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Searching for genetic evidence of demographic decline in an arctic seabird: beware of overlapping generations

Abstract

Genetic data are useful for detecting sudden population declines in species that are difficult to study in the field. Yet this indirect approach has its own drawbacks, including population structure, mutation patterns, and generation overlap. The ivory gull (Pagophila eburnea), a long-lived Arctic seabird, is currently suffering from rapid alteration of its primary habitat (i.e., sea ice), and dramatic climatic events affecting reproduction and recruitment. However, ivory gulls live in remote areas, and it is difficult to assess the population trend of the species across its distribution. Here we present complementary microsatellite- and SNP-based genetic analyses to test a recent bottleneck genetic signal in ivory gulls over a large portion of their distribution. With attention to the potential effects of population structure, mutation patterns, and sample size, we found no significant signatures of population decline worldwide. At a finer scale, we found a significant bottleneck signal at one location in Canada. These results were compared with predictions from simulations showing how generation time and generation overlap can delay and reduce the bottleneck microsatellite heterozygosity excess signal. The consistency of the results obtained with independent methods strongly indicates that the species shows no genetic evidence of an overall decline in population size. However, drawing conclusions related to the species’ population trends will require a better understanding of the effect of age structure in long-lived species. In addition, estimates of the effective global population size of ivory gulls were surprisingly low (~1000 ind.), suggesting that the evolutionary potential of the species is not assured.

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Fig. 1: Map of the study area illustrating the high-Arctic distribution of ivory gull (Pagophila eburnea) colonies.
Fig. 2: Pairwise comparison of expected heterozygosity (HE) versus expectedheterozygosity.
Fig. 3: Heterozygosity-excess (ΔH) at 15-microsatellite loci in four breeding regions of ivory gull, obtained with Bottleneck software for two mutational models.
Fig. 4: Effect of sample size.
Fig. 5: Likelihood profile of parameters 4NEμ and 4NE,pastμ estimated by Migraine (note the log scale on both axes).
Fig. 6: Temporal dynamics of ΔH calculated from stochastic simulations of microsatellite markers.

Data availability

Genotypic data are deposited in DRYAD: https://doi.org/10.5061/dryad.j0zpc86gk and the raw reads have been deposited in the SRA (Bioproject: PRJNA81085).

References

  • ACIA (2004) Impacts of a Warming Arctic: Arctic Climate Impact Assessment. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Alsos IG, Ehrich D, Thuiller W, Eidesen PB, Tribsch A, Schonswetter P et al. (2012) Genetic consequences of climate change for northern plants. Proc R Soc B-Biol Sci 279:2042–2051

    Article  Google Scholar 

  • Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA (2016) Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet 17:81–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Archer FI, Adams PE, Schneiders BB (2017) strataG: an R package for manipulating, summarizing and analysing population genetic data. Mol Ecol Resour 17:5–11

    Article  CAS  PubMed  Google Scholar 

  • Arenas M, Ray N, Currat M, Excoffier L (2011) Consequences of range contractions and range shifts on molecular diversity. Mol Biol Evol 29:207–218

    Article  PubMed  CAS  Google Scholar 

  • Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benjamini Y, Hochberg Y (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Soc Series B 57:289–300

  • BirdLife International (2018). Pagophila eburnea. The IUCN Red List of Threatened Species 2018: e.T22694473A132555020. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22694473A132555020.en. Downloaded on11 June 2020

  • Boertmann D, Petersen IK, Nielsen HH (2020) Ivory Gull population status in Greenland 2019. Dan Orn Foren Tidsskr 114:141–150

    Google Scholar 

  • Boitard S, Rodríguez W, Jay F, Mona S, Austerlitz F (2016) Inferring population size history from large samples of genome-wide molecular data - an approximate Bayesian computation approach. PLOS Genet 12:1–36

    Article  CAS  Google Scholar 

  • Box JE, Colgan WT, Christensen TR, Schmidt NM, Lund M, Parmentier F-JW et al. (2019) Key indicators of Arctic climate change: 1971–2017. Environ Res Lett 14:045010

    Article  CAS  Google Scholar 

  • Braune BM, Mallory ML, Gilchrist HG (2006) Elevated mercury levels in a declining population of ivory gulls in the Canadian Arctic. Mar Pollut Bull 52:978–982

