Data from: Genetic responsiveness of African buffalo to environmental stressors: a role for epigenetics in balancing autosomal and sex chromosome interactions?
Hooft, W.F. van; Dougherty, Eric R. ; Getz, Wayne M. ; Greyling, Barend J. ; Zwaan, B.J. ; Bastos, Armanda D.S. - \ 2018
Wageningen University & Research
sex-ratio distorter - sex-ratio suppressor - sex-ratio adjustment - microsatellite - deleterious allele - sexually-antagonistic allele - African buffalo - Syncerus caffer - Kruger National Park - epigenetics - epigenetic modification - Y chromosome - frequency-dependent selection - bovine tuberculosis - body condition
In the African buffalo (Syncerus caffer) population of the Kruger National Park (South Africa) a primary sex-ratio distorter and a primary sex-ratio suppressor have been shown to occur on the Y chromosome. A subsequent autosomal microsatellite study indicated that two types of deleterious alleles with a negative effect on male body condition, but a positive effect on relative fitness when averaged across sexes and generations, occur genome-wide and at high frequencies in the same population. One type negatively affects body condition of both sexes, while the other acts antagonistically: it negatively affects male but positively affects female body condition. Here we show that high frequencies of male-deleterious alleles are attributable to Y-chromosomal distorter-suppressor pair activity and that these alleles are suppressed in individuals born after three dry pre-birth years, likely through epigenetic modification. Epigenetic suppression was indicated by statistical interactions between pre-birth rainfall, a proxy for parental body condition, and the phenotypic effect of homozygosity/heterozygosity status of microsatellites linked to male-deleterious alleles, while a role for the Y-chromosomal distorter-suppressor pair was indicated by between-sex genetic differences among pre-dispersal calves. We argue that suppression of male-deleterious alleles results in negative frequency-dependent selection of the Y distorter and suppressor; a prerequisite for a stable polymorphism of the Y distorter-suppressor pair. The Y distorter seems to be responsible for positive selection of male-deleterious alleles during resource-rich periods and the Y suppressor for positive selection of these alleles during resource-poor periods. Male-deleterious alleles were also associated with susceptibility to bovine tuberculosis, indicating that Kruger buffalo are sensitive to stressors such as diseases and droughts. We anticipate that future genetic studies on African buffalo will provide important new insights into gene fitness and epigenetic modification in the context of sex-ratio distortion and infectious disease dynamics.
Eight challenges in modelling infectious livestock diseases
Brooks-Pollock, E. ; Jong, M. de; Keeling, M.J. ; Klinkenberg, D. ; Wood, J.L.N. - \ 2015
Epidemics 10 (2015). - ISSN 1755-4365 - p. 1 - 5.
mouth-disease - great-britain - bovine tuberculosis - virus transmission - avian influenza - dynamic-model - uk foot - cattle - epidemic - impact
The transmission of infectious diseases of livestock does not differ in principle from disease transmission in any other animals, apart from that the aim of control is ultimately economic, with the influence of social, political and welfare constraints often poorly defined. Modelling of livestock diseases suffers simultaneously from a wealth and a lack of data. On the one hand, the ability to conduct transmission experiments, detailed within-host studies and track individual animals between geocoded locations make livestock diseases a particularly rich potential source of realistic data for illuminating biological mechanisms of transmission and conducting explicit analyses of contact networks. On the other hand, scarcity of funding, as compared to human diseases, often results in incomplete and partial data for many livestock diseases and regions of the world. In this overview of challenges in livestock disease modelling, we highlight eight areas unique to livestock that, if addressed, would mark major progress in the area.
