Abstract
Weddell seals (Leptonychotes weddellii Lesson) at White Island, Antarctica form a small, completely enclosed, natural population hypothesized to be of recent origin, likely founded by individuals from nearby Erebus Bay. This population constitutes an ideal model to document a founder event and ensuing genetic drift, with implications for conservation. Here we combined historical accounts, census and tagging data since the late 1960s, and genetic data (41 microsatellite loci and mitochondrial DNA sequences) from 84 individuals representing nearly all individuals present between 1990 and 2000 to investigate the history of the founding of the White Island population, document its population dynamics and evaluate possible future threats. We fully resolved parental relationships over three overlapping generations. Cytonuclear disequilibrium among the first generation suggested that it comprised the direct descendants of a founding group. We estimated that the White Island population was founded by a small group of individuals that accessed the island during a brief break in the surrounding sea ice in the mid-1950s, consistent with historical accounts. Direct and indirect methods of calculating effective population size were highly congruent and suggested a minimum founding group consisting of three females and two males. The White Island population showed altered reproductive dynamics compared to Erebus Bay, including highly skewed sex ratio, documented inbred mating events, and the oldest known reproducing Weddell seals. A comparison with the putative source population showed that the White Island population has an effective inbreeding coefficient (F e) of 0.29. Based on a pedigree analysis including the hypothesized founding group, 86% of the individuals for whom parents were known had inbreeding coefficients ranging 0.09–0.31. This high level of inbreeding was correlated with reduced pup survival. Seals at White Island therefore face the combined effects of low genetic variability, lack of immigration, and inbreeding depression. Ultimately, this study provides evidence of the effects of natural isolation on a large, long-lived vertebrate and can provide clues to the potential effects of anthropogenic-caused isolation of similar taxa.
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References
Allendorf FW, Leary RF (1986) Heterozygosity and fitness in natural populations of animals. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, pp 57–76
Armitage AB (1905) Two years in the Antarctic: being a narrative of the British National Antarctic Expedition. Edward Arnold Ltd., London
Boveng PL (1993) Variability in crabeater seal population and the marine ecosystem near the Antarctic Peninsula. Ph.D. Dissertation, Montana State University
Bowcock AM, Ruiz-Linares A, Tomfohrde J et al (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368(6470):455–457. doi:10.1038/368455a0
Cameron MF, Siniff DB (2004) Age-specific survival, abundance, and immigration rates of a Weddell seal (Leptonychotes weddellii) population in McMurdo Sound, Antarctica. Can J Zool 82(4):601–615. doi:10.1139/z04-025
Carmichael LE, Clark W, Strobeck C (2000) Development and characterization of microsatellite loci from lynx (Lynx canadensis), and their use in other felids. Mol Ecol 9(12):2197–2198. doi:10.1046/j.1365-294X.2000.105323.x
Caro TM, Laurenson MK (1994) Ecological and genetic factors in conservation—a cautionary tale. Science 263(5146):485–486. doi:10.1126/science.8290956
Castellini MA, Davis RW, Davis M, Horning M (1984) Antarctic marine life under the McMurdo ice shelf at White Island—a link between nutrient influx and seal population. Polar Biol 2(4):229–231. doi:10.1007/BF00263629
Castellini MA, Davis RW, Kooyman GL (1991) Annual cycles of diving behavior and ecology of the Weddell seal. University of California Press, Berkeley
Caughley G (1959) Observations on the seals of Ross Island during the 1958–1959 summer. Dominion Museum, Wellington
Caughley G (1994) Directions in conservation biology. J Anim Ecol 63(2):215–244. doi:10.2307/5542
