Genome diversity and adaptation of African Taurine and Zebu cattle

Tijjani, Abdulfatai (2019) Genome diversity and adaptation of African Taurine and Zebu cattle. PhD thesis, University of Nottingham.

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There is an overwhelming phenotypic diversity observed among domesticated animals compared with what is observed in wild species. It follows domestication, migrations, human and natural selection of animals including adaptation to different climatic conditions, local environmental and production conditions. Indigenous African cattle represent a unique set of cattle population as of their adaptation to the conditions of their local environments, which is characterized by a diversity of climatic conditions (hot and dry, hot and humid, cold etc.), prevalence of livestock diseases, including parasitic and tick-borne diseases, and periods of food shortages as results of semi-intensive to extensive management system. However, the productivity of African cattle is generally low compared to the exotic cattle breeds in other parts of the world (Andersson 2001, Groeneveld et al., 2010).

We are faced with the challenges of improving livestock productivity on the African continent in order to meet the ever increased demands for livestock product due to population growth. This may be achieved by breeds replacement (importation of exotic breed, but it means changing the production system), within breed improvement (but takes time) or crossbreeding of exotic with local breeds (work but often only for the F1 generation not beyond). In such a context, a possible way forward would be to do ‘informed’ crossbreeding by combining the adaptive traits of the indigenous breeds with the productivity traits of the exotic ones. However, a prerequisite for this approach is the understanding of the genetic mechanism and identification of the genome regions that have been subjected to both natural and artificial selection and underlying economically important traits including environmental adaptation (Ellegren and Sheldon 2008, Cosart et al., 2011, Lee et al., 2013). This may be typically done using genome-wide association in pedigree resource populations. Alternatively, recent approaches have been suggested to identify key genome regions with remarkable footprints due to selection pressures; the detection of signatures of positive selection. The latter is the focus of this work.

Thus, the primary goal of the research presented herein is to unravel at genome-wide level the genome diversity and particularly the genetic basis of economically important phenotypes including morphology (growth traits), productivity (milk production traits) and local environmental adaptation traits such as disease resistance, heat tolerance and tick resistance traits of indigenous African taurine and zebu cattle through signatures of selection analyses. The full genome sequences of an average of ten representative samples of ten different African cattle breeds were recruited in our attempt to achieve this goal. The African breeds involved are two West African taurine; Muturu from Nigeria and N’Dama from Guinea, and eight East African zebu breeds; Aryashai, Baggara, Kenyan Boran, Butana, Fulani, Gash, Kenana and Ogaden. In addition, samples of five reference cattle breeds including Ankole (African Sanga), Holstein and Jersey (European taurine), Hanwoo (Asian taurine) and Gir (Asian zebu) were also included for ease of comparison and interpretation of results.

In the course of this study, 70 new genome cattle sequences were generated, these were complemented with cattle genome sequences obtained from previous studies with sequences data publicly available. We adopted several selection scan approaches including two within population tests; iHS and ZHp, and four population comparison tests; Rsb, XPEHH, XPCLR and FST.

Prior to signature of positive selection analyses, in chapter 2, we performed variants (SNPs and indels) discovery by comparing the sequences of our cattle samples to the UMD3.1 bovine genome assembly. We subsequently carried out an assessment of genetic diversity, population structure and phylogenetic relationships among the different cattle breeds. The aim was to reveal the genome variations and population structure among the cattle breeds, which in turn will guide the basis for the selection breeds for the comparative genomic tests. As expected, we observed higher mean variant numbers (SNPs and indels) and nucleotide diversity in the zebu breeds than in the taurine breeds, with the ratio as high as 2:1 in most zebu breeds. A significant difference of population structure and differentiation was revealed between West African and European taurine populations, and also within the West African taurine breeds. All African zebu were shown to be of at least two ancestry background (indicine and taurine).

In subsequent chapters, we aim to identify signatures of positive selection. In order to increase the reliability of our results, our strategy entailed the combination of within-population tests and between population tests in order to identify a comprehensive list of candidate genes in the different cattle populations studied. The between-population approach involved the comparison of groups of cattle breeds to identify candidate genomes regions and genes related to contrasting phenotypes and environmental challenge. We then performed the functional annotation of the candidate genes to elucidate the function of the candidate genes putatively linked to the phenotypes under study.

