Abstract
Eastern white pine (Pinus strobus L.) is a widespread conifer in eastern North America. A novel dieback phenomenon, as well as increasing global temperatures contributing to the contraction of suitable habitat, is threatening this species’ long-term persistence in the Southern Appalachian Mountains. This southern extent of its current range is where P. strobus is hypothesized to have survived in refugial populations during the last glacial maximum. As a result, extant populations located here may have higher levels of ancestral genetic diversity, and by extension, adaptive potential. We genotyped 432 P. strobus individuals from 23 sites throughout the Southern Appalachians and another 34 individuals from two reference populations in the northern USA, using 10 established microsatellite markers. Levels of genetic diversity in the southern portion of the range were comparable but not higher than reference northern populations. There was an overall heterozygote deficiency and high inbreeding coefficient (FIS = 0.173); however, these values were comparable to published research of P. strobus throughout the northern range. There was low overall genetic differentiation (FST = 0.055) among populations in the Southern Appalachians and population structure was best explained by ecoregions. These results show that P. strobus in the Southern Appalachians is a fairly heterogenous and admixed species with relatively high genetic diversity mostly partitioned within populations. The Southern Appalachians remains an important area for P. strobus conservation, but not necessarily because it is genetically unique.
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References
Abrams MD (2001) Eastern white pine versatility in the presettlement forest. Bioscience 51:967–979
Abrams MD, Orwig DA, Demeo TE (1995) Dendroecological analysis of successional dynamics for a presettlement-origin white-pine mixed-oak forest in the Southern Appalachians, USA. J Ecol 83:123–133
Aitken SN, Yeaman S, Holliday JA, Wang TL, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111
Alfaro RI, Fady B, Vendramin GG, Dawson IK, Fleming RA, Saenz-Romero C, Lindig-Cisneros RA, Murdock T, Vinceti B, Navarro CM, Skroppa T, Baldinelli G, El-Kassaby YA, Loo J (2014) The role of forest genetic resources in responding to biotic and abiotic factors in the context of anthropogenic climate change. Forest Ecol Manag 333:76–87
Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends in Ecol Evol 23:38–44
Beaulieu J, Simon JP (1994) Inheritance and linkage relationships of allozymes in Pinus strobus L. Silvae Genet 43:253–261
Beaulieu J, Simon JP (1995) Mating system in natural populations of eastern white pine in Quebec. Can J For Res 25:1697–1703
Brookfield JFY (1996) A simple new method for estimating null allele frequency from heterozygote deficiency. Mol Ecol 5:453–455
Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1010
Buchert GP, Rajora OP, Hood JV, Dancik BP (1997) Effects of harvesting on genetic diversity in old growth eastern white pine in Ontario, Canada. Conserv Biol 11:747–758
Campagne P, Smouse PE, Varouchas G, Silvain JF, Leru B (2012) Comparing the van Oosterhout and Chybicki-Burczyk methods of estimating null allele frequencies for inbred populations. Mol Ecol Resour 12:975–982
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Chhatre VE, Rajora OP (2014) Genetic divergence and signatures of natural selection in marginal populations of a keystone, long-lived conifer, eastern white pine (Pinus strobus) from northern Ontario. Plos One 9
Chybicki IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113
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
Costanza KKL, Whitney TD, McIntire CD, Livingston WH, Gandhi KJK (2018) A synthesis of emerging health issues of eastern white pine (Pinus strobus) in eastern North America. For Ecol Manag 423:3–17
Davis MB (1983) Quaternary history of deciduous forests of eastern North America and Europe. Ann Mo Bot Gard 70:550–563
Diniz-Filho JA, Soares TN, Lima JS, Dobrovolski R, Landeiro VL, Telles MPD, Rangel TF, Bini LM (2013) Mantel test in population genetics. Genet Mol Biol 36:475–485
Earl DA, Vonholdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Echt CS, May-Marquardt P, Hseih M, Zahorchak R (1996) Characterization of microsatellite markers in eastern white pine. Genome 39:1102–1108
Elith J, Phillips SJ, Hastie T, Dudik M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57
Epperson BK, Chung MG (2001) Spatial genetic structure of allozyme polymorphisms within populations of Pinus strobus (Pinaceae). Am J Bot 88:1006–1010
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567
Fady B, Aravanopoulos FA, Alizoti P, Mátyás C, von Wühlisch G, Westergren M, Belletti P, Cvjetkovic B, Ducci F, Huber G, Kelleher CT, Khaldi A, Kharrat MBD, Kraigher H, Kramer K, Mühlethaler U, Peric S, Perry A, Rousi M, Sbay H, Stojnic S, Tijardovic M, Tsvetkov I, Varela MC, Vendramin GG, Zlatanov T (2016) Evolution-based approach needed for the conservation and silviculture of peripheral forest tree populations. For Ecol Manag 375:66–75
