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Populations are labelled by extant stock or by country of origin, colour coding is as in Fig. The posterior probabilities of population membership were interpolated onto maps to infer the historic distribution of haplogroups. For the mtDNA data set, results were strongly in accordance with the phylogenetic tree and haplotype network Figs 2a and b , Fig. We found the most probable number of spatial clusters in our microsatellite data set to be six Fig.
Colour coding of spatially informed haplogroups follows Fig. Small black dots represent the geographic locations where members of each haplogroup were sampled. Lighter colour gradients within the limits of the historical species range, usually lightest around sampling locations, indicate the regions in which each haplogroup is expected to occur at highest posterior probability. Maps were created using the following R packages: geoR 67 , raster 68 , rgdal 69 and maptools Colour coding follows Fig.
Small black dots are sampling locations.
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Lighter colour gradients within the limits of the historical species range, usually lightest around sampling locations, indicate the regions in which each population is expected to occur at highest posterior probability. We used the inferences above to define units for management of the black rhinoceros. Only one population SE that differentiated through differences in microsatellite allele frequencies Fig. However, since they were sister clades Fig. This is the first study defining the range-wide geographic levels and structure of putatively neutral genetic variation in the black rhinoceros, a highly threatened species for which such an assessment has long been overdue 15 , 32 , This study emphasises the value of historical data in quantifying losses in genetic diversity and inferring effective population size changes across the range of a widely distributed species.
The inclusion of historical material where possible can provide opportunities to investigate demographic histories i. If this study had been conducted on only extant populations, our inferences would certainly have been misled by the widespread extinction of mtDNA lineages and strong post-decline genetic drift, as found in a recent genetic analysis of Indian tigers This is clear by examining a phylogeny that could be reconstructed from just extant samples black lineages; Fig.
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This could suggest histories of differing degrees of population contraction, gene flow and isolation in different parts of the continent. Despite this, the five countries with surviving populations of black rhinoceroses have undergone marked reductions in effective population size Fig. Low levels of genetic variation among these surviving populations were a common feature across all loci, suggesting they resulted from demographic e.
South Africa showed the earliest onset of genetic erosion, inferred as beginning over years ago, whereas decreases in the four other countries were inferred to start within the last years. Similarly, other factors associated with K -selected species such as the high mortality of calves and relatively low reproductive rates 36 have also been responsible for the slow recovery of the species.
By this time, however, South Africa was already a thriving colony for years with much of its wildlife already severely depleted. Today, the remnant KwaZulu-Natal population of South Africa comprises over 2, individuals, all carrying a single mtDNA haplotype 6 leading to speculation about whether this extreme loss in genetic diversity indicated a loss of historic diversity or rather reflected historically low levels of diversity in the region Here, even with a small historic sample, we show that while the historic effective population size in South Africa was among the lowest of the five countries, its pre-bottleneck mtDNA diversity contained six haplotypes Table 1 , which includes a specimen shot in the KwaZulu-Natal province in whose haplotype is not monophyletic with the present day KwaZulu-Natal haplotype.
Namibia also appears to have maintained a lower historic effective population size Fig.
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All five extant populations reached their lowest effective population sizes in the latter part of the 20 th century during the upsurge of illegal hunting of rhinoceroses specifically for their horns. The rhinoceros population of Zimbabwe appears to have reached its lowest effective population size in the last 50 years, but has since recovered to a level similar to that of fifty years previously Fig. This may be credited to the conservation authorities of that country, who recognised the impossibility of protecting the last black rhinoceroses in the Zambezi Valley in the face of unrelenting cross-border poaching from Zambia and Mozambique.
These survivors were translocated out of the valley in the s to more defendable areas within Zimbabwe and subsequently underwent high population growth rates 20 , thus moderating the losses of genetic variation due to drift. We observed the greatest decreases in both effective population size and genetic diversity in East Africa Tanzania and Kenya. The onset of these losses can be inferred to — years ago Fig.
Colonial-era British Kenya and German East Africa Tanzania represented popular venues for big game hunting, with hunting parties touring the region from the late 19 th century 37 , In addition, much land was cleared of game by authorities seeking to establish agriculture in the newly settled colonies. Yet, large numbers of black rhinoceroses were known in East Africa as recently as the early s Therefore, the major declines in diversity and effective population size are likely to have resulted mainly from poaching episode that began in Kenya and Tanzania in the early s.
Dividing the sample into respective local populations improved the resolution of geographic patterns of mtDNA loss. East African populations also featured the highest levels of haplogroup diversity with three populations harbouring up to three mtDNA haplogroups and one, central Tanzania, up to four. The majority of black rhinoceros fossil data, including the oldest known fossil, also originates in this region 41 , and together with its high genetic diversity suggests East Africa as a putative origin for this species.
