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Mitochondrial DNA Variation of the Common Hippopotamus: Evidence for a Recent Population Expansion

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Mitochondrial DNA Variation of the Common Hippopotamus: Evidence for a Recent Population Expansion Heredity (2005) 95, 206–215 & 2005 Nature Publishing Group All rights reserved 0018-067X/05 $30.00 www.nature.com/hdy Mitochondrial DNA variation of the common hippopotamus: evidence for a recent population expansion JBA Okello1, S Nyakaana1, C Masembe1, HR Siegismund2 and P Arctander2 1Molecular Biology Laboratory, Makerere University Institute of Environment & Natural Resources, PO Box 7298, Kampala, Uganda; 2Department of Evolutionary Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark Mitochondrial DNA control region sequence variation was revealed by: (i) lack of clear geographical structure among obtained and the population history of the common hippo- haplotypes, (ii) mismatch distributions of pairwise differences potamus was inferred from 109 individuals from 13 localities (r ¼ 0.0053; P ¼ 0.012) and site-frequency spectra, (iii) Fu’s covering six populations in sub-Saharan Africa. In all, 100 neutrality statistics (FS ¼À155.409; Po0.00001) and (iv) Fu haplotypes were defined, of which 98 were locality specific. A and Li’s statistical tests (D * ¼À3.191; Po0.01, F* ¼À2.668; relatively low overall nucleotide diversity was observed P ¼ 0.01). Mismatch distributions, site-frequency spectra and (p ¼ 1.9%), as compared to other large mammals so far neutrality statistics performed at subspecies level also studied from the same region. Within populations, nucleotide supported expansion of Hippopotamus amphibius across diversity varied from 1.52% in Zambia to 1.92% in Queen Africa. We interpret observed common hippopotamus popu- Elizabeth and Masai Mara. Overall, low but significant lation history in terms of Pleistocene drainage overflow and genetic differentiation was observed in the total data set (FST ¼ suggest recognising the three subspecies that were sampled 0.138; P ¼ 0.001), and at the population level, patterns of in this study as separate management units in future differentiation support previously suggested hippopotamus conservation planning. subspecies designations (FCT ¼ 0.103; P ¼ 0.015). Evidence Heredity (2005) 95, 206–215. doi:10.1038/sj.hdy.6800711; that the common hippopotamus recently expanded were published online 20 July 2005 Keywords: mitochondrial DNA; common hippopotamus; control region; variation; population history; recent expansion Introduction appeared in the East African Lower Miocene (Kingdon, 1989). The genus Hippopotamus itself appeared about The common hippopotamus (Hippopotamus amphibius), 2.5 million years ago (Turner and Wood, 1993) and commonly referred to as the hippo, is a semiaquatic was established by the Plio-Pleistocene, evidenced by artiodactyl found in sub-Saharan Africa (Kingdon, 1989; their fossil records (Coryndon, 1970, 1973). This was a Eltringham, 1999). Hippos have become much more period of major climatic changes and regional uplift restricted in their distribution over recent decades as a that influenced large-mammalian evolution in Africa result of rampant hunting by humans for their meat and (deMenocal, 1995; Patridge et al, 1995). ivory and continued harassment by farmers as agricul- Despite the hippo’s popularity, little is known about its tural pest. Only about 157 000 individuals now occur, in general biology, dispersal phase of its life history and its fragmented populations in rivers and lakes within some population genetics (Eltringham, 1999). This has partly protected areas of eastern, western and southern Africa been due to the aquatic and nocturnal habits, and (Eltringham, 1993). Five subspecies of hippos have been difficulty in obtaining samples. Hippos are territorial in proposed (Lydekker, 1915; Grubb, 1993), but this water, where males hold a linear territory consisting of a classification has not been generally accepted (Eltring- shoreline and a narrow strip of the bank that is heavily ham, 1999). Above the species level, recent molecular defended against challenging bulls (Klingel, 1991). The data have supported a sister-group relationship between territorial male has an absolute mating right to the hippopotomids and cetaceans (Ursing and A´ rnason, females attracted to his territory, and this depends on 1998; Gatesy et al, 1999; Matthee et al, 2001; Amrine- the male’s quality and the topographical features of his Madsen et al, 2003). territory (Eltringham, 1999). The average age at puberty The earliest origin of hippopotamuses remains unclear of the common hippopotamus is 7.5 and 9.5 years for (Boisserie, 2005), although the first fossil Hippoptamidae males and females, respectively (Laws and Clough, 1966). Since there is currently an interconnected network of water system in Africa and hippos rely