Colonialism in South Africa leaves a lasting legacy of reduced genetic diversity in Cape buffalo

Abstract

The iconic Cape buffalo has experienced several documented population declines in recent history. These declines have been largely attributed to the late 19th century rinderpest pandemic. However, the effect of the rinderpest pandemic on their genetic diversity remains contentious, and other factors that have potentially affected this diversity include environmental changes during the Pleistocene, range expansions and recent human activity. Motivated by this, we present analyses of whole genome sequencing data from 59 individuals from across the Cape buffalo range to assess present‐day levels of genome‐wide genetic diversity and what factors have influenced these levels. We found that the Cape buffalo has high average heterozygosity overall (0.40%), with the two southernmost populations having significantly lower heterozygosity levels (0.33% and 0.29%) on par with that of the domesticated water buffalo (0.29%). Interestingly, we found that these lower levels are probably due to recent inbreeding (average fraction of runs of homozygosity 23.7% and 19.9%) rather than factors further back in time during the Pleistocene. Moreover, detailed investigations of recent demographic history show that events across the past three centuries were the main drivers of the exceptional loss of genetic diversity in the southernmost populations, coincident with the onset of colonialism in the southern extreme of the Cape buffalo range. Hence, our results add to the growing body of studies suggesting that multiple recent human‐mediated impacts during the colonial period caused massive losses of large mammal abundance in southern Africa.

Continent-wide genomic analysis of the African buffalo (Syncerus caffer)

“…However, the S. c. nanus and South African S. c. caffer Hluhluwe-Umfolozi samples showed high levels of homozygosity, meaning that further population-specific work is required in order to assess inbreeding risk. The S. c. caffer Hluhluwe-Umfolozi population is known to derive from very small number of founder animals, and our finding is in agreement with previous data that has indicated high inbreeding coefficients and low genome-wide heterozygosity levels in this population [9,10].…”

“…in Ruaha and Nyerere NPs) could potentially identify animals that are genetically intermediate between the 'Northern' and 'Southern' clusters, and reveal that there is a steady cline of differentiation within S. c. caffer from North to South, as supported by the isolation-by-distance analysis. The data are consistent with the findings of a previous genomic study of S. c. caffer across its range, which also concluded that there was a primary split between northern and southern S. c. caffer populations approximately 50,000 years ago, followed by gene flow [10].…”

“…The genetic understanding of population diversity and structure across the species range mostly derives from the application of low resolution tools, such as mitochondrial D-loop sequences, microsatellites and mitogenomes [5][6][7], with a more recent study using genome-wide single-nucleotide polymorphisms (SNPs) [8]. The two studies to analyse diversity at the genome level, focused on South African S. c. caffer animals (n=40) in protected areas [9] and S. c. caffer populations (n=59) from East and Southern Africa [10]. These studies have collectively highlighted that the current subspecies classification may not be supported by genetic data, and that there is striking population substructuring within and between the putative subspecies.…”

Extensive population structure highlights an apparent paradox of stasis in the impala (Aepyceros melampus)

“…The genetic diversity in impalas is exceptionally low (range 0.001-0.002), relative to other African mammals such as the African buffalo (0.0026-0.0051, (Quinn et al 2023), warthog (0.0025-0.0035, (Garcia-Erill et al 2022), African leopard (0.0020, (Pečnerová et al 2021), and waterbuck (0.0030-0.0055, (Wang et al 2022). This is surprising, given that impalas are both very abundant (East 1998) and evolutionarily successful, traits typically associated with high population sizes and genetic diversity.…”

Genomic footprints of (pre) colonialism: Population declines in urban and forest túngara frogs coincident with historical human activity

“…Demographic history may also play an important role in shaping contemporary patterns of genomic variation and a population's ability to adapt to environmental changes. Human activity and environmental disturbances on both recent and older timescales may leave a lasting legacy on the pattern of genomic variation (Duvernell et al., 2008; Quinn et al., 2023). For example, low levels of genomic diversity may not be related to contemporary anthropogenic pressures but instead reflect the legacy of historical disturbances such as deforestation and agriculture (Wei et al., 2021) and/or natural environmental disturbances (e.g., population bottlenecks during the Pleistocene; Hewitt, 2000).…”