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Toward the genetic origins of a potentially non-native population of threespine stickleback (Gasterosteus aculeatus) in Alberta

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Abstract

Disentangling the origin of putatively introduced/invasive species is of increasing priority in conservation biology. The presence of a previously undocumented species may be due to an undetected recent population or range expansion associated with environmental change, or due to an introduction by humans. We used molecular tools to address the origin of a population of threespine stickleback (Gasterosteus aculeatus) first identified in central Alberta, Canada in 1980 from a single lake. We characterized this inland, high elevation Alberta population in comparison to samples from five representative geographic regions worldwide, using mtDNA and nine microsatellite loci to elucidate genetic structure and estimate divergence times. We found significantly lower levels of genetic variation in the Alberta population, which could reflect either a recent colonization or periodic bottlenecks associated with winterkills. While we did find that the Alberta samples were most closely related to the North American West Coast populations, we did not uncover a putative source population. Alberta samples formed a clade in phylogenetic analyses, with divergence time estimates between the Alberta and British Columbia samples ca. 250–750 kya. The hypothesis that the Alberta population represents a natural colonization during North America’s last glacial recession could not be rejected. Collectively, these data suggest that the genetic signature of colonizing populations following introductions may be similar to populations at their range limit, contributing to difficulties establishing population origins.

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References

  • Alberta Environment Sustainable Resource and Development (2014) Focus on fisheries management. http://esrd.alberta.ca/about-esrd/documents/FocusOn-FisheriesManagement-2014.pdf

  • Aldenhoven JT, Miller MA, Corneli PS, Shapiro MD (2010) Phylogeny of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits. Mol Ecol 19:4061–4076

    Article  CAS  PubMed  Google Scholar 

  • Ascunce MS, Yang CC, Oakey J, Calcaterra L, Wu WJ, Shih CJ, Shoemaker D (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331(6020):1066–1068

    Article  CAS  PubMed  Google Scholar 

  • Austin JD, Lougheed SC, Boag PT (2004) Controlling for the effects of history and nonequilibrium conditions in gene flow estimates in northern bullfrog (Rana catesbeiana) Populations. Genetics 168:1491–1506

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baker JA, Heins DC, Foster SA, King RW (2008) An overview of life-history variation in female threespine stickleback. Behaviour 145:579–602

    Article  Google Scholar 

  • Barrett RD, Paccard A, Healy TM, Bergek S, Schulte PM, Schluter D, Rogers SM (2010) Rapid evolution of cold tolerance in stickleback. Proc R Soc B 278(1703):233–238

    Article  PubMed Central  PubMed  Google Scholar 

  • Barson NJ, Cable J, van Oosterhout C (2009) Population genetic analysis of microsatellite variation of guppies (Poecilia reticulata) in Trinidad and Tobago: evidence for a dynamic source-sink metapopulation structure, founder events and population bottlenecks. J Evol Biol 22:485–497

    Article  CAS  PubMed  Google Scholar 

  • Bell MA, Foster SA (1994) Introduction. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 1–27

    Google Scholar 

  • Bell MA, Stewart JD, Park PJ (2009) The world’s oldest fossil threespine stickleback fish. Copeia 2:256–265

    Article  Google Scholar 

  • Bernatchez L, Wilson CC (1998) Comparative phylogeography of nearctic and palearctic fishes. Mol Ecol 7:431–452

    Article  Google Scholar 

  • Bryan MB, Zalinski D, Filcek KB, Libants S, Li W, Scribner KT (2005) Patterns of invasion and colonization of the sea lamprey (Petromyzon marinus) in North America as revealed by microsatellite genotypes. Mol Ecol 14(12):3757–3773

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty R, Nei M (1977) Bottleneck effects on average heterozygosity and genetic distance with the stepwise mutation model. Evolution 31:347–356

    Article  Google Scholar 

  • Chapman RW (1986) Mitochondrial and nuclear gene dynamics of introduced populations of Lepomis macrochirus. Genetics 123:399–404

    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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Costello AB, Down TE, Pollard SM, Pacas CJ, Taylor EB (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in bull trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57:328–344

