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Full mitochondrial genome sequences reveal new insights about post-glacial expansion and regional phylogeographic structure in the Atlantic silverside (Menidia menidia)

Marine Biology volume 165, Article number: 124 (2018) Cite this article

Abstract

One of the biggest challenges in population genetics of marine species is to uncover subtle phylogeographic patterns masked by large effective population sizes and/or high gene flow. In this paper, we use 189 full mitochondrial genome sequences from the Atlantic silverside (Menidia menidia), obtained during whole nuclear genome re-sequencing, to address this challenge. With this approach, we were able to provide a high-resolution analysis of the demographic history and current genetic structure of the species. We clearly defined a regional genetic structure that is stronger than previously thought. This structure groups the species into three regional subdivisions: (1) south of Cape Cod; (2) Gulf of Maine; and (3) Gulf of St. Lawrence. Among the regional subdivisions, our data reveal that the two northern groups show the greatest divergence despite their adjacency along the latitudinal gradient, while genetic homogeneity within the southern subdivision suggests connectivity throughout its broad geographical distribution. Furthermore, using approximate Bayesian computation (ABC) methods, we inferred that both northern populations are the result of independent colonization events from the south after the Last Glacial Maximum (LGM). Our analyses indicate that at least one of the northern populations has received two waves of colonization, one timed immediately after the LGM and the other timed after the end of the Younger Dryas glacial re-advance. Finally, we found one locus potentially under positive selection in the mitochondrial genome. The results of this study illustrate the power of full mitochondrial genome sequencing in phylogeographic research, and because the Atlantic silverside is known for its clinal phenotypic variation throughout its range, our findings have important implications for the study of local adaptation.

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Data accessibility

All full mitochondrial genome sequences generated in the study are available in available in NCBI GenBank under accession numbers MH538710–MH538898.

References

  • Adams LD, Rosel PE (2006) Population differentiation of the Atlantic spotted dolphin (Stenella frontalis) in the western North Atlantic, including the Gulf of Mexico. Mar Biol 148:671–681

    Article  Google Scholar 

  • Altschul SF, Gish W (1996) Local alignment statistics. Method Enzymol 266:460–480

    Article  CAS  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard Univ Press, Cambridge, MA

    Google Scholar 

  • Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Barrowclough GF, Zink RM (2009) Funds enough, and time: mtDNA, nuDNA and the discovery of divergence. Mol Ecol 18:2934–2936

    Article  CAS  Google Scholar 

  • Bigg GR, Cunningham CW, Ottersen G, Pogson GH, Wadley MR, Williamson P (2008) Ice-age survival of Atlantic cod: agreement between palaeoecology models and genetics. Proc R Soc B 275:163–173

    Article  PubMed  Google Scholar 

  • Bilton DT, Mirol PM, Mascheretti S, Fredga K, Zima J, Searle JB (1998) Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization. Proc R Soc Lond B 265:1219–1226

    Article  CAS  Google Scholar 

  • Bridle JR, Vines TH (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol Evol 22:140–147

    Article  PubMed  Google Scholar 

  • Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971

    Article  PubMed  CAS  Google Scholar 

  • Burridge CP, Craw D, Fletcher D, Waters JM (2008) Geological dates and molecular rates: fish DNA sheds light on time dependency. Mol Biol Evol 25:624–633

    Article  PubMed  CAS  Google Scholar 

  • Carpenter KE, Munroe T (2015) Menidia menidia. The IUCN Red List of Threatened Species 2015:e.T16441575A16510092. https://doi.org/10.2305/iucn.uk.2015-4.rlts.t16441575a16510092.en

  • Carr SM, Marshall HD (2008) Intraspecific phylogeographic genomics from multiple complete mtDNA genomes in Atlantic cod (Gadus morhua): origins of the “Codmother”, transatlantic vicariance and midglacial population expansion. Genetics 180:381–389