Coltman DW, Bowen WD, Wright JM (1996) PCR primers for harbour seal (phoca vitulina concolour) microsatellites amplify polymorphic loci in other pinniped species. Mol Ecol 5(1):161–163. doi:10.1111/j.1365-294X.1996.tb00303.x
Creel S (1998) Social organization and effective population size in carnivores. In: Caro TM (ed) Behavioral ecology and conservation biology. Oxford University Press, New York, pp 246–265
Davis CS, Strobeck C (1998) Isolation, variability, and cross-species amplification of polymorphic microsatellite loci in the family Mustelidae. Mol Ecol 7(12):1776–1778
Davis CS, Gelatt TS, Siniff D, Strobeck A (2002) Dinucleotide microsatellite markers from the Antarctic seals and their use in other Pinnipeds. Mol Ecol Notes 2(3):203–208. doi:10.1046/j.1471-8286.2002.00187.x
Davis RW, Fuiman LA, Williams TM et al (2003) Classification of Weddell seal dives based on 3-dimensional movements and video-recorded observations. Mar Ecol Prog Ser 264:109–122. doi:10.3354/meps264109
Davis CS, Stirling I, Strobeck C, Coltman DW (2008) Population structure of ice-breeding seals. Mol Ecol 17:3078–3094. doi:10.1111/j.1365-294X.2008.03819.x
Eldridge MDB, King JM, Loupis AK et al (1999) Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Conserv Biol 13(3):531–541. doi:10.1046/j.1523-1739.1999.98115.x
Felsenstein J (1993) PHYLIP (phylogeny inference package) Version 3.572. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle
Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327. doi:10.1038/hdy.1997.46
Frankham R (1998) Inbreeding and extinction: Island populations. Conserv Biol 12(3):665–675. doi:10.1046/j.1523-1739.1998.96456.x
Frankham R, Wilcken J (2006) Does inbreeding distort sex-ratios? Conserv Genet 7(6):879–893. doi:10.1007/s10592-006-9129-6
Franklin IR (1980) Evolutionary change in small populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer, Sunderland, pp 135–149
Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1(1):69–70. doi:10.1111/j.1469-1795.1998.tb00228.x
Garbe JR, Da Y (2006) Pedigraph™ Version 2.3. Department of Animal Science, University of Minnesota, Minneapolis
Gelatt TS (2001) Male reproductive success, relatedness, and the mating system of Weddell seals in McMurdo Sound, Antarctica. Ph.D. Dissertation, University of Minnesota
Gelatt TS, Davis CS, Siniff DB, Strobeck C (2001) Molecular evidence for twinning in Weddell seals (Leptonychotes weddellii). J Mammal 82(2):491–499. doi:10.1644/1545-1542(2001)082<0491:MEFTIW>2.0.CO;2
Gemmell NJ, Allen PJ, Goodman SJ, Reed JZ (1997) Interspecific microsatellite markers for the study of pinniped populations. Mol Ecol 6(7):661–666. doi:10.1046/j.1365-294X.1997.00235.x
Gilpin M, Soulé ME (1986) Minimum viable populations: processes of species extinctions. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, pp 19–34
Hadley GL, Rotella JJ, Garrott RA, Nichols JD (2006) Variation in probability of first reproduction of Weddell seals. J Anim Ecol 75(5):1058–1070. doi:10.1111/j.1365-2656.2006.01118.x
Hastings KK (1996) Juvenile survival and maternal strategies of Weddell seals in McMurdo Sound, Antarctica. M.Sc. Dissertation, University of Alaska
Hastings KK, Testa JW (1998) Maternal and birth colony effects on survival of Weddell seal offspring from McMurdo Sound, Antarctica. J Anim Ecol 67(5):722–740. doi:10.1046/j.1365-2656.1998.00242.x
Hastings KK, Testa JW, Rexstad EA (1999) Interannual variation in survival of juvenile Weddell seals (Leptonychotes weddellii) from McMurdo Sound, Antarctica: effects of cohort, sex and age. J Zool (Lond) 248:307–323. doi:10.1111/j.1469-7998.1999.tb01031.x
Hedrick PW (1996) Conservation genetics and molecular techniques: a perspective. In: Smith RB, Wayne RK (eds) Molecular genetic approaches in conservation. Oxford University Press, New York, pp 459–477
Hedrick PW (2005) Genetics of populations, 3rd edn. Jones and Bartlett, Sudbury
Hedrick PW, Lacy RC, Allendorf FW, Soule ME (1996) Directions in conservation biology: comments on caughley. Conserv Biol 10(5):1312–1320. doi:10.1046/j.1523-1739.1996.10051312.x
Hedrick PW, Gutierrez-Espeleta GA, Lee RN (2001) Founder effect in an island population of bighorn sheep. Mol Ecol 10(4):851–857. doi:10.1046/j.1365-294X.2001.01243.x
Heine AJ (1960) Seals at White Island, Antarctica. Antarctic 2:272–273
