Chloroplast haplotypes suggest preglacial differentiation and separate postglacial migration paths for the threatened North American forest tree Juglans cinerea L.

Abstract

Postglacial migration paths for most of the tree species of Eastern North America remain unknown. The presence of no-analogue forest communities prior to the last glacial advance suggests that individual trees species in Eastern North America may respond differently as climate changes and human impacts increase. In this study, we examined chloroplast haplotypes from natural populations of Juglans cinerea L., a North American forest tree, to infer postglacial migration patterns. Sequences from eight different regions of the chloroplast genome in 197 trees distributed across the range revealed 10 haplotypes. A minimum spanning network, phylogenetic analysis and haplotype distributions revealed that the three most common haplotypes were geographically disjunct and not closely related. Haplotype 6 (73 trees) occurred only in western populations, haplotype 10 (83 trees) occurred only in eastern populations and haplotype 7 (21 trees) occurred only at the southern edge of the native range. The southernmost population contained the most haplotype diversity but included no eastern haplotypes. Haplotype phylogeography suggested geographical differentiation prior to the last glacial advance in eastern populations and separate postglacial migration paths for eastern and western populations. As migration of J. cinerea to Atlantic Canada from southern refugia does not appear possible given known seed dispersal mechanisms, the possibility of northern refugia or dispersal by extinct megafauna merits serious consideration. Differences among species in preglacial history, ecological niche preferences and seed dispersal mechanisms suggest that response to long-term climate change and acute human disturbance may be highly species specific.

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References

  1. Anderson RL, LaMadelaine LA (1978) The distribution of butternut decline in the eastern United States. Northeastern Area State and Private Forestry, USDA Forest Service, Forest Survey Report S-3-78. Northeastern Area State and Private Forestry, Broomall, PA. 5 p

  2. Aradhya M, Potter D, Gao F, Simon C (2007) Molecular phylogeny of Juglans (Juglandaceae): a biogeographic perspective. Tree Gen Genom 3:363–378. doi:10.1007/s11295-006-0078-5

  3. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  4. Birchenko I, Feng Y, Romero-Severson J (2009) Biogeographical distribution of chloroplast diversity in northern red oak (Quercus rubra L.). Am Midl Nat 161:134–145

  5. Bordacs S et al (2002) Chloroplast DNA variation of white oaks in the northern Balkans and in the Carpathian Basin. For Ecol Manag 156:197–209

    Article  Google Scholar 

  6. Borkowski D, McCleary T, McAllister M, Romero-Severson J (2014) Primers for 52 polymorphic regions in the Quercus rubra chloroplast, 47 of which amplify across 11 tracheophyte clades. Tree Genetics & Genomes:1-9 doi:10.1007/s11295-014-0729-x

  7. Boulanger MT, Lyman RL (2014) Northeastern North American Pleistocene megafauna chronologically overlapped minimally with Paleoindians Quaternary Science Reviews 85:35-46 doi:http://dx.doi.org/10.1016/j.quascirev.2013.11.024

  8. Boys J, Cherry M, Dayanandan S (2005) Microsatellite analysis reveals genetically distinct populations of red pine (Pinus resinosa, Pinaceae). Am J Bot 92:833–841. doi:10.3732/ajb.92.5.833

  9. Breen AL, Murray DF, Olson MS (2012) Genetic consequences of glacial survival: the late Quaternary history of balsam poplar (Populus balsamifera L.) in North America. J Biogeogr 39:918–928. doi:10.1111/j.1365-2699.2011.02657.x

  10. Broders KD, Boland GJ (2011) Reclassification of the butternut canker fungus, Sirococcus clavigignenti-juglandacearum, into the genus Ophiognomonia. Fungal Biol 115:70–79. doi:10.1016/j.funbio.2010.10.007

  11. Bryan CF (1965) Butternut (Juglans cinerea L.). In: Fowells HA (ed) Silvics of forest trees of the United States. vol handbook 271. U.S. Department of Agriculture, Washington, DC, pp 208–210

  12. Clark JS et al (1998) Reid's paradox of rapid plant migration—dispersal theory and interpretation of paleoecological records. Bioscience 48:13–24

    Article  Google Scholar 

  13. Cristol DA, Switzer PV (1999) Avian prey-dropping behavior. II. American crows and walnuts. Behav Ecol 10:220–226. doi:10.1093/beheco/10.3.220