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B, Mitrovica JX, Hostetler SW, McCabe AM (2009) The Last Glacial Maximum. Science 325:710–714

    Article  PubMed  CAS  Google Scholar 

  • Clarke LM, Munch SB, Thorrold SR, Conover DO (2010) High connectivity among locally adapted populations of a marine fish (Menidia menidia). Ecology 91:3526–3537

    Article  PubMed  Google Scholar 

  • Conover DO (1984) Adaptive significance of temperature-dependent sex determination in a fish. Am Nat 123:297–313

    Article  Google Scholar 

  • Conover DO, Baumann H (2009) The role of experiments in understanding fishery-induced evolution. Evol Appl 2:276–290

    Article  PubMed  PubMed Central  Google Scholar 

  • Conover DO, Murawski S (1982) Offshore winter migration of the Atlantic silverside, Menidia menidia. Fish Bull 80:145–149

    Google Scholar 

  • Conover DO, Present TM (1990) Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83:316–324

    Article  PubMed  Google Scholar 

  • Conover DO, Arnott SA, Walsh MR, Munch SB (2005) Darwinian fishery science: lessons from the Atlantic silverside (Menidia menidia). Can J Fish Aquat Sci 62:730–737

    Article  Google Scholar 

  • Conover DO, Duffy TA, Hice LA (2009) The covariance between genetic and environmental influences across ecological gradients. Ann NY Acad Sci 1168:100–129

    Article  PubMed  Google Scholar 

  • Cordes JF, Graves JE (2003) Investigation of congeneric hybridization in and stock structure of weakfish (Cynoscion regalis) inferred from analyses of nuclear and mitochondrial DNA loci. Fish Bull 101:443–451

    Google Scholar 

  • Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, Marin J-M, Estoup A (2014) DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30:1187–1189

    Article  PubMed  CAS  Google Scholar 

  • Coscia I, McDevitt AD, King JJ, Roche WK, McLoughlin C, Mariani S (2013) A species-to-be? The genetic status and colonization history of the critically endangered Killarney shad. Mol Phylogenet Evol 69:1190–1195

    Article  PubMed  Google Scholar 

  • Coulson MW, Marshall HD, Pepin P, Carr SM (2006) Mitochondrial genomics of gadine fishes: implications for taxonomy and biogeographic origins from whole-genome data sets. Genome 49:1115–1130

    Article  PubMed  CAS  Google Scholar 

  • Dahlgren TG, Weinberg JR, Halanych KM (2000) Phylogeography of the ocean quahog (Arctica islandica): influences of paleoclimate on genetic diversity and species range. Mar Biol 137:487–495

    Article  Google Scholar 

  • Doellman MM, Trussell GC, Grahame JW, Vollmer SV (2011) Phylogeographic analysis reveals a deep lineage split within North Atlantic Littorina saxatilis. Proc R Soc B 278:3175–3183

    Article  PubMed  Google Scholar 

  • Drumm DT, Kreiser B (2012) Population genetic structure and phylogeography of Mesokalliapseudes macsweenyi (Crustacea: Tanaidacea) in the northwestern Atlantic and Gulf of Mexico. J Exp Mar Biol Ecol 412:58–65

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Edwards S, Bensch S (2009) Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Mol Ecol 18:2930–2933

    Article  PubMed  CAS  Google Scholar 

  • Edwards SV, Kingan SB, Calkins JD, Balakrishnan CN, Jennings WB, Swanson WJ, Sorenson MD (2005) Speciation in birds: genes, geography, and sexual selection. Proc Natl Acad Sci USA 102:6550–6557

    Article  PubMed  CAS  Google Scholar 

  • Efremov RG, Sazanov LA (2011) Structure of the membrane domain of respiratory complex I. Nature 476:414–420

    Article  PubMed  CAS  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. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Flight PA, O’Brien MA, Schmidt PS, Rand DM (2012) Genetic structure and the North American postglacial expansion of the barnacle, Semibalanus balanoides. J Hered 103:153–165