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49
Fowler DP (1965) Natural self-fertilization in three jack pines and its implications in seed orchard management. For Sci 11:55–58
Goudet J (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186
Hamrick JL (2004) Response of forest trees to global environmental changes. For Ecol Manag 197:323–335
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos T Roy Soc B 351:1291–1298
Hamrick JL, Nason JD (1996) Consequences of dispersal in plants. In: Rhodes OE Jr, Chesser RK, Smith MH (eds) Population dynamics in ecological space and time. University of Chicago Press, Chicago, pp 203–236
Hedrick PW (1999) Perspective: Highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318
Hepp TE, Vimmerstedt JP, Smalley GW, McNab WH (2015) Estimating yields of unthinned eastern white pine plantations from current stocking in the Southern Appalachians. For Sci 61:114–122
Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913
Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Hijmans RJ, van Etten J, Cheng J, Mattiuzzi M, Sumner M, Greenberg JA, Lamigueiro OP, Bevan A, Racine EB, Shortridge A, Hijmans MRJ (2017) Package ‘raster’. R package
Housset JM, Nadeau S, Isabel N, Depardieu C, Duchesne I, Lenz P, Girardin MP (2018) Tree rings provide a new class of phenotypes for genetic associations that foster insights into adaptation of conifers to climate change. New Phytol 218:630–645
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Hufford KM, Hamrick JL (2003) Viability selection at three early life stages of the tropical tree, Platypodium elegans (Fabaceae, Papilionoideae). Evolution 57:518–526
Jackson ST, Webb RS, Anderson KH, Overpeck JT, Webb T, Williams JW, Hansen BCS (2000) Vegetation and environment in Eastern North America during the Last Glacial Maximum. Quaternary Sci Rev 19:489–508
Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K=2 conundrum. Mol Ecol 26:3594–3602
Johnson LPV (1945) Reduced vigour, chlorophyll deficiency, and other effects of self-fertilization in Pinus. Can J For Res 23:145–149
Joyce DG, Rehfeldt GE (2013) Climatic niche, ecological genetics, and impact of climate change on eastern white pine (Pinus strobus L.): guidelines for land managers. For Ecol Manag 295:173–192
Jump AS, Marchant R, Penuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58
Kuparinen A, Savolainen O, Schurr FM (2010) Increased mortality can promote evolutionary adaptation of forest trees to climate change. For Ecol Manag 259:1003–1008
Lovett GM, Canham CD, Arthur MA, Weathers KC, Fitzhugh RD (2006) Forest ecosystem responses to exotic pests and pathogens in eastern North America. Bioscience 56:395–405
Mandak B, Hadincova V, Mahelka V, Wildova R (2013) European invasion of North American Pinus strobus at large and fine scales: high genetic diversity and fine-scale genetic clustering over time in the adventive range. PLoS One 8
Mantel N (1967) Detection of diesease clustering and a generalized regression approach. Cancer Res 27:209–220.
Marquardt PE, Echt CS, Epperson BK, Pubanz DM (2007) Genetic structure, diversity, and inbreeding of eastern white pine under different management conditions. Can J For Res 37:2652–2662
Marquardt PE, Epperson BK (2004) Spatial and population genetic structure of microsatellites in white pine. Mol Ecol 13:3305–3315
Mehes M, Nkongolo KK, Michael P (2009) Assessing genetic diversity and structure of fragmented populations of eastern white pine (Pinus strobus) and western white pine (P. monticola) for conservation management. J Plant Ecol 2:143–151
Meirmans PG (2015) Seven common mistakes in population genetics and how to avoid them. Mol Ecol 24:3223–3231
Munzbergova Z, Hadincova V, Wild J, Herben T, Maresova J (2010) Spatial and temporal variation in dispersal pattern of an invasive pine. Biol Invasions 12:2471–2486
Nadeau S, Godbout J, Lamothe M, Gros-Louis M-C, Isabel N, Ritland K (2015) Contrasting patterns of genetic diversity across the ranges of Pinus monticola and P. strobus: a comparison between eastern and western North American postglacial colonization histories. Am J Bot 102:1342–1355
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Nijensohn SE, Schaberg PG, Hawley GJ, DeHayes DH (2005) Genetic subpopulation structuring and its implications in a mature eastern white pine stand. Can J For Res 35:1041–1052
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
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
Petit RJ, Aguinagalde I, de Beaulieu JL et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Potter KM, Jetton RM, Bower A, Jacobs DF, Man G, Hipkins VD, Westwood M (2017) Banking on the future: progress, challenges and opportunities for the genetic conservation of forest trees. New Forest 48:153–180
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Provan J, Bennett KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rajora OP, DeVerno L, Mosseler A, Innes DJ (1998) Genetic diversity and population structure of disjunct Newfoundland and Central Ontario populations of eastern white pine (Pinus strobus). Can J Bot 76:500–508