    Article  CAS  PubMed  Google Scholar 

  • Broquet T, Angelone S, Jaquiéry J, Joly P, Léna JP, Lengagne T et al. (2010) Genetic bottlenecks driven by population disconnection. Conserv Biol 24:1596–1605

    Article  PubMed  Google Scholar 

  • Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186:983–995

    Article  PubMed  PubMed Central  Google Scholar 

  • Collevatti RG, Nabout JC, Diniz-Filho JAF (2011) Range shift and loss of genetic diversity under climate change in Caryocar brasiliense, a Neotropical tree species. Tree Genet Genomes 7:1237–1247

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cotto O, Schmid M, Guillaume F (2020) Nemo-age: spatially explicit simulations of eco-evolutionary dynamics in stage-structured populations under changing environments. Methods Ecol Evol 11:1227–1236

    Article  Google Scholar 

  • Cubaynes S, Doherty PF, Schreiber EA, Gimenez O (2011) To breed or not to breed: a seabird’s response to extreme climatic events. Biol Lett 7:303–306

    Article  PubMed  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994). Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91: 3166–3170

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator V2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445

    Article  CAS  PubMed  Google Scholar 

  • England PR, Cornuet J-M, Berthier P, Tallmon DA, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe biasin small samples. Conserv Genet 7:303

    Article  Google Scholar 

  • Engler JO, Secondi J, Dawson DA, Elle O, Hochkirch A (2016) Range expansion and retraction along a moving contact zone has no effect on the genetic diversity of two passerine birds. Ecography 39:884–893

    Article  Google Scholar 

  • Environment Canada (2014) Recovery Strategy for the Ivory Gull (Pagophila eburnea) in Canada. Species at Risk Act Recovery Strategy Series. Environment Canada, Ottawa. iv+ 21 pp

  • Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. In Carvalho GR (ed) Advances in molecular ecology, 55–85. IOS Press, Burke, Virginia, USA

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1971) Inbreeding and variance effective numbers in populations with overlapping generations. Genetics 168:581–597

    Article  Google Scholar 

  • Fort J, Moe B, Strøm H, Grémillet D, Welcker J, Schultner J et al. (2013) Multicolony tracking reveals potential threats to little auks wintering in the North Atlantic from marine pollution and shrinking sea ice cover. Diversity Distrib 19:1322–1332

    Article  Google Scholar 

  • Fraïsse C, Popovic I, Mazoyer C, Spataro B, Delmotte S, Romiguier J et al. (2021). DILS: Demographic inferences with linked selection by using ABC. Mol Ecol Resourc 21:2629–2644

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genetical Res 66:95–107

    Article  Google Scholar 

  • Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  • Garnier J, Lewis MA (2016) Expansion under climate change: the genetic consequences. Bull Math Biol 78:2165–2185

    Article  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Gavrilo M, Martynova D (2017) Conservation of rare species of marine flora and fauna of the Russian Arctic National Park, included in the Red Data Book of the Russian Federation and in the IUCN Red List. Nat Conserv Res 2:10–42

    Article  Google Scholar 

  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17:167–178

    Article  CAS  PubMed  Google Scholar 

  • Gilchrist HG, Mallory ML (2005) Declines in abundance and distribution of the ivory gull (Pagophila eburnea) in Arctic Canada. Biol Conserv 121:303–309

    Article  Google Scholar 

  • Gilchrist HG, Strøm H, Gavrilo MV, Mosbech A (2008). International ivory gull conservation strategy and action plan. CAFF International Secretariat,Circumpolar Seabird Group (CBird), CAFF Technical Report No. 18

  • Gilg O, Boertmann D, Merkel F, Aebischer A, Sabard B (2009) Status of the endangered ivory gull, Pagophila eburnea, in Greenland. Polar Biol 32:1275–1286

    Article  Google Scholar 

  • Gilg O, Istomina L, Heygster G, Strøm H, Gavrilo M, Mallory ML et al. (2016) Living on the edge of a shrinking habitat: the ivory gull, Pagophila eburnea, an endangered sea-ice specialist. Biol Lett 12:20160277

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilg O, Kovacs KM, Aars J, Fort J, Gauthier G, Gremillet D et al. (2012) Climate change and the ecology and evolution of Arctic vertebrates. Ann N Y Acad Sci 1249:166–190