    Article  PubMed  CAS  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  PubMed Central  CAS  Google Scholar 

  • Goudet J (2005) hierfstat, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5:184–186

    Article  Google Scholar 

  • Hare MP (2001) Prospects for nuclear gene phylogeography. Trends Ecol Evol 16:700–706

    Article  Google Scholar 

  • Harrison RG (1989) Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol Evol 4:6–11

    Article  PubMed  CAS  Google Scholar 

  • Harrisson K, Pavlova A, Gan HM, Lee YP, Austin CM, Sunnucks P (2016) Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species. Heredity 116:506–515

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Herman JS, Searle JB (2011) Post-glacial partitioning of mitochondrial genetic variation in the field vole. Proc R Soc B 278:3601–3607

    Article  PubMed  Google Scholar 

  • Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Article  Google Scholar 

  • Hice LA, Duffy TA, Munch SB, Conover DO (2012) Spatial scale and divergent patterns of variation in adapted traits in the ocean: adaptive genetic variation in the ocean. Ecol Lett 15:568–575

    Article  PubMed  Google Scholar 

  • Hickerson MJ, Cunningham CW, Orti G (2005) Contrasting quaternary histories in an ecologically divergent sister pair of low-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis. Evolution 59:344–360

    Article  PubMed  Google Scholar 

  • Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2010) Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301

    Article  PubMed  CAS  Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of the cytochrome b gene of mammals. J Mol Evol 32:128–144

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki W, Fukunaga T, Isagozawa R, Yamada K, Maeda Y, Satoh TP, Sado T, Mabuchi K, Takeshima H, Miya M, Nishida M (2013) MitoFish and MitoAnnotator: a mitochondrial genome database of fish with an accurate and automatic annotation pipeline. Mol Biol Evol 30:2531–2540

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jacobsen MW, da Fonseca RR, Bernatchez L, Hansen MM (2016) Comparative analysis of complete mitochondrial genomes suggests that relaxed purifying selection is driving high nonsynonymous evolutionary rate of the NADH2 gene in whitefish (Coregonus ssp.). Mol Phylogenet Evol 95:161–170

    Article  PubMed  CAS  Google Scholar 

  • Kelley JL, Brown AP, Therkildsen NO, Foote AD (2016) The life aquatic: advances in marine vertebrate genomics. Nat Rev Genet 17:523–534

    Article  PubMed  CAS  Google Scholar 

  • Kelly DW, MacIsaac HJ, Heath DD (2006) Vicariance and dispersal effects on phylogeographic structure and speciation in a widespread estuarine invertebrate. Evolution 60:257–267

    Article  PubMed  Google Scholar 

  • Kim I-C, Kweon H-S, Kim YJ, Kim C-B, Gye MC, Lee W-O, Lee Y-S, Lee J-S (2004) The complete mitochondrial genome of the Javeline goby Acanthogobius hasta (Perciformes, Gobiidae) and phylogenetic considerations. Gene 336:147–153

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576

    PubMed  PubMed Central  CAS  Google Scholar 

  • Kocher TD, Stepien CA (eds) (1997) Molecular systematics of fishes. Academic Press, San Diego, CA

    Google Scholar 

  • Korneliussen TS, Albrechtsen A, Nielsen R (2014) ANGSD: analysis of next generation sequencing data. BMC Bioinform 15:356

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  PubMed  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Leigh JW, Bryant D (2015) Popart: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mach ME, Sbrocco EJ, Hice LA, Duffy TA, Conover DO, Barber PH (2011) Regional differentiation and post-glacial expansion of the Atlantic silverside, Menidia menidia, an annual fish with high dispersal potential. Mar Biol 158:515–530

    Article  PubMed  Google Scholar 

  • Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Väinölä R, Viard F, Wares J (2008) Evaluating signatures of glacial refugia for north Atlantic benthic marine taxa. Ecology 89:S108–S122