    Article  CAS  PubMed  Google Scholar 

  • Crispo E, Chapman LJ (2008) Population genetic structure across dissolved oxygen regimes in an African cichlid fish. Mol Ecol 17:2134–2148

    Article  CAS  PubMed  Google Scholar 

  • Crispo E, Hendry AP (2005) Does time since colonization influence isolation by distance? A meta-analysis. Conserv Genet 6:665–682

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772

    Article  CAS  PubMed  Google Scholar 

  • Davy CM, Ménndez de la Cruz FR, Lathrop A, Murphy RM (2011) Seri Indian traditional knowledge and molecular biology agree: no express train for island-hopping spiny-tailed iguanas in the Sea of Cortés. J Biogeogr 38:272–284

    Article  Google Scholar 

  • DeFaveri J, Merilä J (2013) Variation in age and size in Fennoscandian threespined sticklebacks (Gasterosteus aculeatus). PLoS ONE 8(11):e80866

    Article  PubMed Central  PubMed  Google Scholar 

  • DeHaan PW, Adams BA, Tabor RA, Hawkins DK, Thompson B (2014) Historical and contemporary forces shape genetic variation in the Olympic mudminnow (Novumbra hubbsi) from Washington State, USA. Conservation Genetics, pp 1–15

  • Dennenmoser S, Nolte AW, Vamosi SM, Rogers SM (2013) Conservation genetics of prickly sculpin (Cottus asper) at the periphery of its distribution range in Peace River, Canada. Conserv Genet 14(3):735–739

    Article  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. Genetics 91:3166–3170

    Google Scholar 

  • Dieringer D, Schlštterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3(1):167–169

    Article  CAS  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  CAS  PubMed  Google Scholar 

  • Drinan DP, Kalinowski ST, Vu NV, Shepard BB, Muhlfeld CC, Campbell MR (2011) Genetic variation in westslope cutthroat trout Oncorhynchus clarkii lewisi: implications for conservation. Conserv Genet 12:1513–1523

    Article  Google Scholar 

  • Drummond AJ, Ho SYW, Philips MJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214–221

    Article  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29(8):1969–1973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361

    Article  Google Scholar 

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-margin hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10:564–567

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Grover A, Sharma PC (2011) Is spatial occurrence of microsatellites in the genome a determinant of their function and dynamics contributing to genome evolution? Curr Sci 6:859–869

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Herborg LM, Mandrak NE, Cudmore BC, MacIsaac HJ (2007) Comparative distribution and invasion risk of snakehead (Channidae) and asian carp (Cyprinidae) species in North America. Can J Fish Aquat Sci 64(12):1723–1735

    Article  Google Scholar 

  • Hey J (2005) On the number of New World founders: a population genetic portrait of the peopling of the Americas. PLoS Biol 3(6):e193

    Article  PubMed Central  PubMed  Google Scholar 

  • Houston DD, Shiozawa DK, Smith BT, Riddle BR (2014) Investigating the effects of Pleistocene events on genetic divergence within Richardsonius balteatus, a widely distributed western North American minnow. BMC Evol Biol 14:111

    Article  PubMed Central  PubMed  Google Scholar 

  • Hubert N, Hanner R, Holm E, Mandrak NE, Taylor E, Burridge M, Watkinson D, Dumont P, Curry A, Bentzen P, Zhang J, April J, Bernatchez L (2008) Identifying Canadian freshwater fishes through DNA barcodes. PLoS ONE 3:e2490

    Article  PubMed Central  PubMed  Google Scholar 

  • Huey JA, Baker AM, Hughes JM (2011) Evidence for multiple historical colonizations of an endoreic drainage basin by an Australian freshwater fish. J Fish Biol 79:1047–1067

    Article  CAS  PubMed  Google Scholar 

  • Jackson LJ, Lauridsen TL, Søndergaard M, Jeppesen E (2007) A comparison of shallow Danish and Canadian lakes and implications of climate change. Freshw Biol 52:1782–1792

    Article  CAS  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jones FC, Grabherr MG, Chan YF, Russell P, Mauceli E et al (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55–61

