-00200, Nairobi, Kenya.

C Biosciences Eastern and Central Africa – International Livestock Research Institute (BecA-ILRI) Hub, PO Box 30709-00100, Nairobi, Kenya.

* Correspondence to: R.Pelle@cgiar.org

Handling Editor: Robyn Alders

Animal Production Science 63(3) 213-226 https://doi.org/10.1071/AN21452
Submitted: 30 August 2021  Accepted: 28 September 2022   Published: 4 November 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Chickens are the most important livestock in the Democratic Republic of Congo in particular and in Africa in general; they are kept for their meat and eggs for nutrition and economic status. The availability of chicken diversity information is very important in selection of breeds and in conservation of genetic resources.

Aims: This study aimed to determine allelic variability, genetic diversity, and genetic relationships of the indigenous chicken populations from the South Kivu region to support breeding programs and genetic resource conservations.

Methods: The LEI0258 microsatellite marker within the major histocompatibility complex gene region was used for genotyping. The LEI0258 locus amplicon sequences of 163 indigenous chickens were analysed.

Key results: The number of R13 and R12 repeats varied from 1 to 21 and from 3 to 21 respectively, whereas several combinations of indels and single-nucleotide polymorphisms were observed in the microsatellite flanking regions. In total, 45 different LEI0258 alleles ranging from 193 to 473 bp were determined, including 14 private alleles (Np). Expected heterozygosity (He) varied from 0.864 (Mwenga) to 0.938 (Bukavu), with a mean of 0.911, and observed heterozygosity (Ho) ranged from 0.417 (Uvira) to 0.667 (Mwenga), with a mean of 0.519. The analysis of molecular variance (AMOVA) showed higher genetic variation within individuals (56%) than among individuals (43%) and among chicken populations (1%). Clustering into three admixed gene pools (K = 3) showed the relationships among the chicken populations.

Conclusion: The present study showed the existence of high genetic diversity in chicken populations from South Kivu.

Implications: This study provides information useful for better conservation and breeding strategies of indigenous chicken populations in South Kivu.

Keywords: breeding and conservation, gene pools, genetic variation, haplotype network, indels and SNPs, indigenous chicken, LEI0258 microsatellite marker, private alleles.


References

Bot J, Karlsson LJE, Greef J, Witt C (2004) Association of the MHC with production traits in Merino ewes. Livestock Production Science 86, 85–91.
Association of the MHC with production traits in Merino ewes.Crossref | GoogleScholarGoogle Scholar |

Chang CS, Chen CF, Berthouly-Salazar C, Chazara O, Lee YP, Chang CM, Chang KH, Bed’Hom B, Tixier-Boichard M (2012) A global analysis of molecular markers and phenotypic traits in local chicken breeds in Taiwan. Animal Genetics 43, 172–182.
A global analysis of molecular markers and phenotypic traits in local chicken breeds in Taiwan.Crossref | GoogleScholarGoogle Scholar |

Chazara O, Juul-Madsen HR, Chang C-S, Tixier-Boichard M, Bed’hom B (2011) Correlation in chicken between the marker LEI0258 alleles and Major Histocompatibility Complex sequences. BMC Proceedings 5, S29
Correlation in chicken between the marker LEI0258 alleles and Major Histocompatibility Complex sequences.Crossref | GoogleScholarGoogle Scholar |

Chazara O, Chang C-S, Bruneau N, Benabdeljelil K, Fotsa J-C, Kayang BB, Loukou NE, Osei-Amponsah R, Yapi-Gnaore V, Youssao IAK, Chen C-F, Pinard-van der Laan M-H, Tixier-Boichard M, Bed’Hom B (2013) Diversity and evolution of the highly polymorphic tandem repeat LEI0258 in the chicken MHC-B region. Immunogenetics 65, 447–459.
Diversity and evolution of the highly polymorphic tandem repeat LEI0258 in the chicken MHC-B region.Crossref | GoogleScholarGoogle Scholar |