heavily on water in their movement and habitation, a relatively Correspondence: JBA Okello, Molecular Biology Laboratory, Makerere homogenised genetic pattern among hippopotamus University Institute of Environment & Natural Resources, PO Box 7298, populations is expected, albeit with quantifiable histo- Kampala, Uganda. E-mails: [email protected], [email protected] rical signatures. Received 23 April 2005; accepted 7 June 2005; published online 20 Mitochondrial DNA sequence variation has been July 2005 used intensively in phylogeograhic studies, where the A recent population expansion of hippopotamus JBA Okello et al 207 distribution of its haplotypes across the range of a northern Democratic Republic of Congo, extending West species can infer its population history and structure. to Gambia and further south to Tanzania and Mozambi- Phylogeographical studies on many mammals in Africa que. Hippopotamus amphibius tschadensis: populations of have revealed that their genetic structures were influ- this subspecies occur in Chad and Niger. Hippopotamus enced by geological and climatic events of the Pleisto- amphibius kiboko: occur in Kenya and Somalia. Hippopo- cene, which resulted in repeated isolation of populations tamus amphibius capensis: distributed from Zambia south into refugia, and subsequent expansion of the surviving to South Africa. Hippopotamus amphibius constrictus: occur individuals when environmental conditions became in Angola, southern Democratic Republic of Congo and favourable (Arctander et al, 1999; Flagstad et al, 2001; Namibia. Nersting and Arctander, 2001; Muwanika et al, 2003a). Skin biopsy samples were collected from hippos using These climatic events of the Pleistocene are also expected a modified remote biopsy sampling technique of Karesh to have influenced the genetic history of the common et al (1987). A total of 109 samples were collected from hippopotamus, in terms of population reductions and hippopotamuses in national parks and game reserves in subsequent expansion when climate became favourable. eastern and southern Africa covering three of the In this study, we present the first population data on proposed subspecies above (details in Figure 1). Samples hippos in Africa based on patterns of mitochondrial were preserved in 25% dimethylsulphoxide saturated control region sequence variation and infer the popula- with sodium chloride (Amos and Hoelzel, 1991), stored tion processes that have led to the current genetic pattern at ambient temperature in the field and at À801C in the in the species. The above information is necessary in laboratory. formulating an effective management strategy for this highly fragmented but intrinsically charismatic species. DNA extraction, mtDNA amplification and sequencing Total genomic DNA was extracted from samples using DNeasys Tissue Kit (Qiagen) according to the manufac- Methods turer’s instructions. Approximately 530 bp of the 50-end segment of the mitochondrial DNA control region was Distribution and sampling PCR amplified using primers Ham-1 (50-CCACCATCAG The former range of the hippopotamus is shown in CACCCAAA-30) and Ham-2 (50-GAGATGTCTTATT Figure 1, together with sampling localities. The demarca- TAAGGGGAA-30). One primer was 50 biotinylated for tion of the subspecies is not clear and based on national each strand, and both strands were amplified and boundaries. Hippopotamus amphibius amphibius: the nomi- sequenced. Amplifications were carried out in 50 ml nate race is said to occur in southern Sudan, Ethiopia and reaction volumes containing 2–5 ng of genomic DNA, 50 mM dNTPs, 20 pmol of each of the primers, 1 U of Taq DNA polymerase (Boehringer Manheim GmbH) and N 50 mM MgCl2 (Boehringer Manheim GmbH). The fol- lowing cycling parameters were used: one cycle of initial Uganda denaturation at 941C for 5 min, followed by 32 cycles of 2 denaturation at 941C for 1 min, annealing at 461C for 1 1 min and extension at 721C for 2 min. The double- stranded PCR products were cleaned using QIAquickt PCR Purification Kit (Qiagen) and separated into single strands using M-280 streptavidin-coated paramagnetic beads (Dynalt). The single-stranded DNA template was Kenya 11 10 directly sequenced by the dideoxy chain-termination method (Sanger et al, 1977) using Sequenaset 2.0 Kit (United States Biochemical), a35S-dATP (Amersham) and 34 primers complimentary to the template. The sequencing 56 reaction products were electrophoresed in 6% polyacry- 7 Tanzania 12 8 lamide/7 M urea gel, fixed, dried and visualised after 9 13 autoradiography. Zambia Genetic diversity and structure Figure 1 Schematic map showing 13 sampling localities of Sequences were aligned by eye in the program BIOEDIT hippopotamus in eastern and southern Africa. Sampling sites, 5.0.9 (Hall, 1999). The nucleotide diversity, p (Nei, 1987; population and subspecies groupings are: 1, Murchison Falls 10.5) for
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