Like most other West African Bos taurus, the shorthorn Muturu is under imminent threat of replacement or crossbreeding with zebu population and their populations have been reduced to a few hundred breeding individuals only. Hence, they have been classified as an endangered breed. In chapter 3, for the first time, we present the genome-wide selection signatures of the endangered trypanotolerant West African shorthorn Muturu based on two complimentary selection scan tests; iHS and Rsb. The results were also compared to N’Dama, a West African longhorn trypanotolerant taurine, and two European taurine breeds (Holstein and Jersey). Among the most remarkable selection signatures regions found in the Muturu cattle, are regions which overlap with members of the major histocompatibility complex (MHC) class I and class II genes and other genes with functions related to both innate and adaptive immunity. These genes particularly the MHC class II genes and genes linked to heat tolerance, such as INTS6, are shared with the N’Dama. Considering the production environment of both West African Bos taurus (WAT) breed studied, which is characterized by high disease prevalence and harsh environmental climatic pressures such as heat (high temperature) and UV radiation, the signature of selection signals detected here may be the consequence of the innate adaptation mechanisms contributing to the survival of these two taurine cattle living in tropical areas.

In chapter 4, the genomic signatures of the two trypanotolerant West African taurine breeds; shorthorn Muturu and longhorn N’Dama, were further investigated. Our analysis was based on candidate genes identified by six selection scan tests; iHS, ZHp, Rsb, XPEHH, XPCLR and FST. Each of the trypanotolerant cattle was compared to two groups of trypanosusceptible cattle populations (African zebu and European taurine) in order to detect candidate genes that may be related to their common trypanotolerance phenotype. Following the annotation of the detected candidate gene sets in each breed, the candidate genes were revealed to be involved in pathways relevant to trypanosomiasis disease progression. The list of common genes between the breeds in these pathways was then investigated further. A major finding of this chapter is the major role that the PTPN6 gene may play in the genetic control of trypanotolerance in West African cattle, with several lines of supportive evidence. These are – a unique WAT haplotype in the region of the gene and a protein-protein interaction network indicating the most likely central role of PTPN6, through its interactions with bovine MHC class II genes and other genes to initiate a cascade of biological processes that may confer protective immunity for the survival of cattle following trypanosome infection.

Finally, in chapter 5, we investigated the genetic control of tropical adaptation and production traits in eight indigenous African zebu breeds. Among the common selective sweeps identified in a majority of the African zebu breeds are genome regions which overlapped candidate genes such as HMGA2 and PTPRG that are related to growth and conformation traits. Candidate genes related to immune response, feeding behaviour, coat colour were also identified across breeds. In addition, heat stress response and tick resistance response gene were investigated by comparing African cattle to non-African taurine breeds. Last but not least we identified candidate genes related to milk yield, protein yield and fat yield in the African zebu dairy breeds (Kenana and Butana) following the comparison of each of this breed to African non-dairy zebu.

Put together, the findings of this thesis buttress the facts that African cattle are a group of unique cattle whose genetic resources could be exploited for the genetic improvement of livestock productivity in sub-Saharan African. The new sequences generated within the course of this project serve as a valuable addition to the limited publicly available genetic resources of livestock from Africa. We envisaged that our results will encourage further investigation into the genome dynamics of the African cattle.

Item Type: Thesis (University of Nottingham only) (PhD)
Supervisors: Hanotte, Olivier
Emes, Richard
Keywords: Genome diversity; Cattle; Phenotypes; Genome sequences; Genome dynamics
Subjects: S Agriculture > SF Animal culture
Faculties/Schools: UK Campuses > Faculty of Medicine and Health Sciences > School of Life Sciences
Item ID: 55806
Depositing User: Tijjani, Abdulfatai
Date Deposited: 19 Jul 2019 04:40
Last Modified: 07 May 2020 11:47

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