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The Elephants of the Namib Desert Yasuko Ishida1, Peter J

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The Elephants of the Namib Desert Yasuko Ishida1, Peter J Genetic connectivity across marginal habitats: the elephants of the Namib Desert Yasuko Ishida1, Peter J. Van Coeverden de Groot2, Keith E. A. Leggett3,4, Andrea S. Putnam5, Virginia E. Fox6, Jesse Lai2, Peter T. Boag2, Nicholas J. Georgiadis7, and Alfred L. Roca1,8 1Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana IL USA; 2Department of Biology, Queen's University, Kingston, ON Canada; 3Namibian Elephant and Giraffe Trust, Outjo, Namibia; 4Current address: Fowlers Gap Arid Zone Research Station, University of New South Wales, Kensington, NSW, Australia; 5Department of Life Sciences, San Diego Zoo Global, San Diego, CA USA; 6Elephant Human Relations Aid, Swakopmund, Namibia; 7Puget Sound Institute, University of Washington, Tacoma, WA USA; 8Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana IL USA Abstract Results • PCoA did not distinguish desert from Locally isolated populations in marginal habitats may be Mitochondrial DNA Analyses Etosha elephants for any of the first three genetically distinctive and of heightened conservation • In the Caprivi Strip (Fig 1), among eight coordinates (Fig 3B; coordinate 3 not concern. Elephants inhabiting the Namib Desert have been shown) . reported to show distinctive behavioral and phenotypic elephants, there were four CR haplotypes adaptations in that severely arid environment. The genetic identified (Fig 2A) that were not found • The program STRUCTURE did not place distinctiveness of Namibian desert elephants relative to other African savanna elephant (Loxodonta africana) populations has elsewhere across Africa. desert and Etosha elephants into different not been established. To investigate the genetic structure of • Outside the Caprivi Strip, 80 Namibian partitions. elephants in Namibia, we determined the mitochondrial (mt) DNA Fig 3. Genetic analyses control region sequences and genotyped 17 microsatellite loci in elephants carried 4 distinct haplotypes A 0.060 of Namibian elephants desert elephants (n = 8) from the Hoanib River catchment and U (Figs 1, 2A); the two most common using genotypes at 17 0.030 the Hoarusib River catchment. We compared these to the microsatellite loci. r haplotypes were carried by both desert and r 0.000 r genotypes of elephants (n = 77) from other localities in Namibia. (A) Spatial genetic L U The mtDNA haplotype sequences and frequencies among desert autocorrelograms of 55 non-desert elephants. -0.030 L elephants were similar to those of elephants in Etosha National Namibian elephants. The • F was high and significant when Caprivi genetic similarity between -0.060 Park, the Huab River catchment, the Ugab River catchment, and ST 1 2 3 4 5 pairs of individuals (y-axis) is central Kunene, although the geographically distant Caprivi Strip Fig 1. Map showing the sampling locations for Namibian elephants and the Distance Class (End Point) Strip elephants were compared to those of shown relative to their had different mtDNA haplotypes. Likewise, analyses of the mtDNA haplotype distributions. The top panel has a shaded inset map geographic separation (x- microsatellite genotypes of desert-dwelling elephants revealed showing the location of Namibia within southwestern Africa, and the location any other Namibian locality; the values B axis). r: spatial Principal Coordinates Analysis that they were not genetically distinctive from Etosha elephants, of the Namib Desert. In the top panel, Etosha National Park (NP) is shown in were low and not significant when any two autocorrelation coefficient. U: light green, with Etosha Pan in blue. The lower panel shows the Caprivi Strip and there was no evidence for isolation by distance across the upper 95% randomization region of northeast Namibia that is surrounded by Angola, Botswana, populations within Namibia outside of Etosha region. These results, and a review of the historical limits of r. L: lower 95% Zambia, and Zimbabwe. Pie charts show the frequencies of 316 bp record, suggest that a high learning capacity and long-distance Caprivi were compared. randomization limits of r. Non-desert haplotypes of the mtDNA control region for each geographic group. Pop1elephant migrations allowed Namibian elephants to regularly shift their (B) Principal coordinate Pop2 ranges to survive in the face of high variability in climate and in • Three desert elephants and 57 non-desert analysis showing the genetic Coordinate 2 Desert elephant hunting pressure. Methods (continued) elephants primarily from Etosha NP were relationship of Namibian desert elephants (n = 4) to Coordinate 1 Mitochondrial DNA Analyses sequenced for 4258 bp mtDNA. Nine Etosha elephants (n = 51) haplotypes were identified