Abstract
Conservation biologists often deal with species that have small, fragmented populations throughout their range, making it necessary to prioritize populations for management. Genetics provides tools to assist with prioritization according to the levels and distribution of genetic diversity and evolutionary distinctiveness. Many studies have used nuclear microsatellite loci to measure genetic diversity in disparate populations and mitochondrial DNA to assess genetic distinctiveness. However, comparing metrics based on microsatellite genotypes ascertained in different laboratories is complicated by the selection of different loci with distinct nucleotide repeat motifs. This issue may be resolved by comparing metrics to a well-characterized reference population with shared microsatellite markers. The Asian elephant, Elephas maximus, is an endangered species with 50–60% of populations in India and Sri Lanka, and small, fragmented populations throughout southeast and insular Asia. We assessed range-wide genetic diversity of the Asian elephant by directly comparing allelic diversity and heterozygosity estimates from 35 populations, overcoming marker selection bias by calibrating metrics to a large population on the Nakai Plateau, Lao PDR, genotyped at 25 loci. We coupled these results with mtDNA analysis to evaluate genetic distinctiveness and identify potential conservation management units. We found the greatest diversity in the populations of southeast Asia and the greatest genetic distinctiveness among the subspecies designations, particularly Borneo and Sumatra, and other southeast Asian populations. The populations of southeast Asia, albeit small, fragmented, and at high risk of extirpation, contain valuable diversity and distinctiveness and are thus of high priority for the preservation of the Asian elephant.
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Data availability
Data from the yardstick population (Nakai Plateau, 25 microsatellite loci) and the R code used to calculate the diversity ratios have been deposited in DRYAD: https://doi.org/10.5061/dryad.vdncjsz11. Genetic diversity data from populations used for comparison to the yardstick population are provided in Table 1. Accession numbers for all mtDNA sequences used in the evolutionary distinctiveness analyses are shown in Supplementary Table 2.
References
Ahlering MA, Hedges S, Johnson A, Tyson M, Schuttler SG, Eggert LS (2011) Genetic diversity, social structure and conservation value of the elephants of the Nakai Plateau, Lao PDR, based on non-invasive sampling. Conserv Genet 12:413–422
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744
Bandelt H, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48
Blake S, Hedges S (2004) Sinking the flagship: the case of forest elephants in Asia and Africa. Conserv Biol 18:1191–1202
Budd K (2021) Conservation genetics of conflict in the asian elephant, Elephas maximus. University of Missouri–Columbia (PhD dissertation). https://doi.org/10.32469/10355/88043
Chakraborty R, Kimmel M, Stivers DN, Davison LJ, Deka R (1997) Relative mutation rates at di-, tri-, and tetranucleotide loci. Proc Nat Acad of Sci USA 94(3):1041–1046
Chakraborty S, Boominathan D, Desai AA, Vidya TNC (2014) Using genetic analyses to estimate population size, sex ratio, and social organization in an asian elephant population in conflict with humans in Alur, southern India. Conserv Genet 15:897–907
Choudhury A, Lahiri Choudhury DK, Desai A, Duckworth JW, Easa PS, Johnsingh AJT, Fernando P, Hedges S, Gunawardena M, Kurt F, Karanth U, Lister A, Menon V, Riddle H, Rübel A, Wikramanayake E, IUCN SSC Asian Elephant Specialist Group (2008) Elephas maximus. IUCN Red List Threat Species. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T7140A12828813.en
Colli L, Milanesi M, Vajana E, Iamartino D, Bomba L, Puglisi F, Del Corvo M, Nicolazzi EL, Ahmed SSE, Herrera JRV, Cruz L, Zhang S, Liang A, Hua G, Yang L, Hao X, Zuo F, Lai S-J, Wang S, Liu R, Gong Y, Mokhber M, Ym Mao, Guan F, Vlaic A, Vlaic B, Ramunno L, Cosenza G, Ahmad A, Soysal I, Ünal E, Ketudat-Cairns M, Garcia JF, Utsunomiya YT, Baruselli PS, Amaral MEJ, Parnpai R, Drummond MG, Galbusera P, Burton J, Hoal E, Yusnizar Y, Sumantri C, Moioli B, Valentini A, Stella A, Williams JL, Ajmone-Marsan P (2018) New insights on water buffalo genomic diversity and post-domestication migration routes from medium density SNP chip data. Front Genet. https://doi.org/10.3389/fgene.2018.00053