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49(4):725

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kinnison MT, Bentzen P, Unwin MJ, Quinn TP (2002) Reconstructing recent divergence: evaluating nonequilibrium population structure in New Zealand chinook salmon. Mol Ecol 11:739–754

    Article  CAS  PubMed  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kolar CS, Chapman DC, Courtenay WR Jr, Housel CM, Williams JD, Jennings DP (2005) Asian carps of the genus Hypophthalmichthys (Pisces, Cyprinidae)—a biological synopsis and environmental risk assessment. U.S Fish and Wildlife Service, Washington

    Google Scholar 

  • Leberg PL (1992) Effects of populations bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46(2):477–494

    Article  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lindholm AK, Breden F, Alexander HJ, Chan WK, Thakurta SG, Brooks R (2005) Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol Ecol 14:3671–3682

    Article  CAS  PubMed  Google Scholar 

  • McCairns R, Bernatchez L (2008) Landscape genetic analyses reveal cryptic population structure and putative selection gradients in a large-scale estuarine environment. Mol Ecol 17:3901–3916

    Article  PubMed  Google Scholar 

  • McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488

    Article  Google Scholar 

  • McPhail JD (1994) Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 399–437

    Google Scholar 

  • Mee JA, Moore J-S (2014) Guest editorial: the ecological and evolutionary implications of microrefugia. J Biogeogr 41(5):837–841

    Article  Google Scholar 

  • Mee JA, Bernatchez L, Reist JD, Rogers SM, Taylor EB (2015) Identifying evolutionarily significant units for intraspecific conservation prioritization: a hierarchical approach applied to the lake whitefish species complex (Coregonus spp.). Evol Appl. doi:10.1111/eva.12247

  • Menotti-Raymond M, O’Brien SJ (1993) Dating the genetic bottleneck of the African cheetah. Proc Natl Acad Sci USA 90:3172–3176

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meyer A, Kocher TD, Basasibwaki P, Wilson AC (1990) Monophyletic origin of Lake Victoria fishes suggested by mitochondrial DNA sequences. Nature 347:550–553

    Article  CAS  PubMed  Google Scholar 

  • Morris MRJ, Richard R, Leder EH, Barrett RD, Aubin-Horth N, Rogers SM (2014) Gene expression plasticity evolves in response to colonization of freshwater lakes in threespine stickleback. Mol Ecol 23:3226–3240

    Article  PubMed  Google Scholar 

  • Münzing J (1963) The evolution of variation and distributional patterns in European populations of the three-spined stickleback, Gasterosteus aculeatus. Evolution 17:320–332

    Article  Google Scholar 

  • Neff BD, Fu P, Gross MR (1999) Microsatellite evolution in sunfish Centrarchidae). Can J Fish Aquat Sci 56:1198–1205

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nelson JS, Harris MA (1987) Morphological characteristics of an introduced threespine stickleback, Gasterosteus aculeatus, from Hasse Lake, Alberta: a first occurrence in the interior plains of North America. Environ Biol Fishes 18:173–181

    Article  Google Scholar 

  • Peichel CL, Nereng KS, Ohgi KA, Cole B, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414:901–905

    Article  CAS  PubMed  Google Scholar 

  • Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends Ecol Evol 24(9):497–504

    Article  PubMed  Google Scholar 

  • Prentis PJ, Wilson JRU, Dormontt EE, Richardson DM, Lowe AJ (2008) Adaptive evolution in invasive species. Trends Plant Sci 13:288–294

    Article  CAS  PubMed  Google Scholar 

  • Price TD, Sol D (2008) Genetics of colonizing species. Am Nat 172(S1):S1–S3

    Article  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rafiński J, Bańgbura J, Przybylski M (1989) Genetic differentiation of freshwater and marine sticklebacks, (Gasterosteus aculeatus) of Eastern Europe. J Zool Syst Evol Res 27:33–43

    Article  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.4. Available from http://beast.bio.ed.ac.uk/Tracer

  • Rawlinson SE, Bell MA (1982) A stickleback fish (Pungitius) from the Neogene Sterling Formation, Kanai Peninsula, Alaska. J Paleontol 56:583–588