    Article  PubMed  Google Scholar 

  • Goutte A, Kriloff M, Weimerskirch H, Chastel O (2011) Why do some adult birds skip breeding? A hormonal investigation in a long-lived bird. Biol Lett 7:790–792

    Article  PubMed  PubMed Central  Google Scholar 

  • Guillaume F, Rougemont J (2006) Nemo: an evolutionary and population genetics programming framework. Bioinformatics 22:2556–2557

    Article  CAS  PubMed  Google Scholar 

  • Hill WG (1972) Effective size of populations with overlapping generations. Theor Popul Biol 3:278–289

    Article  CAS  PubMed  Google Scholar 

  • Hoban SM, Mezzavilla M, Gaggiotti OE, Benazzo A, van Oosterhout C, Bertorelle G (2013) High variance in reproductive success generates a false signature of a genetic bottleneck in populations of constant size: a simulation study. BMC Bioinforma 14:309

    Article  Google Scholar 

  • Hoffmann AA, Sgrò CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  PubMed  Google Scholar 

  • Hohenlohe PA, Funk WC, Rajora OP (2021) Population genomics for wildlife conservation and management. Mol Ecol 30:62–82

    Article  PubMed  Google Scholar 

  • Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584

    Article  PubMed  Google Scholar 

  • Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laporte V, Charlesworth B (2002) Effective population size and population subdivision in demographically structured populations. Genetics 162:501–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leblois R, Pudlo P, Néron J, Bertaux F, Reddy Beeravolu C, Vitalis R et al. (2014) Maximum-Likelihood Inference of Population Size Contractions from Microsatellite Data. Mol Biol Evol 31:2805–2823

    Article  CAS  PubMed  Google Scholar 

  • Li H, Durbin R (2011) Inference of human population history from individual whole-genome sequences. Nature 475:493–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Fu Y-X (2015) Exploring population size changes using SNP frequency spectra. Nat Genet 47:555–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lucia M, Verboven N, Strom H, Miljeteig C, Gavrilo MV, Braune BM et al. (2015) Circumpolar contamination in eggs of the high-arctic ivory gull Pagophila eburnea. Environ Toxicol Chem 34:1552–1561

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Mallory ML, Allard KA, Braune BM, Gilchrist HG, Thomas VG (2012) New longevity record for ivory gulls (Pagophila eburnea) and evidence of natal philopatry. Arctic 65:98–101

    Article  Google Scholar 

  • Marandel F, Charrier G, Lamy J-B, Le Cam S, Lorance P, Trenkel VM (2020) Estimating effective population size using RADseq: Effects of SNP selection and sample size. Ecol Evol 10:1929–1937

    Article  PubMed  PubMed Central  Google Scholar 

  • McInerny GJ, Turner JRG, Wong HY, Travis JMJ, Benton TG (2009) How range shifts induced by climate change affect neutral evolution. Proc R Soc B: Biol Sci 276:1527–1534

    Article  CAS  Google Scholar 

  • McRae L, Deinet S, Gill M, Collen B (2012) Arctic species trend index: tracking trends in Arctic marine populations. CAFF Assessment Series No. 7. Conservation of Arctic Flora and Fauna, Iceland

    Google Scholar 

  • Meredith M, Sommerkorn M, Cassotta S, Derksen C, Ekaykin A, Hollowed A et al. (2020) Polar Regions. In: Pörtner HO, Roberts DC, Masson-Delmotte V, Zhai P, Tignor M, Poloczanska E, Mintenbeck K, Alegría A, Nicolai M, Okem A, Petzold J, Rama B, Weyer NM (eds.) IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. Intergovernmental Panel on Climate Change (IPCC)) Geneva, pp 203–320

  • Miljeteig C, Strom H, Gavrilo MV, Volkov A, Jenssen BM, Gabrielsen GW (2009) High levels of contaminants in ivory gull Pagophila eburnea eggs from the Russian and Norwegian Arctic. Environ Sci Technol 43:5521–5528

    Article  CAS  PubMed  Google Scholar 

  • Miller MP, Haig SM, Mullins TD, Popper KJ, Green M (2012) Evidence for population bottlenecks and subtle genetic structure in the yellow rail. Condor 114:100–112

    Article  Google Scholar 

  • Nadachowska-Brzyska K, Li C, Smeds L, Zhang G, Ellegren H (2015) Temporal dynamics of avian populations during Pleistocene revealed by whole-genome sequences. Curr Biol 25:1375–1380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341