Comstock KE, Wasser SK, Ostrander EA (2000) Polymorphic microsatellite DNA loci identified in the african elephant (Loxodonta africana). Mol Ecol 9:1004–1006
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Cracraft J (1982) Geographic differentiation, cladistics, and vicariance biogeography: reconstructing the tempo and mode of evolution. Am Zool 22:411–424. https://doi.org/10.1093/icb/22.2.411
de Groot GA, Nowak C, Skrbinsek T, Andersen LW, Aspi J, Fumagalli L, Godinho R, Harms V, Jansman HAH, Liberg O, Marucco F, Myslajek RW, Nowak S, Pilot M, Randi E, Reinhardt I, Smietana W, Szewczyk M, Taberlet P, Vila C, Munoz-Fuentes V (2016) Decades of population genetic research reveal the need for harmonization of molecular markers: the grey wolf Canis lupus as a case study. Mamm Rev 46:44–59
Duckworth W, Hedges S (1998). Tracking Tigers: a review of the status of tiger, asian elephant, gaur, and banteng in Vietnam, Laos, Cambodia, and Yunnan (China), with recommendations for future conservation action, 1st edn. WWF Indochina Programme, Hanoi
Eggert LS, Ramakrishnan U, Mundy NI, Woodruff DS (2000) Polymorphic microsatellite DNA markers in the african elephant (Loxodonta africana) and their use in the asian elephant (Elephas maximus). Mol Ecol 9:2223–2225
Eggert LS, Beadell JS, McClung A, McIntosh CE, Fleischer RC (2009) Evolution of microsatellite loci in the adaptive radiation of hawaiian honeycreepers. J Hered 100:137–147. https://doi.org/10.1093/jhered/esn111
Eggert LS, Ruiz-Lopez M (2011) Analysis of fecal DNA samples to estimate size and sex ratio of the elephant population at Seima biodiversity conservation area in Cambodia using capture-recapture methods. Report to the Wildlife Conservation Society
Eggert LS, Ruiz-Lopez M (2012a) Analysis of fecal DNA samples to estimate the sex ratio and size of the sepon asian elephant population in the Lao PDR using capture-recapture methods. Report to the Wildlife Conservation Society
Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. https://doi.org/10.1038/nrg1348
Fernando P, Lande R (2000) Molecular genetics and behavioral analysis of social organization in the asian elephant (Elephas maximus). Behav Ecol Sociobiol 48(84):84–91
Fernando P, Pfrender ME, Encalada SE, Lande R (2000) Mitochondrial DNA variation, phylogeography and population structure of the asian elephant. Heredity 84:362–372
Fernando P, Vidya TNC, Melnick DJ (2001) Isolation and characterization of tri- and tetranucleotide microsatellite loci in the asian elephant, Elephas maximus. Mol Ecol Notes 1:232–233
Fernando P, Vidya TNC, Payne J, Stuewe M, Davison G, Alfred RJ, Andau P, Bosi E, Kilbourn A, Melnick DJ (2003) DNA analysis indicates that asian elephants are native to Borneo and are therefore a high priority for conservation. PLoS Biol 1(1):e6
Fleischer RC, Perry EA, Muralidharan K, Stevens EE, Wemmer CM (2001) Phylogeography of the asian elephant (Elephas maximus) based on mitochondrial DNA. Evolution 55(9):1882–1892
Frankham R (2005) Genetics and extinction. Biol Conserv 126(2):131–140
Galtier N, Nabholz B, Glémin S, Hurst GDD (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550
Gobush KS, Edwards CTT, Balfour D, Wittemyer G, Maisels F, Taylor RD (2021) Loxodonta africana. IUCN Red List Threat Species 2021:e.T181008073A181022663
Goossens B, Sharma R, Othman N, Kun-Rodrigues C, Sakong R, Ancrenaz M, Ambu LN, Jue NK, O’Neill RJ, Bruford MW, Chikhi L (2016) Habitat fragmentation and genetic diversity in natural population of the Bornean elephant: implications for conservation. Biol Conserv 196:80–92
Gray TNE, Vidya YNC, Potdar S, Bharti DK, Sovanna P (2014) Population size estimation of an asian elephant population in eastern Cambodia through non-invasive mark-recapture sampling. Conserv Genet 15:803–810
He C, Du J, Zhu D, Zhang L (2020) Population viability analysis of small population: a case study for asian elephant in China. Integr Zool 15:350–362
Hedges S (2006) Conservation. In: Fowler ME, Mikota SK (eds) Biology, Medicine and surgery of elephants. Blackwell Publishing, Oxford, pp 475–490