    Google Scholar 

  • Richmond JQ, Wood DA, Stanford JW, Fisher RN (2014) Testing for multiple invasion routes and source populations for the invasive brown treesnake (Boiga irregularis) on Guam: implications for pest management. Biol Invasions 17:1–13

    Google Scholar 

  • Rogers SM, Tamkee P, Summers B, Balabahadra S, Marks M, Kingsley DM, Schluter D (2012) Genetic signature of adaptive peak shift in threespine stickleback. Evolution 66(8):2439–2450

    Article  PubMed Central  PubMed  Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8:103–106

    Article  PubMed  Google Scholar 

  • Seyfert AL, Cristescu MEA, Frisse L, Schaack S, Thomas WK, Lynch M (2008) The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex. Genetics 178:2113–2121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shafer BA, Cullingham CI, Côté 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  PubMed  Google Scholar 

  • Shikano T, Shimada Y, Herczeg G, Merilä J (2010) History vs. habitat type: explaining the genetic structure of European nine-spined stickleback (Pungitius pungitius) populations. Mol Ecol 19:1147–1161

    Article  PubMed  Google Scholar 

  • Smith TW (1989) Feeding interactions of sticklebacks and rainbow trout of Hasse Lake, Alberta. M.Sc. thesis, Department of Zoology, University of Alberta. Edmonton

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75(5):758–771

    Article  Google Scholar 

  • Stamford MD, Taylor EB (2004) Phylogeographical lineages of Arctic grayling (Thymallus arcticus) in North America: divergence, origins and affinities with Eurasian Thymallus. Mol Ecol 13(6):1533–1549

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taylor BW, Bothwell ML (2014) The origin of invasive microorganisms matters for science, policy, and management: the case of Didymosphenia geminate. Bioscience 64(6):531–538

    Article  Google Scholar 

  • Vamosi SM (2003) The presence of other fish species affects speciation in threespine sticklebacks. Evol Ecol Res 5:717–730

    Google Scholar 

  • Wang Y, Williams DA, Gaines MS (2005) Evidence for a recent genetic bottleneck in the endangered Florida Keyes silver rice rat (Oryzomys argentatus) revealed by microsatellite DNA analyses. Conserv Genet 6:575–585

    Article  CAS  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B 360:1847–1857

    Article  CAS  Google Scholar 

  • Wilson CC, Herbert PDN (1998) Phylogeography and postglacial dispersal of lake trout (Salvelinus namaycush) in North America. Can J Fish Aquat Sci 55:1010–1024

    Article  Google Scholar 

  • Yoshida K, Makino T, Yamaguchi K, Shigenobu S, Hasebe M, Kawata M, Kume M, Mori S, Peichel CL, Toyoda A, Fujiyama A, Kitano J (2014) Sex chromosome turnover contributes to genomic divergence between incipient stickleback species. PLoS Genet 10(3):e1004223

    Article  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr. Stephen Spencer of Environment and Sustainable Resource Development Alberta, and Stevi Vanderzwan for help collecting the Alberta samples. Thanks to Jacquelin DeFaveri of the Ecological Genetics Research Unit at the University of Helsinki, Finland, Scott McCairns of Université Laval, Canada, and Ella Bowles of the University of Calgary, Canada, for providing the Norwegian, East Coast, and Alaskan fish samples, respectively. The authors thank Matthew Morris for providing comments on a draft of the manuscript. SMR and SMV are supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant program. SMR was supported by an Alberta Innovates Technology Futures New Faculty Award. EC was supported by an NSERC Postdoctoral Fellowship. SMR and EC were supported by the Alberta Conservation Association. SMR would like to thank the late Dr. Joseph Nelson (1937–2011) who graciously provided many key reprints and advice in 2010 during the inception of this research.

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Correspondence to Sean M. Rogers.

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Sequence data are provided in GenBank (accession numbers KP823059 - KP823216) and the microsatellite genotypes are archived in Dryad (doi:10.5061/dryad.pc1th).

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Rezansoff, A.M., Crispo, E., Blair, C. et al. Toward the genetic origins of a potentially non-native population of threespine stickleback (Gasterosteus aculeatus) in Alberta. Conserv Genet 16, 859–873 (2015). https://doi.org/10.1007/s10592-015-0706-4

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