High diversity, inbreeding and a dynamic Pleistocene demographic history revealed by African buffalo genomes

Abstract

Genomes retain records of demographic changes and evolutionary forces that shape species and populations. Remnant populations of African buffalo (Syncerus caffer) in South Africa, with varied histories, provide an opportunity to investigate signatures left in their genomes by past events, both recent and ancient. Here, we produce 40 low coverage (7.14×) genome sequences of Cape buffalo (S. c. caffer) from four protected areas in South Africa. Genome-wide heterozygosity was the highest for any mammal for which these data are available, while differences in individual inbreeding coefficients reflected the severity of historical bottlenecks and current census sizes in each population. PSMC analysis revealed multiple changes in Ne between approximately one million and 20 thousand years ago, corresponding to paleoclimatic changes and Cape buffalo colonisation of southern Africa. The results of this study have implications for buffalo management and conservation, particularly in the context of the predicted increase in aridity and temperature in southern Africa over the next century as a result of climate change.

Contrasting genomic consequences of anthropogenic reintroduction and natural recolonisation in high-arctic wild reindeer

“…Inferences of demographic history using RoH length distributions are imprecise because spatial and temporal variation in generation times and the random nature of recombination result in high variation around the mean expected length of RoH (Druet & Gautier 2017). Moreover, sequencing coverage, sequencing error rates, biased genotype likelihood estimates as well as filtering, and parameter settings can all affect estimates of heterozygosity (Fuentes-Pardo & Ruzzante 2017; de Jager et al . 2021; Sánchez-Barreiro et al .…”

A continent-wide high genetic load in African buffalo revealed by clines in the frequency of deleterious alleles, genetic hitchhiking and linkage disequilibrium

“…If so, then we predict low heterozygosity to be genome-region specific (i.e., near male-deleterious alleles) and not genome wide. It is relevant to note here that multilocus heterozygosity at microsatellites is a reliable indicator of genome-wide heterozygosity, considering that relative differences in multilocus heterozygosity among South African populations were similar between genome-wide sequence data and microsatellites (observed heterozygosity genome-wide sequence data: KNP = 0.00324, HiP = 0.00261, Addo NP = 0.00222; multilocus H e microsatellites: KNP = 0.686 [38 loci], HiP = 0.581 [38 loci], Addo NP = 0.447 [18 loci]; S8 Table ) [ 20 , 22 , 68 , 71 , 76 , 77 ].…”

“…Interestingly, pairwise sequentially Markovian coalescent (PSMC) models based on whole-genome sequences indicate relatively high instantaneous coalescence rates since ~20,000 years ago in South Africa, but not in Kenya [ 71 , 72 ]. According to population genetic theory, high coalescence rates are associated with low heterozygosity because heterozygosity is proportional to the coalescent time [ 73 ].…”

“…Long-distance LD appears to occur genome-wide considering that significant LD has earlier been observed in KNP at genomic distances of 7.7–17.9 Mb at three locus pairs (six loci) in a 34 Mb region, occurring on chromosome 5 in cattle ( D ’ = 0.28–0.43; i.e., LD is at 28–43% of its maximum possible value) [ 54 , 68 ]. The observation of long-distance LD in KNP at chromosomal distances ≥ 5.9 Mb is surprising, especially considering that high haploid and autosomal diversity indicate a large historical effective population size for the KNP buffalo (34 mitochondrial D-loop haplotypes with gene diversity H = 0.94; 15 Y-chromosomal haplotypes with H = 0.74; whole-genome sequencing: high genome-wide observed heterozygosity compared to other mammals: H = 0.00324, low median inbreeding coefficient: f = 0.00060) [ 21 , 24 , 71 , 78 ]. According to population genetic theory, a large effective population size limits long-distance LD because of increased LD decay with chromosomal distance [ 62 ].…”

“…c . caffer : ~ 48,000) [ 71 ] and to be stable after their recovery from the rinderpest pandemic of 1889–1895 that decimated buffalo populations across the whole of Africa [ 33 , 88 ]. At face value, this seems to support the view, advocated by some population geneticists, that genetic load and genetic diversity in general play a smaller role in ecology than one might expect [ 6 , 89 ].…”