Chen L-C, Lan H, Sun L, Deng Y-L, Tang K-Y, Wan Q-H (2015) Genomic organization of the crested ibis MHC provides new insight into ancestral avian MHC structure. Scientific Reports 5, 7963
Genomic organization of the crested ibis MHC provides new insight into ancestral avian MHC structure.Crossref | GoogleScholarGoogle Scholar |

Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method.Crossref | GoogleScholarGoogle Scholar |

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.Crossref | GoogleScholarGoogle Scholar |

FAO/UNEP (2000) ‘World watch list for domestic animal diversity.’ 3rd edn. (Ed. BD Scherf) (FAO/UNEP: Rome, Italy)

FAO and IFAD (2022) ‘Farmer field schools for family poultry producers – a practical manual for facilitators.’ (FAO and IFAD: Rome, Italy) https://doi.org/
| Crossref |

Fulton JE, Juul-Madsen HR, Ashwell CM, McCarron AM, Arthur JA, O’Sullivan NP, Taylor RL (2006) Molecular genotype identification of the Gallus gallus major histocompatibility complex. Immunogenetics 58, 407–421.
Molecular genotype identification of the Gallus gallus major histocompatibility complex.Crossref | GoogleScholarGoogle Scholar |

Guèye EF (2002) Employment and income generation through family poultry in low-income food-deficit countries. World’s Poultry Science Journal 58, 541–557.
Employment and income generation through family poultry in low-income food-deficit countries.Crossref | GoogleScholarGoogle Scholar |

Habimana R, Okeno TO, Ngeno K, Mboumba S, Assami P, Gbotto AA, Keambou CT, Nishimwe K, Mahoro J, Yao N (2020) Genetic diversity and population structure of indigenous chicken in Rwanda using microsatellite markers. PLoS ONE 15, e0238966
Genetic diversity and population structure of indigenous chicken in Rwanda using microsatellite markers.Crossref | GoogleScholarGoogle Scholar |

Hailu A, Kyallo M, Yohannes T, Sendeku W, Getu A, Dagnachew S, Dejen M, Wolde Y, Engdaw F, Kidane A, Dessie T, Tarekegn GM, Githae D, Pelle R (2020) Genetic Diversity and Population Structure of Indigenous Chicken Ecotypes (Gallus gallus domesticus) in Ethiopia using LEI0258 Microsatellite. International Journal of Poultry Science 19, 102–110.

Hako Touko BA, Keambou CT, Han J-M, Bembidé C, Skilton RA, Ogugo M, Manjeli Y, Osama S, Cho C-Y, Djikeng A (2015) Molecular typing of the major histocompatibility complex B microsatellite haplotypes in Cameroon chicken. Animal Genetic Resources 56, 47–54.
Molecular typing of the major histocompatibility complex B microsatellite haplotypes in Cameroon chicken.Crossref | GoogleScholarGoogle Scholar |

Han B, Lian L, Qu L, Zheng J, Yang N (2013) Abundant polymorphisms at the microsatellite locus LEI0258 in indigenous chickens. Poultry Science 92, 3113–3119.
Abundant polymorphisms at the microsatellite locus LEI0258 in indigenous chickens.Crossref | GoogleScholarGoogle Scholar |

Kannaki TR, Reddy MR, Raja Ravindra KS, Chatterjee RN (2017) Genetic diversity analysis of the major histocompatibility complex (MHC) region in Indian native chicken breeds and pureline chickens using the LEI0258 microsatellite marker. Indian Journal of Animal Research 51, 998–1001.
Genetic diversity analysis of the major histocompatibility complex (MHC) region in Indian native chicken breeds and pureline chickens using the LEI0258 microsatellite marker.Crossref | GoogleScholarGoogle Scholar |

