Skip to main content
SpringerLink
Log in

Integrating Different Data Sources Using a Bayesian Hierarchical Model to Unveil Glacial Refugia

  • Published:
Journal of Agricultural, Biological and Environmental Statistics Aims and scope Submit manuscript

Abstract

Rapid anthropogenic climate change has elevated the interest in studying the biotic responses of species during the Last Glacial Maximum. During this period, species retreated to highly spatially restricted geographic regions where survival was possible, known as glacial micro-refugia, from which they migrated and expanded when conditions became more suitable. Several distinct sources of evidence have contributed to developing a new understanding of how these regions might have impacted the sustainability of the natural populations of many species. Pollen records in Eastern Beringia have been used to explore the possibility that the region harbored glacial refugia for several plants from the arctic tundra and/or the boreal forest biomes common to the region. Our study focuses on Alnus viridis and Picea glauca, two predominant species of arcto-boreal vegetation. We propose to integrate genomic, SDM, and existing fossil data in a hierarchical Bayesian modeling (HBM) framework to determine whether multiple refugia existed in isolated geographic areas. This study demonstrates how the flexibility of HBMs makes the formal synthesis of such disparate data sources feasible. Our results highlight the regions of plausible refugia that can guide future investigations into studying the role of glacial refugia during climate change. Supplementary materials accompanying this paper appear online.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Abbott RJ, Brochmann C (2003) History and evolution of the arctic flora: in the footsteps of Eric hultén. Mol Ecol 12(2):299–313

    Article  Google Scholar 

  • Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43(6):1223–1232

    Article  Google Scholar 

  • Anderson PM, Brubaker LB (1994) Vegetation history of northcentral alaska: a mapped summary of late-quaternary pollen data. Quatern Sci Rev 13(1):71–92

    Article  Google Scholar 

  • Anderson LL, Hu FS, Nelson DM, Petit RJ, Paige KN (2006) Ice-age endurance: Dna evidence of a white spruce refugium in alaska. Proc Natl Acad Sci 103(33):12447–12450

    Article  Google Scholar 

  • Anderson LL, Hu FS, Paige KN (2011) Phylogeographic history of white spruce during the last glacial maximum: uncovering cryptic refugia. J Hered 102(2):207–216

    Article  Google Scholar 

  • Aoki K, Tamaki I, Nakao K, Ueno S, Kamijo T, Setoguchi H, Murakami N, Kato M, Tsumura Y (2019) Approximate Bayesian computation analysis of est-associated microsatellites indicates that the broadleaved evergreen tree castanopsis sieboldii survived the last glacial maximum in multiple refugia in japan. Heredity 122(3):326–340

    Article  Google Scholar 

  • Bakka H, Rue H, Fuglstad G-A, Riebler A, Bolin D, Illian J, Krainski E, Simpson D, Lindgren F (2018) Spatial modeling with r-inla: a review. WIREs Comput Stat 10(6):e1443

    Article  MathSciNet  Google Scholar 

  • Bigelow NH, Brubaker LB, Edwards ME, Harrison SP, Prentice IC, Anderson PM, Andreev A A, Bartlein PJ, Christensen TR, Cramer W, Kaplan JO, Lozhkin AV, Matveyeva NV, Murray, DF, McGuire,AD, Razzhivin VY, Ritchie JC, Smith B, Walker DA, Gajewski K, Wolf V, Holmqvist BH, Igarashi Y, Kremenetskii K, Paus A, isaric MFJ, Volkova VS (2003) Climate change and arctic ecosystems: 1. vegetation changes north of \(55^{\circ }\)n between the last glacial maximum, mid-holocene, and present. J Geophys Res Atmosp 108(D19)

  • Botkin DB, Saxe H, Araújo MB, Betts R, Bradshaw RHW, Cedhagen T, Chesson P, Dawson TP, Etterson JR, Faith DP, Ferrier S, Guisan A, Hansen AS, Hilbert DW, Loehle C, Margules C, New M, Sobel MJ, Stockwell DRB (2007) Forecasting the effects of global warming on biodiversity. Bioscience 57(3):227–236

    Article  Google Scholar 

  • Brown JL, Knowles LL (2012) Spatially explicit models of dynamic histories: examination of the genetic consequences of pleistocene glaciation and recent climate change on the American Pika. Mol Ecol 21(15):3757–3775