    Article  PubMed  Google Scholar 

  • Nunney L, Elam DR (1994) Estimating the Effective Population Size of Conserved Populations. Conserv Biol 8:175–184

    Article  Google Scholar 

  • Nunziata SO, Weisrock DW (2018) Estimation of contemporary effective population size and population declines using RAD sequence data. Heredity 120:196–207

    Article  CAS  PubMed  Google Scholar 

  • Nyström V, Angerbjörn A, Dalén L (2006) Genetic consequences of a demographic bottleneck in the Scandinavian arctic fox. Oikos 114:84–94

    Article  Google Scholar 

  • Orive ME (1993) Effective population size in organisms with complex life-histories. Theor Popul Biol 44:316–340

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Parreira BR, Chikhi L (2015) On some genetic consequences of social structure, mating systems, dispersal, and sampling. Proc Natl Acad Sci USA 112:E3318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parreira B, Quéméré E, Vanpé C, Carvalho I, Chikhi L (2020) Genetic consequences of social structure in the golden-crowned sifaka. Heredity 125:328–339

    Article  PubMed  PubMed Central  Google Scholar 

  • Peart CR, Tusso S, Pophaly SD, Botero-Castro F, Wu C-C, Aurioles-Gamboa D et al. (2020) Determinants of genetic variation across eco-evolutionary scales in pinnipeds. Nat Ecol Evol 4:1095–1104

    Article  PubMed  Google Scholar 

  • Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Bëer E, Robinson S et al. (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Heredity 90:502–503

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249

    Article  Google Scholar 

  • Rousset F (1999) Genetic Differentiation in Populations with Different Classes of Individuals. Theor Popul Biol 55:297–308

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the Genepop software for windows and linux. Mol Ecol Notes 8:103–1006

    Article  Google Scholar 

  • Rousset F, Beeravolu CR, Leblois R (2018) Likelihood computation and inference of demographic and mutational parameters from population genetic data under coalescent approximations. J de la Société Française de Statistique 159:142–166

    Google Scholar 

  • Rubidge EM, Patton JL, Lim M, Burton AC, Brashares JS, Moritz C (2012) Climate-induced range contraction drives genetic erosion in an alpine mammal. Nat Clim Change 2:285–288

    Article  Google Scholar 

  • Shafer ABA, Gattepaille LM, Stewart REA, Wolf JBW (2015) Demographic inferences using short-read genomic data in an approximate Bayesian computation framework: in silico evaluation of power, biases and proof of concept in Atlantic walrus. Mol Ecol 24:328–345

    Article  PubMed  Google Scholar 

  • Spencer NC, Gilchrist HG, Mallory ML (2014) Annual movement patterns of endangered ivory gulls: the importance of sea ice. Plos ONE 9:e115231

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stenhouse IJ, Robertson GJ, Gilchrist HG (2004) Recoveries and survival rates of ivory gulls (Pagophila eburnea) banded in Nunavut, Canada 1971–1999. Waterbirds 27:486–492

    Article  Google Scholar 

  • Storz J, Ramakrishnan U, Alberts S (2002) Genetic effective size of a wild primate population: influence of current and historical demography. Evolution 56:817–29

    Article  PubMed  Google Scholar 

  • Strøm H, Bakken V, Skoglund, Descamps S, Fjeldheim VB, Steen H (2020) Population status and trend of the threatened ivory gull Pagophila eburnea in Svalbard. Endanger Species Res 43:435–445

    Article  Google Scholar 

  • Volkov AE, de Korte J (2000) Breeding ecology of the Ivory Gull (Pagophila eburnea) in Sedov Archipelago, Severnaya Zemlya. Heritage of the Russian Arctic. Research, conservation and international cooperation. Ecopros Publishers, Moscow, p 483–500

    Google Scholar 

  • Waples RS (2016) Life-history traits and effective population size in species with overlapping generations revisited: the importance of adult mortality. Heredity 117:241–250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780

    Article  PubMed  PubMed Central  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolut Appl 3:244–262

    Article  Google Scholar 

  • Waples RS, Luikart G, Faulkner JR, Tallmon DA (2013) Simple life-history traits explain key effective population size ratios across diverse taxa. Proc R Soc B: Biol Sci 280:20131339

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  • Wogan GOU, Voelker G, Oatley G, Bowie RCK (2020) Biome stability predicts population structure of a southern African aridland bird species. Ecol Evol 10:4066–4081

