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doi: 10.1038/srep41417.

Extinctions, genetic erosion and conservation options for the black rhinoceros (Diceros bicornis)

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Extinctions, genetic erosion and conservation options for the black rhinoceros (Diceros bicornis)

Yoshan Moodley et al. Sci Rep..

Abstract

The black rhinoceros is again on the verge of extinction due to unsustainable poaching in its native range. Despite a wide historic distribution, the black rhinoceros was traditionally thought of as depauperate in genetic variation, and with very little known about its evolutionary history. This knowledge gap has hampered conservation efforts because hunting has dramatically reduced the species' once continuous distribution, leaving five surviving gene pools of unknown genetic affinity. Here we examined the range-wide genetic structure of historic and modern populations using the largest and most geographically representative sample of black rhinoceroses ever assembled. Using both mitochondrial and nuclear datasets, we described a staggering loss of 69% of the species' mitochondrial genetic variation, including the most ancestral lineages that are now absent from modern populations. Genetically unique populations in countries such as Nigeria, Cameroon, Chad, Eritrea, Ethiopia, Somalia, Mozambique, Malawi and Angola no longer exist. We found that the historic range of the West African subspecies (D. b. longipes), declared extinct in 2011, extends into southern Kenya, where a handful of individuals survive in the Masai Mara. We also identify conservation units that will help maintain evolutionary potential. Our results suggest a complete re-evaluation of current conservation management paradigms for the black rhinoceros.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1. Decrease in black rhinoceros numbers and the distribution of the species across sub-Saharan Africa.
(a) Decreases in black rhinoceros numbers across Africa in the latter half of the 20th century. Dashed lines indicate extant aboriginal populations. Data from the African Rhino Specialist Group (AfRSG) and (b) Range-wide distribution of the black rhinoceros in sub-Saharan Africa. Subspecies mapped are according to du Toit (1987) and this is thestatus quo for conservation management by the AfRSG. This map was created using the following R packages: geoR, raster, rgdal and maptools.
Figure 2
Figure 2. Phylogenetic and network analyses.
(a) Bayesian phylogeny of 64 mitochondrial DNA (mtDNA) control region haplotypes, obtained from a sample of 403 individual sequences. The maximum clade credibility tree was constructed from the combined posterior tree sample of five independent runs. Only branches with a posterior probability of 1 are shown. Lineages are labelled along each branch. Haplotypes coloured in black were isolated from at least one extant individual, whereas haplotypes from red were isolated only from museum samples, assumed extinct and (b) median-joining network of 64 mitochondrial DNA (mtDNA) control region haplotypes showing haplogroup relationships. Each white and/or red filled circle denotes a haplotype, the size of each circle is proportional to the frequency at which that haplotype was observed in the data set, and the proportion of red/white fill is the ratio of museum/extant samples belonging to each haplotype. Small black circles denote median vectors. Small black lines denote the number of mutation steps separating distant haplotypes. All other haplotypes are separated by one or two mutations. Both phylogeny and network show support for seven reciprocally monophyletic haplogroups (WW, NE, CV, EA, CE, RU, SN), but spatial structuring increased resolution to nine haplogroups, adding SE and SW. Spatially informed haplogroups are colour coded and superimposed onto both phylogeny and network. WW, west of the Shari-Logone River system; CV, east of the Shari-Logone to East Africa; NE, North-East Africa; EA, East Africa to the Zambezi River; CE, Central Africa to the Zambezi River; RU, Ruvuma region between Kilombero and Shire Rivers; SN, Southern Africa (Northern); SE, Southern Africa (Eastern); SW, Southern Africa (Western).
Figure 3
Figure 3. Extinctions and genetic erosion at historic localities across the black rhinoceros’ range and how these map onto surviving populations.
n = number of samples, H = number of haplotypes, PH = number of private haplotypes, SH = number of surviving haplotypes, SPH = number of surviving private haplotypes. Localities in red are globally or genetically extinct and those in blue are locally extinct. Only localities in black are still extant. Black arrows map shared haplotypes between locally-defined historic populations and extant populations. Red arrows, genetic erosion by extralimital introduction of the KwaZulu-Natal population; blue arrows, genetic erosion by extralimital introduction of Koakoland-Damaraland population; green arrows, reintroduction of the Zambezi Valley-Sebungwe population to South Africa.
Figure 4
Figure 4. Bayesian skyline method for estimating demographic history from mitochondrial DNA (mtDNA) sequences.
(af) Bayesian skyline plots showing changes in effective size over recent time for each of the five extant populations and the species overall. Solid black lines indicate the posterior density of the effective population size (Ne) estimates, and dashed grey lines indicate the 95% highest posterior density (HPD) intervals. Time in years on the x-axis represents time in years from the present.
Figure 5
Figure 5. Range-wide nuclear genetic structure of the black rhinoceros.
(a) Bayesian population assignments carried out from microsatellite data in Structure using the admixture model revealed five population groups and (b) spatially informed population assignment carried out in BAPS revealed a sixth population in the Victoria Nyanza Basin. Populations are labelled by extant stock or by country of origin, colour coding is as in Fig. 2.
Figure 6
Figure 6. Historic ranges of nine black rhinoceros mitochondrial DNA (mtDNA) haplogroups.
(ai) Bayesian spatial structure of each haplogroup was interpolated onto separate range-wide distribution maps, thereby defining the historic distributions of each haplogroup. Colour coding of spatially informed haplogroups follows Fig. 2. 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, raster, rgdal and maptools.
Figure 7
Figure 7. Historic distribution of six nuclear DNA (nDNA) black rhinoceros populations.
(af) Structure of each populations was interpolated onto separate range-wide distribution maps, defining the historic distributions of each population. Colour coding follows Fig. 2. Small black dots are sampling locations. 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. Maps were created using the following R packages: geoR, raster, rgdal and maptools.
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