Heine AJ (1963) Ice breakout around the southern end of Ross Island, Antarctica. NZ J Geol Geophys 6:395–401
Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment. Mol Ecol 16(5):1099–1106. doi:10.1111/j.1365-294X.2007.03089.x
Kluge AG, Farris JS (1969) Quantitative phyletics and the evolution of anurans. Syst Zool 18(1):1–32. doi:10.2307/2412407
Lacy RC, Ballou JD, Princee F (1995) Pedigree analysis for population management. In: Ballou JD, Gilpin M, Foose TJ et al (eds) Population management for survival and recovery. Columbia University Press, New York, pp 57–75
Lande R, Barrowclough GF (1987) Effective population size, genetic variation, and their use in population management. In: Soulé ME (ed) Viable populations for conservation. Cambridge University Press, Cambridge, pp 87–123
MacDonald WJP, Hatherton T (1961) Movement of the Ross Ice Shelf near scott base. J Glaciol 3(29):859–866
Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7(5):639–655. doi:10.1046/j.1365-294x.1998.00374.x
May RM (1995) The cheetah controversy. Nature 374(6520):309–310. doi:10.1038/374309a0
Menotti-Raymond M, O’Brien SJ (1995) Hypervariable genomic variation to reconstruct the natural history of populations—lessons from the big cats. Electrophoresis 16(9):1771–1774. doi:10.1002/elps.11501601293
Nei M, Roychouddhoury AK (1974) Sampling variances of heterozygosity and genetic distance. Genetics 76(2):379–390
Nunney L, Campbell KA (1993) Assessing minimum viable population size—demography meets population genetics. Trends Ecol Evol 8(7):234–239. doi:10.1016/0169-5347(93)90197-W
Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA) n markers for genetic mapping in dog. Genomics 16(1):207–213. doi:10.1006/geno.1993.1160
Packer C, Pusey AE, Rowley H et al (1991) Case study of a population bottleneck—lions of the ngorongoro crater. Conserv Biol 5(2):219–230. doi:10.1111/j.1523-1739.1991.tb00127.x
Paetkau D, Strobeck C (1995) The molecular basis and evolutionary history of a microsatellite null allele in bears. Mol Ecol 4:519–520. doi:10.1111/j.1365-294X.1995.tb00248.x
Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size Version 1.3. Department of Primary Industries and Fisheries, Queensland Government, Queensland
Prebble MM (1967) Ice breakout, McMurdo Sound, Antarctica. NZ J Geol Geophys 11:908–921
Proffitt KM, Garrott RA, Rotella JJ, Wheatley KE (2007) Environmental and senescent related variations in Weddell seal body mass: implications for age-specific reproductive performance. Oikos 116:1683–1690. doi:10.1111/j.0030-1299.2007.16139.x
Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144(1):383–387
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population Genetics Software for exact tests and ecumenicism. J Hered 86(3):248–249
Riedman M (1990) The pinnipeds: seals, sea lions, and walruses. University of California Press, Berkeley
Schreer JF, Hastings KK, Testa JW (1996) Preweaning mortality of Weddell seal pups. Can J Zool 74(9):1775–1778. doi:10.1139/z96-195
Seaver G (1933) Edward Wilson of the Antarctic: naturalist and friend: together with a memoir of Oriana Wilson. John Murray, London
Senner J (1980) Inbreeding depression and survival of zoo populations. In: Soulé ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 209–224
Shaughnessy PD (1969) Transferrin polymorphism and population structure of Weddell seal Leptonychotes weddelli (Lesson). Aust J Biol Sci 22(6):1581–1584
Shields GF, Kocher TD (1991) Phylogenetic relationships of North American ursids based on analysis of mitochondrial DNA. Evol Int J Org Evol 45(1):218–221. doi:10.2307/2409495
Siniff DB, Demaster DP, Hofman RJ, Eberhardt LL (1977) Analysis of dynamics of a Weddell seal population. Ecol Monogr 47(3):319–335. doi:10.2307/1942520
Stewart BS, Yochem PK, Gelatt TS, Siniff DB (2000) Dispersion and habitat use of Weddell seals (Leptonychotes weddelli) in the Ross Sea, Antarctica, during their first year of life. In: Davison WC, Howard-Williams C, Broady P (eds) Antarctic ecosystems: models for wider ecological understanding. Caxton Press, Christchurch, New Zealand, pp 71–76
Stirling I (1966) The seals at White Island: a hypothesis on their origin. Antarctic 4:310–313
Stirling I (1969) Ecology of Weddell Seal in McMurdo Sound, Antarctica. Ecology 50(4):573–586. doi:10.2307/1936247
Stirling I (1971a) Leptonychotes weddelli. Mamm Species 6:1–5. doi:10.2307/3503841
Stirling I (1971b) Variation in sex ratio of newborn Weddell seals during pupping season. J Mammal 52(4):842–844. doi:10.2307/1378943
Stirling I (1971c) Population dynamics of the Weddell seal (Leptonychotes weddelli) in McMurdo Sound, Antarctica, 1966–1968. In: Burt WH (ed) Antarctic pinnipedia. Antarctic research series, vol 18. American Geophysical Union, Washington, pp 141–161
Stirling I (1972) Regulation of numbers of an apparently isolated population of Weddell seals (Leptonychotes weddelli). J Mammal 53(1):107–115. doi:10.2307/1378831
Stuart AW, Bull C (1963) Glaciological observations on the Ross Ice Shelf near scott base, Antarctica. J Glaciol 4(34):399–414
Swithinbank C (1970) Ice movement in the McMurdo Sound area of Antarctica. In: Gow AJ et al. (eds) Proceedings of the international symposium on Antarctic glaciological exploration, Hanover, New Hampshire 3–7 September 1968. International Association of Scientific Hydrology
Testa JW (1994) Over-winter movements and diving behavior of female Weddell seals (Leptonychotes weddellii) in the Southwestern Ross Sea, Antarctica. Can J Zool 72(10):1700–1710. doi:10.1139/z94-229
Testa JW, Scotton BD (1999) Dynamics of an isolated population of Weddell seals (Leptonychotes weddellii) at White Island, Antarctica. J Mammal 80(1):82–90. doi:10.2307/1383210
Testa JW, Siniff DB (1987) Population dynamics of Weddell seals (Leptonychotes weddelli) in McMurdo Sound, Antarctica. Ecol Monogr 57(2):149–165. doi:10.2307/1942622
Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14(11):3335–3352. doi:10.1111/j.1365-294X.2005.02673.x
Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7(2):167–184. doi:10.1007/s10592-005-9100-y
Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Res 8(4):753–756. doi:10.1111/j.1755-0998.2007.02061.x
Waples RS, Yokota M (2007) Temporal estimates of effective population size in species with overlapping generations. Genetics 175(1):219–233. doi:10.1534/genetics.106.065300
Wilson EA (1907) Pinnipedia. In: Natural history. British National Antarctic Expedition 1901–04, vol 2. British Museum, London, pp 1–66
Worsley FA (1931) Endurance: an epic of polar adventure. W.W. Norton, New York
Acknowledgments
Many persons graciously supplied samples, contacts, personal accounts, letters, field notes or pertinent reports, including J. Basset, M. Castellini, M. Crawley, A. DeVries, R. Eisert, L. Fuiman, R. Gee, B. Karl, H. Keys, G. Knox, G. Kooyman, L. Rea, C. Swithinbank, J. W. Testa and P. Wilson. Samples AF31, AF32, AF37 and AF0875 were provided by the University of Alaska museum, frozen tissue collection (J. A. Cook and G. H. Jarrell). We especially thank G. Knox for donating his field journals. M. Castellini, W. Testa and students, University of Alaska, Fairbanks, tagged seals and collected data at White Island, 1990–1994. K. Abernathy, A. Brunet, M. Cameron, C. Counard, S. Dahl, J. Degroot, R. Jensen, R. Johnson, D. McNulty, S. Melin, D. Monson, R. Reichle, B. Stewart and P. Yochem assisted with fieldwork during 1995–1999. R. Garrott, K. Proffitt and students at Montana State University provided recent population data collected since 2000. We thank D. Ainley, B. Dickerson, G. Duke, H. Huber, W. Testa, and two anonymous reviewers for manuscript reviews. Laboratory analyses were performed at the University of Alberta. Logistical support was provided by USAP. All sampling was carried out under US Marine Mammal Permit No. 976 and University of Minnesota Animal Care guidelines. This research was funded by National Science Foundation grants OPP-9420818 and OPP-9725820.
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Gelatt, T.S., Davis, C.S., Stirling, I. et al. History and fate of a small isolated population of Weddell seals at White Island, Antarctica. Conserv Genet 11, 721–735 (2010). https://doi.org/10.1007/s10592-009-9856-6
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DOI: https://doi.org/10.1007/s10592-009-9856-6