Conservation - Scientific Papers

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Contrasting evolutionary history, anthropogenic declines and genetic contact in the northern and southern white rhinoceros (Ceratotherium simum)

Yoshan Moodley, Isa-Rita M. Russo, Jan Robovský, Desiré L. Dalton, Antoinette Kotzé, Steve Smith, Jan Stejskal, Oliver A. Ryder, Robert Hermes, Chris Walzer, Michael W. Bruford
Published 7 November 2018.DOI: 10.1098/rspb.2018.1567

Abstract
The white rhinoceros (Ceratotherium simum) has a discontinuous African distribution, which is limited by the extent of sub-Saharan grasslands. The southern population (SWR) declined to its lowest number around the turn of the nineteenth century, but recovered to become the world's most numerous rhinoceros. In contrast, the northern population (NWR) was common during much of the twentieth century, declining rapidly since the 1970s, and now only two post-reproductive individuals remain. Despite this species's conservation status, it lacks a genetic assessment of its demographic history. We therefore sampled 232 individuals from extant and museum sources and analysed ten microsatellite loci and the mtDNA control region. Both marker types reliably partitioned the species into SWR and NWR, with moderate nuclear genetic diversity and only three mtDNA haplotypes for the species, including historical samples. We detected ancient interglacial demographic declines in both populations. Both populations may also have been affected by recent declines associated with the colonial expansion for the SWR, and with the much earlier Bantu migrations for the NWR. Finally, we detected post-divergence secondary contact between NWR and SWR, possibly occurring as recently as the last glacial maximum. These results suggest the species was subjected to regular periods of fragmentation and low genetic diversity, which may have been replenished upon secondary contact during glacial periods. The species's current situation thus reflects prehistoric declines that were exacerbated by anthropogenic pressure associated with the rise of late Holocene technological advancement in Africa. Importantly, secondary contact suggests a potentially positive outcome for a hybrid rescue conservation strategy, although further genome-wide data are desirable to corroborate these results.

1. Introduction
The white rhinoceros (Ceratotherium simum) is the most common of the world's five remaining rhinoceros species. It has borne the brunt of rhinoceros losses during the global acceleration in illegal hunting, which began in 2008 because of increasing demand for horn products in southeast and east Asia. The species is an obligate grazer, thriving historically in two geographically separated grassland areas in sub-Saharan Africa, and has consequently been divided by taxonomists. The southern white rhinoceros (SWR) is endemic to southern Africa, historically occurring in much of the sub-region, south of the Zambezi river, including Namibia, Botswana, Zimbabwe and South Africa (electronic supplementary material, figure S1A,B, after [1]). The northern white rhinoceros (NWR) was endemic to a narrow belt of grassland from west of the Nile River and Albertine Rift, comprising parts of Uganda, South Sudan, the Democratic Republic of the Congo (DRC), Chad and the Central African Republic (electronic supplementary material, figure S1A,B). The recent histories of both populations are well known and independent, and contrastingly reflect events occurring in Africa and the Middle East since the eighteenth century (electronic supplementary material, figure S1C).

In southern Africa, the northwards spread of colonialism from the Cape of Good Hope resulted in the extermination of the SWR across most of the sub-region [2]. Even before the turn of the nineteenth century, the SWR had undergone a population decline so severe that only 100–200 individuals remained, restricted to around the confluence of the Black and White Umfolozi Rivers in Zululand [3]. However, in 1895 colonial authorities declared the white rhinoceros royal game and proclaimed the area the Umfolozi Junction Reserve [4]. With the dedicated conservation action of wildlife authorities in South Africa, this small population increased steadily throughout the twentieth century (electronic supplementary material, figure S1C) to become a conservation success story. The current severe poaching epidemic is threatening to undo these gains, and it is predicted that if present trends continue, the SWR population will start to decline again in 2018 [5]. Efforts to curb recent losses are ineffective with only marginal decreases in poaching rates in 2015 and 2016, with more than 1000 African rhinoceros killed every year since 2013. Such a population contraction, in the absence of gene flow from other sources, could negatively affect the genetic diversity and evolutionary potential of the SWR through genetic drift.

The demographic recovery of the SWR is all the more remarkable because the twentieth century also brought the near eradication of all other rhinoceros populations across the world. The NWR was still common throughout most of its range at the turn of the nineteenth century [6,7], and numbers were still relatively high until the 1960s [8], when demand for rhino horn, mainly on the Arabian peninsula, precipitated the penultimate poaching epidemic. Political instability and ineffective conservation measures during the ensuing period saw the rapid decline of NWR numbers in the wild (electronic supplementary material, figure S1C), with the last wild individuals extirpated in Uganda by 1980 [9], in Sudan by 1984 [8] and finally in Garamba National Park, Democratic Republic of the Congo [10], declared extinct in 2008. The NWR now survives only in captivity, and with two post-reproductive females remaining, its chances of survival look bleak. The imminent extinction of the NWR has sparked several conservation efforts to prevent the loss of what little remains of the population's genetic diversity.

For a complete reading, follow the link: http://rspb.royalsocietypublishing.org/content/285/1890/20181567

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