    Article  PubMed  Google Scholar 

  • Marshall DJ, Monro K, Bode M, Keough MJ, Swearer S (2010) Phenotype–environment mismatches reduce connectivity in the sea. Ecol Lett 13:128–140

    Article  PubMed  CAS  Google Scholar 

  • McCartney MA, Burton ML, Lima TG (2013) Mitochondrial DNA differentiation between populations of black sea bass (Centropristis striata) across Cape Hatteras, North Carolina (USA). J Biogeogr 40:1386–1398

    Article  Google Scholar 

  • Meraner A, Cornetti L, Gandolfi A (2014) Defining conservation units in a stocking-induced genetic melting pot: unraveling native and multiple exotic genetic imprints of recent and historical secondary contact in Adriatic grayling. Ecol Evol 4:1313–1327

    Article  PubMed  PubMed Central  Google Scholar 

  • Morales HE, Pavlova A, Joseph L, Sunnucks P (2015) Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Mol Ecol 24:2820–2837

    Article  PubMed  CAS  Google Scholar 

  • Morin PA, Archer FI, Foote AD, Vilstrup J, Allen EE, Wade P, Durban J, Parsons K, Pitman R, Li L, Bouffard P, Nielsen SCA, Rasmussen M, Willerslev E, Gilbert MTP, Harkins T (2010) Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species. Genome Res 20:908–916

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nielsen R, Slatkin M (2013) An introduction to population genetics: theory and applications. Sinauer, Sunderland, MA

    Google Scholar 

  • Pelletier TA, Carstens BC (2014) Model choice for phylogeographic inference using a large set of models. Mol Ecol 23:3028–3043

    Article  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Rambaut A (2016) FigTree. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 15 Nov 2016

  • Rasmussen SO, Andersen KK, Svensson AM, Steffensen JP, Vinther BM, Clausen HB, Siggaard-Andersen M-L, Johnsen SJ, Larsen LB, Dahl-Jensen D, Bigler M, Röthlisberger R, Fischer H, Goto-Azuma K, Hansson ME, Ruth U (2006) A new Greenland ice core chronology for the last glacial termination. J Geophys Res Atmos 111:D06102

    Article  CAS  Google Scholar 

  • Reitzel AM, Herrera S, Layden MJ, Martindale MQ, Shank TM (2013) Going where traditional markers have not gone before: utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Mol Ecol 22:2953–2970

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rull V (2009) Microrefugia. J Biogeogr 36:481–484

    Article  Google Scholar 

  • Sanford E, Kelly MW (2011) Local adaptation in marine invertebrates. Annu Rev Mar Sci 3:509–535

    Article  Google Scholar 

  • Setiamarga DHE, Miya M, Yamanoue Y, Mabuchi K, Satoh TP, Inoue JG, Nishida M (2008) Interrelationships of Atherinomorpha (medakas, flyingfishes, killifishes, silversides, and their relatives): the first evidence based on whole mitogenome sequences. Mol Phylogenet Evol 49:598–605

    Article  PubMed  CAS  Google Scholar 

  • Shafer ABA, 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 19:4589–4621

    Article  PubMed  Google Scholar 

  • Shaw J, Gareau P, Courtney RC (2002) Palaeogeography of Atlantic Canada 13–0 kyr. Quat Sci Rev 21:1861–1878

    Article  Google Scholar 

  • Steffensen JP, Andersen KK, Bigler M, Clausen HB, Dahl-Jensen D, Fischer H, Goto-Azuma K, Hansson M, Johnsen SJ, Jouzel J, Masson-Delmotte V, Popp T, Rasmussen SO, Röthlisberger R, Ruth U, Stauffer B, Siggaard-Andersen M-L, Sveinbjörnsdóttir ÁE, Svensson A, White JWC (2008) High-resolution Greenland ice core data show abrupt climate change happens in few years. Science 321:680–684