    Article  Google Scholar 

  14. Cruzan MB, Templeton AR (2000) Paleoecology and coalescence: phylogeographic analysis of hypotheses from the fossil record. Trends Ecol Evol 15:491–496. doi:10.1016/S0169-5347(00)01998-4

    Article  PubMed  Google Scholar 

  15. Delcourt HR (1979) Late quaternary vegetation history of the eastern highland rim and adjacent cumberland plateau of Tennessee. Ecol Monogr 49:255–280. doi:10.2307/1942485

    Article  Google Scholar 

  16. Delcourt PA, Delcourt HR, Brister RC, Lackey LE (1980) Quaternary vegetation history of the Mississippi embayment. Quat Res 13:111–132. doi:10.1016/0033-5894(80)90086-1

    Article  Google Scholar 

  17. Demesure B, Sodzi N, Petit RJ (1995) A set of universal primers for amplification of polymorphic noncoding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4:129–131

    Article  CAS  PubMed  Google Scholar 

  18. Dumolin-Lapegue S, Pemonge M, Petit R (1997) An enlarged set of consensus primers for the study of organelle DNA in plants. Mol Ecol 6:393–397

    Article  CAS  PubMed  Google Scholar 

  19. Feng Y, Sun W, Romero-Severson J (2008) Heterogeneity and spatial autocorrelation for chloroplast haplotypes in three old growth populations of northern red oak. Silvae Genet 57:212–220

    Google Scholar 

  20. Finkelstein SA, Gajewski K, Viau AE (2006) Improved resolution of pollen taxonomy allows better biogeographical interpretation of post-glacial forest development: analyses from the North American Pollen. Data J Ecol 94:415–430. doi:10.1111/j.1365-2745.2005.01087.x

    Article  Google Scholar 

  21. Furnier GR, Stolz AM, Mustaphi RM, Ostry ME (1999) Genetic evidence that butternut canker was recently introduced into North America. Can J Botan-Rev Canadienne De Botanique 77:783–785

    Article  Google Scholar 

  22. Fyles JG, Hills LV, Matthews JV Jr, Barendregt R, Baker J, Irving E, Jetté H (1994) Ballast brook and beaufort formations (late Tertiary) on Northern Banks Island, Arctic Canada. Quat Int 22–23:141–171. doi:10.1016/1040-6182(94)90010-8

    Article  Google Scholar 

  23. Gill JL, Williams JW, Jackson ST, Lininger KB, Robinson GS (2009) Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326:1100–1103. doi:10.1126/science.1179504

    Article  CAS  PubMed  Google Scholar 

  24. Godbout J, Jaramillo-Correa JP, Beaulieu J, Bousquet J (2005) A mitochondrial DNA minisatellite reveals the postglacial history of jack pine (Pinus banksiana), a broad-range North American conifer. Mol Ecol 14:3497–3512. doi:10.1111/j.1365-294X.2005.02674.x

  25. Godbout J, Beaulieu J, Bousquet J (2010) Phylogeographic structure of jack pine (Pinus banksiana; Pinaceae) supports the existence of a coastal glacial refugium in northeastern North America. Am J Bot 97:1903–1912. doi:10.3732/ajb.1000148

  26. Goheen JR, Swihart RK (2003) Food-hoarding behavior of gray squirrels and North American red squirrels in the central hardwoods region: implications for forest regeneration. Can J Zool 81:1636–1639

    Article  Google Scholar 

  27. Gonzales LM, Williams JW, Grimm EC (2009) Expanded response-surfaces: a new method to reconstruct paleoclimates from fossil pollen assemblages that lack modern analogues. Quat Sci Rev 28:3315–3332. doi:10.1016/j.quascirev.2009.09.005

    Article  Google Scholar 

  28. Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Mol Ecol 8:521–523

    CAS  PubMed  Google Scholar 

  29. Hickey LJ, Johnson KR, Dawson MR (1988) The stratigraphy, sedimentology, and fossils of the haughton formation: a post-impact crater-fill, Devon Island, N.W.T., Canada. Meteoritics 23:221–231. doi:10.1111/j.1945-5100.1988.tb01284.x

    Article  Google Scholar 

  30. Hills LV, Klovan JE, Sweet AR (1974) Juglans eocinerea n. sp., beaufort formation (Tertiary), southwestern Banks Island, Arctic Canada. Can J Bot 52:65–90. doi:10.1139/b74-011