    Article  Google Scholar 

  • Brubaker LB, Anderson PM, Edwards ME, Lozhkin AV (2005) Beringia as a glacial refugium for boreal trees and shrubs: new perspectives from mapped pollen data. J Biogeogr 32(5):833–848

    Article  Google Scholar 

  • Budde K, González-Martínez SC, Hardy OJ, Heuertz M (2013) The ancient tropical rainforest tree symphonia globulifera l. f. (clusiaceae) was not restricted to postulated Pleistocene refugia in Atlantic equatorial Africa. Heredity 111(1):66–76

    Article  Google Scholar 

  • Clark JS (2005) Why environmental scientists are becoming bayesians. Ecol Lett 8(1):2–14

    Article  Google Scholar 

  • Cornejo-Romero A, Vargas-Mendoza CF, Aguilar-Martínez GF, Medina-Sánchez J, Rendón-Aguilar B, Valverde PL, Zavala-Hurtado JA, Serrato A, Rivas-Arancibia S, Pérez-Hernández MA et al (2017) Alternative glacial-interglacial refugia demographic hypotheses tested on cephalocereus columna-trajani (cactaceae) in the intertropical Mexican drylands. PLoS ONE 12(4):e0175905

    Article  Google Scholar 

  • Cressie N, Johannesson G (2008) Fixed rank kriging for very large spatial data sets. J R Stat Soc Ser B Stat Methodol 70(1):209–226

    Article  MathSciNet  MATH  Google Scholar 

  • Datta A, Banerjee S, Finley AO, Gelfand AE (2016) Hierarchical nearest-neighbor gaussian process models for large geostatistical datasets. J Am Stat Assoc 111(514):800–812

    Article  MathSciNet  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292(5517):673–679

    Article  Google Scholar 

  • Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332(6025):53–58

    Article  Google Scholar 

  • De Lafontaine G, Ducousso A, Lefèvre S, Magnanou E, Petit RJ (2013) Stronger spatial genetic structure in recolonized areas than in refugia in the European beech. Mol Ecol 22(17):4397–4412

    Article  Google Scholar 

  • de Lafontaine G, Amasifuen Guerra CA, Ducousso A, Sanchez-Goni M-F, Petit RJ (2014) Beyond skepticism: uncovering cryptic refugia using multiple lines of evidence. New Phytol 204(3):450–454

    Article  Google Scholar 

  • de Lafontaine G, Turgeon J, Payette S (2010) Phylogeography of white spruce (Picea glauca) in eastern north America reveals contrasting ecological trajectories. J Biogeogr 37(4):741–751

    Article  Google Scholar 

  • de Lafontaine G, Napier JD, Petit RJ, Hu FS (2018) Invoking adaptation to decipher the genetic legacy of past climate change. Ecology 99(7):1530–1546

    Article  Google Scholar 

  • Espíndola A, Pellissier L, Maiorano L, Hordijk W, Guisan A, Alvarez N (2012) Predicting present and future intra-specific genetic structure through niche hindcasting across 24 millennia. Ecol Lett 15(7):649–657

    Article  Google Scholar 

  • Excoffier L, Smouse PE (1994) Using allele frequencies and geographic subdivision to reconstruct gene trees within a species: molecular variance parsimony. Genetics 136(1):343–359

    Article  Google Scholar 

  • Feurdean A, Bhagwat SA, Willis KJ, Birks HJB, Lischke H, Hickler T (2013) Tree migration-rates: narrowing the gap between inferred post-glacial rates and projected rates. PLoS ONE 8(8):e71797

    Article  Google Scholar 

  • Franklin J (2010) Mapping species distributions: spatial inference and prediction. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Fuglstad G-A, Simpson D, Lindgren F, Rue H (2019) Constructing priors that penalize the complexity of gaussian random fields. J Am Stat Assoc 114(525):445–452

    Article  MathSciNet  MATH  Google Scholar 

  • Gao J, Wang B, Mao JF, Ingvarsson P, Zeng QY, Wang XR (2012) Demography and speciation history of the homoploid hybrid pine Pinus densata on the Tibetan plateau. Mol Ecol 21(19):4811–4827