Hindrikson M, Remm J, Pilot M, Godinho R, Stronen AV, Baltrūnaité L, Cazanomska SD, Leonard JA, Randi E, Nowak C, Åkesson M, López-Bao JV, Álvares F, Llaneza L, Echegaray J, Vilà C, Ozolins J, Rungis D, Aspi J, Paule L, Skrbinšek T, Saarma U (2016) Wolf population genetics in Europe: a systematic review, meta-analysis and suggestions for conservation and management. Biol Rev 92:1601–1629. https://doi.org/10.1111/brv.12298
Hoban S (2018) Integrative conservation genetics: prioritizing populations using climate predictions, adaptive potential and habitat connectivity. Mol Ecol Res 18:14–17. https://doi.org/10.1111/1755-0998.12752
Hoban S, Bruford MW, Funk WC, Galbusera P, Griffith MP, Grueber CE, Heuertz M, Hunter ME, Hvilsom C, Stroil BK, Kershaw F, Khoury CK, Laikre L, Lopes-Fernandes M, MacDonald AJ, Mergeay J, Meek M, Mittan C, Mukassabi TA, O’Brien D, Ogden R, Palma-Silva C, Ramakrishnan U, Segelbacher G, Shaw RE, Sjögren-Gulve P, Veličković N, Vernesi C (2021) Global commitments to conserving and monitoring genetic diversity are now necessary and feasible. Bioscience 71:964–976. https://doi.org/10.1093/biosci/biab054
Holland MM, Parson W (2010) GeneMarker HID: a reliable software tool for the analysis of forensic STR data. J Forensic Sci 56(1):29–35
Isaac NJB, Turvey ST, Collen B, Waterman, Baillie JEM (2007) Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS ONE 2(3):e296
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11):1403–1405
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27(21):3070–3071
Karamanlidis AA, Skrbinsek T, de Gabriel Hernando M, Krambokoukis L, Munoz-Fuentes V, Bailey Z, Nowak C, Stonen AV (2018) History-driven population structure and asymmetric gene flow in a recovering large carnivore at the rear-edge of its european range. Heredity 120:168–182
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Thierer T (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26(11):1463–1464
Kemf E, Jackson P (1995) Asian elephants in the wild. World Wide Fund for Nature, Gland
Khounboline K (2011) Current status of asian elephants in Lao PDR. Gajah 35:4
Kongrit C, Siripunkaw C, Brockelman WY, Akkarapatumwong V, Wright TF, Eggert LS (2008) Isolation and characterization of dinucleotide microsatellite loci in the asian elephant (Elephas maximus). Mol Ecol Res 8:175–177
Kusza S, Suchentrunk F, Pucher H, Mar KU, Zachos FE (2018) High levels of mitochondrial genetic diversity in asian elephants (Elephas maximus) from Myanmar. Hystrix 29:152–154
Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449
Lei R, Brenneman RA, Schmitt DL, Louis EE Jr (2011) Genetic diversity in north american captive asian elephants. J Zool 286:38–47
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116
Leimgruber P, Oo ZM, Myint Aung, Kelly DS, Wemmer C, Senior B, Songer M (2011) Current status of elephants in Myanmar. Gajah 35:76–86
Moritz C (1994) Defining evolutionary significant units for conservation. Trends Ecol Evol 9(10):373–375
Moßbrucker AM, Apriyana I, Fickel J, Imron MA, Pudyatmoko S, Sumardi, Suryadi H (2015) Non-invasive genotyping of Sumatran elephants: implications for conservation. Trop Conserv Sci 8:745–759
Murdoch G (2008) Factbox – Threats Facing Asia’s Endangered Wild Elephants. Reuters, Toronto
Murphy SM, Laufenberg JS, Clark JD, Davidson M, Belant JL, Garshelis DL (2018) Genetic diversity, effective population size, and structure among black bear populations in the Lower Mississippi Alluvial Valley, USA. Conserv Genet 19:1055–1067
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nyakaana S, Arctander P (1998) Isolation and characterization of microsatellite loci in the african elephant, Loxodonta africana. Mol Ecol 7:1436–1437
Osborn FV, Vinton MD (eds) (1999) Proceedings of the Conference: Conservation of the Asian Elephant in Indochina. Hanoi, Vietnam, 24–27 November 1999. FFI-Indochina. Asian Elephant Conservation Programme
Zar JH (2005) Spearman rank correlation. In: Armitage P, Colton T (eds) Encyclopedia of Biostatistics. Wiley, New York. https://doi.org/10.1002/0470011815.b2a15150
Parida J, Sharma R, De R, Kalam T, Sedhupathy A, Digal DK, Reddy PA, Goyal SP, Puyravaud J-P, Davidar P (2022) Genetic characterisation of fragmented asian elephant populations with one recent extinction in its eastern-central indian range. Ecol Genet Genom 24:100132
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at https://www.R-project.org
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237
Roca AL, Georgiadis N, O’Brien SJ (2005) Cytonuclear genomic dissociation in african elephant species. Nat Genet 37:96–100
