Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis

• Published in: Nature reviews. Microbiology 2006-09, Vol.4 (9), p.670-681
• Main Authors: Hewinson, R. Glyn, Smith, Noel H, Gordon, Stephen V, de la Rua-Domenech, Ricardo, Clifton-Hadley, Richard S
• Format: Article
• Language: English
• Subjects: Animals; BCG Vaccine; Biomedical and Life Sciences; Cattle; Chromosomes; Evolution; Evolution, Molecular; Genetic Variation; Genome, Bacterial; Humans; Infectious Diseases; Laboratories; Life Sciences; Medical Microbiology; Microbiology; Mutation; Mycobacterium bovis; Mycobacterium bovis - classification; Mycobacterium bovis - genetics; Mycobacterium tuberculosis; Mycobacterium tuberculosis - genetics; Parasitology; Phylogeny; Population genetics; Population structure; Recombination, Genetic; review-article; Tuberculosis; Tuberculosis - epidemiology; Tuberculosis - immunology; Tuberculosis - veterinary; Tuberculosis, Bovine - epidemiology; Tuberculosis, Bovine - immunology; Tuberculosis, Bovine - microbiology; United Kingdom - epidemiology; Vaccines; Virology
• ISSN: 1740-1526; 1740-1534
• DOI: 10.1038/nrmicro1472

Key Points The M. tuberculosis complex (with the exception of M. canettii ) shows little evidence for the transfer and recombination of chromosomal genes. We discuss the remarkable consequences of this strict clonality, and show how selective sweeps and population bottlenecks can profoundly reduce the diversity of the population. The clonality of this group of organisms has shaped the phylogeny of the M. tuberculosis complex and we suggest that they might best be described as a group of host-adapted ecotypes rather than species. Our analysis highlights the close sequence similarity of these ecotypes and the facility these organisms have for invading and establishing themselves in new mammalian hosts. The history and molecular epidemiology of bovine tuberculosis in the British Isles is then reviewed. A test and slaughter programme was initially highly successful at reducing the incidence of disease but, since the 1980s (and in contrast to the rest of Europe), has failed to control an exponential increase in incidents. The molecular epidemiology of bovine tuberculosis reveals that a single clonal complex of strains has come to dominate throughout the British Isles and is responsible for over 85% of the bovine tuberculosis in Great Britain. We suggest that the limited diversity of M. bovis in the British Isles is a result of a population bottleneck induced by more than 100 years of bovine tuberculosis control programmes, in particular the extensive test and slaughter regime. The recent dominance and exponential increase of a single clonal complex can best be explained by selection, and two possible selective advantages of the dominant clonal complex in the British Isles are discussed. Finally, we show how an understanding of the population structure and molecular epidemiology of this disease has contributed to our appreciation of the role of cattle movement and badgers in the spread and maintenance of the disease, and we describe the practical application to the development of advanced techniques of diagnosis and vaccination. Unlike many other bacterial pathogens, there is little evidence for genetic recombination in the Mycobacterium tuberculosis complex. Smith et al . review how this strict clonality has shaped the phylogeny of the M. tuberculosis complex, focusing on the consequences of clonality for the population structure of Mycobacterium bovis within the British Isles. Mycobacterium bovis is the cause of tuberculosis in cattle and is a member of the My