The Evolutionary History of the African Buffalo: Is It Truly a Bovine?

Bovine herpesvirus 4 (BoHV-4) has been isolated from cattle throughout the world, but virological and serological studies have suggested that the African buffalo is also a natural host for this virus. It has previously been found that the Bo17 gene of BoHV-4 was acquired from an ancestor of the African buffalo, probably around 1.5 million years ago. Analysis of the variation of the Bo17 gene sequence among BoHV-4 strains suggested a relatively ancient transmission of BoHV-4 from the buffalo to the Bos primigenius lineage, followed by a host-dependent split between zebu and taurine BoHV-4 strains. In the present study, the evolutionary history of BoHV-4 was investigated by analysis of five gene sequences from each of nine strains representative of the viral species: three isolated from African buffalo in Kenya and six from cattle from Europe, North America and India. No two gene sequences had the same evolutionary tree, indicating that recombination has occurred between divergent lineages; six recombination events were delineated for these sequences. Nevertheless, exchange has been infrequent enough that a clonal evolutionary history of the strains could be discerned, upon which the recombination events were superimposed. The dates of divergence among BoHV-4 lineages were estimated from synonymous nucleotide-substitution rates. The inferred evolutionary history suggests that African buffalo were the original natural reservoir of BoHV-4 and that there have been at least three independent transmissions from buffalo to cattle, probably via intermediate hosts and--at least in the case of North American strains--within the last 500 years.

The reduced cost of next-generation sequencing (NGS) has allowed researchers to generate nuclear and mitochondrial genome data to gain deeper insights into the phylogeography, evolutionary history and biology of non-model species. While the Cape buffalo (Syncerus caffer caffer) has been well-studied across its range with traditional genetic markers over the last 25 years, researchers are building on this knowledge by generating whole genome, population-level data sets to improve understanding of the genetic composition and evolutionary history of the species. Using publicly available NGS data, we assembled 40 Cape buffalo mitochondrial genomes (mitogenomes) from four protected areas in South Africa, expanding the geographical range and almost doubling the number of mitogenomes available for this species. Coverage of the mitogenomes ranged from 154 to 1036X. Haplotype and nucleotide diversity for Kruger National Park (n = 15) and Mokala National Park (n = 5) were similar to diversity levels in southern and eastern Africa. Hluhluwe-iMfolozi Park (n = 15) had low levels of genetic diversity, with only four haplotypes detected, reflecting its past bottleneck. Addo Elephant National Park (n = 5) had the highest nucleotide diversity of all populations across Africa, which was unexpected, as it is known to have low nuclear diversity. This diversity was driven by a highly divergent mitogenome from one sample, which was subsequently identified in another sample via Sanger sequencing of the cytochrome b gene. Using a fossil-calibrated phylogenetic analysis, we estimated that this lineage diverged from all other Cape buffalo lineages approximately 2.51 million years ago. We discuss several potential sources of this mitogenome but propose that it most likely originated through introgressive hybridisation with an extinct buffalo species, either S. acoelotus or S. antiquus. We conclude by discussing the conservation consequences of this finding for the Addo Elephant National Park population, proposing careful genetic management to prevent inbreeding depression while maintaining this highly unique diversity.

The African buffalo (Syncerus caffer) is a wild bovid with a historical distribution across much of sub-Saharan Africa. Genomic analysis can provide insights into the evolutionary history of the species, and the key selective pressures shaping populations, including assessment of population level differentiation, population fragmentation, and population genetic structure. In this study we generated the highest quality de novo genome assembly (2.65 Gb, scaffold N50 69.17 Mb) of African buffalo to date, and sequenced a further 195 genomes from across the species distribution. Principal component and admixture analyses provided little support for the currently described four subspecies. Estimating Effective Migration Surfaces analysis suggested that geographical barriers have played a significant role in shaping gene flow and the population structure. Estimated effective population sizes indicated a substantial drop occurring in all populations 5-10,000 years ago, coinciding with the increase in human populations. Finally, signatures of selection were enriched for key genes associated with the immune response, suggesting infectious disease exert a substantial selective pressure upon the African buffalo. These findings have important implications for understanding bovid evolution, buffalo conservation and population management.

Understanding the dynamics of foot-and-mouth disease virus (FMDV), an endemic and economically constraining disease, is critical in designing control programmes in Africa. This study investigates the evolutionary epidemiology of SAT1 and SAT2 FMDV in Eastern Africa, as well as between cattle and wild African buffalo. Bayesian phylodynamic models were used to analyse SAT1 and SAT2 VP1 gene segments collected between 1975 and 2016, focusing on the SAT1 and SAT2 viruses currently circulating in Eastern Africa. The root state posterior probabilities inferred from our analyses suggest Zimbabwe as the ancestral location for SAT1 currently circulating in Eastern Africa (p=0.67). For the SAT2 clade, Kenya is inferred to be the ancestral location for introduction of the virus into other countries in Eastern Africa (p=0.72). Salient (Bayes factor >10) viral dispersal routes were inferred from Tanzania to Kenya, and from Kenya to Uganda for SAT1 and SAT2, respectively. Results suggest that cattle are the source of the SAT1 and SAT2 clades currently circulating in Eastern Africa. In addition, our results suggest that the majority of SAT1 and SAT2 in livestock come from other livestock rather than wildlife, with limited evidence that buffalo serve as reservoirs for cattle. Insights from the present study highlight the role of cattle movements and anthropogenic activities in shaping the evolutionary history of SAT1 and SAT2 in Eastern Africa. While the results may be affected by inherent limitations of imperfect surveillance, our analysis elucidates the dynamics between host species in this region, which is key to guiding disease intervention activities.

