Abstract
Arctic relict populations, which persist in disjunct locations far south of a species’ normal range, are at the frontline of climate change and may be especially susceptible to the negative impacts of climate warming. Further, these relict populations may face increasing contact with, or become outcompeted by, invasive species if the invasive taxa are spreading along with the warming climate. Relict populations are simultaneously of particular conservation importance due to their unique genetic make-up and potential for adaptations to warmer temperatures compared to populations at the core of the species range. In this study, we used genotyping-by-sequencing to study the population genetics of Euphrasia hudsoniana, a polyploid arctic disjunct of conservation concern, at the southern edge of its range along the northwestern shore of Lake Superior. In addition, we examined evidence for hybridization with its invasive congener, E. stricta. Overall, we found clear differentiation between the native and invasive species indicated by nearly all analyses. There was limited evidence for gene flow from the invasive into the native species, but patterns were consistent with more extensive gene flow in the opposite direction. Differentiation among native populations was low, yet two of the five populations fell into a separate, distinct group based on STRUCTURE analyses. Continued genetic monitoring of these populations will help elucidate whether hybridization with invasives is a burgeoning threat for this arctic relict.
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 12:299–313
Bauert MR, KÄLin M, Baltisberger M, Edwards PJ (1998) No genetic variation detected within isolated relict populations of Saxifraga cernua in the Alps using RAPD markers. Mol Ecol 7:1519–1527
Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529
Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635
Brochmann C, Steen SW (1999) Sex and genes in the flora of Svalbard—implications for conservation biology and climate change. Det Norske Videnskaps-Akademi I Matematisk-Naturvitenskapelig Klasse Skrifter, Ny Serie 38:33–72
Clevenger JP, Ozias-Akins P (2015) SWEEP: a tool for filtering high-quality SNPs in polyploid crops. G3 5:1797–1803. doi:10.1534/g3.115.019703
Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evol Int J Org Evol 62:1908–1920
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. doi:10.1093/bioinformatics/btr330
Davis MB, Shaw RG, Etterson JR (2005) Evolutionary responses to changing climate. Ecology 86:1704–1714
Doak DF, Morris WF (2010) Demographic compensation and tipping points in climate-induced range shifts. Nature 467:959–962
Downie SR, McNeill J (1988) Description and distribution of Euphrasia stricta in North America. Rhodora 90:223–231
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
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. doi:10.1007/s12686-011-9548-7
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Evol Syst 24:217–242
Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE. doi:10.1371/journal.pone.0019379
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. doi:10.1111/j.1365-294X.2005.02553.x
French GC, Ennos RA, Silverside AJ, Hollingsworth PM (2005) The relationship between flower size, inbreeding coefficient and inferred selfing rate in British Euphrasia species. Heredity 94:44–51
Given DR, Soper JH (1981) The artic-alpine element of the vascular flora at lake superior. National Museum of Natural Resources Publications in Botany, No. 10
Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE 9:e90346
Gomert Z, Buerkle CA (2009) A powerful regression-based method for admixture mapping of isolation across the genome of hybrids. Mol Ecol 18:1207–1224
Gomert Z, Buerkle CA (2010) introgress: a software package for mapping components of isolation in hybrids. Mol Ecol Resour 10:378–384
Gross BL, Rieseberg LH (2005) The ecological genetics of homoploid hybrid speciation. J Hered 96:241–252
Gusarova G, Popp M, Vitek E, Brochmann C (2008) Molecular phylogeny and biogeography of the bipolar Euphrasia (Orobanchaceae): recent radiations in an old genus. Mol Phylogenet Evol 48:444–460
Hampe A, Jump AS (2011) Climate relicts: past, present, future. Annu Rev Ecol Evol Syst 42:313–333
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467
Hegland SJ, Totland Ø (2012) Interactions for pollinator visitation and their consequences for reproduction in a plant community. Acta Oecol 43:95–103
Holsbeek G, Mergeay J, Hotz H, Plotner J, Volckaert FA, De Meester L (2008) A cryptic invasion within an invasion and widespread introgression in the European water frog complex: consequences of uncontrolled commercial trade and weak international legislation. Mol Ecol 17:5023–5035
Huff A, Thomas A (2014) Lake Superior climate change impacts and adaptation. Prepared for the Lake Superior Lakewide Action and Management Plan – Superior Work Group
Johnson MG, Lang K, Manos P, Golet GH, Schierenbeck KA (2016) Evidence for genetic erosion of a California native tree, Platanus racemosa, via recent, ongoing introgressive hybridization with an introduced ornamental species. Conserv Genet 17:593–602
Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol. doi:10.1093/molbev/msw054
Lesica P, McCune B (2004) Decline of arctic-alpine plants at the southern margin of their range following a decade of climatic warming. J Veg Sci 15:679–690
Liebst B (2008) Do they really hybridize? A field study in artificially established mixed populations of Euphrasia minima and E. salisburgensis (Orobanchaceae) in the Swiss Alps. Plant Syst Evol 273:179–189
Liebst B, Schneller J (2005) How selfing and intra-and interspecific crossing influence seed set, morphology and ploidy level in Euphrasia: an experimental study of species occurring in the Alps of Switzerland. Plant Syst Evol 255:193–214