and two of them performed on the genetic distance matrix. Only the first and second Introduction ØHigh-quality DNA: 4258 bp of continuous coordinates are shown here; neither differentiated between desert elephants were carried by both desert and non-desert and Etosha elephants, nor did the third coordinate. Coordinates 1, 2, and 3 • For species with continuous distributions mtDNA sequence from the MT-ND5 gene explained 24.15, 21.22, and 16.06% of the total variance, respectively. elephants. One haplotype is common covering an environmental gradient, higher to the control region (CR) across African savanna localities but the phenotypic plasticity is expected to evolve, ØLow-quality DNA: 316 bp of the control others were specific to Namibia. Conclusions which can enable the invasion of new region • There was no genetic differentiation habitats. Fig 2. Network showing the • Median-joining (MJ) networks were A H76 South-central relationships among evident using mtDNA or microsatellite F clade • The elephants of the Namib Desert constructed (including previously published H03 F subclade mitochondrial haplotype markers between desert-dwelling sequences of elephants represent an opportunity to examine the sequences) using the software Network. from Namibia and across elephants and savanna elephants in other evolution of a peripheral population. H58 Africa. (A) 4258 bp mtDNA regions of Namibia, except the Caprivi • The mtDNA FST between locations within from MT-ND5 to control • The elephants in the Namib Desert were Namibia was calculated using Arlequin ver. S clade region5 and (B) 316 bp of Strip. The Caprivi Strip elephants showed H63 control region sequences. The 1 H77 first documented as early as 1793 . 3.11. number of nucleotide mtDNA differences attributed to geographic Namibian elephants H75 Desert-dwelling differences between Savanna-wide S subclade distance and female matrilocality. • Said to be taller with a leaner build, longer Microsatellite Analyses C. Kunene, Etosha, Ugab, and Huab connected haplotypes is one Caprivi Strip unless otherwise indicated by • Changes in behavior of legs, and larger feet than other savanna • 22 loci were genotyped. Non-Namibian 9 South-central F subclade hatch marks or by a number. desert-dwelling elephants elephants, and described as a separate B F clade Circle sizes are proportionate • Deviation from Hardy-Weinberg equilibrium 12 11 to the haplotype frequency in are likely not due to subspecies, Loxodonta africana 29 8 170 (B), and are numbered in 2 and linkage disequilibrium were tested 75 5 zukowsky . 15 descending order of frequency genetic differences. 12 65 using Genepop 4.2. 25 6 4 within Namibia. For (A), • Despite their genetic • Reported to travel for up to 4 days without 3 frequencies were not available • Observed (Ho) and expected (He) S clade 1 for all haplotypes but were drinking water to access food sources as 7 2 similarity to other available for all Namibian heterozygosity and FST were calculated far as 70 km from waterholes, and also Savanna-wide S subclade elephants. savanna elephants, using Arlequin 3.5.1.3. desert-dwelling elephants engage in thermoregulatory behaviors that Table 1. Population differentiation and FST between Namibian elephants 3 • GenAlEx 6.5 was used to independently are rarely used by elephants elsewhere . Caprivi Desert C. Kunene Etosha Ugab Huab play an irreplaceable role calculate FST and used for principal Caprivi – ** NS ** ** * in the desert ecosystem. coordinates analyses (PCoA) and for tests Desert 0.41* – NS NS NS NS Aim C. Kunene 0.46* 0.05 – NS NS NS of spatial autocorrelation. AcKnowledgments Etosha 0.44** 0.00 0.24 – NS NS We thank the U.S. Fish and Wildlife Service African Elephant Examine whether desert elephants form a • STRUCTURE 2.3.4 was used to infer Ugab 0.68** 0.29 0.10 0.36 – NS Conservation Fund Grant AFE-0778-F12AP01143 for support. We thank population that is genetically different from population structure without the use of prior Huab 0.45* 0.00 0.00 0.15 0.07 – the Ministry of Environment and Tourism of the government of Namibia savanna elephants elsewhere in Namibia. information on locality, under the Analyses are based on 316-bp mtDNA control region sequences. Results of for research permits to collect samples. Elephant photos by Betsy Fox exact tests of population differentiation are above the diagonal, and EHRA. admixture-correlated model, with each and FST results are below the diagonal. iteration using at least 1 million Markov *indicates P < 0.05, **indicates P < 0.01, and NS indicates “not significant” Method chain Monte Carlo generations following a (Bonferroni corrections applied). Geographic groups and samples (Fig 1) burn-in of at least 100,000 steps. Microsatellite Analyses ØDesert (4 blood samples and 14 dung) • 17 loci were polymorphic, not in LD,
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