Age structure changes indicate direct and indirect population impacts in illegally harvested black rhino.

Overharvesting affects the size and growth of wildlife populations and can impact population trajectories. Overharvesting can also severely alter population structure and may result in changes in spatial organisation, social dynamics and recruitment. Understanding the relationship between overharvesting and population growth is therefore crucial for the recovery of exploited species. The black rhinoceros (Diceros bicornis; black rhino) is a long-lived megaherbivore native to sub-Saharan Africa, listed as Critically Endangered on the IUCN Red List of Threatened Species. Since 2009, the targeted illegal killing of rhino for their horns has escalated dramatically in South Africa. Given their slow life trajectories, spatial structure and social dynamics, black rhino may be susceptible to both direct and indirect impacts of overharvesting. Our study compared black rhino demography before and during extensive poaching to understand the impact of illegal killing. The population exhibited significant changes in age structure after four years of heavy poaching; these changes were primarily explained by a decrease in the proportion of calves over time. Population projections incorporating both direct poaching removals and decreased fecundity/recruitment were most similar to the observed demographic profile in 2018, suggesting that indirect impacts are also contributing to the observed population trajectory. These indirect impacts are likely a result of decreased density, through processes such as reduced mate-finding, population disturbance and/or increased calf predation. This study illustrates the combined effect of direct and indirect impacts on an endangered species, providing a more comprehensive approach by which to evaluate exploited populations.

Ecological opportunity drives individual dietary specialization in leopards.

Individual specialization, when individuals exploit only a subset of resources utilized by the population, is a widespread phenomenon. It provides the basis for evolutionary diversification and can impact population and community dynamics. Both phenotypic traits and environmental conditions are predicted to influence individual specialization; however, its adaptive consequences are poorly understood, particularly among large mammalian carnivores that play an important role in shaping ecosystems. We used observations of 2,960 kills made by 49 leopards Panthera pardus in the Sabi Sand Game Reserve, South Africa, to quantify the magnitude of individual dietary specialization in a solitary large carnivore, and to examine the proximate and ultimate drivers of this behaviour. We found evidence of individual specialization in leopard diet, with respect to both the species and size of prey killed. Males tended to be more specialized than females, likely because they could access a wider range of prey due to larger body size. Similarly, individuals that encountered a greater diversity of prey tended to be more specialized. Our results confirmed that ecological opportunity was a key determinant of individual specialization; however, contrary to predictions, per capita resource availability (and by extension, intraspecific competition) did not affect the degree of specialization exhibited by individuals. Surprisingly, dietary specialization appeared to disadvantage male leopards. Specialist males overlapped with fewer resident females, had fewer cubs born on their home ranges and had fewer cubs survive to independence on their home ranges than generalist males. This may have resulted from the high degree of environmental stochasticity experienced during our study, as dietary specialization is expected to advantage individuals more during periods of resource predictability. In summary, we showed that a species usually considered to be a dietary generalist was in fact a heterogeneous collection of specialist and generalist individuals. Individual specialization is typically assumed to be maintained by disruptive and/or fluctuating selection; hence, the somewhat paradoxical coexistence of both in the same population might be explained by a dynamic evolutionary equilibrium that exists between specialists and generalists, in which each benefit under different conditions.

Risk alleles for tuberculosis infection associate with reduced immune reactivity in a wild mammalian host.

Integrating biological processes across scales remains a central challenge in disease ecology. Genetic variation drives differences in host immune responses, which, along with environmental factors, generates temporal and spatial infection patterns in natural populations that epidemiologists seek to predict and control. However, genetics and immunology are typically studied in model systems, whereas population-level patterns of infection status and susceptibility are uniquely observable in nature. Despite obvious causal connections, organizational scales from genes to host outcomes to population patterns are rarely linked explicitly. Here we identify two loci near genes involved in macrophage (phagocyte) activation and pathogen degradation that additively increase risk of bovine tuberculosis infection by up to ninefold in wild African buffalo. Furthermore, we observe genotype-specific variation in IL-12 production indicative of variation in macrophage activation. Here, we provide measurable differences in infection resistance at multiple scales by characterizing the genetic and inflammatory variation driving patterns of infection in a wild mammal.

Species-specific drought impacts on black and white rhinoceroses.