  31. Hoban SM, Anderson R, McCleary TS, Schlarbaum SE, Romero-Severson J (2008) Thirteen nuclear microsatellite loci for butternut (Juglans cinerea L.). Mol Ecol Resour 8:643–646

  32. Hoban SM, McCleary TS, Schlarbaum SE, Romero-Severson J (2009) Geographically extensive hybridization between the forest trees American butternut and Japanese walnut. Biol Lett 5:324–327. doi:10.1098/rsbl.2009.0031

    Article  PubMed Central  PubMed  Google Scholar 

  33. Hoban SM et al (2010) Range-wide distribution of genetic diversity in the North American tree Juglans cinerea: a product of range shifts, not ecological marginality or recent population decline. Mol Ecol 19:4876–4891. doi:10.1111/j.1365-294X.2010.04834.x

  34. Hoban S, Schlarbaum S, Brosi S, Romero-Severson J (2012a) A rare case of natural regeneration in butternut, a threatened forest tree, is parent and space limited. Conserv Genet 13:1447–1457. doi:10.1007/s10592-012-0386-2

    Article  Google Scholar 

  35. Hoban SM, McCleary TS, Schlarbaum SE, Anagnostakis SL, Romero-Severson J (2012b) Human-impacted landscapes facilitate hybridization between a native and an introduced tree. Evol Appl 5:720–731

    Article  PubMed Central  PubMed  Google Scholar 

  36. Hoban SM, McCleary TS, Schlarbaum SE, Romero-Severson J (2014) Spatial genetic structure in 21 populations of butternut, a temperate forest tree (Juglans cinerea L.), is correlated to spatial arrangement, habitat, and land-use history. For Ecol Manag 314:50–58. doi:10.1016/j.foreco.2013.11.001

  37. Huang SSF, Hwang SY, Lin TP (2002) Spatial pattern of chloroplast DNA variation of Cyclobalanopsis glauca in Taiwan and east Asia. Mol Ecol 11:2349–2358

    Article  CAS  PubMed  Google Scholar 

  38. Ivan JS, Swihart RK (2000) Selection of mast by granivorous rodents of the central hardwood forest region. J Mammal 81:549–562. doi:10.1644/1545-1542(2000)081<0549:SOMBGR>2.0.CO;2

    Article  Google Scholar 

  39. Jackson ST, Weng C (1999) Late quaternary extinction of a tree species in eastern North America. Proc Natl Acad Sci 96:13847–13852. doi:10.1073/pnas.96.24.13847

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Jackson ST, Overpeck JT, Webb- Iii T, Keattch SE, Anderson KH (1997) Mapped plant-macrofossil and pollen records of late quaternary vegetation change in Eastern North America. Quat Sci Rev 16:1–70. doi:10.1016/S0277-3791(96)00047-9

    Article  Google Scholar 

  41. Jackson ST, Webb RS, Anderson KH, Overpeck JT, Webb T III, Williams JW, Hansen BCS (2000) Vegetation and environment in Eastern North America during the last glacial maximum. Quat Sci Rev 19:489–508. doi:10.1016/S0277-3791(99)00093-1

    Article  Google Scholar 

  42. Jaramillo-Correa JP, Beaulieu J, Bousquet J (2004) Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer. Mol Ecol 13:2735–2747. doi:10.1111/j.1365-294X.2004.02258.x

  43. Johnson WC, Thompson Webb III (1989) The role of blue jays (Cyanocitta cristata L.) in the postglacial dispersal of fagaceous trees in Eastern North America. J Biogeogr 16:561–571. doi:10.2307/2845211

  44. Le Corre V, Kremer A (1998) Cumulative effects of founding events during colonisation on genetic diversity and differentiation in an island and stepping-stone model. J Evol Biol 11:195–512

    Article  Google Scholar 

  45. Liu Y, Andersen JJ, Williams JW, Jackson ST (2013) Vegetation history in central Kentucky and Tennessee (USA) during the last glacial and deglacial periods. Quat Res 79:189–198. doi:10.1016/j.yqres.2012.12.005

    Article  CAS  Google Scholar 

  46. Loehle C (2007) Predicting pleistocene climate from vegetation in North America. Clim Past 3:109–118. doi:10.5194/cp-3-109-2007

