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

Authors: QUINN, LIAM - University Of Copenhagen; GARCIA-ERILL, GENIS - University Of Copenhagen; SANTANDER, CINDY - University Of Copenhagen; BRUNICHE-OLSEN, ANNA - University Of Copenhagen; LIU, XIAODONG - University Of Copenhagen; SINDING, MIKKEL-HOLGER - University Of Copenhagen; Heaton, Michael - Mike; Smith, Timothy - Tim; PECNEROVA, PATRICA - University Of Copenhagen; BERTOLA, LAURA - University Of Copenhagen; HANGHOJ, KRISTIAN - University Of Copenhagen; RASMUSSEN, MALTHE SEBRO - University Of Copenhagen; DE JAGER, DEON - University Of Copenhagen; SIEGISMUND, HANS - University Of Copenhagen; ALBRECHTSEN, ANDERS - University Of Copenhagen; HELLER, RASMUS - University Of Copenhagen; MOLTKE, IDA - University Of Copenhagen

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/9/2023
Publication Date: 1/18/2023
Citation: Quinn, L., Garcia-Erill, G., Santander, C., Bruniche-Olsen, A., Liu, X., Sinding, M.S., Heaton, M.P., Smith, T.P.L., Pecnerova, P., Bertola, L.D., Hanghoj, K., Rasmussen, M.S., De Jager, D., Siegismund, H.R., Albrechtsen, A., Heller, R., Moltke, I. 2023. Colonialism in Southern Africa leaves a lasting legacy of reduced genetic diversity in Cape buffalo. Molecular Ecology. Article 16851. https://doi.org/10.1111/mec.16851.
DOI: https://doi.org/10.1111/mec.16851

Interpretive Summary: The iconic Cape buffalo has experienced drastic 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 Cape buffalo 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. Here we present analyses of whole genome sequencing of 59 Cape buffalo from across its range to assess present-day levels of genetic diversity and what factors have shaped these levels. The set of available Cape buffalo samples more broadly covered the subspecies range as opposed to only the southern region. This sampling strategy, combined with the use of a whole genome sequencing, provided insights into the levels of genetic diversity and the associated causative factors. Two of the Eight Cape buffalo populations (Addo Elephant National Park and Hluhluwe-iMfolozi Park) had markedly reduced genetic diversity were identified and likely the result of a rapid population decline driven by colonialism. Since the loss of genetic diversity was due to rapid decline, these populations may be in more particular need of management effort, further illustrating the value of this approach in identifying vulnerable species and populations.

Technical 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 heterozy-gosity 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 pop-ulations, 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.