Unrelenting poaching to feed the illegal trafficking of rhinoceros (rhino) horn remains the principle threat to the persistence of south-central black and southern white rhino that live in the Kruger National Park (Kruger), South Africa. Other global environmental change drivers, such as unpredictable climatic conditions, impose additional uncertainties on the management and persistence of these species. The drought experienced in Kruger over the 2015/2016 rainy season may have affected rhino population growth and thus added an additional population pressure to the poaching pressure already occurring. Under drought conditions, reduced grass biomass predicts increased natural deaths and a subsequent decrease in birth rate for the grazing white rhino. Such variance in natural death and birth rates for the browsing black rhino are not expected under these conditions. We evaluated these predictions using rhino population survey data from 2013 to 2017. Comparisons of natural deaths and birth rates between pre- (2013/2014 and 2014/15), during- (2015/2016) and post-drought (2016/2017) periods in Kruger showed increased natural mortality and decreased births for white rhino, but no significant changes for black rhino, supporting our predictions. As a result, despite reduced poaching rates, the total mortality rate of white rhino remains significantly higher than the birth rate. Decreased poaching, decreased natural deaths and no apparent drought effects in black rhino resulted in a lower total mortality rate than the estimated birth rate in 2017. Active biological management and traditional anti-poaching initiatives together therefore represent the most likely way to buffer the impacts of decreased population growth through climate change and wildlife crime on the persistence of rhinos.

Context-dependent costs and benefits of tuberculosis resistance traits in a wild mammalian host.

Disease acts as a powerful driver of evolution in natural host populations, yet individuals in a population often vary in their susceptibility to infection. Energetic trade-offs between immune and reproductive investment lead to the evolution of distinct life history strategies, driven by the relative fitness costs and benefits of resisting infection. However, examples quantifying the cost of resistance outside of the laboratory are rare. Here, we observe two distinct forms of resistance to bovine tuberculosis (bTB), an important zoonotic pathogen, in a free-ranging African buffalo (Syncerus caffer) population. We characterize these phenotypes as "infection resistance," in which hosts delay or prevent infection, and "proliferation resistance," in which the host limits the spread of lesions caused by the pathogen after infection has occurred. We found weak evidence that infection resistance to bTB may be heritable in this buffalo population (h 2 = 0.10) and comes at the cost of reduced body condition and marginally reduced survival once infected, but also associates with an overall higher reproductive rate. Infection-resistant animals thus appear to follow a "fast" pace-of-life syndrome, in that they reproduce more quickly but die upon infection. In contrast, proliferation resistance had no apparent costs and was associated with measures of positive host health-such as having a higher body condition and reproductive rate. This study quantifies striking phenotypic variation in pathogen resistance and provides evidence for a link between life history variation and a disease resistance trait in a wild mammalian host population.

Toll-like receptor (TLR) diversity influences mycobacterial growth in African buffalo.

Understanding the role of wildlife in the maintenance or spread of emerging infectious diseases is a growing priority across the world. Bovine tuberculosis (BTB) is a chronic, infectious disease caused by Mycobacterium bovis (M. bovis). BTB is widespread within game reserves in southern Africa, and within these ecosystems the primary wildlife host of this disease is the African buffalo. We used a modified bacterial killing assay for mycobacteria to investigate the effect of Toll-like receptor (TLR) genetic diversity and demographic parameters on the ability of African buffalo to restrict mycobacterial growth. Eosinophil count, time delay, bovine PPD response and avian PPD response were negatively correlated with mycobacterial growth. TLR6 diversity and the interaction of age group and sex were positively correlated with mycobacterial growth. Our results suggest that both demographic and individual immune parameters influence the ability to control mycobacterial infection in African buffalo. TLR6 diversity is particularly interesting as this locus has also shown associations with BTB in cattle, suggesting that further research into the effects, selection and role of TLR6 variants in bovine tuberculosis will be productive.

The complete genome sequence of the African buffalo (Syncerus caffer).

BACKGROUND: The African buffalo (Syncerus caffer) is an important role player in the savannah ecosystem. It has become a species of relevance because of its role as a wildlife maintenance host for an array of infectious and zoonotic diseases some of which include corridor disease, foot-and-mouth disease and bovine tuberculosis. To date, no complete genome sequence for S. caffer had been available for study and the genomes of other species such as the domestic cow (Bos taurus) had been used as a proxy for any genetics analysis conducted on this species. Here, the high coverage genome sequence of the African buffalo (S. caffer) is presented. RESULTS: A total of 19,765 genes were predicted and 19,296 genes could be successfully annotated to S. caffer while 469 genes remained unannotated. Moreover, in order to extend a detailed annotation of S. caffer, gene clusters were constructed using twelve additional mammalian genomes. The S. caffer genome contains 10,988 gene clusters, of which 62 are shared exclusively between B. taurus and S. caffer. CONCLUSIONS: This study provides a unique genomic perspective for the S. caffer, allowing for the identification of novel variants that may play a role in the natural history and physiological adaptations.