Kaufman J, Milne S, Göbel TWF, Walker BA, Jacob JP, Auffray C, Zoorob R, Beck S (1999) The chicken B locus is a minimal essential major histocompatibility complex. Nature 401, 923–925.
The chicken B locus is a minimal essential major histocompatibility complex.Crossref | GoogleScholarGoogle Scholar |

Keambou TC, Boukila B, Moussonda G, Manjeli Y (2009) Comparaison de la qualité des oeufs et des performances de croissance des poussins locaux des zones urbaines et rurales de l’Ouest-Cameroun. International Journal of Biological and Chemical Sciences 3, 457–465.
Comparaison de la qualité des oeufs et des performances de croissance des poussins locaux des zones urbaines et rurales de l’Ouest-Cameroun.Crossref | GoogleScholarGoogle Scholar |

Keambou TC, Hako BA, Ommeh S, Bembide C, Ngono EP, Manjeli Y, Wamonje F, Nzuki Wanjala B, Wamalwa M, Cho CY, Skilton RA, Djikeng A (2014) Genetic diversity of the Cameroon indigenous chicken ecotypes. International Journal of Poultry Science 13, 279–291.
Genetic diversity of the Cameroon indigenous chicken ecotypes.Crossref | GoogleScholarGoogle Scholar |

Khobondo JO, Okeno TO, Lihare GO, Wasike CB, Kahi AK (2014) The past, present and future genetic improvement of indigenous chicken of Kenya. Animal Genetic Resources 55, 125–135.
The past, present and future genetic improvement of indigenous chicken of Kenya.Crossref | GoogleScholarGoogle Scholar |

Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15, 1179–1191.
CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K.Crossref | GoogleScholarGoogle Scholar |

Lima-Rosa CAV, Canal CW, Fallavena PRV, Freitas LB, Salzano FM (2005) LEI0258 microsatellite variability and its relationship to B-F haplotypes in Brazilian (blue-egg Caipira) chickens. Genetics and Molecular Biology 28, 386–389.
LEI0258 microsatellite variability and its relationship to B-F haplotypes in Brazilian (blue-egg Caipira) chickens.Crossref | GoogleScholarGoogle Scholar |

Lwelamira J, Kifaro GC, Gwakisa PS, Msoffe PLM (2008) Association of LEI0258 microsatellite alleles with antibody response against Newcastle disease virus vaccine and body weight in two Tanzania chicken ecotypes. African Journal of Biotechnology 7, 714–720.

Magothe TM, Okeno TO, Muhuyi WB, Kahi AK (2012) Indigenous chicken production in Kenya: I. Current status. World’s Poultry Science Journal 68, 119–132.
Indigenous chicken production in Kenya: I. Current status.Crossref | GoogleScholarGoogle Scholar |

McConnell SKJ, Dawson DA, Wardle A, Burke T (1999) The isolation and mapping of 19 tetranucleotide microsatellite markers in the chicken. Animal Genetics 30, 183–189.
The isolation and mapping of 19 tetranucleotide microsatellite markers in the chicken.Crossref | GoogleScholarGoogle Scholar |

Meirmans PG (2020) GENODIVE version 3.05: easy-to-use software for the analysis of genetic data of diploids and polyploids. Molecular Ecology Resources 20, 1126–1131.
GENODIVE version 3.05: easy-to-use software for the analysis of genetic data of diploids and polyploids.Crossref | GoogleScholarGoogle Scholar |

Mogesse HH (2007) Phenotypic and genetic characterization indigenous chicken population in Northwest Ethiopia. PhD Thesis, University of the Free State, Bloemfontein, South Africa.