Positive Selection of Deleterious Alleles through Interaction with a Sex-Ratio Suppressor Gene in African Buffalo: A Plausible New Mechanism for a High Frequency Anomaly
Hooft, W.F. van; Greyling, B.J. ; Getz, W.M. ; Helden, P.D. van; Zwaan, B.J. ; Bastos, A.D.S. - \ 2014
PLoS ONE 9 (2014)11. - ISSN 1932-6203
heterozygosity-fitness correlations - bovine tuberculosis - syncerus-caffer - inbreeding depression - population-levels - complex traits - software - disease - wild - flow
Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints. Here we present a possible new mechanism that explains the attainment of high frequencies of deleterious alleles in the African buffalo (Syncerus caffer) population of Kruger National Park, through positive selection of these alleles that is ultimately driven by a sex-ratio suppressor. We have previously shown that one in four Kruger buffalo has a Y-chromosome profile that, despite being associated with low body condition, appears to impart a relative reproductive advantage, and which is stably maintained through a sex-ratio suppressor. Apparently, this sex-ratio suppressor prevents fertility reduction that generally accompanies sex-ratio distortion. We hypothesize that this body-condition-associated reproductive advantage increases the fitness of alleles that negatively affect male body condition, causing genome-wide positive selection of these alleles. To investigate this we genotyped 459 buffalo using 17 autosomal microsatellites. By correlating heterozygosity with body condition (heterozygosity-fitness correlations), we found that most microsatellites were associated with one of two gene types: one with elevated frequencies of deleterious alleles that have a negative effect on body condition, irrespective of sex; the other with elevated frequencies of sexually antagonistic alleles that are negative for male body condition but positive for female body condition. Positive selection and a direct association with a Y-chromosomal sex-ratio suppressor are indicated, respectively, by allele clines and by relatively high numbers of homozygous deleterious alleles among sex-ratio suppressor carriers. This study, which employs novel statistical techniques to analyse heterozygosity-fitness correlations, is the first to demonstrate the abundance of sexually-antagonistic genes in a natural mammal population. It also has important implications for our understanding not only of the evolutionary and ecological dynamics of sex-ratio distorters and suppressors, but also of the functioning of deleterious and sexually-antagonistic alleles, and their impact on population viability
The elephant interferon gamma assay: a contribution to diagnosis of tuberculosis in elephants
Angkawanish, T. ; Morar, D. ; Kooten, P.J. ; Bontekoning, I. ; Schreuder, J. ; Maas, M. ; Wajjwalku, W. ; Sirimalaisuwan, A. ; Michel, A.L. ; Tijhaar, E. ; Rutten, V.P.M.G. - \ 2013
Transboundary and Emerging Diseases 60 (2013)S1. - ISSN 1865-1674 - p. 53 - 59.
captive asian elephants - mycobacterium-tuberculosis - bovine tuberculosis - ifn-gamma - infection - transmission - responses - antigens - african - disease
Mycobacterium tuberculosis (M. tb) has been shown to be the main causative agent of tuberculosis in elephants worldwide. M. tb may be transmitted from infected humans to other species including elephants and vice versa, in case of prolonged intensive contact. An accurate diagnostic approach covering all phases of the infection in elephants is required. As M. tb is an intracellular pathogen and cell-mediated immune (CMI) responses are elicited early after infection, the skin test is the CMI assay of choice in humans and cattle. However, this test is not applicable in elephants. The interferon gamma (IFN-) assay is considered a good alternative for the skin test in general, validated for use in cattle and humans. This study was aimed at development of an IFN- assay applicable for diagnosis of tuberculosis in elephants. Recombinant elephant IFN- (rEpIFN-) produced in eukaryotic cells was used to immunize mice and generate the monoclonal antibodies. Hybridomas were screened for IFN--specific monoclonal antibody production and subcloned, and antibodies were isotyped and affinity purified. Western blot confirmed recognition of the rEpIFN-. The optimal combination of capture and detection antibodies selected was able to detect rEpIFN- in concentrations as low as 1 pg/ml. The assay was shown to be able to detect the native elephant IFN-, elicited in positive-control cultures (pokeweed mitogen (PWM), phorbol myristate acetate plus ionomycin (PMA/I)) of both Asian and African elephant whole-blood cultures (WBC). Preliminary data were generated using WBC from non-infected elephants, a M. tb infection-suspected elephant and a culture-confirmed M. tb-infected elephant. The latter showed measurable production of IFN- after stimulation with ESAT6/CFP10 PPDB and PPDA in concentration ranges as elicited in WBC by Mycobacterium tuberculosis complex (MTBC)-specific antigens in other species. Hence, the IFN- assay presented potential as a diagnostic tool for the detection of elephant tuberculosis. Validation of the assay will require its application in large populations of non-infected and infected elephants.