Lu F, Lipka AE, Glaubitz J, Elshire R, Cherney JH, Casler MD, Buckler ES, Costich DE (2013) Switchgrass genomic diversity, ploidy, and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 9:e1003215
Lucek K (2016) Cryptic invasion drives phenotypic changes in central European threespine stickleback. Conserv Genet 17:993–999
McAllister CA, Miller AJ (2016) Single nucleotide polymorphism discovery via genotyping by sequencing to assess population genetic structure and recurrent polyploidization in Andropogon gerardii. Am J Bot 103:1314–1325
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Meirmans PG, Van Tienderen PH (2013) The effects of inheritance in tetraploids on genetic diversity and population divergence. Heredity 110:131–137
MN DNR (2016) Euphrasia hudsoniana var. ramosior. Minnesota’s endangered, threatened, and special concern species: rare species guide. http://www.dnr.state.mn.us/rsg/profile.html?action=elementDetailandselectedElement=PDSCR0P053
Nimis P, Malyshev L, Bolognini G, Friesen N (1998) A multivariate phytogeographic analysis of plant diversity in the Putorana Plateau (N. Siberia). Opera Bot 136:1–72
Owens GL, Baute GJ, Rieseberg LH (2016) Revisiting a classic case of introgression: hybridization and gene flow in Californian sunflowers. Mol Ecol 25:2630–2643
Pembleton LW, Cogan NO, Forster JW (2013) StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13:946–952
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Reznicek AA, Voss EG, Walters BS (2011) Michigan Flora Online. University of Michigan. Web. August 11, 2016. http://michiganflora.net/species.aspx?id=1865
Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Evol Syst 27:83–109
Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Evol Syst 28:359–389
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Saltonstall K (2002) Cryptic invasion by a non-native genotype of the common reed, Phragmites australis, into North America. Proc Natl Acad Sci USA 99:2445–2449
Sell PD, Yeo PF (1970) A revision of the North American species of Euphrasia L. (Scrophulariaceae). Bot J Linn Soc 63:189–234
Smith W (1988) Vascular plants, Chapter 1. In: Coffin B, Pfannmuller L (eds) Minnesota’s endangered flora and fauna. University of Minnesota Press, Minneapolis, p 185
Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci USA 101:11030–11035
Thuiller W, Richardson DM, Midgley GF (2007) Will climate change promote alien plant invasions? In: Nentwig W (ed) Biological invasions. Springer, New York, pp 197–211
Todesco M, Pascual MA, Owens GL, Ostevik KL, Moyers BT, Hübner S, Heredia SM, Hahn MA, Caseys C, Bock DG, Rieseberg LH (2016) Hybridization and extinction. Evol Appl 9:892–908
Winkler KJ, Etterson JR (2015) Natural selection in populations of Euphrasia hudsoniana var. ramosior along the north shore of Lake Superior. Technical report for Minnesota’s Lake Superior Coastal Program
Yeo PF (1968) The evolutionary significance of the speciation of Euphrasia in Europe. Evolution 22:736–747. doi:10.2307/2406899
Acknowledgements
We acknowledge L. Gerdes and G. Gusarova for sharing their expertise on Euphrasia species, M Cleveland, A McCormick, the Grand Portage Band of Lake Superior Chippewa, the Minnesota Department of Natural Resources, and United States Forest Service for facilitating or providing permission to collect samples, J. Manolis for assistance collecting samples, A. Boser, J. Horky, A. Schumann, and M. Wedger for lab support, the Gross, Strasburg, and Etterson labs, and two anonymous reviewers for helpful comments on this manuscript. This work was funded in part by the Coastal Zone Management Act of 1972, as amended, administered by the Office for Coastal Management, National Oceanic and Atmospheric Administration under Award NA14NOS4190055 provided to the Minnesota Department of Natural Resources for Minnesota’s Lake Superior Coastal Program.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10592_2017_995_MOESM1_ESM.tif
Fig S1. MDS analysis of SNP data, filtered separately for each species then merged (196 SNPs), for a) Euphrasia hudsoniana and Euphrasia stricta individuals sampled from five and two populations respectively along the north shore of Lake Superior and b) the E. hudsoniana individuals only. The first two principal coordinates are plotted. (TIF 38300 KB)
10592_2017_995_MOESM2_ESM.tif
Fig S2. Neighbor joining tree based on SNPs filtered separately for each species then merged (196 SNPs), for a) Euphrasia hudsoniana and Euphrasia stricta individuals sampled from five and two populations respectively and b) E. hudsoniana individuals only. Bootstrap values greater than 0.5 are shown. (TIF 74414 KB)
10592_2017_995_MOESM3_ESM.tif
Fig S3. Delta K values for putative clusters of Euphrasia hudsoniana and E. stricta individuals (a) and E. hudsoniana individuals (b) (‘filtered together’ dataset; 972 SNPs). Delta K = mean(|L”(K)|)/sd(L(K)). (TIF 23852 KB)
10592_2017_995_MOESM4_ESM.tif
Fig S4. STRUCTURE results based on SNP data filtered separately for each species then merged (196 SNPs) for best supported values of K for a) Euphrasia hudsoniana and Euphrasia stricta individuals sampled from five and two populations respectively (K=2) and b) Euphrasia hudsoniana individuals (K=2). (TIF 24219 KB)
10592_2017_995_MOESM5_ESM.tif
Fig S5. Neighbor joining tree based on SNPs ‘filtered together’ (972 SNPs) for a) Euphrasia hudsoniana and E. stricta individuals sampled from five and two populations respectively and b) E. hudsoniana individuals only. Bootstrap values greater than 0.5 are shown. (TIF 74477 KB)
Rights and permissions
About this article
Cite this article
Zlonis, K.J., Gross, B.L. Genetic structure, diversity, and hybridization in populations of the rare arctic relict Euphrasia hudsoniana (Orobanchaceae) and its invasive congener Euphrasia stricta . Conserv Genet 19, 43–55 (2018). https://doi.org/10.1007/s10592-017-0995-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-017-0995-x