    Article  PubMed  CAS  Google Scholar 

  • Stewart JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends Ecol Evol 16:608–613

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Strasser CA, Barber PH (2008) Limited genetic variation and structure in softshell clams (Mya arenaria) across their native and introduced range. Conserv Genet 10:803–814

    Article  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  PubMed Central  CAS  Google Scholar 

  • Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526

    PubMed  CAS  Google Scholar 

  • Teacher AG, André C, Merilä J, Wheat CW (2012) Whole mitochondrial genome scan for population structure and selection in the Atlantic herring. BMC Evol Biol 12:248

    Article  PubMed  PubMed Central  Google Scholar 

  • Therkildsen NO, Palumbi SR (2017) Practical low-coverage genomewide sequencing of hundreds of individually barcoded samples for population and evolutionary genomics in nonmodel species. Mol Ecol Resour 17:194–208

    Article  PubMed  CAS  Google Scholar 

  • Thomé MTC, Carstens BC (2016) Phylogeographic model selection leads to insight into the evolutionary history of four-eyed frogs. Proc Natl Acad Sci USA 113:8010–8017

    Article  PubMed  CAS  Google Scholar 

  • Tigano A, Friesen VL (2016) Genomics of local adaptation with gene flow. Mol Ecol 25:2144–2164

    Article  PubMed  Google Scholar 

  • Wetterstrand KA (2015) DNA sequencing costs: data from the NHGRI genome sequencing program (GSP). www.genome.gov/sequencingcosts. Accessed 29 May 2017

  • Willette D, Allendorf F, Barber P, Barshis D, Carpenter K, Crandall E, Cresko W, Fernandez-Silva I, Matz M, Meyer E, Santos M, Seeb L, Seeb J (2014) So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute. Bull Mar Sci 90:79–122

    Article  Google Scholar 

  • Wilson AC, Cann RL, Carr SM, George M, Gyllensten UB, Helm-Bychowski KM, Higuchi RG, Palumbi SR, Prager EM, Sage RD, Stoneking M (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc 26:375–400

    Article  Google Scholar 

  • Ye F, Samuels DC, Clark T, Guo Y (2014) High-throughput sequencing in mitochondrial DNA research. Mitochondrion 17:157–163

    Article  PubMed  CAS  Google Scholar 

  • Zhang D-X, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol 11:247–251

    Article  PubMed  CAS  Google Scholar 

  • Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We are most indebted to Stephen Palumbi, who provided funding and valuable insights to this project. We would also like to thank Steve Munch and Hannes Baumann for helping transport samples for this study, Beth Sheets for assistance in the laboratory, Anna Tigano and two anonymous reviewers for their valuable comments on the manuscript, and Vivienne Liu for helping with the figures. The data were generated with support from National Science Foundation Grant OCE-1434325 to Stephen Palumbi.

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  1. Nina O. Therkildsen and Jeremy B. Searle contributed equally.

Authors and Affiliations

  1. Department of Natural Resources, Cornell University, Ithaca, NY, 14853, USA

    Runyang Nicolas Lou, Aryn P. Wilder & Nina O. Therkildsen

  2. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA

    Nicholas K. Fletcher & Jeremy B. Searle

  3. San Diego Zoo Institute for Conservation Research, Escondido, CA, 92027, USA

    Aryn P. Wilder

  4. University of Oregon, Eugene, OR, 97403, USA

    David O. Conover

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  1. Runyang Nicolas Lou
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Correspondence to Runyang Nicolas Lou.

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Lou, R.N., Fletcher, N.K., Wilder, A.P. et al. Full mitochondrial genome sequences reveal new insights about post-glacial expansion and regional phylogeographic structure in the Atlantic silverside (Menidia menidia). Mar Biol 165, 124 (2018). https://doi.org/10.1007/s00227-018-3380-5

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