Bovine TB in livestock and wildlife: what's in the genes?

Bovine tuberculosis (BTB) is a chronic, infectious disease found in domestic livestock and wildlife. It is caused predominantly by Mycobacterium bovis, which forms part of the Mycobacterium tuberculosis complex. BTB has serious implications for the movement of animals and animal products, biodiversity, and public health and is of significant economic concern. The existence of wildlife maintenance hosts makes it extremely difficult to eradicate BTB, even when established control strategies are in place, creating the need for alternative methods for controlling this disease. There are multiple factors that influence the outcome of infection by a pathogen, one of which is the host's genome. The identification of genetic variants involved in the susceptibility to BTB would supply a new selection of potential drug targets as well as the possibility for the breeding of animals with greater disease resistance. In this review, we collate the results of the BTB heritability and association studies performed in cattle and wildlife, discuss considerations and other methodologies (such as gene expression work) to be taken into account when performing genetic studies, and make some recommendations for future work in this area.

Gene polymorphisms in African buffalo associated with susceptibility to bovine tuberculosis infection.

Bovine tuberculosis (BTB) is a chronic, highly infectious disease that affects humans, cattle and numerous species of wildlife. In developing countries such as South Africa, the existence of extensive wildlife-human-livestock interfaces poses a significant risk of Mycobacterium bovis transmission between these groups, and has far-reaching ecological, economic and public health impacts. The African buffalo (Syncerus caffer), acts as a maintenance host for Mycobacterium bovis, and maintains and transmits the disease within the buffalo and to other species. In this study we aimed to investigate genetic susceptibility of buffalo for Mycobacterium bovis infection. Samples from 868 African buffalo of the Cape buffalo subspecies were used in this study. SNPs (n = 69), with predicted functional consequences in genes related to the immune system, were genotyped in this buffalo population by competitive allele-specific SNP genotyping. Case-control association testing and statistical analyses identified three SNPs associated with BTB status in buffalo. These SNPs, SNP41, SNP137 and SNP144, are located in the SLC7A13, DMBT1 and IL1α genes, respectively. SNP137 remained significantly associated after permutation testing. The three genetic polymorphisms identified are located in promising candidate genes for further exploration into genetic susceptibility to BTB in buffalo and other bovids, such as the domestic cow. These polymorphisms/genes may also hold potential for marker-assisted breeding programmes, with the aim of breeding more BTB-resistant animals and herds within both the national parks and the private sector.

Novel SNP Discovery in African Buffalo, Syncerus caffer, using high-throughput Sequencing.

The African buffalo, Syncerus caffer, is one of the most abundant and ecologically important species of megafauna in the savannah ecosystem. It is an important prey species, as well as a host for a vast array of nematodes, pathogens and infectious diseases, such as bovine tuberculosis and corridor disease. Large-scale SNP discovery in this species would greatly facilitate further research into the area of host genetics and disease susceptibility, as well as provide a wealth of sequence information for other conservation and genomics studies. We sequenced pools of Cape buffalo DNA from a total of 9 animals, on an ABI SOLiD4 sequencer. The resulting short reads were mapped to the UMD3.1 Bos taurus genome assembly using both BWA and Bowtie software packages. A mean depth of 2.7× coverage over the mapped regions was obtained. Btau4 gene annotation was added to all SNPs identified within gene regions. Bowtie and BWA identified a maximum of 2,222,665 and 276,847 SNPs within the buffalo respectively, depending on analysis method. A panel of 173 SNPs was validated by fluorescent genotyping in 87 individuals. 27 SNPs failed to amplify, and of the remaining 146 SNPs, 43-54% of the Bowtie SNPs and 57-58% of the BWA SNPs were confirmed as polymorphic. dN/dS ratios found no evidence of positive selection, and although there were genes that appeared to be under negative selection, these were more likely to be slowly evolving house-keeping genes.