    Article  PubMed  PubMed Central  Google Scholar 

  • Xenikoudakis G, Ersmark E, Tison J-L, Waits L, Kindberg J, Swenson JE et al. (2015) Consequences of a demographic bottleneck on genetic structure and variation in the Scandinavian brown bear. Mol Ecol 24:3441–3454

    Article  CAS  PubMed  Google Scholar 

  • Yannic G, Broquet T, Strøm H, Aebischer A, Dufresnes C, Gavrilo MV et al. (2016) Genetic and morphological sex identification methods reveal a male-biased sex ratio in the Ivory Gull Pagophila eburnea. J Ornithol 157:861–873

    Article  Google Scholar 

  • Yannic G, Sermier R, Aebischer A, Gavrilo MV, Gilg O, Miljeteig C et al. (2011) Description of microsatellite markers and genotyping performances using feathers and buccal swabs for the ivory gull (Pagophila eburnea). Mol Ecol Resour 11:877–889

    Article  PubMed  Google Scholar 

  • Yannic G, Yearsley J, Sermier R, Dufresnes C, Gilg O, Aebischer A et al. (2016) High connectivity in a long-lived high-Arctic seabird, the ivory gull Pagophila eburnea. Polar Biol 39:221–236

    Article  Google Scholar 

  • Yurkowski DJ, Auger-Méthé M, Mallory ML, Wong SNP, Gilchrist G, Derocher AE et al. (2019) Abundance and species diversity hotspots of tracked marine predators across the North American Arctic. Diversity Distrib 25:328–345

    Article  Google Scholar 

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Acknowledgements

We thank Adrian Aebischer, Christophe Dufresnes, Emmanuelle Pouivé, Roberto Sermier, and Brigitte Sabard for lab and field assistance. We wish to thank the two reviewers and the subject editor for their constructive and challenging comments that improved the quality of the paper. This work was supported by grants from the foundation Ellis Elliot (Switzerland), Société vaudoise des Sciences naturelles (Switzerland) and Nos Oiseaux (Switzerland) to GY, by a foundation Agassiz (Switzerland) grant to TB and by Nicolas Perrin’s research group, Department of Ecology and Evolution at University of Lausanne, Switzerland. This work benefited from access to the Biogenouest genomic platform at Station Biologique de Roscoff and we are grateful to the Roscoff Bioinformatics platform ABiMS (http://abims.sb-roscoff.fr), the national INRA MIGALE (http://migale.jouy.inra.fr) and GENOTOUL (Toulouse Midi-Pyrénées) bioinformatics HPC platforms, as well as the CBGP and the local Montpellier Bioinformatics Biodiversity (MBB, supported by the LabEx CeMEB ANR-10-LABX-04-01) HPC platform services for providing storage and computing resources. RL was supported by the Agence Nationale de la Recherche (projects GENOSPACE ANR-16-CE02-0008 and INTROSPEC ANR-19-CE02-0011). The sampling in Canada was funded by the Department of Environment and Climate Change Canada. The sampling in Greenland was supported by the Groupe de Recherche in Ecologie Arctique (GREA) and funded by the French Polar Institute-IPEV (Program ‘Ivory 1210’). The sampling in Svalbard was funded by the Norwegian Polar Institute and the Norwegian seabird monitoring program SEAPOP (www.seapop.no, grant number 192141). The sampling in Russia was part of the work plan of the Joint Norwegian-Russian Commission on Environmental Protection and funded by the Norwegian Ministry of Environment, Arctic and Antarctic Research Institute and the Russian IPY 2007/08 program.

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GY and TB conceived the project and designed the study. OG, MG, HS, MLM, RIGM, HGG, and GY contributed to sample collection. CD and GY performed lab work and genotyping. TB and GY performed the bioinformatic analysis. EC, GY, and TB performed the population genetic analysis, with inputs/help from LC, EM, RL, CR, and JMY. EC, GY and TB wrote the paper, with comments from all authors. All authors have read and approved the paper.

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Correspondence to Glenn Yannic.

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Charbonnel, E., Daguin-Thiébaut, C., Caradec, L. et al. Searching for genetic evidence of demographic decline in an arctic seabird: beware of overlapping generations. Heredity 128, 364–376 (2022). https://doi.org/10.1038/s41437-022-00515-3

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