    Article  Google Scholar 

  47. Magni CR, Ducousso A, Caron H, Petit RJ, Kremer A (2005) Chloroplast DNA variation of Quercus rubra L. in North America and comparison with other Fagaceae. Mol Ecol 14:513–524

  48. Marsico TD, Hellmann JJ, Romero-Severson J (2009) Patterns of seed dispersal and pollen flow in Quercus garryana (Fagaceae) following post-glacial climatic changes. J Biogeogr 36:929–941. doi:10.1111/j.1365-2699.2008.02049.x

  49. Martínez-Meyer E, Peterson AT (2006) Conservatism of ecological niche characteristics in North American plant species over the pleistocene-to-recent transition. J Biogeogr 33:1779–1789. doi:10.1111/j.1365-2699.2006.01482_33_10.x

    Article  Google Scholar 

  50. McCleary TS, Robichaud RL, Nuanes S, Anagnostakis SL, Schlarbaum SE, Romero-Severson J (2009) Four cleaved amplified polymorphic sequence (CAPS) markers for the detection of the Juglans ailantifolia chloroplast in putatively native J. cinerea populations. Mol Ecol Resour 9:525–527. doi:10.1111/j.1755-0998.2008.02465.x

  51. McCleary T, McAllister M, Coggeshall M, Romero-Severson J (2013) EST-SSR markers reveal synonymies, homonymies and relationships inconsistent with putative pedigrees in chestnut cultivars. Genet Resour Crop Evol 60:1209–1222. doi:10.1007/s10722-012-9912-9

    Article  Google Scholar 

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

    Article  Google Scholar 

  53. Middleton B (2000) Hydrochory, seed banks, and regeneration dynamics along the landscape boundaries of a forested wetland. Plant Ecol 146:167–181. doi:10.1023/A:1009871404477

    Article  Google Scholar 

  54. Moore JE, McEuen AB, Swihart RK, Contreras TA, Steele MA (2007) Determinants of seed removal distance by scatter-hoarding rodents in deciduous forests. Ecology 88:2529–2540. doi:10.2307/27651399

    Article  PubMed  Google Scholar 

  55. Omar S, Lemonnier B, Jones N, Ficker C, Smith ML, Neema C, Towers GHN, Goel K, Arnason JT (2000) Antimicrobial activity of extracts of eastern North American hardwood trees and relation to traditional medicine. J Ethnopharmacol 73:161–170

    Article  CAS  PubMed  Google Scholar 

  56. Parks A, Jenkins M, Ostry M, Zhao P, Woeste K (2014) Biotic and abiotic factors affecting the genetic structure and diversity of butternut in the southern Appalachian Mountains, USA. Tree Genet Gen 10:541–554. doi:10.1007/s11295-014-0702-8

    Article  Google Scholar 

  57. Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  58. Petit RJ et al (2002) Chloroplast DNA variation in European white oaks: phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manag 156:5–26. doi:10.1016/S0378-1127(01)00645-4

    Article  Google Scholar 

  59. Petit RJ et al (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

    Article  CAS  PubMed  Google Scholar 

  60. Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245

    PubMed Central  CAS  PubMed  Google Scholar 

  61. Posada D, Crandall K (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  62. Ronquist F et al (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed Central  PubMed  Google Scholar 

  63. Royall PD, Delcourt PA, Delcourt HR (1991) Late quaternary paleoecology and paleoenvironments of the Central Mississippi Alluvial Valley. Geol Soc Am Bull 103:157–170. doi:10.1130/0016-7606(1991)103<0157:lqpapo>2.3.co;2

    Article  Google Scholar 

  64. Schlarbaum SE, Hebard F, Spaine PC, Kamalay JC (1997) Three American tragedies: chestnut blight, butternut canker, and Dutch elm disease. In: Britton KO (ed) Proceedings, exotic pests of eastern forests. vol 1997 April 8-10. Tennessee Exotic Pest Plant Council, Nashville, pp 45–54

    Google Scholar 

  65. Schultz J (2003) Conservation assessment for butternut or white walnut (Juglans cinerea L.). USDA Forest Service, Eastern Region, Milwaukee, WI. 76 p. www.fs.fed.us/r9/wildlife/tes/ca-overview/docs/plant_juglans_cinera-Butternut2003.pdf

  66. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94:275–288. doi:10.3732/ajb.94.3.275

    Article  CAS  PubMed  Google Scholar 

  67. Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS (2006) Comparative phylogeography of unglaciated eastern North America. Mol Ecol 15:4261–4293