Sampson C, McEvoy J, Oo ZM, Chit AM, Chan AN, Tonkyn D, Leimgruber P (2018) New elephant crisis in Asia—early warning signs from Myanmar. PLoS ONE 13(3):e0194113
Sharma R, Goossens B, Heller R, Rasterio R, Othman N, Bruford MW, Chikhi L (2018) Genetic analyses favour an ancient and natural origin of elephants on Borneo. Sci Rep 8:880
Skrbinsek T, Jelencic M, Waits LP, Potocnik H, Kos I, Trontelj P (2012) Using a reference population yardstick to calibrate and compare genetic diversity reported in different studies: an example from the brown bear. Heredity 109:299–305
Stanley RRE, Jeffrey NW, Wringe BF, Dibacco C, Bradbury IR (2017) Genepopedit: a simple and flexible tool for manipulating multilocus molecular data in R. Mol Ecol Res 17:12–18
Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland
Thitaram C, Somgird C, Mahasawangkul S, Angkavanich T, Roongsri R, Thongtip N, Colenbrander B, van Steenbeek F, Lenstra J J (2010) Genetic assessment of captive elephant (Elephas maximus) populations in Thailand. Conserv Genet 11:325–330
Thitaram T, Dejchaisri S, Somgrid C, Angkawanish T, Brown J, Phumphuay R, Chomdech S, Kangwanpong D (2015) Social group formation and genetic relatedness in reintroduced asian elephants (Elephas maximus) in Thailand. Appl Anim Behav Sci 172:52–57
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680
Toews DPL, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21:3907–3930
Vidya TNC, Fernando P, Melnick DJ, Sukumar R (2005a) Population differentiation within and among asian elephant (Elephas maximus) population in southern India. Heredity 94:71–80
Vidya TNC, Fernando P, Melnick DJ, Sukumar R (2005b) Population genetic structure and conservation of asian elephants (Elephas maximus) across India. Anim Conserv 8:377–388
Vidya TNC, Varma S, Dang NX, Van Thanh T, Sukumar R (2007) Minimum population size, genetic diversity and social structure of the asian elephant in Cat Tien National Park and its adjoining areas, Vietnam based on molecular genetic analyses. Conserv Genet 8:1471–1478
Vidya TNC, Sukumar R, Melnick DJ (2009) Range-wide mtDNA phylogeography yields insights into the origins of asian elephants. Proc R Soc Lond B 276:893–902
Villesen P (2007) FaBox: an online toolbox for fasta sequences. Mol Ecol Notes 7:965–968
Wiley EO (1978) The evolutionary species concept reconsidered. Syst Zool 27:17–26
Williams C, Tiwari SK, Goswami VR, de Silva S, Kumar A, Baskaran N, Yoganand K, Menon V (2020) Elephas maximus. IUCN Red List Threat Species 2020:e.T7140A45818198
Zhang L, Dong L, Lin L, Feng L, Yan F, Wang L, Guo X, Luo A (2015) Asian elephants in China: estimating population size and evaluating habitat suitability. PLoS ONE 10(5):e0124834
Acknowledgements
We are grateful to the Lao Ministry of Agriculture and Forestry’s Department of Forestry, the Government of Lao PDR’s Provincial and District Agriculture and Forestry Offices (PAFO and DAFO) and the Nam Theun 2 Power Company Ltd. (NTPC) for their assistance with the survey of the Nakai Plateau area. This work would not have been possible without the wildlife survey guides, technicians, and administrative support from the Nam Theun 2 Watershed Management and Protection Authority (WMPA).
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This research was funded by the American Philosophical Society Lewis and Clark Field Grant and the TransWorld Airline Scholarship fund. KB was funded by a National Science Foundation Graduate Research Fellowship. This is KBS contribution number 2355.
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KB designed the study and carried out the labwork, initial data analyses and writing of the first draft of the manuscript. JG and LLS conducted data analyses, data interpretation and contributed substantially to the writing of the final draft of the manuscript. LSE administered the project and contributed to the writing of the final draft of the manuscript. All authors reviewed and approved the final version of the manuscript.
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Budd, K., Gunn, J.C., Sullivan, L.L. et al. Identification of conservation priority units in the Asian elephant, Elephas maximus. Conserv Genet 24, 827–837 (2023). https://doi.org/10.1007/s10592-023-01542-1
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DOI: https://doi.org/10.1007/s10592-023-01542-1