Other centres of historic haplotype diversity were the Luangwa and Zambezi Valleys in Central southern Africa. Extirpation of seven local populations did not result in the loss of unique mtDNA haplotypes. This is because local extinctions were all within the geographic extent of haplogroups EA and CE north of the Zambezi and SN and SE to the south, and thus shared with populations under more intensive protection in Kenya, Zimbabwe and South Africa.
Therefore, the extant populations in these countries may serve as ideal sources for the reintroduction of black rhinoceroses to those places where they have become locally extinct. We inferred genetic structure from both mtDNA and nuclear microsatellite markers.
Differences in evolutionary dynamics and inheritance between these marker types mean that they often do not detect the same patterns of species-wide genetic structure 42 , Despite this, we were able to infer similar geographic structuring of genetic variation in both marker types. The haplogroups resulting from these early divergences such as WW and NE were not distinguishable from microsatellite allele frequencies.
This could be because high evolutionary rates and constraints in microsatellite allele size are known to result in high homoplasy 44 , 45 suggesting that these nuclear markers reached the limit of their evolutionary resolution among the most phylogenetically divergent lineages L1 and L2. On the other hand, microsatellite loci were able to resolve more recently diverged populations Fig.
This is exemplified by the haplogroup RU, where only mtDNA data were available for most of the historic specimens from the region. This may also help explain why the magnitude of erosion of genetic diversity was much greater for mtDNA than for microsatellites. Maternally inherited mtDNA haplotypes are four times more prone to extinction through genetic drift than nuclear alleles.
A future examination of our extant and historic genetic data set using the greater number of molecular markers afforded by newer generation sequencing technologies and methods that enable reliable data generation from museum specimens e. Taxonomic delineations based on a limited number of morphological characteristics are often not congruent with molecular genetic structure 46 , 47 , 48 , In the black rhinoceros, nDNA and mtDNA structure complemented each other, neither mapped clearly onto any of the major competing subspecies definitions based on geographic differences in skull morphology.
All other major taxonomies invoke a single south-central subspecies D. The geographic isolation of the RU mtDNA haplogroup in the east of this region also suggests additional genetic structuring, however, RU may correspond to D. This specimen from Kommadagga, and another from what is now the Eastern Cape province of South Africa, both clustered within the spatial distribution of the SE haplogroup, together with historic samples from KwaZulu-Natal, the South African Highveld and the extant KwaZulu-Natal haplotype.
Several taxonomists recognised the evolutionary distinctiveness of populations in North-eastern and North-western Africa, but only Spinage 51 hinted that they may be sister taxa. The now extinct NE haplogroup can be associated with D. If this genetic discontinuity was taken to denote subspecies, then the name longipes would correspond to haplogroup CV because it includes a DNA sequence from the type location of this subspecies in Mogrum, which is on the eastern bank of the Shari in Chad.
Limited resources necessitate prioritisation or ranking of management areas for conservation. This may have been partly because of a focus on populations with larger numbers, but also because the idea of distinctiveness was based entirely on taxonomy. Although four of the eight ESUs defined from mtDNA monophyly were geographically distinct, half of them WW and NE are already globally extinct and therefore will not be considered further for conservation. The future of the south-western black rhinoceros looks promising, with high population growth rates it has become even more numerous than the ubiquitous KwaZulu-Natal type However, this success is partly due to introductions from Namibia to the Northern Cape province of South Africa, where the south-western black rhinoceros has become established extralimitally.
In contrast, almost nothing is known about the existence of the small population inhabiting the Selous, but given the recent reports of elephant poaching in Tanzania, it is unlikely that this population still persists. We have therefore listed this population as globally extinct Fig. It is highly unlikely that more than a handful of this genetic lineage exists, and its success may depend on the management of the small Masai Mara-Serengeti black rhinoceros population. EA remains in high frequency in both in situ and ex situ Kenyan populations, so the management of this ESU could be straightforward.
In contrast, the geographic distribution of the CE ESU suggests that it would be best managed by conserving what remains of the black rhinoceros population in Tanzania. This suggests that black rhinoceroses across Kenya were not only more diverse, but also more structured historically, and that recent consolidation by the Kenya Wildlife Service from — into several mixed populations, but which excluded the Masai Mara Muya et al.
Furthermore, the typically KwaZulu-Natal microsatellite profile of one Makueni individual is evidence that this population was not kept as well separated while they were sequestered in South Africa as the public was led to believe.
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