Moula N, Farnir F, Salhi A, Iguer-Ouada M, Leroy P, Antoine-Moussiaux N (2012) Backyard poultry in Kabylie (Algeria): from an indigenous chicken to a local poultry breed? Animal Genetic Resources 50, 87–96.
Backyard poultry in Kabylie (Algeria): from an indigenous chicken to a local poultry breed?Crossref | GoogleScholarGoogle Scholar |

Mugumaarhahama Y, Ayagirwe RBB, Mutwedu VB, Sadiki JM, Baenyi P, Mushagalusa AC, Bisimwa EB (2016) Caractérisation des systèmes de production de poule locale dans deux zones agro-écologiques du Sud-Kivu (R.D. Congo). Livestock Research for Rural Development 28,

Mwacharo JM, Bjørnstad G, Han JL, Hanotte O (2013) The history of African village chickens: an archaeological and molecular perspective. African Archaeological Review 30, 97–114.
The history of African village chickens: an archaeological and molecular perspective.Crossref | GoogleScholarGoogle Scholar |

Mwambene PL, Kyallo M, Machuka E, Githae D, Pelle R (2019) Genetic diversity of 10 indigenous chicken ecotypes from Southern Highlands of Tanzania based on major histocompatibility complex-linked microsatellite LEI0258 marker typing. Poultry Science 98, 2734–2746.
Genetic diversity of 10 indigenous chicken ecotypes from Southern Highlands of Tanzania based on major histocompatibility complex-linked microsatellite LEI0258 marker typing.Crossref | GoogleScholarGoogle Scholar |

Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution 19, 153–170.
Accuracy of estimated phylogenetic trees from molecular data.Crossref | GoogleScholarGoogle Scholar |

Ngeno K, van Der Waaij EH, Megens HJ, Kahi AK, van Arendonk JAM, Crooijmans RPMA (2015) Genetic diversity of different indigenous chicken ecotypes using highly polymorphic MHC-linked and non-MHC microsatellite markers. Animal Genetic Resources 56, 1–7.
Genetic diversity of different indigenous chicken ecotypes using highly polymorphic MHC-linked and non-MHC microsatellite markers.Crossref | GoogleScholarGoogle Scholar |

Ohwojakpor O, Olowofeso O, Adebambo OA, Onagbesan OM (2012) Genetic diversity of chicken populations in South-South region of Nigeria using microsatellite markers. Egyptian Poultry Science 32, 263–271.

Olowofeso O, Wang JY, Dai DJ, Yang Y, Mekki DM, Musa HH (2005) Measurement of genetic parameters within and between Haimen chicken populations using microsatellite markers. International Journal of Poultry Science 4, 143–148.
Measurement of genetic parameters within and between Haimen chicken populations using microsatellite markers.Crossref | GoogleScholarGoogle Scholar |

Paradis E (2018) Analysis of haplotype networks: The randomized minimum spanning tree method. British Ecological Society 9, 1308–1317.
Analysis of haplotype networks: The randomized minimum spanning tree method.Crossref | GoogleScholarGoogle Scholar |

Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update. Bioinformatics 28, 2537–2539.
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research: an update.Crossref | GoogleScholarGoogle Scholar |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
Inference of population structure using multilocus genotype data.Crossref | GoogleScholarGoogle Scholar |

Sarma DK, Singh S, Bhattacharyya DR, Mohapatra PK, Sarma NP, Ahmed GU, Mahanta J, Anil Prakash (2014) Suitability of the boiling method of DNA extraction in mosquitoes for routine molecular analyses. International Journal of Mosquito Research 1, 15–17.

Schou TW, Permin A, Juul-Madsen HR, Sorensen P, Labouriau R, Nguyen TLH, Fink M, Pham SL (2007) Gastrointestinal helminths in indigenous and exotic chickens in Vietnam: association of the intensity of infection with the major histocompatibility complex. Parasitology 134, 561–573.
Gastrointestinal helminths in indigenous and exotic chickens in Vietnam: association of the intensity of infection with the major histocompatibility complex.Crossref | GoogleScholarGoogle Scholar |

Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society B: Biological Sciences 277, 979–988.
How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings.Crossref | GoogleScholarGoogle Scholar |

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar |