Abstract
Multigenerational pedigrees have been developed for free-ranging populations of many species, are frequently used to describe mating systems, and are used in studies of quantitative genetics. Here, we document the development of a 4449-individual pedigree for the Western Hudson Bay subpopulation of polar bears (Ursus maritimus), created from relationships inferred from field and genetic data collected over six generations of bears sampled between 1966 and 2011. Microsatellite genotypes for 22–25 loci were obtained for 2945 individuals, and parentage analysis was performed using the program FRANz, including additional offspring–dam associations known only from capture data. Parentage assignments for a subset of 859 individuals were confirmed using an independent medium-density set of single nucleotide polymorphisms. To account for unsampled males in our population, we performed half-sib–full-sib analysis to reconstruct males using the program COLONY, resulting in a final pedigree containing 2957 assigned maternities and 1861 assigned paternities with only one observed case of inbreeding between close relatives. During genotyping, we identified two independently captured 2-year-old males with identical genotypes at all 25 loci, showing—for the first time—a case of monozygotic twinning among polar bears. In addition, we documented six new cases of cub adoption, which we attribute to cub misidentification or misdirected maternal care by a female bereaved of her young. Importantly, none of these adoptions could be attributed to reduced female vigilance caused by immobilization to facilitate scientific handling, as has previously been suggested.
Similar content being viewed by others
References
Amstrup SC (1993) Human disturbances of denning polar bears in Alaska. Arctic 46:246–250. doi:10.14430/arctic1349
Anderson AE, Wallmo OC (1984) Odocoileus hemionus. Mamm Species 219:1–9. doi:10.2307/3504024
Atkinson SN, Cattet MRL, Polischuk SC, Ramsay MA (1996) A case of offspring adoption in free-ranging polar bears (Ursus maritimus). Arctic 49:94–96. doi:10.14430/arctic1187
Belikov SE (1976) Behavioral aspects of the polar bear, Ursus maritimus. Bears Their Biol Manag 3:37–40. doi:10.2307/3872752
Bellemain E, Zedrosser A, Manel S, Waits LP, Taberlet P, Swenson JE (2006) The dilemma of female mate selection in the brown bear, a species with sexually selected infanticide. Proc R Soc B 273:283–291. doi:10.1098/Rspb.2005.3331
Bulmer MG (1970) The biology of twinning in man. Clarendon Press, Oxford
Calvert W, Ramsay MA (1998) Evaluation of age determination of polar bears by counts of cementum growth layer groups. Ursus 10:449–453. doi:10.2307/3873156
Carmichael L, Nagy JA, Strobeck C (2009) Monozygotic twin wolves with divergent life histories. Arctic 61:329–331. doi:10.14430/arctic29
Clutton-Brock TH, Albon SD, Guinness FE (1989) Fitness costs of gestation and lactation in wild mammals. Nature 337:260–262. doi:10.1038/337260a0
Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Costello CM, Creel SR, Kalinowski ST, Vu NV, Quigley HB (2008) Sex-biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses. Mol Ecol 17:4713–4723. doi:10.1111/j.1365-294X.2008.03930.x
Creel SR, Monfort SL, Wildt DE, Waser PM (1991) Spontaneous lactation is an adaptive result of pseudopregnancy. Nature 351:660–662. doi:10.1038/351660a0
Crompton AE, Obbard ME, Petersen SD, Wilson PJ (2014) Corrigendum to “Population genetic structure in polar bears (Ursus maritimus) from Hudson Bay, Canada: Implications of future climate change” [Biol. Conserv. 141(10) (2008) 2528–2539]. Biol Conserv 179:152. doi: 10.1016/j.biocon.2014.08.015
Cronin MA, Shideler R, Waits L, Nelson RJ (2005) Genetic variation and relatedness on grizzly bears in the Prudhoe Bay region and adjacent areas in northern Alaska. Ursus 16:70–84. doi:10.2192/1537-6176(2005)016[0070:Gvarig]2.0.Co;2
De Barba M, Waits LP, Garton EO, Genovesi P, Randi E, Mustoni A, Groff C (2010) The power of genetic monitoring for studying demography, ecology and genetics of a reintroduced brown bear population. Mol Ecol 19:3938–3951. doi:10.1111/J.1365-294x.2010.04791.X
Derocher AE, Stirling I (1990) Distribution of polar bears (Ursus maritimus) during the ice-free period in western Hudson Bay. Can J Zool 68:1395–1403. doi:10.1139/z90-208
Derocher AE, Stirling I (1996) Aspects of survival in juvenile polar bears. Can J Zool 74:1246–1252. doi:10.1139/z96-138
Derocher AE, Wiig Ø (1999) Observation of adoption in polar bears (Ursus maritimus). Arctic 52:413–415. doi:10.14430/arctic946
Derocher AE, Stirling I, Andriashek D (1992) Pregnancy rates and serum progesterone levels of polar bears in western Hudson Bay. Can J Zool 70:561–566. doi:10.1139/z92-084
Derocher AE, Stirling I, Calvert W (1997) Male-biased harvesting of polar bears in western Hudson Bay. J Wildl Manag 61:1075–1082. doi:10.2307/3802104
Derocher AE, Andersen M, Wiig Ø, Aars J (2010) Sexual dimorphism and the mating ecology of polar bears (Ursus maritimus) at Svalbard. Behav Ecol Sociobiol 64:939–946. doi:10.1007/s00265-010-0909-0
Fricke PM (2001) Review: twinning in dairy cattle. Prof Anim Sci 17:61–67
Gleeson SK, Clark AB, Dugatkin LA (1994) Monozygotic twinning: an evolutionary hypothesis. Proc Natl Acad Sci 91:11363–11367. doi:10.1073/pnas.91.24.11363
Glenn LP, Lentfer JW, Faro JB, Miller LH (1976) Reproductive biology of female brown bears (Ursus arctos), McNeil River, Alaska. Bears Their Biol Manag 3:381–390. doi:10.2307/3872788
Gorrell JC, McAdam AG, Coltman DW, Humphries MM, Boutin S (2010) Adopting kin enhances inclusive fitness in asocial red squirrels. Nat Commun 1:22. doi:10.1038/Ncomms1022
Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. Univeristy of Chicago Press, Chicago, pp 454–471
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372. doi:10.2307/2532296
Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16. doi:10.1016/0022-5193(64)90038-4
Hardy ICW (1995) Protagonists of polyembryony. Trends Ecol Evol 10:179–180. doi:10.1016/S0169-5347(00)89045-X
Hoffman JI, Forcada J (2009) Genetic analysis of twinning in Antarctic fur seals (Arctocephalus gazella). J Mammal 90:621–628. doi:10.1644/08-MAMM-A-264R1.1
Hua P, Zhang L, Zhu G, Jones G, Zhang S, Rossiter SJ (2011) Hierarchical polygyny in multiparous lesser flat-headed bats. Mol Ecol 20:3669–3680. doi:10.1111/j.1365-294X.2011.05192.x
Itoh T, Sato Y, Kobayashi K, Mano T, Iwata R (2012) Effective dispersal of brown bears (Ursus arctos) in eastern Hokkaido, inferred from analyses of mitochondrial DNA and microsatellites. Mamm Study 37:29–41. doi:10.3106/041.037.0104
Jamieson A, Taylor SS (1997) Comparisons of three probability formulae for parentage exclusion. Anim Genet 28:397–400. doi:10.1111/J.1365-2052.1997.00186.X
Johnson PCD, Haydon DT (2007) Maximum-likelihood estimation of allelic dropout and false allele error rates from microsatellite genotypes in the absence of reference data. Genetics 175:827–842. doi:10.1534/Genetics.106.064618
Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. doi:10.1111/J.1755-0998.2009.02787.X
Kearney SR (1989) The polar bear alert program at Churchill, Manitoba. In: Bromley M (ed) Bear-people conflicts: proceedings of a symposium on management strategies. Northwest Territories Department of Renewable Resources, Yellowknife, pp 83–92
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi:10.1016/S0169-5347(02)02489-8
Kompanje EJO, Hermans JJ (2008) Cephalopagus conjoined twins in a leopard cat (Prionailurus bengalensis). J Wildl Dis 44:177–180. doi:10.7589/0090-3558-44.1.177
Livingston JE, Poland BJ (1980) A study of spontaneoulsy aborted twins. Teratology 21:139–148. doi:10.1002/tera.1420210202
Lunn NJ (1986) Observations of nonaggressive behavior between polar bear family groups. Can J Zool 64:2035–2037. doi:10.1139/Z86-307