Rajora OP, Rahman MH, Buchert GP, Dancik BP (2000) Microsatellite DNA analysis of genetic effects of harvesting in old-growth eastern white pine (Pinus strobus) in Ontario, Canada. Mol Ecol 9:339–348
Raymond M, Rousset F (1995) GENEPOP (Version-1.2) - Population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rogers LL, Lindquist EL (1992) Supercanopy white pine and wildlife. In: Stine RA (ed) White pine symposium. Duluth, Minnesota, pp 39–43
Savolainen O, Bokma F, Garcia-Gil R, Komulainen P, Repo T (2004) Genetic variation in cessation of growth and frost hardiness and consequences for adaptation of Pinus sylvestris to climatic changes. For Ecol Manag 197:79–89
Savolainen O, Pyhajarvi T, Knurr T (2007) Gene flow and local adaptation in trees. Annu Rev Ecol Evol S 38:595–619
Schaberg PG, DeHayes DH, Hawley GJ, Nijensohn SE (2008) Anthropogenic alterations of genetic diversity within tree populations: implications for forest ecosystem resilience. For Ecol Manag 256:855–862
Soltis DE, Gitzendanner MA, Strenge DD, Soltis PS (1997) Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Syst Evol 206:353–373
Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS (2006) Comparative phylogeography of unglaciated eastern North America. Mol Ecol 15:4261–4293
Strauss SH (1986) Heterosis at allozyme loci under inbreeding and crossbreeding in Pinus attenuata. Genetics 113:115–134
Talarico L, Babik W, Marta S, Mattoccia M (2019) Genetic drift shaped MHC IIB diversity of an endangered anuran species within the Italian glacial refugium. J Zool 307:61–70
U.S. Environmental Protection Agency (2013) Level III ecoregions of the continental United States. U.S. EPA - National Health and Environmental Effects Research Laboratory, Corvallis
Varela S, Lima-Ribeiro MS, Terribile LC (2015) A short guide to the climatic variables of the last glacial maximum for biogeographers. PLoS One 10:e0129037
Vimmerstedt JP (1962) Southern Appalachian white pine plantations site, volume, and yield. USDA Forest Service, Southeastern Forest Experimental Station, p. 15
Walter R, Epperson BK (2001) Geographic pattern of genetic variation in Pinus resinosa: area of greatest diversity is not the origin of postglacial populations. Mol Ecol 10:103–111
Walter R, Epperson BK (2004) Microsatellite analysis of spatial structure among seedlings in populations of Pinus strobus (Pinaceae). Am J Bot 91:549–557
Wendel GW, Smith HC (1990) Pinus strobus L. eastern white pine. In: Burns RM, Honkala BH (eds) Silvics of North America. USDA Forest Service, Washington DC, pp 476–488
Wielstra B, Crnobrnja-Isailovic J, Litvinchuk SN, Reijnen BT, Skidmore AK, Sotiropoulos K, Toxopeus AG, Tzankov N, Vukov T, Arntzen JW (2013) Tracing glacial refugia of Triturus newts based on mitochondrial DNA phylogeography and species distribution modeling. Front Zool 10
Williams CG (2010) Long-distance pine pollen still germinates after meso-scale dispersal. American J Bot 97:846–855
Wilson RW, McQuilkin WE (1963) Silvical characteristics of eastern white pine (Pinus strobus). USDA Forest Service Northeasten Forest Experimental Station Research Paper 13:1–28
Zinck JWR, Rajora OP (2016) Post-glacial phylogeography and evolution of a wide-ranging highly-exploited keystone forest tree, eastern white pine (Pinus strobus) in North America: single refugium, multiple routes. BMC Evol Biol 16:56
Acknowledgements
We are grateful to those who assisted with P. strobus sampling: Chris Asaro (USDA Forest Service), Brittany Barnes (University of Georgia), Megan Bartz (USDA Forest Service), Amanda Block (USDA Forest Service), William Caudill (USDA Forest Service), Lori Chamberlain (Virginia Department of Forestry), Beth Christensen (USDA Forest Service), Kara Costanza (University of New Brunswick), Don Grosman (Arborjet), TJ Hall (Pennsylvania DCNR), Bob Heyd (USDA Forest Service), Erica Roberts (USDA Forest Service), Derek Robertson (USDA Forest Service), Laura Vincent (USDA Forest Service), and Joe White (USDA Forest Service). We also thank Nathan Havill, Joseph Nairn, Kenneth Ross, and two anonymous reviewers for their helpful comments on an earlier version of this manuscript. This research was supported in part by the USDA Forest Service, Southern Research Station (13CA11330129056 and 16CS11330129045), Southern Region-Forest Health Protection, and the University of Georgia (2015) Innovative and Interdisciplinary Research Grant.
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Microsatellite genotypes at all loci for all samples can be found in the supplementary information (Table S4).
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Whitney, T.D., Gandhi, K.J.K., Hamrick, J.L. et al. Extant population genetic variation and structure of eastern white pine (Pinus strobus L.) in the Southern Appalachians. Tree Genetics & Genomes 15, 74 (2019). https://doi.org/10.1007/s11295-019-1380-3
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DOI: https://doi.org/10.1007/s11295-019-1380-3