Dataset Information

Large-scale genomic analysis reveals the genetic cost of chicken domestication.

ABSTRACT:

Background

Species domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species. These include not only inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, but also post-divergence gene flow and introgression. Although domestication potentially affects the occurrence of both desired and undesired mutations, the way wild relatives of domesticated species evolve and how expensive the genetic cost underlying domestication is remain poorly understood. Here, we investigated the demographic history and genetic load of chicken domestication.

Results

We analyzed a dataset comprising over 800 whole genomes from both indigenous chickens and wild jungle fowls. We show that despite having a higher genetic diversity than their wild counterparts (average π, 0.00326 vs. 0.00316), the red jungle fowls, the present-day domestic chickens experienced a dramatic population size decline during their early domestication. Our analyses suggest that the concomitant bottleneck induced 2.95% more deleterious mutations across chicken genomes compared with red jungle fowls, supporting the "cost of domestication" hypothesis. Particularly, we find that 62.4% of deleterious SNPs in domestic chickens are maintained in heterozygous states and masked as recessive alleles, challenging the power of modern breeding programs to effectively eliminate these genetic loads. Finally, we suggest that positive selection decreases the incidence but increases the frequency of deleterious SNPs in domestic chicken genomes.

Conclusion

This study reveals a new landscape of demographic history and genomic changes associated with chicken domestication and provides insight into the evolutionary genomic profiles of domesticated animals managed under modern human selection.

SUBMITTER: Wang MS

PROVIDER: S-EPMC8207802 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Publications

Large-scale genomic analysis reveals the genetic cost of chicken domestication.

Wang Ming-Shan MS Zhang Jin-Jin JJ Guo Xing X Li Ming M Meyer Rachel R Ashari Hidayat H Zheng Zhu-Qing ZQ Wang Sheng S Peng Min-Sheng MS Jiang Yu Y Thakur Mukesh M Suwannapoom Chatmongkon C Esmailizadeh Ali A Hirimuthugoda Nalini Yasoda NY Zein Moch Syamsul Arifin MSA Kusza Szilvia S Kharrati-Koopaee Hamed H Zeng Lin L Wang Yun-Mei YM Yin Ting-Ting TT Yang Min-Min MM Li Ming-Li ML Lu Xue-Mei XM Lasagna Emiliano E Ceccobelli Simone S Gunwardana Humpita Gamaralalage Thilini Nisanka HGTN Senasig Thilina Madusanka TM Feng Shao-Hong SH Zhang Hao H Bhuiyan Abul Kashem Fazlul Haque AKFH Khan Muhammad Sajjad MS Silva Gamamada Liyanage Lalanie Pradeepa GLLP Thuy Le Thi LT Mwai Okeyo A OA Ibrahim Mohamed Nawaz Mohamed MNM Zhang Guojie G Qu Kai-Xing KX Hanotte Olivier O Shapiro Beth B Bosse Mirte M Wu Dong-Dong DD Han Jian-Lin JL Zhang Ya-Ping YP

BMC biology 20210616 1

<h4>Background</h4>Species domestication is generally characterized by the exploitation of high-impact mutations through processes that involve complex shifting demographics of domesticated species. These include not only inbreeding and artificial selection that may lead to the emergence of evolutionary bottlenecks, but also post-divergence gene flow and introgression. Although domestication potentially affects the occurrence of both desired and undesired mutations, the way wild relatives of dom ...[more]

PMID: 34130700

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Project description:BackgroundBody weight and size are important economic traits in chickens. While many growth-related quantitative trait loci (QTLs) and candidate genes have been identified, further research is needed to confirm and characterize these findings. In this study, we investigate genetic and genomic markers associated with chicken body weight and size. This study provides new insights into potential markers for genomic selection and breeding strategies to improve meat production in chickens.MethodsWe performed whole-genome resequencing of and Wenshang Barred (WB) chickens (n = 596) and three additional breeds with varying body sizes (Recessive White (RW), WB, and Luxi Mini (LM) chickens; (n = 50)). We then used selective sweeps of mutations coupled with genome-wide association study (GWAS) to identify genomic markers associated with body weight and size.ResultsWe identified over 9.4 million high-quality single nucleotide polymorphisms (SNPs) among three chicken breeds/lines. Among these breeds, 287 protein-coding genes exhibited positive selection in the RW and WB populations, while 241 protein-coding genes showed positive selection in the LM and WB populations. Genomic heritability estimates were calculated for 26 body weight and size traits, including body weight, chest breadth, chest depth, thoracic horn, body oblique length, keel length, pelvic width, shank length, and shank circumference in the WB breed. The estimates ranged from 0.04 to 0.67. Our analysis also identified a total of 2,522 genome-wide significant SNPs, with 2,474 SNPs clustered around two genomic regions. The first region, located on chromosome 4 (7.41-7.64 Mb), was linked to body weight after ten weeks and body size traits. LCORL, LDB2, and PPARGC1A were identified as candidate genes in this region. The other region, located on chromosome 1 (170.46-171.53 Mb), was associated with body weight from four to eighteen weeks and body size traits. This region contained CAB39L and WDFY2 as candidate genes. Notably, LCORL, LDB2, and PPARGC1A showed highly selective signatures among the three breeds of chicken with varying body sizes.ConclusionOverall this study provides a comprehensive map of genomic variants associated with body weight and size in chickens. We propose two genomic regions, one on chromosome 1 and the other on chromosome 4, that could helpful for developing genome selection breeding strategies to enhance meat yield in chickens.

Project description:The stress response has been largely modified in all domesticated animals, offering a strong tool for genetic mapping. In chickens, ancestral Red Junglefowl react stronger both in terms of physiology and behavior to a brief restraint stress than domesticated White Leghorn, demonstrating modified functions of the hypothalamic-pituitary-adrenal (HPA) axis. We mapped quantitative trait loci (QTL) underlying variations in stress-induced hormone levels using 232 birds from the 12th generation of an advanced intercross between White Leghorn and Red Junglefowl, genotyped for 739 genetic markers. Plasma levels of corticosterone, dehydroepiandrosterone (DHEA), and pregnenolone (PREG) were measured using LC-MS/MS in all genotyped birds. Transcription levels of the candidate genes were measured in the adrenal glands or hypothalamus of 88 out of the 232 birds used for hormone assessment. Genes were targeted for expression analysis when they were located in a hormone QTL region and were differentially expressed in the pure breed birds. One genome-wide significant QTL on chromosome 5 and two suggestive QTL together explained 20% of the variance in corticosterone response. Two significant QTL for aldosterone on chromosome 2 and 5 (explaining 19% of the variance), and one QTL for DHEA on chromosome 4 (explaining 5% of the variance), were detected. Orthologous DNA regions to the significant corticosterone QTL have been previously associated with the physiological stress response in other species but, to our knowledge, the underlying gene(s) have not been identified. SERPINA10 had an expression QTL (eQTL) colocalized with the corticosterone QTL on chromosome 5 and PDE1C had an eQTL colocalized with the aldosterone QTL on chromosome 2. Furthermore, in both cases, the expression levels of the genes were correlated with the plasma levels of the hormones. Hence, both these genes are strong putative candidates for the domestication-induced modifications of the stress response in chickens. Improved understanding of the genes associated with HPA-axis reactivity can provide insights into the pathways and mechanisms causing stress-related pathologies.

Dataset Information

Large-scale genomic analysis reveals the genetic cost of chicken domestication.

Background

Results

Conclusion

Publications

Large-scale genomic analysis reveals the genetic cost of chicken domestication.

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