    Article  PubMed  Google Scholar 

  68. Stapanian MA, Smith CC (1986) How fox squirrels influence the invasion of prairies by nut-bearing trees. J Mammal:326-332

  69. Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613. doi:10.1016/S0169-5347(01)02338-2

    Article  Google Scholar 

  70. Stewart JR, Lister AM, Barnes I, Dalén L (2010) Refugia revisited: individualistic responses of species in space and time. Proc R Soc B Biol Sci 277:661–671. doi:10.1098/rspb.2009.1272

    Article  Google Scholar 

  71. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  72. Victory ER, Glaubitz JC, Rhodes OE Jr, Woeste KE (2006) Genetic homogeneity in Juglans nigra (Juglandaceae) at nuclear microsatellites. Am J Bot 93:118–126. doi:10.3732/ajb.93.1.118

  73. Wall SBV (2001) The evolutionary ecology of nut dispersal. Bot Rev 67:74–117. doi:10.2307/4354385

    Article  Google Scholar 

  74. Watts WA (1975) Vegetation record for the last 20,000 years from a small marsh on Lookout Mountain, northwestern Georgia. Geol Soc Am Bull 86:287–291. doi:10.1130/0016-7606(1975)86<287:vrftly>2.0.co;2

    Article  Google Scholar 

  75. Watts WA (1979) Late quaternary vegetation of central Appalachia and the New Jersey coastal plain. Ecol Monogr 49:427–469. doi:10.2307/1942471

    Article  Google Scholar 

  76. Whitlock C, Dawson MR (1990) Pollen and vertebrates of the early Neogene Haughton formation, Devon Island, Arctic Canada. Arctic 43:324–330. doi:10.2307/40510958

  77. Williams JW, Jackson ST (2007) Novel climates, no-analog communities, and ecological surprises. Front Ecol Environ 5:475–482. doi:10.1890/070037

    Article  Google Scholar 

  78. Williams JW, Shuman BN, Webb T (2001) Dissimilarity analyses of late-quaternary vegetation and climate in eastern North America. Ecology 82:3346–3362

    Google Scholar 

  79. Wolfe JA (1980) Tertiary climates and floristic relationships at high latitudes in the northern hemisphere. Palaeogeogr Palaeoclimatol Palaeoecol 30:313–323. doi:10.1016/0031-0182(80)90063-2

    Article  Google Scholar 

  80. Zaya D, Howe H (2009) The anomalous Kentucky coffeetree: megafaunal fruit sinking to extinction? Oecologia 161:221–226. doi:10.1007/s00442-009-1372-3

    Article  PubMed  Google Scholar 

  81. Zhang WH, Chen ZD, Li JH, Chen HB, Tang YC (2003) Phylogeny of the Dipsacales s.l. based on chloroplast trnL-F and ndhF sequences. Mol Phylogenet Evol 26:176–189

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Acknowledgments

We thank Bob Anderson, Paul Berrang, Sunshine Brosi, Bryan Connolly, Brice Leech, Scott Schlarbaum and Barb Boysen for assisting in sample collection. We also thank the private landowners, state governments and the provincial governments of Ontario and New Brunswick for allowing us access to state, provincial and private forests. This project was funded in part by an NSF Research Experience for Undergraduates summer program grant to Kristen Laricchia. Sean Hoban is supported as a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, funded by NSF Award #DBI-1300426, and The University of Tennessee, Knoxville.

Conflict of interest

The authors affirm that they have no conflicts of interest.

Data archiving statement

Sequences for haplotypes 2, 5, 6 and 10, which show all the polymorphisms we detected except one, are deposited at NCBI. Accessions numbers are listed in Table S1. The polymorphic region of ndhK-ndhC, being <200 bp and thus too short to deposit, is reported in Table S2.

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Correspondence to Jeanne Romero-Severson.

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Communicated by R. Sederoff

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Laricchia, K.M., McCleary, T.S., Hoban, S.M. et al. Chloroplast haplotypes suggest preglacial differentiation and separate postglacial migration paths for the threatened North American forest tree Juglans cinerea L.. Tree Genetics & Genomes 11, 30 (2015). https://doi.org/10.1007/s11295-015-0852-3

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Keywords

  • Chloroplast haplotypes
  • Juglans cinerea
  • Postglacial migration