Development of a lion-specific interferon-gamma assay
Maas, M. ; Kooten, P.J.S. van; Schreuder, J. ; Morar, D. ; Tijhaar, E. ; Michel, A.L. ; Rutten, V.P.M.G. - \ 2012
Veterinary Immunology and Immunopathology 149 (2012)3-4. - ISSN 0165-2427 - p. 292 - 297.
bovine tuberculosis - mycobacterium-bovis - ifn-gamma - diagnostic-techniques - feline tuberculosis - panthera-leo - wildlife - tests - infection - responses
The ongoing spread of bovine tuberculosis (BTB) in African free-ranging lion populations, for example in the Kruger National Park, raises the need for diagnostic assays for BTB in lions. These, in addition, would be highly relevant for zoological gardens worldwide that want to determine the BTB status of their lions, e.g. for translocations. The present study concerns the development of a lion-specific IFN-¿ assay, following the production and characterization of monoclonal antibodies specific for lion interferon-gamma (IFN-¿). Recombinant lion IFN-¿ (rLIFN-¿) was produced in mammalian cells and used to immunize mice to establish hybridoma cell lines producing monoclonal antibodies. These were used to develop a sensitive, lion IFN-¿-specific capture ELISA, able to detect rLIFN-¿ to the level of 160 pg/ml. Recognition of native lion IFN-¿ was shown in an initial assessment of supernatants of mitogen stimulated whole blood cultures of 11 known BTB-negative lions. In conclusion, the capture ELISA shows potential as a diagnostic assay for bovine tuberculosis in lions. Preliminary results also indicate the possible use of the test for other (feline) species
Rainfall-driven sex-ratio genes in African buffalo suggested by correlations between Y-chromosomal haplotype frequencies and foetal sex ratio
Hooft, W.F. van; Prins, H.H.T. ; Getz, W.M. ; Jolles, A.E. ; Wieren, S.E. van; Greyling, B.J. ; Helden, P.D. ; Bastos, A.D.S. - \ 2010
BMC Evolutionary Biology 10 (2010). - ISSN 1471-2148 - 11 p.
cattle bos-taurus - syncerus-caffer - male-fertility - meiotic drive - bovine tuberculosis - drosophila-melanogaster - microsatellite analysis - natural-populations - sperm - selection
Background - The Y-chromosomal diversity in the African buffalo (Syncerus caffer) population of Kruger National Park (KNP) is characterized by rainfall-driven haplotype frequency shifts between year cohorts. Stable Y-chromosomal polymorphism is difficult to reconcile with haplotype frequency variations without assuming frequency-dependent selection or specific interactions in the population dynamics of X- and Y-chromosomal genes, since otherwise the fittest haplotype would inevitably sweep to fixation. Stable Y-chromosomal polymorphism due one of these factors only seems possible when there are Y-chromosomal distorters of an equal sex ratio, which act by negatively affecting X-gametes, or Y-chromosomal suppressors of a female-biased sex ratio. These sex-ratio (SR) genes modify (suppress) gamete transmission in their own favour at a fitness cost, allowing for stable polymorphism. Results - Here we show temporal correlations between Y-chromosomal haplotype frequencies and foetal sex ratios in the KNP buffalo population, suggesting SR genes. Frequencies varied by a factor of five; too high to be alternatively explained by Y-chromosomal effects on pregnancy loss. Sex ratios were male-biased during wet and female-biased during dry periods (male proportion: 0.47-0.53), seasonally and annually. Both wet and dry periods were associated with a specific haplotype indicating a SR distorter and SR suppressor, respectively. Conclusions - The distinctive properties suggested for explaining Y-chromosomal polymorphism in African buffalo may not be restricted to this species alone. SR genes may play a broader and largely overlooked role in mammalian sex-ratio variation
Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo
Jolles, A.E. ; Ezenwa, V.O. ; Etienne, R.S. - \ 2008
Ecology 89 (2008)8. - ISSN 0012-9658 - p. 2239 - 2250.