Lunn NJ, Paetkau D, Calvert W, Atkinson S, Taylor M, Strobeck C (2000) Cub adoption by polar bears (Ursus maritimus): determining relatedness with microsatellite markers. J Zool 251:23–30. doi:10.1111/j.1469-7998.2000.tb00589.x
Lunn NJ, Stirling I, Andriashek D, Richardson E (2004) Selection of maternity dens by female polar bears in western Hudson Bay, Canada and the effects of human disturbance. Polar Biol 27:350–356. doi:10.1007/s00300-004-0604-6
Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766
Malenfant RM, Coltman DW, Davis CS (2015) Design of a 9K Illumina BeadChip for polar bears (Ursus maritimus) from RAD and transcriptome sequencing. Mol Ecol Resour 15:587–600. doi:10.1111/1755-0998.12327
Medill S, Derocher AE, Stirling I, Lunn N, Moses RA (2009) Estimating cementum annuli width in polar bears: identifying sources of variation and error. J Mammal 90:1256–1264. doi:10.1644/08-Mamm-a-186.1
Messier F (2000) Effects of capturing, tagging and radio-collaring polar bears for research and management purposes in Nunavut and Northwest Territories. Department of Biology, University of Saskatchewan, Saskatoon, p 64
Moore J, Ali R (1984) Are dispersal and inbreeding avoidance related? Anim Behav 32:94–112. doi:10.1016/S0003-3472(84)80328-0
Moore JA, Xu R, Frank K, Draheim H, Scribner KT (2015) Social network analysis of mating patterns in American black bears (Ursus americanus). Mol Ecol 24:4010–4022. doi:10.1111/mec.13290
Morrissey MB, Wilson AJ (2010) PEDANTICS: an R package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing. Mol Ecol Resour 10:711–719. doi:10.1111/J.1755-0998.2009.02817.X
Norman AJ, Spong G (2015) Single nucleotide polymorphism-based dispersal estimates using noninvasive sampling. Ecol Evol. doi:10.1002/ece3.1588
Onorato DP, Hellgren EC, Van Den Bussche RA, Skiles JR (2004) Paternity and relatedness of American black bears recolonizing a desert montane island. Can J Zool 82:1201–1210. doi:10.1139/Z04-097
Paterson T, Graham M, Kennedy J, Law A (2012) VIPER: a visualisation tool for exploring inheritance inconsistencies in genotyped pedigrees. BMC Bioinform 13:16. doi:10.1186/1471-2105-13-s8-s5
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295. doi:10.1111/J.1471-8286.2005.01155.X
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539. doi:10.1093/Bioinformatics/Bts460
Pemberton JM (2008) Wild pedigrees: the way forward. Proc R Soc B 275:613–621. doi:10.1098/rspb.2007.1531
Poissant J, Hogg JT, Davis CS, Miller JM, Maddox JF, Coltman DW (2010) Genetic linkage map of a wild genome: genomic structure, recombination and sexual dimorphism in bighorn sheep. BMC Genom. doi:10.1186/1471-2164-11-524
Pond CM, Mattacks CA, Colby RH, Ramsay MA (1992) The anatomy, chemical composition, and metabolism of adipose tissue in wild polar bears (Ursus maritimus). Can J Zool 70:326–341. doi:10.1139/z92-049
Proctor MF, McLellan BN, Strobeck C, Barclay RMR (2004) Gender-specific dispersal distances of grizzly bears estimated by genetic analysis. Can J Zool 82:1108–1118. doi:10.1139/Z04-077
Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11:201–206. doi:10.1016/0169-5347(96)10028-8
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275. doi:10.2307/2409206
Ramsay MA, Stirling I (1986) Long-term effects of drugging and handling free-ranging polar bears. J Wildl Manag 50:619–626. doi:10.2307/3800972
Ramsay MA, Stirling I (1988) Reproductive biology and ecology of female polar bears (Ursus maritimus). J Zool 214:601–634. doi:10.1111/j.1469-7998.1988.tb03762.x
Ramsay MA, Mattacks CA, Pond CM (1992) Seasonal and sex differences in the structure and chemical composition of adipose tissue in wild polar bears (Ursus maritimus). J Zool 228:533–544. doi:10.1111/j.1469-7998.1992.tb04453.x