    Article  Google Scholar 

  • Gavin DG, Fitzpatrick MC, Gugger PF, Heath KD, Rodríguez-Sánchez F, Dobrowski SZ, Hampe A, Hu FS, Ashcroft MB, Bartlein PJ et al (2014) Climate refugia: joint inference from fossil records, species distribution models and phylogeography. New Phytol 204(1):37–54

    Article  Google Scholar 

  • Graham CH, VanDerWal J, Phillips SJ, Moritz C, Williams SE (2010) Dynamic refugia and species persistence: tracking spatial shifts in habitat through time. Ecography 33(6):1062–1069

    Article  Google Scholar 

  • Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8(9):993–1009

    Article  Google Scholar 

  • Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annu Rev Ecol Evol Syst 42:313–333

    Article  Google Scholar 

  • Hao Q, de Lafontaine G, Guo D, Gu H, Hu FS, Han Y, Song Z, Liu H (2018) The critical role of local refugia in postglacial colonization of Chinese pine: joint inferences from dna analyses, pollen records, and species distribution modeling. Ecography 41(4):592–606

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405(6789):907–913

    Article  Google Scholar 

  • Hopkins D, Smith P, Matthews J (1981) Dated wood from Alaska and the Yukon: implications for forest refugia in Beringia. Quatern Res 15(3):217–249

    Article  Google Scholar 

  • Katzfuss M (2017) A multi-resolution approximation for massive spatial datasets. J Am Stat Assoc 112(517):201–214

    Article  MathSciNet  Google Scholar 

  • Keppel G, Van Niel KP, Wardell-Johnson GW, Yates CJ, Byrne M, Mucina L, Schut AG, Hopper SD, Franklin SE (2012) Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob Ecol Biogeogr 21(4):393–404

    Article  Google Scholar 

  • Knowles LL, Alvarado-Serrano DF (2010) Exploring the population genetic consequences of the colonization process with spatio-temporally explicit models: insights from coupled ecological, demographic and genetic models in montane grasshoppers. Mol Ecol 19(17):3727–3745

    Article  Google Scholar 

  • Lemey P, Rambaut A, Drummond AJ, Suchard MA (2009) Bayesian phylogeography finds its roots. PLoS Comput Biol 5(9):e1000520

    Article  MathSciNet  Google Scholar 

  • Lemey P, Rambaut A, Welch JJ, Suchard MA (2010) Phylogeography takes a relaxed random walk in continuous space and time. Mol Biol Evol 27(8):1877–1885

    Article  Google Scholar 

  • Lemmon AR, Lemmon EM (2008) A likelihood framework for estimating phylogeographic history on a continuous landscape. Syst Biol 57(4):544–561

    Article  Google Scholar 

  • Li B, Nychka DW, Ammann CM (2010) The value of multiproxy reconstruction of past climate. J Am Stat Assoc 105(491):883–895

    Article  MathSciNet  MATH  Google Scholar 

  • Li L, Abbott RJ, Liu B, Sun Y, Li L, Zou J, Wang X, Miehe G, Liu J (2013) Pliocene intraspecific divergence and plio-pleistocene range expansions within Picea likiangensis (Lijiang spruce), a dominant forest tree of the Ginghai-tibet plateau. Mol Ecol 22(20):5237–5255

    Article  Google Scholar 

  • Lindgren F, Rue H (2015) Bayesian spatial modelling with R-INLA. J Stat Softw 63(19)

  • Lindgren F, Rue H, Lindström J (2011) An explicit link between gaussian fields and Gaussian Markov random fields: the stochastic partial differential equation approach. J Roy Stat Soc Ser B (Stat Methodol) 73(4):423–498

    Article  MathSciNet  MATH  Google Scholar 

  • Luoto M, Heikkinen RK (2008) Disregarding topographical heterogeneity biases species turnover assessments based on bioclimatic models. Glob Change Biol 14(3):483–494

    Article  Google Scholar 

  • Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Lataıowa M, Litt T, Paule L, Roure JM, Tantau I, Van Der Knaap WO, Petit RJ, De Beaulieu J-L (2006) A new scenario for the quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 171(1):199–221

    Article  Google Scholar 

  • Manolopoulou I, Emerson BC (2012) Phylogeographic ancestral inference using the coalescent model on haplotype trees. J Comput Biol 19(6):745–755