kruger-national-park - fecal egg counts - bovine tuberculosis - syncerus-caffer - environmental-change - parasitic diseases - host populations - responses - wildlife - susceptibility
Epidemiological studies typically focus on single-parasite systems, although most hosts harbor multiple parasite species; thus, the potential impacts of co-infection on disease dynamics are only beginning to be recognized. Interactions between macroparasites, such as gastrointestinal nematodes, and microparasites causing diseases like TB, AIDS, and malaria are particularly interesting because co-infection may favor transmission and progression of these important diseases. Here we present evidence for strong interactions between gastrointestinal worms and bovine tuberculosis (TB) in free-ranging African buffalo (Syncerus caffer). TB and worms are negatively associated at the population, among-herd, and within-herd scales, and this association is not solely the result of demographic heterogeneities in infection. Combining data from 1362 buffalo with simple mechanistic models, we find that both accelerated mortality of co-infected individuals and TB transmission heterogeneity caused by trade-offs in immunity to the two types of parasites likely contribute to observed infection patterns. This study is one of the first to examine the relevance of within-host immunological trade-offs for understanding parasite distribution patterns in natural populations.
Quantification of the relative efficiency of factory surveillance in the disclosure of tuberculosis lesions in attested Irish cattle
Frankena, K. ; White, P.W. ; O'Keeffe, O. ; Costello, E. ; Martin, S.W. ; Grevenhof, E.M. van; More, S.J. - \ 2007
Veterinary Record 161 (2007)20. - ISSN 0042-4900 - p. 679 - 684.
bovine tuberculosis - inspection - badgers
In Ireland, factory surveillance of cattle for gross lesions is an important supplementary method for detecting herds infected with bovine tuberculosis (TB), and in recent years between 27 and 46 per cent of all new herd breakdowns in any year have been detected by this method. The aim of this study was to determine the relative efficiency of factories in detecting lesions among attested cattle slaughtered during 2003 and 2004. National databases were available on animal slaughter, programmes of tuberculin testing for bovine TB and laboratory confirmation of suspected lesions. Factories were ranked according to their submission risk (number of animals submitted with lesions/number of attested animals killed) and confirmation risk (number of animals with laboratory-confirmed lesions/number of animals submitted with lesions), adjusting for the risk profile of the animals slaughtered, including potential confounding factors such as their age and sex, whether they were purchased or homebred, the test history of their herd, the prevalence of bovine TB in the area and the season of slaughter. Approximately 3·7 million cattle were slaughtered in 42 Irish export-licensed factories during the two years. Complete data were available for 2,374,987 animals from 84,510 attested herds in 2845 District Electoral Divisions. Samples from 7398 animals with suspected TB lesions were submitted for laboratory examination; 4767 (64·4 per cent) were positive, 2011 were negative and 620 were inconclusive. The average unadjusted submission risk for all the factories was 22 per 10,000, ranging from 0 to 58 per 10,000. The unadjusted factory confirmation risk (excluding factories that had sent in fewer than 10 lesions) varied between 34·3 per cent and 86·3 per cent. The unadjusted and adjusted submission and confirmation risks were highly correlated, and animal-related factors (including their characteristics and origin) therefore did not contribute to the variations in factory-level submission and confirmation risks.
Independent and competing disease risks: Implications for host Populations in variable environments
Jolles, A.E. ; Etienne, R.S. - \ 2006
American Naturalist 167 (2006)5. - ISSN 0003-0147 - p. 745 - 757.
emerging infectious-diseases - buffalo syncerus caffer - kruger-national-park - african buffalo - red grouse - trichostrongylus-tenuis - bovine tuberculosis - large herbivores - parasite system - climate-change
Disease models usually assume disease to act independently of other mortality- and morbidity-causing factors. Alternatively, disease may function as a competing risk factor, for example, killing already moribund hosts. Using tuberculosis (TB) in African buffalo as a model system, we explore consequences of competing or independent disease effects for host population dynamics. We include scenarios with density-dependent and density-independent effects of environmental variation, exemplified by variable food availability (driven by rainfall) and catastrophic droughts, respectively. Independent disease effects reduce population size linearly with prevalence, irrespective of the nature of environmental variation. Competing disease risks alter population size only if density-independent variation is present; then, disease reduces population size nonlinearly. Field data indicate that the net effect of TB on buffalo likely falls between the extremes of total independence and competition with other risk factors: TB increases mortality and decreases fecundity in some prime-aged buffalo, suggesting independent disease risks in these individuals, while similar disease effects in senescent buffalo may act as competing risks. Moreover, increased survival and fecundity of TB-negative buffalo may compensate for some disease-related losses. Model assumptions on independent or competing disease risks and environmental variability should be considered explicitly when assessing disease effects on wildlife populations.