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reid JM, Arcese P, Sardell RJ, Keller LF (2011) Additive genetic variance, heritability, and inbreeding depression in male extra-pair reproductive success. Am Nat 177:177–187. doi:10.1086/657977
Richardson ES (2014) The mating system and life history of the polar bear. Dissertation, University of Alberta
Richardson E, Branigan M, Calvert W, Cattet M, Derocher AE, Doidge W, Hedman D, Lunn NJ, McLoughlin P, Obbard ME, Stirling I, Taylor M (2006) Research on polar bears in Canada 2001–2004. In: Aars J, Lunn NJ, Derocher AE (eds) Polar bears: proceedings of the 14th working meeting of the IUCN/SSC polar bear specialist group, 20–24 June 2005, Seattle, Washington, USA. IUCN, Gland, pp 117–132
Riedman ML (1982) The evolution of alloparental care and adoption in mammals and birds. Q Rev Biol 57:405–435. doi:10.1086/412936
Riedman ML, Boeuf BJ (1982) Mother-pup separation and adoption in northern elephant seals. Behav Ecol Sociobiol 11:203–215. doi:10.1007/BF00300063
Riester M, Stadler PF, Klemm K (2009) FRANz: reconstruction of wild multi-generation pedigrees. Bioinformatics 25:2134–2139. doi:10.1093/Bioinformatics/Btp064
Riester M, Stadler PF, Klemm K (2010) Reconstruction of pedigrees in clonal plant populations. Theor Popul Biol 78:109–117. doi:10.1016/J.Tpb.05.002
Rode KD, Pagano AM, Bromaghin JF, Atwood TC, Durner GM, Simac KS, Amstrup SC (2014) Effects of capturing and collaring on polar bears: findings from long-term research on the southern Beaufort Sea population. Wildl Res 41:311–322. doi:10.1071/WR13225
Rosing-Asvid A, Born E, Kingsley M (2002) Age at sexual maturity of males and timing of the mating season of polar bears (Ursus maritimus) in Greenland. Polar Biol 25:878–883. doi:10.1007/s00300-002-0430-7
Roulin A (2002) Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. Anim Behav 63:201–208. doi:10.1006/anbe.2001.1895
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/J.1471-8286.2007.01931.X
Saunders BL (2005) The mating system of polar bears in the Central Canadian Arctic. M.Sc. thesis, Queen’s University
Silva del Río N, Kirkpatrick BW, Fricke PM (2006) Observed frequency of monozygotic twinning in Holstein dairy cattle. Theriogenology 66:1292–1299. doi:10.1016/j.theriogenology.2006.04.013
Slate J, Visscher PM, MacGregor S, Stevens D, Tate ML, Pemberton JM (2002) A genome scan for quantitative trait loci in a wild population of red deer (Cervus elaphus). Genetics 162:1863–1873
Spotte S (1982) The incidence of twins in pinnipeds. Can J Zool 60:2226–2233. doi:10.1139/z82-285
Stirling I, Derocher AE (2012) Effects of climate warming on polar bears: a review of the evidence. Global Change Biol 18:2694–2706. doi:10.1111/j.1365-2486.2012.02753.x
Stirling I, Lunn NJ, Iacozza J (1999) Long-term trends in the population ecology of polar bears in western Hudson Bay in relation to climatic change. Arctic 52:294–306. doi:10.14430/arctic935
Szulkin M, Stopher KV, Pemberton JM, Reid JM (2013) Inbreeding avoidance, tolerance, or preference in animals? Trends Ecol Evol 28:205–211. doi:10.1016/j.tree.2012.10.016
Taylor M, Larsen T, Schweinsburg RE (1985) Observations of intraspecific aggression and cannibalism in polar bears (Ursus maritimus). Arctic 38:303–309. doi:10.14430/arctic2149
Taylor MK, McLoughlin PD, Messier F (2008) Sex-selective harvesting of polar bears Ursus maritimus. Wildl Biol 14:52–60. doi:10.2981/0909-6396(2008)14[52:SHOPBU]2.0.CO;2
Taylor RW, Boon AK, Dantzer B, Réale D, Humphries MM, Boutin S, Gorrell JC, Coltman DW, McAdam AG (2012) Low heritabilities, but genetic and maternal correlations between red squirrel behaviours. J Evol Biol 25:614–624. doi:10.1111/j.1420-9101.2012.02456.x
Thiemann GW, Iverson SJ, Stirling I (2008) Polar bear diets and arctic marine food webs: insights from fatty acid analysis. Ecol Monogr 78:591–613. doi:10.1890/07-1050.1
Vibe C (1976) Preliminary report on the second danish polar bear expedition to North East Greenland, 1974. In: Proceedings of the fifth working meeting of the polar bear specialist group. IUCN, Morges, Switzerland, pp 91–97
Viengkone M (2015) Population structure and space-use of Polar bears (Ursus maritimus) in Hudson Bay. Thesis, University of Alberta, M.Sc
Villinger J, Waldman B (2012) Social discrimination by quantitative assessment of immunogenetic similarity. Proc R Soc B 279:4368–4374. doi:10.1098/rspb.2012.1279
Wang JL (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215
Wang JL (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145. doi:10.1111/J.1755-0998.2010.02885.X
Weber DS, Van Coeverden De Groot PJ, Peacock E, Schrenzel MD, Perez DA, Thomas S, Shelton JM, Else CK, Darby LL, Acosta L, Harris C, Youngblood J, Boag P, Desalle R (2013) Low MHC variation in the polar bear: implications in the face of Arctic warming? Anim Conserv 16:671–683. doi:10.1111/acv.12045
Wilkinson GS (1992) Communal nursing in the evening bat, Nycticeius humeralis. Behav Ecol Sociobiol 31:225–235. doi:10.1007/BF00171677
Williams GC (1975) Sex and evolution. Princeton University Press, Princeton
Zedrosser A, Støen O-G, Sæbø S, Swenson JE (2007) Should I stay or should I go? Natal dispersal in the brown bear. Anim Behav 74:369–376. doi:10.1016/j.anbehav.2006.09.015
Zeyl E, Aars J, Ehrich D, Bachmann L, Wiig Ø (2009a) The mating system of polar bears: a genetic approach. Can J Zool 87:1195–1209. doi:10.1139/Z09-107
Zeyl E, Aars J, Ehrich D, Wiig Ø (2009b) Families in space: relatedness in the Barents Sea population of polar bears (Ursus maritimus). Mol Ecol 18:735–749. doi:10.1111/J.1365-294x.2008.04049.X
Acknowledgments
The authors would like to thank the Manitoba Department of Conservation and the Government of Nunavut for providing some of the samples, as well as Dennis Andriashek and Wendy Calvert for long-term data collection and maintenance. We would also like to acknowledge the contributions of Andrew Derocher and the late Malcolm Ramsay, who gathered some of the field data used in this study. DNA extractions for most pre-2006 tissue samples were conducted by Jennifer Bonneville Davis. Robert Cope helpfully recommended the use of the program FRANz. This project was funded by grants to CSD from Environment Canada and by a Natural Sciences and Engineering Research Council Discovery Grant to DWC (Grant ID 312207-2011). RMM is funded by scholarships from Alberta Innovates Technology Futures, the University of Alberta, and the Province of Alberta. Financial and logistical support of the long-term study of polar bears in western Hudson Bay have been provided by Care for the Wild International, the Churchill Northern Studies Centre, Environment Canada, the Isdell Family Foundation, Manitoba Conservation, Natural Sciences and Engineering Research Council, Nunavut Wildlife Research Trust Fund, Parks Canada Agency, the Strategic Technology Applications of Genomics in the Environment (STAGE) funding program, Wildlife Media Inc., World Wildlife Fund (Canada), and World Wildlife Fund Arctic Programme. Josh Miller and Jamie Gorrell provided advice and comments on an earlier version of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical standards
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Environment Canada’s animal-handling procedures were approved annually by their Prairie and Northern Region Animal Care Committee, and all research was conducted under wildlife research permits issued by the Province of Manitoba and by Parks Canada Agency.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Malenfant, R.M., Coltman, D.W., Richardson, E.S. et al. Evidence of adoption, monozygotic twinning, and low inbreeding rates in a large genetic pedigree of polar bears. Polar Biol 39, 1455–1465 (2016). https://doi.org/10.1007/s00300-015-1871-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-015-1871-0