    Article  MathSciNet  Google Scholar 

  • Marion G, McInerny GJ, Pagel J, Catterall S, Cook AR, Hartig F, O’Hara RB (2012) Parameter and uncertainty estimation for process-oriented population and distribution models: data, statistics and the niche. J Biogeogr 39(12):2225–2239

    Article  Google Scholar 

  • Marske KA, Leschen RA, Buckley TR (2012) Concerted versus independent evolution and the search for multiple refugia: comparative phylogeography of four forest beetles. Evolut Int J Organ Evolut 66(6):1862–1877

    Article  Google Scholar 

  • McLachlan JS, Clark JS, Manos PS (2005) Molecular indicators of tree migration capacity under rapid climate change. Ecology 86(8):2088–2098

    Article  Google Scholar 

  • Meirmans PG, Liu S (2018) Analysis of molecular variance (Amova) for autopolyploids. Front Ecol Evol 6:66

    Article  Google Scholar 

  • Mosblech NAS, Bush MB, van Woesik R (2011) On metapopulations and microrefugia: palaeoecological insights. J Biogeogr 38(3):419–429

    Article  Google Scholar 

  • Napier JD, de Lafontaine G, Heath KD, Hu FS (2019) Rethinking long-term vegetation dynamics: multiple glacial refugia and local expansion of a species complex. Ecography 42(5):1056–1067

    Article  Google Scholar 

  • Napier JD, de Lafontaine G, Chipman ML (2020a) The evolution of paleoecology. Trends Ecol Evolut 35(4):293–295

    Article  Google Scholar 

  • Napier JD, Fernandez MC, de Lafontaine G, Hu FS (2020b) Ice-age persistence and genetic isolation of the disjunct distribution of larch in Alaska. Ecol Evol 10(3):1692–1702

    Article  Google Scholar 

  • Nogués-Bravo D (2009) Predicting the past distribution of species climatic niches. Glob Ecol Biogeogr 18(5):521–531

    Article  Google Scholar 

  • Nychka D, Bandyopadhyay S, Hammerling D, Lindgren F, Sain S (2015) A multiresolution gaussian process model for the analysis of large spatial datasets. J Comput Graph Stat 24(2):579–599

    Article  MathSciNet  Google Scholar 

  • Pagel J, Schurr FM (2012) Forecasting species ranges by statistical estimation of ecological niches and spatial population dynamics. Glob Ecol Biogeogr 21(2):293–304

    Article  Google Scholar 

  • Parducci L, Jørgensen T, Tollefsrud MM, Elverland E, Alm T, Fontana SL, Bennett KD, Haile J, Matetovici I, Suyama Y, Edwards ME, Andersen K, Rasmussen M, Boessenkool S, Coissac E, Brochmann C, Taberlet P, Houmark-Nielsen M, Larsen NK, Orlando L, Gilbert MTP, Kjær KH, Alsos IG, Willerslev E (2012) Glacial survival of boreal trees in northern Scandinavia. Science 335(6072):1083–1086

    Article  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu J-L, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Müller-Starck G, Demesure-Musch B, Palmé A, Martín JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300(5625):1563–1565

    Article  Google Scholar 

  • Porto TJ, Carnaval AC, da Rocha PLB (2013) Evaluating forest refugial models using species distribution models, model filling and inclusion: a case study with 14 Brazilian species. Divers Distrib 19(3):330–340

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    Article  Google Scholar 

  • Provan J, Bennett K (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evolut 23(10):564–571

    Article  Google Scholar 

  • Randin CF, Engler R, Normand S, Zappa M, Zimmermann NE, Pearman PB, Vittoz P, Thuiller W, Guisan A (2009) Climate change and plant distribution: local models predict high-elevation persistence. Glob Change Biol 15(6):1557–1569

    Article  Google Scholar 

  • Ren G, Mateo RG, Liu J, Suchan T, Alvarez N, Guisan A, Conti E, Salamin N (2017) Genetic consequences of quaternary climatic oscillations in the Himalayas: Primula tibetica as a case study based on restriction site-associated dna sequencing. New Phytol 213(3):1500–1512

    Article  Google Scholar 

  • Rue H, Martino S, Chopin N (2009) Approximate Bayesian inference for latent gaussian models by using integrated nested Laplace approximations. J Roy Stat Soc Ser B (Stat Methodol) 71(2):319–392