1 Department of Biology, University of Washington, Seattle, WA, USA 2 Department of Fisheries and Wildlife Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA 3 Department of Biology, Valdosta State University, Valdosta, GA, USA 4 New Mexico Museum of Natural History, Albuquerque, NM, USA 5 Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, CO, USA 6 School of Molecular and Life Sciences, University of Limpopo, Sovenga, South Africa

The tick-borne protozoan parasite Theileria parva causes an acute, often fatal disease in cattle throughout a large part of eastern and southern Africa. Infection of African buffalo (Syncerus caffer) is also widespread in this region but does not cause clinical disease in this species. This difference most likely reflects the evolutionary history of the parasites in these species, in that cattle were only introduced into Africa within the last 8000 years. In both hosts, T. parva establishes a carrier state, involving persistence of small numbers of parasites for many months following the acute phase of infection. This persistence is considered important for maintaining the parasite populations. Although cattle and buffalo parasites both produce severe disease when transmitted to cattle, the buffalo-derived parasites are usually not transmissible from infected cattle. Recent studies of the molecular and antigenic composition of T. parva, in addition to demonstrating heterogeneity in the populations in both host species, have revealed that infections in individual animals are genotypically mixed. The results of these studies have also shown that buffalo T. parva exhibit much greater genotypic diversity than the cattle population and indicate that cattle parasites represent a subpopulation of T. parva that has adapted to maintenance in cattle. The parasites in cattle and buffalo appear to be maintained largely as separate populations. This insight into the genotypic composition of T. parva populations has raised important questions on how host adaptation of the parasite has evolved and whether there is scope for further adaptation of buffalo-maintained populations to cattle.

Inferring the past, recent and future evolutionary history of species At the end of the last century, the renowned scientist John Avise introduced the phylogeography concept in reference to the study of the historical principles and processes that govern the geographical distribution of genealogical lineages (Avise et al. 1987; Avise 2000). Considered as a biogeography subdiscipline, phylogeography emphasizes historical aspects of the contemporary distribution of lineages (Avise & Hamrick 1996; Avise 2000; Hewitt & Butlin 1997). Widely studied, climatic changes have been shown to engender major fluctuations in the demography and distribution of wild species on an evolutionary time scale. Climatic changes (e.g. influence of Quaternary climatic fluctuations) sometimes entail long-lasting isolation of populations, subsequently leading to ecological differentiation or speciation (Lister 2004; Vrba 1995a, 1995b). These phylogeographic patterns shape the evolutionary history of contemporary taxa. Phylogeographical studies have flourished over the last few decades, especially in Europe, but not in Africa, although this continent still hosts large megafaunal communities (Barnosky et al. 2004). Understanding how African wildlife responded to climatic changes in the past facilitates the identification of biodiversity hotspots (i.e. glacial refugia), forecasting future population dynamics and developing adapted management strategies.

Combining multiple autosomal introns for studying shallow phylogeny and taxonomy of Laurasiatherian mammals: Application to the tribe Bovini (Cetartiodactyla, Bovidae)

The increased mortality caused by ageing represents a fitness cost to organisms. This paper develops techniques for determining the proportions of that cost that accrue at each age. A variety of analyses using several different sources of data on human ageing—palaeodemographic life tables and life tables from more recent societies with high mortality rates—all suggest that the ‘fitness cost’ of ageing was high during most of our evolutionary history, and was largely due to physiological changes occurring early in adult life. These results imply that predictions about the nature of senescence based on evolutionary theory should be tested using data from middle-aged individuals. They also have implications about the relative importances for human evolution of the ‘pleiotropy’ and ‘mutation-accumulation’ theories of the evolution of senescence, and for the validity of ‘Gompertz’ Law' for the shape of the relationship between mortality and age. An analysis of a life table of the African buffalo suggests that the costs of ageing early in adult life are relatively high in at least one non-human species in its natural environment.

Six highly repeated DNA families were analyzed using Southern blotting and fluorescence in situ hybridization in a comparative study of 46 species of artiodactyls belonging to seven of the eight extant taxonomic families. Two of the repeats, the dispersed bovine-Pst family and the localized 1.715 component, were found to have the broadest taxonomic distributions, being present in all pecoran ruminants (Giraffidae, Cervidae, Antilocapridae, and Bovidae), indicating that these repeats may be 25-40 million years old. Different 1.715 restriction patterns were observed in different taxonomic families, indicating that independent concerted evolution events have homogenized different motifs in different lineages. The other four satellite arrays were restricted to the Bovini and sometimes to the related Boselaphini and Tragelaphini. Results reveal that among the two compound satellites studied, the two components of the 1.711a originated simultaneously, whereas the two components of the 1.711b originated at two different historical times, perhaps as many as 15 million years apart. Systematic conclusions support the monophyly of the infraorder Pecora, the monophyly of the subfamily Bovinae (containing the Boselaphini, Bovini, and Tragelaphini), an inability to resolve any interrelationships among the other tribes of bovids, paraphyly of the genus Bos with respect to Bison, and a lack of molecular variation among two morphologically and ecologically distinct subspecies of African buffaloes (Syncerus caffer cafer and S. c. nanus). Cytogenetically, a reduction in diploid chromosome numbers through centric fusion in derived karyotypes is accompanied by a loss of centromeric satellite DNA. The nilgai karyotype contains an apparent dicentric chromosome as evidenced by the sites of 1.715 hybridization. Telomeric sequences have been translocated to the centromeres without concomitant chromosomal rearrangement in Thompson's gazelle.