    Article  MathSciNet  MATH  Google Scholar 

  • Schurr FM, Pagel J, Cabral JS, Groeneveld J, Bykova O, O’Hara RB, Hartig F, Kissling WD, Linder HP, Midgley GF et al (2012) How to understand species’ niches and range dynamics: a demographic research agenda for biogeography. J Biogeogr 39(12):2146–2162

    Article  Google Scholar 

  • Shafer AB, Cullingham CI, Cote SD, Coltman DW (2010) Of glaciers and refugia: a decade of study sheds new light on the phylogeography of northwestern North America. Mol Ecol 19(21):4589–4621

    Article  Google Scholar 

  • Simpson D, Rue H, Riebler A, Martins TG, Sørbye SH (2017) Penalising model component complexity: a principled, practical approach to constructing priors. Stat Sci 32(1):1–28

    Article  MathSciNet  MATH  Google Scholar 

  • Stein ML (1999) Interpolation of spatial data: some theory for kriging. Springer, Berlin

    Book  MATH  Google Scholar 

  • Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc Roy Soc B Biol Sci 277(1682):661–671

    Google Scholar 

  • Svenning J-C, Fløjgaard C, Marske KA, Nógues-Bravo D, Normand S (2011) Applications of species distribution modeling to paleobiology. Quatern Sci Rev 30(21–22):2930–2947

    Article  Google Scholar 

  • Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) Biomod-a platform for ensemble forecasting of species distributions. Ecography 32(3):369–373

    Article  Google Scholar 

  • Tsuda Y, Chen J, Stocks M, Källman T, Sønstebø JH, Parducci L, Semerikov V, Sperisen C, Politov D, Ronkainen T et al (2016) The extent and meaning of hybridization and introgression between Siberian spruce (Picea obovata) and Norway spruce (Picea abies): cryptic refugia as stepping stones to the west? Mol Ecol 25(12):2773–2789

    Article  Google Scholar 

  • Urban MA, Nelson DM, Kelly R, Ibrahim T, Dietze M, Pearson A, Hu FS (2013) A hierarchical Bayesian approach to the classification of c3 and c4 grass pollen based on spiral \(\delta \)13c data. Geochim Cosmochim Acta 121:168–176

    Article  Google Scholar 

  • Wang Q, Liu J, Allen GA, Ma Y, Yue W, Marr KL, Abbott RJ (2016) Arctic plant origins and early formation of circumarctic distributions: a case study of the mountain sorrel, Oxyria digyna. New Phytol 209(1):343–353

    Article  Google Scholar 

  • Warren E, de Lafontaine G, Gérardi S, Senneville S, Beaulieu J, Perron M, Jaramillo-Correa JP, Bousquet J (2016) Joint inferences from cytoplasmic dna and fossil data provide evidence for glacial vicariance and contrasted post-glacial dynamics in tamarack, a transcontinental conifer. J Biogeogr 43(6):1227–1241

    Article  Google Scholar 

  • Whittle P (1954) On stationary processes in the plane. Biometrika 41(3/4):434–449

    Article  MathSciNet  MATH  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the anonymous referees, an Associate Editor, and the Editor for their constructive comments that improved the quality of this paper.

Funding

This research is supported by NSF-1418339, NSF-2124576 and NSF-2118329.

Author information

Authors and Affiliations

  1. Department of Statistics, University of Illinois, Urbana-Champaign, USA

    Mauricio Campos & Bo Li

  2. Département de biologie, chimie et géographie, Université du Québec, Rimouski, Canada

    Guillaume de Lafontaine

  3. Department of Integrative Biology, University of Texas, Austin, USA

    Joseph Napier

  4. Department of Biology, Washington University, St. Louis, USA

    Feng Sheng Hu

  5. Department of Earth and Planetary Sciences, Washington University, St. Louis, USA

    Feng Sheng Hu

Authors
  1. Mauricio Campos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guillaume de Lafontaine
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joseph Napier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Feng Sheng Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mauricio Campos.

Ethics declarations

Conflicts of interest

The authors declare no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file 1 (pdf 239 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Campos, M., Li, B., de Lafontaine, G. et al. Integrating Different Data Sources Using a Bayesian Hierarchical Model to Unveil Glacial Refugia. JABES (2023). https://doi.org/10.1007/s13253-023-00582-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13253-023-00582-x

Keywords

Search

Navigation